Marine66 PDF

ADVANCES IN MARINE BIOLOGY
Series Editor
MICHAEL LESSER
Department of Molecular, Cellular and Biomedical Sciences
University of New Hampshire, Durham, USA
Editors Emeritus
LEE A. FUIMAN
University of Texas at Austin
CRAIG M. YOUNG
Oregon Institute of Marine Biology
Advisory Editorial Board
ANDREW J. GOODAY
Southampton Oceanography Centre
SANDRA E. SHUMWAY
University of Connecticut
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CONTRIBUTORS TO VOLUME 66
Valerie Allain
Oceanic Fisheries Programme, Secretariat of the Pacific Community, BP D5, Noumea,
New Caledonia
Serge Andréfouët
Institut de recherche pour le développement (IRD), LabEx-CORAIL, UR 227 ‘CoReUs’,
BP A5, Noumea, New Caledonia
Griselda Avila-Soria
James Cook University, 1 James Cook Dr Douglas, Townsville, Queensland, Australia
Nicholas J. Bax
Wealth from Oceans Flagship, CSIRO Marine and Atmospheric Research, Castray
Esplanade, and Institute for Marine and Antarctic Studies, University of Tasmania, Private
Bag 49, Hobart, Tasmania, Australia
Robin Beaman
School of Earth and Environmental Sciences, James Cook University, PO Box 6811, Cairns,
Queensland, Australia
April M.H. Blakeslee
Biology Department, Long Island University-Post, Brookville, New York, and Marine Invasions
Laboratory, Smithsonian Environmental Research Center, Edgewater, Maryland, USA
Philippe Borsa
IRD-UR 227 ‘CoReUs’ c/o Universitas Udayana, Jl Sesetan Gang Markisa no.6, Denpasar,
Indonesia
David Brewer
CSIRO Marine and Atmospheric Research, EcoSciences Precinct, GPO Box 2583, Dutton
Park 4001, Qld, Australia
Richard Brinkman
Australian Institute of Marine Science, PMB No. 3, TMC, Townsville, Queensland, Australia
Rodrigo H. Bustamante
Wealth from Oceans Flagship, CSIRO Marine and Atmospheric Research, Ecosciences
Precinct, GPO Box 2583, Dutton Park 4001, Qld, Australia
Robert Campbell
Esplanade, Hobart, Tasmania, Australia
Mike Cappo
Australian Institute of Marine Science, PMB No. 3, TMC, Townsville, Queensland,
Australia
Daniela M. Ceccarelli
Marine Ecology Consultant, PO Box 215, Magnetic Island, Queensland, Australia
v
vi Contributors to Volume 66
Scott Condie
CSIRO Marine and Atmospheric Research, Castray Esplanade, Hobart, Tasmania,
Australia
Sophie Cravatte
Institut de Recherche pour le Développement, LEGOS, Nouméa, New Caledonia, and
LEGOS, Observatoire Midi-Pyrénées, Université de Toulouse/IRD/CNRS/CNES,
Toulouse, France
Stéphanie D’Agata
Catherine M. Dichmont
Piers K. Dunstan
Cécile Dupouy
Mediterranean Institute of Oceanography, UMR CNRS/IRD/AMU/USTV 7294, 235,
Graham Edgar
Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 49, Hobart,
Tasmania, Australia
Richard Farman
Aquarium des Lagons, BP 8185, Nouméa, New Caledonia
Peter J. Fenner
Occupational Health Mackay, PO Box 3080, North Mackay, Queensland, Australia
Adrian Flynn
Fathom Pacific Pty Ltd, Kensington, Victoria, Australia
Amy E. Fowler
Marine Invasions Laboratory, Smithsonian Environmental Research Center, Edgewater,
Maryland, and Marine Resources Research Institute, South Carolina Department of Natural
Resources, Charleston, South Carolina, USA
Miles Furnas
Claire Garrigue
Opération Cétacés, BP 12827, Noumea, New Caledonia
Lisa-ann Gershwin
CSIRO Marine and Atmospheric Research, Castray Esplanade, Hobart, Tasmania,
Australia
Daniel C. Gledhill
Contributors to Volume 66 vii
Russell Hore
Reef Biosearch, Meridian Marina, Port Douglas, Queensland, Australia
Trevor Hutton
Carolyn L. Keogh
Odum School of Ecology, University of Georgia, Athens, Georgia, USA
Rudy J. Kloser
CSIRO Marine and Atmospheric Research, Castray Esplanade, Hobart, Tasmania, Australia
Michel Kulbicki
IRD-UR 227 ‘CoReUs’, LABEX “Corail”, c/o Laboratoire Arago, BP 44,
Banyuls-sur-mer, France
Yves Letourneur
Université de la Nouvelle-Calédonie, BP R4, Nouméa Cedex, New Caledonia
Dhugal Lindsay
Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-
cho, Yokosuka City, Kanagawa Prefecture, Japan
John Lippmann
Divers Alert Network Asia-Pacific, PO Box 384 (49A Karnak Road), Ashburton, Victoria,
Australia
A. David McKinnon
Christophe Menkes
UMR 7159 LOCEAN (IRD/CNRS/UPMC/MNHN), Université Pierre et Marie Curie,
Case 100, Paris, France, and Institut de recherche pour le Développement-LOCEAN,
Nouméa, New Caledonia
David Mouillot
5119 ECOSYM (CNRS-UM2-IFREMER-IRD), Université Montpellier 2 cc 093,
Montpellier Cedex 5, France
Valeriano Parravicini
IRD-UR 227 ‘CoReUs’, LABEX “Corail”, c/o Laboratoire Arago, BP 44,
Banyuls-sur-mer, France
Claude Payri
Bernard Pelletier
UMR 7329 GEOAZUR (UNS-CNRS-IRD-OCA), BP A5, Noumea, New Caledonia
Anthony J. Richardson
Park 4001, Qld, and Centre for Applications in Natural Resource Mathematics (CARM),
School of Mathematics and Physics, University of Queensland, St Lucia, 4072, Brisbane,
Queensland, Australia
viii Contributors to Volume 66
Bertrand Richer de Forges

Muséum National d’Histoire Naturelle, Département Systématique et Evolution, 57 rue
Cuvier 75005 Paris Cedex 5, France
Ken Ridgway
Martine Rodier
Mediterranean Institute of Oceanography, UMR CNRS/IRD/AMU/USTV 7294, 235,
BP A5, Noumea, New Caledonia, and UMR 241 EIO (IRD-Ifremer-UPF-ILM) BP 529,
PK 3, 5 chemin de l’Arahiri, ARUE, Papeete, French Polynesia
Michael P. Russell
Biology Department, Villanova University, Villanova, Pennsylvania, USA
Sarah Samadi
Muséum National d’Histoire Naturelle, Département Systématique et Evolution, 57 rue
Cuvier 75005 Paris Cedex 5, France
David Schoeman
Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast,
Locked Bag 4, Maroochydore DC, Queensland, Australia
Tim Skewes
Andy Steven
Park 4001, Qld, Australia
Steven Swearer
Department of Zoology, University of Melbourne, Melbourne, Victoria, Australia
Laurent Vigliola
Laurent Wantiez
Alan Williams
Ashley Williams
Oceanic Fisheries Programme, Secretariat of the Pacific Community, BP D5, Noumea,
New Caledonia
Kenneth D. Winkel
Australian Venom Research Unit, Department of Pharmacology and Therapeutics,
University of Melbourne, Parkville, Victoria, Australia
Jock Young
SERIES CONTENTS FOR LAST FIFTEEN YEARS*
Volume 35, 1999.

Creasey, S. S. and Rogers, A. D. Population genetics of bathyal and abyssal
organisms. pp. 1–151.
Brey, T. Growth performance and mortality in aquatic macrobenthic inver-
tebrates. pp. 153–223.
Volume 36, 1999.

Shulman, G. E. and Love, R. M. The biochemical ecology of marine fishes.
pp. 1–325.
Volume 37, 1999.

His, E., Beiras, R. and Seaman, M. N. L. The assessment of marine
pollution—bioassays with bivalve embryos and larvae. pp. 1–178.
Bailey, K. M., Quinn, T. J., Bentzen, P. and Grant, W. S. Population
structure and dynamics of walleye pollock, Theragra chalcogramma.
pp. 179–255.
Volume 38, 2000.

Blaxter, J. H. S. The enhancement of marine fish stocks. pp. 1–54.
Bergström, B. I. The biology of Pandalus. pp. 55–245.
Volume 39, 2001.

Peterson, C. H. The “Exxon Valdez” oil spill in Alaska: acute indirect and
chronic effects on the ecosystem. pp. 1–103.
Johnson, W. S., Stevens, M. and Watling, L. Reproduction and develop-
ment of marine peracaridans. pp. 105–260.
Rodhouse, P. G., Elvidge, C. D. and Trathan, P. N. Remote sensing of the
global light-fishing fleet: an analysis of interactions with oceanography,
other fisheries and predators. pp. 261–303.
Volume 40, 2001.

Hemmingsen, W. and MacKenzie, K. The parasite fauna of the Atlantic cod,
Gadus morhua L. pp. 1–80.
*The full list of contents for volumes 1–37 can be found in volume 38
xi
xii Series Contents for Last Fifteen Years
Kathiresan, K. and Bingham, B. L. Biology of mangroves and mangrove

ecosystems. pp. 81–251.
Zaccone, G., Kapoor, B. G., Fasulo, S. and Ainis, L. Structural, histochem-
ical and functional aspects of the epidermis of fishes. pp. 253–348.
Volume 41, 2001.

Whitfield, M. Interactions between phytoplankton and trace metals in the
ocean. pp. 1–128.
Hamel, J.-F., Conand, C., Pawson, D. L. and Mercier, A. The sea cucumber
Holothuria scabra (Holothuroidea: Echinodermata): its biology and
exploitation as beche-de-Mer. pp. 129–223.
Volume 42, 2002.

Zardus, J. D. Protobranch bivalves. pp. 1–65.
Mikkelsen, P. M. Shelled opisthobranchs. pp. 67–136.
Reynolds, P. D. The Scaphopoda. pp. 137–236.
Harasewych, M. G. Pleurotomarioidean gastropods. pp. 237–294.
Volume 43, 2002.

Rohde, K. Ecology and biogeography of marine parasites. pp. 1–86.
Ramirez Llodra, E. Fecundity and life-history strategies in marine inverte-
brates. pp. 87–170.
Brierley, A. S. and Thomas, D. N. Ecology of southern ocean pack ice.
pp. 171–276.
Hedley, J. D. and Mumby, P. J. Biological and remote sensing perspectives
of pigmentation in coral reef organisms. pp. 277–317.
Volume 44, 2003.

Hirst, A. G., Roff, J. C. and Lampitt, R. S. A synthesis of growth rates in
epipelagic invertebrate zooplankton. pp. 3–142.
Boletzky, S. von. Biology of early life stages in cephalopod molluscs.
pp. 143–203.
Pittman, S. J. and McAlpine, C. A. Movements of marine fish and decapod
crustaceans: process, theory and application. pp. 205–294.
Cutts, C. J. Culture of harpacticoid copepods: potential as live feed for
rearing marine fish. pp. 295–315.
Volume 45, 2003.

Cumulative Taxonomic and Subject Index.
Series Contents for Last Fifteen Years xiii
Volume 46, 2003.

Gooday, A. J. Benthic foraminifera (Protista) as tools in deep-water
palaeoceanography: environmental influences on faunal characteristics.
pp. 1–90.
Subramoniam,T. and Gunamalai,V. Breeding biology of the intertidal sand
crab, Emerita (Decapoda: Anomura). pp. 91–182.
Coles, S. L. and Brown, B. E. Coral bleaching—capacity for acclimatization
and adaptation. pp. 183–223.
Dalsgaard J., St. John M., Kattner G., Müller-Navarra D. and Hagen W. Fatty
acid trophic markers in the pelagic marine environment. pp. 225–340.
Volume 47, 2004.

Southward, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J.,
Boalch, G. T., Dando, P. R., Genner, M. J., Joint, I., Kendall, M. A.,
Halliday, N. C., Harris, R. P., Leaper, R., Mieszkowska, N., Pingree,
R. D., Richardson, A. J., Sims, D.W., Smith, T., Walne, A. W. and
Hawkins, S. J. Long-term oceanographic and ecological research in the
western English Channel. pp. 1–105.
Queiroga, H. and Blanton, J. Interactions between behaviour and physical
forcing in the control of horizontal transport of decapod crustacean larvae.
pp. 107–214.
Braithwaite, R. A. and McEvoy, L. A. Marine biofouling on fish farms and
its remediation. pp. 215–252.
Frangoulis, C., Christou, E. D. and Hecq, J. H. Comparison of marine
copepod outfluxes: nature, rate, fate and role in the carbon and nitrogen
cycles. pp. 253–309.
Volume 48, 2005.

Canfield, D. E., Kristensen, E. and Thamdrup, B. Aquatic Geomicrobiology.
pp. 1–599.
Volume 49, 2005.

Bell, J. D., Rothlisberg, P. C., Munro, J. L., Loneragan, N. R., Nash, W. J.,
Ward, R. D. and Andrew, N. L. Restocking and stock enhancement of
marine invertebrate fisheries. pp. 1–358.
Volume 50, 2006.

Lewis, J. B. Biology and ecology of the hydrocoral Millepora on coral reefs.
pp. 1–55.
xiv Series Contents for Last Fifteen Years
Harborne, A. R., Mumby, P. J., Micheli, F., Perry, C. T., Dahlgren, C. P.,
Holmes, K. E., and Brumbaugh, D. R. The functional value of Caribbean
coral reef, seagrass and mangrove habitats to ecosystem processes.
pp. 57–189.
Collins, M. A. and Rodhouse, P. G. K. Southern ocean cephalopods.
pp. 191–265.
Tarasov, V. G. Effects of shallow-water hydrothermal venting on biological
communities of coastal marine ecosystems of the western Pacific.
pp. 267–410.
Volume 51, 2006.

Elena Guijarro Garcia. The fishery for Iceland scallop (Chlamys islandica) in
the Northeast Atlantic. pp. 1–55.
Jeffrey, M. Leis. Are larvae of demersal fishes plankton or nekton?
pp. 57–141.
John C. Montgomery, Andrew Jeffs, Stephen D. Simpson, Mark Meekan
and Chris Tindle. Sound as an orientation cue for the pelagic larvae of
reef fishes and decapod crustaceans. pp. 143–196.
Carolin E. Arndt and Kerrie M. Swadling. Crustacea in Arctic and Antarctic
sea ice: Distribution, diet and life history strategies. pp. 197–315.
Volume 52, 2007.

Leys, S. P., Mackie, G. O. and Reiswig, H. M. The Biology of Glass Spon-
ges. pp. 1–145.
Garcia E. G. The Northern Shrimp (Pandalus borealis) Offshore Fishery in
the Northeast Atlantic. pp. 147–266.
Fraser K. P. P. and Rogers A. D. Protein Metabolism in Marine Animals:
The Underlying Mechanism of Growth. pp. 267–362.
Volume 53, 2008.

Dustin J. Marshall and Michael J. Keough. The Evolutionary Ecology of
Offspring Size in Marine Invertebrates. pp. 1–60.
Kerry A. Naish, Joseph E. Taylor III, Phillip S. Levin, Thomas P. Quinn,
James R. Winton, Daniel Huppert, and Ray Hilborn. An Evaluation
of the Effects of Conservation and Fishery Enhancement Hatcheries on
Wild Populations of Salmon. pp. 61–194.
Shannon Gowans, Bernd Würsig, and Leszek Karczmarski. The Social
Structure and Strategies of Delphinids: Predictions Based on an
Ecological Framework. pp. 195–294.
Series Contents for Last Fifteen Years xv
Volume 54, 2008.

Bridget S. Green. Maternal Effects in Fish Populations. pp. 1–105.
Victoria J. Wearmouth and David W. Sims. Sexual Segregation in Marine
Fish, Reptiles, Birds and Mammals: Behaviour Patterns, Mechanisms and
Conservation Implications. pp. 107–170.
David W. Sims. Sieving a Living: A Review of the Biology, Ecology and
Conservation Status of the Plankton-Feeding Basking Shark Cetorhinus
Maximus. pp. 171–220.
Charles H. Peterson, Kenneth W. Able, Christin Frieswyk DeJong, Michael
F. Piehler, Charles A. Simenstad, and Joy B. Zedler. Practical Proxies for
Tidal Marsh Ecosystem Services: Application to Injury and Restoration.
pp. 221–266.
Volume 55, 2008.

Annie Mercier and Jean-Francois Hamel. Introduction. pp. 1–6.
Annie Mercier and Jean-Francois Hamel. Gametogenesis. pp. 7–72.
Annie Mercier and Jean-Francois Hamel. Spawning. pp. 73–168.
Annie Mercier and Jean-Francois Hamel. Discussion. pp. 169–194.
Volume 56, 2009.

Philip C. Reid, Astrid C. Fischer, Emily Lewis-Brown, Michael P.
Meredith, Mike Sparrow, Andreas J. Andersson, Avan Antia, Nicholas
R. Bates, Ulrich Bathmann, Gregory Beaugrand, Holger Brix, Stephen
Dye, Martin Edwards, Tore Furevik, Reidun Gangst, Hjalmar Hatun,
Russell R. Hopcroft, Mike Kendall, Sabine Kasten, Ralph Keeling,
Corinne Le Quere, Fred T. Mackenzie, Gill Malin, Cecilie Mauritzen,
Jon Olafsson, Charlie Paull, Eric Rignot, Koji Shimada, Meike Vogt,
Craig Wallace, Zhaomin Wang and Richard Washington. Impacts of
the Oceans on Climate Change. pp. 1–150.
Elvira S. Poloczanska, Colin J. Limpus and Graeme C. Hays. Vulnerability
of Marine Turtles to Climate Change. pp. 151–212.
Nova Mieszkowska, Martin J. Genner, Stephen J. Hawkins and David W.
Sims. Effects of Climate Change and Commercial Fishing on Atlantic
Cod Gadus morhua. pp. 213–274.
Iain C. Field, Mark G. Meekan, Rik C. Buckworth and Corey J. A.
Bradshaw. Susceptibility of Sharks, Rays and Chimaeras to Global
Extinction. pp. 275–364.
Milagros Penela-Arenaz, Juan Bellas and Elsa Vazquez. Effects of the
Prestige Oil Spill on the Biota of NW Spain: 5 Years of Learning.
pp. 365–396.
xvi Series Contents for Last Fifteen Years
Volume 57, 2010.

Geraint A. Tarling, Natalie S. Ensor, Torsten Fregin, William P. Good-all-
Copestake and Peter Fretwell. An Introduction to the Biology of
Northern Krill (Meganyctiphanes norvegica Sars). pp. 1–40.
Tomaso Patarnello, Chiara Papetti and Lorenzo Zane. Genetics of Northern
Krill (Meganyctiphanes norvegica Sars). pp. 41–58.
Geraint A. Tarling. Population Dynamics of Northern Krill (Meganyctiphanes
norvegica Sars). pp. 59–90.
John I. Spicer and Reinhard Saborowski. Physiology and Metabolism of
Katrin Schmidt. Food and Feeding in Northern Krill (Meganyctiphanes
norvegica Sars). pp. 127–172.
Friedrich Buchholz and Cornelia Buchholz. Growth and Moulting in
Janine Cuzin-Roudy. Reproduction in Northern Krill. pp. 199–230.
Edward Gaten, Konrad Wiese and Magnus L. Johnson. Laboratory-Based
Observations of Behaviour in Northern Krill (Meganyctiphanes norvegica
Sars). pp. 231–254.
Stein Kaartvedt. Diel Vertical Migration Behaviour of the Northern Krill
(Meganyctiphanes norvegica Sars). pp. 255–276.
Yvan Simard and Michel Harvey. Predation on Northern Krill
(Meganyctiphanes norvegica Sars). pp. 277–306.
Volume 58, 2010.

A. G. Glover, A. J. Gooday, D. M. Bailey, D. S. M. Billett, P. Chevaldonné,
A. Colaço, J. Copley, D. Cuvelier, D. Desbruyères, V. Kalogeropoulou,
M. Klages, N. Lampadariou, C. Lejeusne, N. C. Mestre, G. L. J. Paterson,
T. Perez, H. Ruhl, J. Sarrazin, T. Soltwedel, E. H. Soto, S. Thatje,
A. Tselepides, S. Van Gaever, and A. Vanreusel. Temporal Change in
Deep-Sea Benthic Ecosystems: A Review of the Evidence From Recent
Time-Series Studies. pp. 1–96.
Hilario Murua. The Biology and Fisheries of European Hake, Merluccius
merluccius, in the North-East Atlantic. pp. 97–154.
Jacopo Aguzzi and Joan B. Company. Chronobiology of Deep-Water
Decapod Crustaceans on Continental Margins. pp. 155–226.
Martin A. Collins, Paul Brickle, Judith Brown, and Mark Belchier. The
Patagonian Toothfish: Biology, Ecology and Fishery. pp. 227–300.
Volume 59, 2011.

Charles W. Walker, Rebecca J. Van Beneden, Annette F. Muttray, S. Anne
Böttger, Melissa L. Kelley, Abraham E. Tucker, and W. Kelley Thomas.
Series Contents for Last Fifteen Years xvii
p53 Superfamily Proteins in Marine Bivalve Cancer and Stress Biology.

pp 1–36.
Martin Wahl, Veijo Jormalainen, Britas Klemens Eriksson, James A. Coyer,
Markus Molis, Hendrik Schubert, Megan Dethier, Anneli Ehlers, Rolf
Karez, Inken Kruse, Mark Lenz, Gareth Pearson, Sven Rohde, Sofia
A. Wikström, and Jeanine L. Olsen. Stress Ecology in Fucus: Abiotic,
Biotic and Genetic Interactions. pp. 37–106.
Steven R. Dudgeon and Janet E. Kübler. Hydrozoans and the Shape of
Things to Come. pp. 107–144.
Miles Lamare, David Burritt, and Kathryn Lister. Ultraviolet Radiation and
Echinoderms: Past, Present and Future Perspectives. pp. 145–187.
Volume 60, 2011.

Tatiana A. Rynearson and Brian Palenik. Learning to Read the Oceans:
Genomics of Marine Phytoplankton. pp. 1–40.
Les Watling, Scott C. France, Eric Pante and Anne Simpson. Biology of
Deep-Water Octocorals. pp. 41–122.
Cristián J. Monaco and Brian Helmuth. Tipping Points, Thresholds and the
Keystone Role of Physiology in Marine Climate Change Research.
pp. 123–160.
David A. Ritz, Alistair J. Hobday, John C. Montgomery and Ashley J.W.
Ward. Social Aggregation in the Pelagic Zone with Special Reference
to Fish and Invertebrates. pp. 161–228.
Volume 61, 2012.

Gert Wörheide, Martin Dohrmann, Dirk Erpenbeck, Claire Larroux,
Manuel Maldonado, Oliver Voigt, Carole Borchiellini and Denis
Lavrov. Deep Phylogeny and Evolution of Sponges (Phylum Porifera).
pp. 1–78.
Paco Cárdenas, Thierry Pérez and Nicole Boury-Esnault. Sponge System-
atics Facing New Challenges. pp. 79–210.
Klaus Rützler. The Role of Sponges in the Mesoamerican Barrier-Reef
Ecosystem, Belize. pp. 211–272.
Janie Wulff. Ecological Interactions and the Distribution, Abundance, and
Diversity of Sponges. pp. 273–344.
Maria J. Uriz and Xavier Turon. Sponge Ecology in the Molecular Era.
pp. 345–410.
Volume 62, 2012.

Sally P. Leys and April Hill. The Physiology and Molecular Biology of
Sponge Tissues. pp. 1–56.
xviii Series Contents for Last Fifteen Years
Robert W. Thacker and Christopher J. Freeman. Sponge–Microbe Symbi-

oses: Recent Advances and New Directions. pp. 57–112.
Manuel Maldonado, Marta Ribes and Fleur C. van Duyl. Nutrient Fluxes
Through Sponges: Biology, Budgets, and Ecological Implications.
pp. 113–182.
Grégory Genta-Jouve and Olivier P. Thomas. Sponge Chemical Diversity:
From Biosynthetic Pathways to Ecological Roles. pp. 183–230.
Xiaohong Wang, Heinz C. Schröder, Matthias Wiens, Ute Schloßmacher
and Werner E. G. Müller. Biosilica: Molecular Biology, Biochemistry
and Function in Demosponges as well as its Applied Aspects for Tissue
Engineering. pp. 231–272.
Klaske J. Schippers, Detmer Sipkema, Ronald Osinga, Hauke Smidt, Shirley
A. Pomponi, Dirk E. Martens and René H. Wijffels. Cultivation of Spon-
ges, Sponge Cells and Symbionts: Achievements and Future Prospects.
pp. 273–338.
Volume 63, 2012.

Michael Stat, Andrew C. Baker, David G. Bourne, Adrienne M. S. Correa,
Zac Forsman, Megan J. Huggett, Xavier Pochon, Derek Skillings, Robert
J. Toonen, Madeleine J. H. van Oppen, and Ruth D. Gates. Molecular
Delineation of Species in the Coral Holobiont. pp. 1–66.
Daniel Wagner, Daniel G. Luck, and Robert J. Toonen. The Biology
and Ecology of Black Corals (Cnidaria: Anthozoa: Hexacorallia:
Antipatharia). pp. 67–132.
Cathy H. Lucas, William M. Graham, and Chad Widmer. Jellyfish Life
Histories: Role of Polyps in Forming and Maintaining Scyphomedusa
Populations. pp. 133–196.
T. Aran Mooney, Maya Yamato, and Brian K. Branstetter. Hearing in Ceta-
ceans: From Natural History to Experimental Biology. pp. 197–246.
Volume 64, 2013.

Dale Tshudy. Systematics and Position of Nephrops Among the Lobsters.
pp. 1–26.
Mark P. Johnson, Colm Lordan, and Anne Marie Power. Habitat and Ecol-
ogy of Nephrops norvegicus. pp. 27–64.
Emi Katoh, Valerio Sbragaglia, Jacopo Aguzzi, and Thomas Breithaupt.
Sensory Biology and Behaviour of Nephrops norvegicus. pp. 65–106.
Edward Gaten, Steve Moss, and Magnus L. Johnson. The Reniform
Reflecting Superposition Compound Eyes of Nephrops norvegicus: Optics,
Susceptibility to Light-Induced Damage, Electrophysiology and a Ray
Tracing Model. pp. 107–148.
Series Contents for Last Fifteen Years xix
Susanne P. Eriksson, Bodil Hernroth, and Susanne P. Baden. Stress Biology

and Immunology in Nephrops norvegicus. pp. 149–200.
Adam Powell and Susanne P. Eriksson. Reproduction: Life Cycle, Larvae
and Larviculture. pp. 201–246.
Anette Ungfors, Ewen Bell, Magnus L. Johnson, Daniel Cowing, Nicola C.
Dobson, Ralf Bublitz, and Jane Sandell. Nephrops Fisheries in European
Waters. pp. 247–314.
Volume 65, 2013.

Isobel S.M. Bloor, Martin J. Attrill, and Emma L. Jackson. A Review of the
Factors Influencing Spawning, Early Life Stage Survival and Recruitment
Variability in the Common Cuttlefish (Sepia officinalis). pp. 1–66.
Dianna K. Padilla and Monique M. Savedo. A Systematic Review of
Phenotypic Plasticity in Marine Invertebrate and Plant Systems.
pp. 67–120.
Leif K. Rasmuson. The Biology, Ecology and Fishery of the Dungeness
crab, Cancer magister. pp. 121–174.
CHAPTER ONE
Biology and Ecology of Irukandji

Jellyfish (Cnidaria: Cubozoa)
Lisa-ann Gershwin*,1, Anthony J. Richardson†,{, Kenneth D. Winkel},
Peter J. Fenner}, John Lippmann||, Russell Hore#, Griselda Avila-
Soria**, David Brewer†, Rudy J. Kloser*, Andy Steven†, Scott Condie*
*CSIRO Marine and Atmospheric Research, Castray Esplanade, Hobart, Tasmania, Australia
†
CSIRO Marine and Atmospheric Research, EcoSciences Precinct, GPO Box 2583, Dutton Park 4001,
Qld, Australia
{
Centre for Applications in Natural Resource Mathematics (CARM), School of Mathematics and Physics,
University of Queensland, St Lucia, 4072, Brisbane, Queensland, Australia
}
Australian Venom Research Unit, Department of Pharmacology and Therapeutics, University of Melbourne,
Parkville, Victoria, Australia
}
Occupational Health Mackay, PO Box 3080, North Mackay, Queensland, Australia
||
Divers Alert Network Asia-Pacific, PO Box 384 (49A Karnak Road), Ashburton, Victoria, Australia
#
Reef Biosearch, Meridian Marina, Port Douglas, Queensland, Australia
**James Cook University, 1 James Cook Dr Douglas, Townsville, Queensland, Australia
1
Corresponding author: e-mail address: Lisa-Ann.Gershwin@csiro.au
Contents
1. Introduction 2
1.1 History of study 6
2. Biology of Irukandji 11
2.1 Taxonomy 11
2.2 Evolution 22
2.3 Reproduction and life cycle 24
2.4 Eyes and vision 30
2.5 Behaviour 34
3. Ecology of Irukandji 35
3.1 Diet and feeding 35
3.2 Geographic distribution 36
3.3 Vertical distribution 41
3.4 Temporal changes 44
3.5 Movements and aggregations 52
3.6 Environmental variables 57
4. Toxins 58
4.1 Which part of the animal is toxic? 64
4.2 Evolution of Irukandji toxins 65
5. Stinger Management 65
5.1 Prediction 66
5.2 Detection 67
5.3 Prevention 68
5.4 Treatment 68
Advances in Marine Biology, Volume 66 # 2013 Elsevier Ltd 1

ISSN 0065-2881 All rights reserved.
http://dx.doi.org/10.1016/B978-0-12-408096-6.00001-8
2 Lisa-ann Gershwin et al.
6. Research Gaps 69
Acknowledgements 71
Appendix A. Notes on Rearing and Life Cycle of Carukia barnesi 72
Appendix B. Notes on Australian Alatina mordens Occurrence 75
References 76
Abstract
Irukandji stings are a leading occupational health and safety issue for marine industries in
tropical Australia and an emerging problem elsewhere in the Indo-Pacific and Caribbean.
Their mild initial sting frequently results in debilitating illness, involving signs of sympathetic
excess including excruciating pain, sweating, nausea and vomiting, hypertension and a
feeling of impending doom; some cases also experience acute heart failure and pulmonary
oedema. These jellyfish are typically small and nearly invisible, and their infestations are gen-
erally mysterious, making them scary to the general public, irresistible to the media, and
disastrous for tourism. Research into these fascinating species has been largely driven by
the medical profession and focused on treatment. Biological and ecological information
is surprisingly sparse, and is scattered through grey literature or buried in dispersed pub-
lications, hampering understanding. Given that long-term climate forecasts tend toward
conditions favourable to jellyfish ecology, that long-term legal forecasts tend toward
increasing duty-of-care obligations, and that bioprospecting opportunities exist in the
powerful Irukandji toxins, there is a clear need for information to help inform global research
and robust management solutions. We synthesise and contextualise available information
on Irukandji taxonomy, phylogeny, reproduction, vision, behaviour, feeding, distribution,
seasonality, toxins, and safety. Despite Australia dominating the research in this area, there
are probably well over 25 species worldwide that cause the syndrome and it is an under-
studied problem in the developing world. Major gaps in knowledge are identified for future
research: our lack of clarity on the socio-economic impacts, and our need for time series and
spatial surveys of the species, make this field particularly enticing.
Keywords: Irukandji syndrome, Marine stingers, Envenomation, Jellyfish

blooms, Carybdeida, Carukia, Malo, Morbakka, Gerongia, Alatina
1. INTRODUCTION
Seemingly minor stings from certain species of jellyfish can result in a
constellation of debilitating symptoms in human victims, which in turn result
in high medical costs, closed beaches, negative publicity, fear in the recrea-
tional public, and financial impacts for the tourism industry (see Box 1.1).
These jellyfish, loosely grouped under the common name Irukandji, are
understudied relative to their medical, financial, and social implications.
Irukandji syndrome typically manifests as severe lower back and abdominal
pain, relentless nausea and vomiting, full-body cramps and spasms, difficulty
breathing, profuse sweating, anxiety, muscular restlessness, headaches, and a
BOX 1.1 Why Irukandji research matters?
Top: (A) Mild sting to chest resulting in full-blown Irukandji syndrome, note
localised sweating (copyright S. Cohen). (B) Beach closed due to Irukandji. (C).
Mild bell-shaped sting to bicep resulting in Irukandji syndrome (copyright
B. Currie). (D) Five-year-old female, whose Irukandji sting required 3 days in inten-
sive care (copyright J. Margaglione). Bottom: A sample of media headlines about
Irukandji (from the collection of K. Moss).
Irukandji jellyfish meet all the criteria for a Hollywood horror film: Many are the
size of a peanut and invisible in water; their four tentacles are 100 times their body
length and as thin as cobwebs; their mild sting is rarely noticed, but within half an
hour, the victim’s whole body is in agony and experiencing a bizarre constellation
of seemingly unrelated symptoms. Many victims require hospitalisation, some
require life support and some die. And Irukandji occasionally infest the most pop-
ular tropical beaches en masse. But consistent with the very best of Hitchcock,
nobody has known when or where (or who) the danger will strike. These features
make them downright scary and predictably attractive to the media.
feeling of impending doom (Williamson et al., 1996). Many victims also expe-
rience coughing and/or involuntary grunting, shivering and teeth chattering, a
creepy skin feeling, and, in some cases, priapism (prolonged erection) in males.
In some cases hypertension is severe and life-threatening: the highest reading
published as part of a case history is 280/180 (Fenner and Carney, 1999),
and readings >300 have also been reported (Gershwin et al., 2009). These cases
of hypertension may lead to pulmonary oedema (fluid on the lungs) and,
rarely, to cerebral haemorrhage (stroke). A small proportion of cases develop
some form of acute cardiac failure (Fenner and Carney, 1999; Huynh et al.,
2003; Macrokanis et al., 2004; Nickson et al., 2009) and some, as yet undefined
number, may have ongoing or recurrent symptoms.
Two people died in Australia in 2002 from complications arising from
Irukandji syndrome (Fenner and Hadok, 2002; Huynh et al., 2003).
Another fatality in 2012 and two more in 2013 are still under investigation
for a potential Irukandji basis. However, the actual death toll is likely to be
much higher. Often with little or no mark on the body and nothing to test
for postmortem, the mechanism of death would be a heart attack, stroke, or
drowning or could even mimic decompression illness, and the underlying
cause may never be recognised (Gershwin et al., 2009). Some larger
Irukandji species, such as Morbakka prevalent in the Gulf of Thailand, can
cause immediate severe pain and large weals prior to the onset of systemic
symptoms and possible death (DAN AP Case reports; Fenner and
Lippmann, 2009; Fenner et al., 2010).
Although Irukandji are largely (but not entirely) unknown in temperate
regions, in the tropics, the scale of the problem extends far beyond the med-
ical effects. A conservative estimate placed the losses to the tourism industry
due to negative publicity at more than $65 million in 2002 (Williams, 2004).
Stings from Irukandji are considered the number one occupational health
and safety issue for Australia’s tropical lobster fishery, pearling industry,
and bêche-de-mer fishery (Gershwin et al., 2009). Industrial downtime,
as either the result of stings or the threat of stings, has impacted the Australian
Navy, the oil and gas industry, and quite likely many other industries where
personnel come in contact with tropical waters.
One of the most unusual features of the Irukandji story, however, is
that despite their danger to humans, the problem is poorly acknowledged
globally and has received little attention from biologists and ecologists.
Indeed, much of what we know about these animals beyond their medical
effects is based on conjecture or scant anecdotal evidence, and even the
Biology and Ecology of Irukandji Jellyfish 5
World Health Organization failed to recognise the hazard in their 2003

and 2009 Guidelines for Safe Recreational Water Environments (WHO,
2003, 2009). Even in regions with dozens of hospitalisations per year
and decades of awareness programmes, the high number of stings suggests
that the safety message is often ignored (Gershwin et al., 2009; Sando
et al., 2010).
Progress in research and management is compromised by our fragmented
understanding of these species. For example, most of the literature has
focused on envenomation and was published primarily in medical journals.
Taxonomic information has largely appeared in taxonomic journals. Biolog-
ical and ecological information is scattered through the pages of medical and
taxonomic works or has appeared in grey literature. The lack of available
information has likely exacerbated the reluctance of authorities in certain
countries to acknowledge and provide information about the incidence
and management of stings in their waters.
The purpose of this chapter is to combine and summarise the disparate
and often scant information about the biology and ecology of Irukandji jel-
lyfish. We have tried to summarise global knowledge, but there is bias
toward Australia because this is where most of the species are known and
where they have been studied the longest. The emphasis on Carukia barnesi
in the Great Barrier Reef region underscores the fact that we still know so
little about other species from other regions. In many instances in this chap-
ter, we draw on knowledge of other cubozoans to develop hypotheses about
what features Irukandji are likely to have.
This chapter is likely to be useful for researchers across a wide variety of
disciplines including biology, ecology, taxonomy, toxinology, and evolu-
tionary science and to medical researchers and rural and remote medical
practitioners, those concerned with marine tourism threats, and managers
concerned with provision of safety at beaches, tourism resorts, dive destina-
tions, and marine industrial facilities. Those seeking detailed information on
the medical and societal aspects of Irukandji syndrome are directed else-
where (Fenner and Carney, 2001; Fenner and Hadok, 2002; Gershwin
et al., 2009; Williamson et al., 1996), as these subjects are covered only
briefly here.
We hope that this comparative synthesis will help stimulate future
research into these understudied species and, in so doing, contribute to
an informed understanding of how to manage the threats they pose to
human health.
1.1. History of study

The name Irukandji was taken from an anglicized version of the name of the
original aboriginal custodians of the lands between Cairns and Port Douglas
(the Yirrganydji people), where Irukandji syndrome was first reported
(Flecker, 1952). Prior to the first use of this term in 1952, a number of cli-
nicians had noted a range of severe constitutional effects following a minor
sting without skin wealing (Flecker, 1945, Southcott, 1952). Southcott and
Powys (1944) termed these ‘type A stingings’ (formally published in
Southcott, 1952). In late 1944, unbeknownst to these investigators, an army
doctor in New Guinea had similar cases but had the sting skin lesions and
causative agent (a small transparent jellyfish) pointed out by a local witch
doctor (Barnes, 1964). Before that, a few scattered reports had emerged
around the world noting clusters of stings with severe symptoms in common
(Lord and Wilks, 1918; Old, 1908, 1912; Stenning, 1928).
It was not until 1961 that an unclassified species of jellyfish was proven to be
a causal agent of Irukandji syndrome, when Dr. Jack Barnes of Cairns,
used a single specimen to sting himself, his 9-year-old son and a volunteer surf
life-saver, all of whom became ill (Barnes, 1964). This jellyfish was later named
Carukia barnesi, after its intrepid discoverer, and was long referred to as ‘the
Irukandji jellyfish’ (Southcott, 1967). Only some 40 years later were additional
species discovered and linked with variations of the syndrome (Gershwin,
2005b,c, 2007, 2008; Gershwin and Alderslade, 2005). The important
advances in Irukandji syndrome research were reviewed by Tibballs and his
colleagues (2012) and are expanded here in Table 1.1 to include Irukandji
biology and ecology.
To summarise the global knowledge of Irukandji, we conducted a meta-
analysis of published literature using ISI Web of Knowledge Search
Table 1.1 Timeline of the history of Irukandji research
Date Event and reference
1935–1936 A Cairns medical conference in 1935 recommended the collection of
information on injuries, including marine stings, from around North
Queensland. This commenced under the care of Dr. Hugo Flecker
who began registering stingings, including cases of what was
retrospectively recognised as Irukandji syndrome, from December
1935 (reported in Flecker, 1952, and commented on by Barnes, 1960)
1944 Retrospectively reported in 1964, two cases of Irukandji syndrome
from Noemfoer Island offshore northwest Papua in late 1944 were
attributed to the sting of a “small (3–5 cm) almost colourless . . .
medusa by a local ‘witch doctor’” (Barnes, 1964)
Table 1.1 Timeline of the history of Irukandji research—cont'd

1945 First formal recognition of the basic symptomatology and
epidemiology of what is now known as the Irukandji syndrome;
grouped as category (e) of “injuries by unknown agents to bathers in
north Queensland” (Flecker, 1945a,b)
1952 Southcott retrospectively reports about 90 cases of ‘severe
constitutional effects without wealing’ from ‘the beaches around
Cairns’ in the summer of 1943–1944 and calls them ‘type A stingings’
(Southcott, 1952)
The term ‘Irukandji syndrome’ is first used as a descriptor reflecting the
major focus of cases around Cairns and recognising the traditional
aboriginal custodians of that locality, the Yirrganydji people (Flecker,
1952). Flecker begins to define the epidemiology of the stingings
drawing on his long-term register of North Queensland cases
1960 Barnes details the largest series of Jellyfish stingings, including
comparative data from Irukandji cases from around Cairns, reflecting
records from Cairns Ambulance Centre and Base Hospital during
1956–1960 (Barnes, 1960)
1961 Small carybdeid jellyfish captured off Cairns beach on 10 December
and used in experimental stinging to recapitulate the features of
Irukandji syndrome (retrospectively reported in Barnes, 1964)
1967 Carybdeid jellyfish causing Irukandji syndrome described and classified
as Carukia barnesi (Southcott, 1967)
1970 Box jellyfish antivenom (CSL Limited) released for clinical use and the
first instance of its use for systemic envenoming, by Dr. Jack Barnes,
most likely attributable to Irukandji syndrome, recorded by CSL
(retrospectively reported in Winkel et al., 2003). Barnes reported the
treatment as ‘ineffective’
1986 First formal published report of Chironex fleckeri box jellyfish
antivenom being used for the treatment of two Irukandji syndrome
cases—without consistent benefit (Fenner et al., 1986)
Irukandji syndrome with severe hypertension hypothesised due to
sympathetic overstimulation leading to the suggestion that a- and
b-adrenoceptor antagonists be considered for treatment (Fenner et al.,
1986)
1987 Acute pulmonary oedema, with left ventricular dysfunction,
recognised as a component of Irukandji syndrome (Fenner et al., 1988;
Herceg, 1987)
Continued

1988 Jack Barnes’ recognition of the diversity of Irukandji-like carybdeids
and the associated variable envenomation syndromes, reported by
Barbara Kinsey (1988)
1997 The first report of a sting victim recalling being stung by a small
carybdeid jellyfish prior to developing the syndrome (Hadok, 1997)
First report of papilloedema and coma associated with Irukandji
syndrome (probably due to cerebral oedema) (Fenner and
Heazlewood, 1997)
1998 Irukandji-like syndrome presents to Geelong Hospital, Victoria
(Cheng et al., 1999)
2000 Carukia barnesi extracts reported as causing massive release of
catecholamines in experimental animals (Tibballs et al., 2000)
2001 Life-threatening cardiac failure occurs in a case of Irukandji syndrome
(Little et al., 2001)
2002 Possible Irukandji-like syndrome cases reported from Hawaii, USA
(Yoshimoto and Yanagihara, 2002)
Two fatalities attributed to Irukandji syndrome in Queensland, both
due to intracerebral haemorrhage secondary to hypertension (Fenner
and Hadok, 2002; Huynh et al., 2003; Pereira et al., 2010)
2003 Huynh et al. (2003) identified nematocyst scrapings from one of the
fatalities as not belonging to Carukia barnesi—the first nonanecdotal
evidence that other species may cause Irukandji syndrome. These
nematocysts were linked by Gershwin (2007) with the new Irukandji
species Malo kingi. It was later reargued by Pereira et al. (2010) that the
nematocysts originated from hitherto unobserved mature Carukia
barnesi. This series reported the variable clinical outcome after
Carukia barnesi stingings
Irukandji syndrome recognised in Florida, USA (Grady and Burnett,
2003)
2003 Intravenous magnesium infusion first used for treatment of the
sympathetic features of Irukandji syndrome (Corkeron, 2003)
2004 Intravenous magnesium reported as being used effectively, in a
nonrandomised, unblended case series, to treat the pain and
hypertension of Irukandji syndrome (Corkeron et al., 2004)
Irukandji syndrome documented in Broome along with ecological
conclusions (Macrokanis et al., 2004)

2005 New genera and species of Irukandji jellyfish described: Malo maxima,
Carukia shinju, Alatina mordens, and Gerongia rifkinae (Gershwin,
2005b,c; Gershwin and Alderslade, 2005)
Pharmacological analysis of Carukia barnesi venom extracts confirming
release of catecholamines (Ramasamy et al., 2005; Winkel et al., 2005)
and modulation of neural sodium channels (Winkel et al., 2005)
Probable Irukandji-like syndrome reported from Guadeloupe,
Caribbean (Pommier et al., 2005)
2006 Irukandji syndrome described from Thailand (de Pender et al., 2006)
2007 Description of Irukandji species linked with fatal case in 2002: Malo
kingi (Gershwin, 2007)
2008 New genus and species of Irukandji described: Morbakka fenneri
(Gershwin, 2008)
Catecholamine release demonstrated experimentally as being caused
by the offshore North Queensland Irukandji Alatina mordens (Winter
et al., 2008)
2009 Unpublished Ph.D. thesis reports the establishment of the first
Irukandji cDNA libraries (Ávila-Soria, 2009)
First case series of Irukandji syndrome cases reported from the
Northern Territory, reflecting data collected from 1990 to 2007
(Nickson et al., 2009)
2010 Irukandji syndrome cases reported from Malaysia (Lippmann et al.,
2011)
2011 Experimental studies of Malo maxima venom effects reported,
confirming Irukandji-type effects on sympathetic neurotransmitter
release (Li et al., 2011)
2012 CSIRO developed a preliminary model for forecasting weather
conditions linked to Irukandji infestations (Gershwin et al., 2012)
2013 Anomalous high-latitude clusters of Irukandji stings at Fraser Island,
southern Queensland (7 stings), and around Ningaloo Reef, Western
Australia (23 stings plus 2 potential fatalities); both clusters occurred
with unusual climatic conditions
Adapted and updated from Tibballs et al. (2012).
A
Cumulative number of Irukandji papers (WOS)
120 200,000
Irukandji
Cumulative number of marine papers

Global marine
100
150,000
80
globally (WOS)
60 100,000
40
50,000
20
0 0
1980 1985 1990 1995 2000 2005 2010
Year
B C
USA
Biology
Medical
SOUTH KOREA
ENGLAND
CHINA
CANADA
AUSTRALIA BRAZIL
Toxicology
Molecular Pharmacology
Figure 1.1 ISI Web of Science search conducted on 30 June 2013. (A) The cumulative
number of Irukandji papers (left axis: search term ¼ Irukandji þ Carukia þ Carybdeida þ
Morbakka þ Gerongia þ Alatina) and global marine research (right axis: search term ¼
‘marine’). (B) Research areas addressed in the Irukandji papers, based on ISI WOS
categories (classification Medical ¼ ANESTHESIOLOGY þ CARDIOVASCULAR SYSTEM
CARDIOLOGY þ EMERGENCY MEDICINE þ GENERAL INTERNAL MEDICINE þ LIFE SCIENCES
BIOMEDICINE OTHER TOPICS þ NEUROSCIENCES NEUROLOGY þ PHYSIOLOGY þ PUBLIC
ENVIRONMENTAL OCCUPATIONAL HEALTH þ RESEARCH EXPERIMENTAL MEDICINE þ
SPORT SCIENCES; Biology ¼ ENVIRONMENTAL SCIENCES ECOLOGY þ EVOLUTIONARY
BIOLOGY þ MARINE FRESHWATER BIOLOGY þ ZOOLOGY; Toxicology ¼ TOXICOLOGY;
Pharmacology ¼ PHARMACOLOGY PHARMACY; Molecular ¼ BIOCHEMISTRY MOLECULAR
BIOLOGY þ GENETICS HEREDITY). (C) The global distribution of knowledge on Irukandji,
based on ISI Web of Knowledge search.
(Figure 1.1). Since 1980, there have been 119 scientific articles on Irukandji.
Based on the cumulative number of papers, there was relatively very little
Irukandji research throughout the 1980s and 1990s compared with global
marine research (using the search term ‘marine’ as an index). Irukandji
research accelerated during the 2000s and is now keeping pace with the
ongoing increase in global marine research. We classified the scientific arti-
cles on Irukandji into five research areas provided in the Web of Science.
Medical is by far the largest research area, followed by toxicology and biol-
ogy (including taxonomy) (Figure 1.1B). Irukandji research is rare in coun-
tries other than Australia and the United States, which recorded 76% and
16% of all papers respectively (Figure 1.1C).
Based on an extensive online search of newspapers in Australia, we found
1670 articles about Irukandji since 2001 (Figure 1.2). There has been an
increase in newspaper reports about Irukandji over the past 10 years, with
considerable interannual variation. The spike in newspaper articles in
2002 followed the death of the two tourists on the Great Barrier Reef. There
were relatively few articles about Irukandji in 2011, and this dip cor-
responded to few stings in that year.
2. BIOLOGY OF IRUKANDJI
2.1. Taxonomy
It is suspected that up to 25 species may be able to cause Irukandji syndrome
(Table 1.2). The ‘box jellyfish’ species that cause Irukandji syndrome are all
in the order Carybdeida and closely resemble the more familiar species in the
genus Carybdea, that is, they have unforked pedalia with only a single ten-
tacle attached to each corner of the bell (Figure 1.3). However, not all mem-
bers of the order cause Irukandji syndrome, and there are even species that
produce the syndrome in other classes of jellyfish. Additional species are
likely to exist and may explain regional variations in the syndrome.
When originally identified, the first Irukandji jellyfish, namely, Carukia
barnesi, was distinguished from the more familiar genus Carybdea based pri-
marily on its unusual tentacles. All cubozoans have their tentacular nemato-
cysts concentrated in numerous transverse bands. In most species, the bands
are simple, smoothly rounded, and alike (Figure 1.4C). Some species of
cubozoans may have repeating patterns of broader bands alternating with
narrower ones, but the bands are still simple and smoothly rounded. In some
Irukandji, however, the bands may be decorated. In Carukia barnesi, alter-
nating bands are ‘tailed’ on one side (Figure 1.4A and B). The later-named
120
Number of newspaper articles
100
80
60
40
20
0
01
02
03
04
05
06
07
08
09
10
11
12
20
20
20
20
20
20
20
20
20
20
20
20
Year
Figure 1.2 Irukandji in the media. The annual number of articles in Australian newspa-
pers since 2001.
Malo kingi has a ‘halo-tentacled’ form, in which each shelf-like band has a
ring of nematocysts arranged end on, fanning out like a missile array
(Figure 1.4D).
The two main families containing species that produce Irukandji
syndrome are easily distinguished (Figure 1.5). The family Carukiidae is
characterised by the lack of gastric phacellae, that is, the clumps of cirri
typically found in cubozoan stomachs. These species also have frown-
shaped rhopalial niche openings where both the upper and lower covering
scales are undivided, similar to species in the more familiar genus Tamoya,
which does not cause illness. In contrast, the family Alatinidae is
characterised by having T-shaped rhopalial niche openings, where the
lower covering scale is divided at the midline and the gastric cirri are
arranged in large crescentic bundles in each corner of the stomach. All
Irukandji species in the Carukiidae also possess ‘rhopaliar horns’, peculiar
blind canals of unknown function pushing upward from the rhopalial
niches. Species in the Alatinidae do not possess these structures. Within
these families, the genera can be distinguished using readily observable
structural characteristics (Table 1.3); these were treated comprehensively
by Gershwin (2005a).
Table 1.2 Summary of ecology and syndrome characteristics of species known or believed to cause Irukandji syndrome
Mature size Typical Associated Evidence of Main
Species (bell height) Habitat Seasonality Swarming depth with salps Syndrome Irukandji Locality refs.
Alatina 80 mm Outer reef 8th–10th Yes Surface Unknown Life- Eyewitness Outer Great 1
mordens nights after threatening Barrier Reef,
full moon QLD
Alatina 85 mm Beach 8th–12th Yes Surface Unknown Moderate Eyewitness Hawaii 2, 3
moseri days after
full moon
Alatina sp. 1 Unknown Reef Unknown Unknown Unknown Unknown Moderate Expert West Indies, 4–8
statement Puerto Rico,
Florida Keys,
Guadeloupe,
Grand
Cayman
Alatina sp. 2 500 mm Reef Unknown No Near Unknown Moderate Eyewitness Ningaloo 1
bottom Reef, WA
Carukia 9–14 mm Beach Height of Yes Surface Yes Moderate Experimental Tropical, 10, 11
barnesi summer sting QLD
Carukia 17 mm Unknown Unknown Unknown Surface Yes Unknown Phylogenetic Broome 12
shinju (caught inference region, WA
April)
Carybdea 15 mm Beach Height of Yes Surface No Moderate Circumstantial Perth, WA; 13, 14
xaymacana summer Cooktown
and Port
Douglas,
QLD
Continued
Table 1.2 Summary of ecology and syndrome characteristics of species known or believed to cause Irukandji syndrome—cont'd
Gerongia 60 mm Coastal Year Sometimes Surface Unknown Mild Experimental NT and Gulf 15
rifkinae round, sting of
particularly Carpentaria,
late QLD
summer
Malo kingi 30 mm Shelf/ Late Sometimes Not Yes Mild to Nematocyst Primarily 16
coastal summer/ surface severe recovery offshore
autumn (lethal) Great Barrier
Reef, QLD
Malo maxima 50 mm Shelf Late Yes 8–9 m Yes Severe Eyewitness Primarily 12
summer/ offshore
autumn Broome, WA
Malo 40 mm Unknown Unknown Unknown Unknown Unknown Possible Phylogenetic Philippines 17, 18
philippina fatality inference
Malo sp. 20 mm Reefs Unknown Unknown Unknown Unknown Unknown Phylogenetic Montebello 19
inference Islands, WA
Morbakka 150 mm Beach Year No Not No Mild to Eyewitness Moreton Bay 20
fenneri round, surface life- to Cape
particularly threatening York, QLD
autumn
Morbakka 150 mm Inland sea Autumn, Unknown Unknown Unknown Unknown Phylogenetic Japan 17, 21
virulenta winter inference
Morbakka sp. 65 mm Beach Unknown No Unknown Unknown Mild to Phylogenetic New South 20
severe inference Wales,
Australia
Morbakka sp. >100 mm Beaches November No Variable Unknown Moderate Phylogenetic Thailand 22, 23
and reefs to February to severe inference and
photographs
Acromitoides 115 mm Beach All seasons Very Shallows Unknown Mild to Experimental Manila, 24
purpurus (as common in and moderate sting Philippines
Catostylus) Manila estuaries
Nemopilema Bell to 2 m Coastal June to Often Shallow Unknown Severe Eyewitness China, Japan, 25
nomurai diameter and November occur in Korea
and 200 kg oceanic vast blooms
Lobonema 50–100 cm In the Summer Blooms Unknown Unknown Moderate Speculative Philippines 26, 27
smithii diameter harbour to severe
Physalia sp. Float to Beach No Huge Floats at No Mild to Eyewitness QLD, NSW 28
15 cm apparent armadas surface moderate
season
Gonionemus 5–15 mm Rocky Mid-June Unknown Among No Moderate Experimental Japan 29
oshoro diameter seashore to end of Sargassum to severe
August seaweed
Gonionemus Diameter Sandy July to Venomous Shallow No Mild to Eyewitness Russia and 30, 31
vertens typically Zostera August in dense moderate New
2 cm beds swarms England
Unidentified 10 cm bell, Beach Unknown Unknown Shallow Unknown Severe Eyewitness, North coast 32
tentacles (spring?) light blue of Efate,
20 cm long carybdeid Vanuatu
Continued
Table 1.2 Summary of ecology and syndrome characteristics of species known or believed to cause Irukandji syndrome—cont'd
At least nine other species are probable but remain almost entirely unknown except for their stings; their disparate locations suggest
potential taxonomic distinction when found:
a summertime beach sting in Victoria, Australia 33
a cluster of beach stings in North Wales, U.K. 34
stings in Fiji 35
beach stings in Papua New Guinea 36, 37
a reef sting in the Gulf Sea, Qatar 38
numerous stings in Phuket and the Gulf of Thailand that co-occur with salps and onshore breezes 39, 40
beach stings in Malaysia between May and July 41
a reef sting along the mid-east coast of Bali 42
a beach sting in Goa, India 43
Main references are noted numerically in far right column and are summarised in the succeeding text. Australian localities: QLD, Queensland; WA, Western Australia; NT, Northern
Territory.
References: 1Gershwin (2005c), 2Thomas et al. (2001), 3Yoshimoto and Yanagihara (2002), 4 Kramp (1970), 5Cutress in Williamson et al. (1996), 6 Grady and Burnett (2003), 7
Pommier et al. (2005), 8 Anonymous (2011b), 10 Barnes (1964), 11 Kinsey (1988), 12 Gershwin (2005b), 13 Little et al. (2006), 14 Gershwin (2006b), 15 Gershwin and Alderslade
(2005), 16 Gershwin (2007), 17 Bentlage and Lewis (2012), 18 Old (1908, 1912), 19 Gershwin (2005a), 20 Gershwin (2008), 21 Kishinouye (1910), 22 Fenner et al. (2010), 23 Divers
Alert Network Asia-Pacific case reports/photos, 24 Light (1921), 25 Mingliang Zhang in Williamson et al. (1996: 215), 26 Mayer (1910), 27 Light (1914), 28 Fenner et al. (1993), 29 Otsuru
et al. (1974), 30 Yakovlev and Vaskovsky (1993), 31 Evans (2010), 32DAN Asia-Pacific unpublished records 3 October 2010, 33 Cheng et al. (1999), 34 Lord and Wilks (1918), 35 Flecker
(1957a, 1957b), 36 Tyson (1957); 37 Barnes (1964), 38 Salam et al. (2003), 39 Fenner and Lippmann (2009), 40 Fenner et al. (2010), 41 Lippmann et al. (2011), 42DAN Asia-Pacific
unpublished records 2003, 43Gershwin unpublished notes 2006.
Figure 1.3 Species of Australian Irukandji jellyfish. (A) Alatina sp. from Ningaloo Reef,
Western Australia (image by P. Baker). (B) Malo kingi from North Queensland. (C)
Morbakka fenneri from Central Queensland. (D) Carukia barnesi from North Queensland.
(E) Carukia shinju from Broome, Western Australia. (F) Malo maxima from Broome, West-
ern Australia (image by M. Alexander, Paspaley Pearling Company). (G) Gerongia rifkinae
from Northern Territory. (H) Carukia sp. from the Great Barrier Reef. (I) Alatina mordens
from the Outer Great Barrier Reef. (J) Morbakka sp. from New South Wales. Images not
otherwise noted are copyright L. Gershwin.
2.1.1 Nematocysts
Nematocysts (stinging cells) are essentially a capsule with a harpoon coiled
inside and bathed in venom, with a hair trigger on one end. Rapid discharge
is accomplished by explosive uncoiling of the harpoon as it everts. When
discharged, the nematocyst is clearly divided into three functional portions:
the bulbous capsule, the stiff shaft that acts as the penetrative portion, and the
long flexible tubule that holds most of the venom. Identification is based on
the size and shape of the capsule and the number and position of spines on
the shaft (Figure 1.6).
Irukandji species have nematocysts of various types and sizes that are use-
ful for species identification and diagnosis of stings (Barnes, 1965; Gershwin,
2006a). One type of nematocyst, the type 4 microbasic mastigophore,
Figure 1.4 Types of tentacles of Irukandji species. (A) Tailed bands of Carukia spp. (B)
Close-up of Carukia tailed band. (C) Undecorated bands of Carybdea, Malo, Gerongia,
Morbakka, and Alatina. (D) Halo-form bands of Malo kingi. All images copyright L.
Gershwin.
Figure 1.5 Anatomy of carybdeid Irukandji jellyfish. Structures useful for taxonomic dis-
tinction are explained in the text.
Table 1.3 Comparison of characteristics useful for distinguishing the genera of cubozoans that produce Irukandji syndrome
Alatina (12 spp.) Carukia (3 spp.) Gerongia (1 sp.) Malo (4 spp.) Morbakka (4 spp.)
Maximum 50 cm 1–2 cm 6 cm 2–5 cm 9–15 cm
bell height
Bell shape Very tall and Small and Cuboid and robust, with Taller than wide, with flat Taller than wide, with flat
slender, with pyramidal, with rounded apex apex apex
narrowed flat rounded apex
apex
Exumbrellar Whitish freckles Red warts Pale freckles Purple freckles Bright pink warts
warts
Rhopaliar T-shaped Frown-shaped Frown-shaped Frown-shaped Frown-shaped
niche ostium
Rhopaliar Lacking Narrow, long, Broad, short, curved; Broad, short, curved; Broad, long, straight,
horns straight; thread- devil-horn-shaped devil-horn-shaped pointy; rabbit-ear-shaped
shaped
Number of 6 (2 median, plus 6 (2 median, plus Unknown, possibly 6 2 median lensed eyes 2 median lensed eyes only,
eyes per 4 lateral); lower 4 lateral) only, lacking laterals lacking laterals
rhopalium lensed eye
enormous
Pedalial Broadly Narrow Broadly rounded, Narrow Scalpel
shape rounded overhanging
Pedalial Simple Simple Thorn Knee-shaped Thorn
canal bend
Tentacles Round in cross Round in cross Round in cross section, Round in cross section, Flat in cross section,
section, very section, with heavy, with flared base fine heavy, with flared base
fine tailed bands
Continued
Table 1.3 Comparison of characteristics useful for distinguishing the genera of cubozoans that produce Irukandji syndrome—cont'd
Alatina (12 spp.) Carukia (3 spp.) Gerongia (1 sp.) Malo (4 spp.) Morbakka (4 spp.)
Gastric Large and Absent Absent Absent Absent
phacellae crescentic
Mesenteries Extremely Flap-like half Robust, flap-like halfway Flap-like one-third way Robust, flap-like halfway
reduced or way; cord-like to to rhopalium, without to rhopalium; cord-like to rhopalium, with fine
lacking rhopalium cord-like extension to rhopalium cord-like extension to
rhopalium
Velarial 3, mostly simple 2, simple or 7, with laminar 1 root, with 3–4 Very complexly
canals (per somewhat branching, lacking lateral unbranched fingers, branched; too many to
octant) branched, lacking diverticula lacking lateral diverticula easily count, with lateral
lateral diverticula diverticula
Perradial Lacking lappets Lacking or single 2 rows of 3–6 (typically 5) 2 rows of 1–4 (typically 2) 2 rows of large warts plus
lappet warts on one side scattered warts
Cnidome Tentacles: Tentacles: egg- or Tentacles: type 4 club- Tentacles: type 4 club- Tentacles: 3 types, type 4
euryteles or lemon-shaped shaped subovate shaped subovate club-shaped microbasic
multiple types tumiteles about microbasic microbasic p-mastigophores
Bell: spherical 25 mm long p-mastigophores about p-mastigophores about 60–70 mm long and large
isorhizas; some Bell: spherical 40–60 mm long 30–50 mm long; oval isorhizas of both tight
species also have isorhizas about Bell: spherical isorhizas significant species and loose tubules, both
other types 20 mm in about 20–25 mm in differences in shaft 50 mm long
Nematocyst diameter diameter spination Bell: 2 types, spherical
sizes are quite Bell: spherical isorhizas isorhizas 30 mm in
variable about 20–30 mm in diameter and an unusual
between species diameter unclassified type with a
thin, papillated, oval
cuticle 45 mm long
Parenthetical numbers after genera indicate number of combined described and undescribed species known at this time for each group; note that not all species of Alatina
are believed to cause Irukandji syndrome, whereas those of the other genera apparently do.
Modified from Gershwin and Alderslade (2005).
appears to be unique to the Carukiidae, though not all species have it

(Gershwin, 2006a).
Nematocysts are obtained either by skin-scraping or by sticky-tape sam-
ple, the latter being more effective, less damaging to the nematocysts and
without scarring to the patient (Currie and Wood, 1995). To obtain a
sticky-tape sample, gently blot or blow-dry the area, arrange sticky tape over
the sting, smooth it once or twice to increase contact, and peel off in one
smooth action; sticky-tape samples affixed to a glass slide or folded back
on themselves can often be readily identified. In some species with multiple
types, the proportions of one nematocyst over another may also be useful
and may change through ontogeny; however, the cnidome of Carukia barnesi
does not change as the animal grows (Underwood and Seymour, 2007).
2.1.2 Statoliths
Another remarkable feature of cubozoans is the statolith, or balance stone.
Each rhopalium contains one large, solid statolith below the cluster of eyes.
The statolith grows by accretion of daily growth rings (Ueno et al., 1995),
similar to the otoliths of fish or like the annual growth rings of trees; these
Figure 1.6 Irukandji nematocysts. (A) Carukia shinju, discharged. (B) Malo maxima,
undischarged. (C) Carukia shinju, undischarged. (D) Malo kingi, discharged. (E) Carukia
shinju, bell nematocysts. All images copyright L. Gershwin.
daily growth rings can be counted for ageing the animal (Gordon et al.,
2004; Kawamura et al., 2003; Ueno et al., 1997), and chemical signatures
in the statolith rings may some day be analysed to identify where and when
the medusa has spent time. Statolith shape is genus-specific, and its use as a
taxonomic indicator was reviewed by Gershwin (2005a). Because statoliths
are the only hard part in an otherwise soft body, they may be useful for iden-
tification of fragmentary specimens, ethanol-preserved or frozen specimens,
or even possibly fossil material.
2.2. Evolution
2.2.1 Phylogeny
Both morphological and partial 18S genetic evidence suggest that the
Irukandji species that lack phacellae and have frown-shaped rhopaliar niche
ostia form a monophyletic group (Figure 1.7): this includes the genera Car-
ukia, Malo, Gerongia, and Morbakka (Gershwin, 2005a). However, the other
Irukandji genus Alatina, which has large crescentic phacellae and T-shaped
rhopaliar niche ostia without horns, appears to be only distantly related.
These patterns were corroborated by later work using both nuclear and
mitochondrial genes (Bentlage et al., 2010).
Intriguingly, although species in the genus Alatina were long considered
to fall within the genus Carybdea until separated into their own family by
Gershwin (2005c), recent genetic analyses suggest that the Alatinidae is in
fact ancestral to other single-tentacled cubozoans and only a distant cousin
of Carybdea (Bentlage et al., 2010).
Identifying which species cause Irukandji syndrome is a compelling quest,
and phylogeny provides interesting argument in at least two cases. First, one
species in the genus Carybdea, the Australian form of Carybdea xaymacana,
has been assumed to cause illness (Kingsford et al., 2012; Little et al., 2006),
but this view has been challenged on phylogenetic grounds and remains spec-
ulative (Gershwin, 2006b). No other species in the genus are linked with the
illness, and vast numbers of non-systemic stings in regions where these species
are common would appear to falsify the hypothesis. Second, at least three spe-
cies in the genus Alatina are credibly linked with the syndrome through eye-
witness sting events: the Hawaiian Alatina moseri (Thomas et al., 2001), the east
Australian Alatina mordens (Gershwin, 2005c), the west Australian A. sp. 1
(Gershwin, 2005c), and the Caribbean A. sp. 2 (Grady and Burnett, 2003;
Kramp, 1970). Whether other species in the genus Alatina cause the syndrome
is unknown, but seems likely given the known distributions of the species and
Figure 1.7 Unrooted phylogeny of Cubozoa (from Gershwin, 2005a). Asterisks denote
species known to cause Irukandji syndrome. From top centre: Chirodectes maculatus
(image by R. Hore), Chironex fleckeri, Chiropsella bart, Chiropsella bronzie, Chiropsalmus
quadrumanus (image by A. Migotto), Carybdea branchi, Carybdea rastonii (image by I.
Bennett/Australian Museum), Carybdea xaymacana, Tripedalia cystophora, Copula
sivickisi, Carukia barnesi, Gerongia rifkinae, Morbakka fenneri (image by G. Cranich/
Queensland Museum), Malo maxima (image by M. Alexander/Paspaley Pearling Com-
pany), Malo kingi, Alatina rainensis, Alatina sp. (image by P. Baker/Western Australian
Museum), and Alatina mordens. Uncredited images by L. Gershwin.
stings. These interesting cases underscore the utility of phylogenetic bases for
prediction of unknown features and for testing of hypotheses.
2.2.2 Fossil evidence

The evolutionary age of Irukandji is unclear. The oldest undisputed fossil
cubozoan is the chirodropid Anthracomedusa turnbulli from the Middle Penn-
sylvanian (ca. 300 mya), near Essex, Illinois (Johnson and Richardson, 1966,
1968). The Essex fauna of the Mazon Creek formation is found in the
Francis Creek Shale, a member of the Liverpool cyclothem of the Car-
bondale group. These spectacularly preserved specimens contain all the
structures one would hope to find in a fossil chirodropid: cuboidal body
form, many tentacles arising from a pedalium at each of the four lower cor-
ners of the bell, and a simple margin.
The notable feature of Anthracomedusa is that it is a fully formed chi-
rodropid, that is to say, if it were found alive today, it would be unlikely
to raise eyebrows as there is nothing particularly ‘primitive’ about it.
Therefore, it seems plausible that the sister group to the Chirodropida,
namely, the Carybdeida, branched off well before Anthracomedusa was
fossilised.
The oldest apparent carybdeids are Bipedalia cerinensis and Paracarybdea lit-
hographica from the Cerin Lagerstätte (Late Kimmeridgian of the Upper
Jurassic, ca. 150 mya) near Ain, Eastern France (Gaillard et al., 2006). Noth-
ing in their morphology suggests an Irukandji affinity of any sort, and
numerous aspects of their morphology draw even their cubozoan affinity
into question. To date, there is no fossil evidence identifiable as Irukandji
jellyfish.
2.3. Reproduction and life cycle

Cubozoans with life cycles that have been resolved have a complex life his-
tory consisting of a primary benthic sedentary polyp, a secondary creeping
polyp, complete or near-complete metamorphosis into a juvenile medusa,
and dioecious adult medusae (Arneson, 1976; Arneson and Cutress, 1976;
Cutress and Studebaker, 1973; Hartwick, 1991a,b; Stangl et al., 2002;
Straehler-Pohl and Jarms, 2005, 2011; Studebaker, 1972; Werner et al.,
1971; Yamaguchi, 1982; Yamaguchi and Hartwick, 1980).
Life cycle and growth data for Irukandji jellyfish are lacking for most spe-
cies, and, even for Carukia barnesi, there is only sketchy knowledge. Early
development of the Caribbean Alatina sp., which is believed to produce
Irukandji syndrome, is similar to that of other cubozoans (Arneson, 1976;
Arneson and Cutress, 1976). No life cycle or growth data have been pub-
lished for carukiid species. A detailed account of observations made while
rearing Carukia barnesi is given in Appendix A. A summary of cubozoan early
life history is provided in Figure 1.8 and Table 1.4; it seems likely that
Irukandji species fall somewhere along this spectrum.
2.3.1 Where do they breed?

Irukandji typically coincide with periods of sustained onshore breeze, so it is
often assumed that they are blown in from offshore (Barnes, 1964; Kinsey,
1988). And because their stings occur on reefs and islands across the shelf, it
seems logical that they must be living and breeding well offshore. However,
Figure 1.8 Hypothesised Carukiidae life cycle. The planula larva and polyp metamor-
phosis are unknown but are likely to be similar to those of other cubozoans. The polyp
pictured here is believed to be that of Carukia barnesi but remains unconfirmed. Images
by L. Gershwin and Heather Walling.
collection data appear to falsify this hypothesis, at least in part. Sampling in

the Cairns region during coastal infestations has yielded a range of sizes and
maturity stages from 2 to 14 mm (Appendix A), suggesting that there are
more local polyp nursery areas.
Barnes (1964) speculated that Irukandji might be breeding around a
small nearshore island or possibly that the islands facilitated retention of
drifting individuals, based on the high incidence of stings on the facing coast.
While there has been at least one claim of discovering such a breeding
ground (Anonymous, 2005), subsequent sampling has been unable to con-
firm its existence and the ‘breeding at the island’ hypothesis remains
speculative.
Kingsford and his colleagues (2012) noted that the greatest numbers of
Irukandji were found near granite islands, again suggesting that this may
be where they bred or that retention is facilitated by oceanographic and wind
Table 1.4 Comparison of the polyp and young medusa characters of the taxa for which the life cycle is known
Carybdea Carybdea
xaymacana (as mora (as Carybdea morandinii
Carybdea Carybdea (possibly ¼ Carybdea Tripedalia Copula Chironex Carukia
marsupialis) rastonii) sivickisi) cystophora sivickisi Alatina sp. fleckeri barnesi
1–4 5 6 7, 8 9 10, 11 12, 13 14
Polyp
Polyp height 1.5 mm 2 mm 1.8 mm 1.4 mm ? 2 mm 1.2 mm 1 mm
No. of 24 ? 16 7–9 ? 16 40–45 To 18
tentacles
Nematocysts Single large Multiple? Single large stenotele Numerous Single 2–3 small Single Single large
at tip of pseudostenotele bean-shaped large euryteles large stenotele
tentacles euryteles stenotele replaced by stenotele
around single single
large stenotele stenotele
Tentacles Solid Solid Solid Solid Solid Solid Solid Solid
Juv. medusa
Umbilical absorbed ? Within 2 days ? ? 10–13 h ? Within
cord within a few (Arneson 2–12 h of
hours (Stangl) says 10–30) capture
Tentacles ? ? Hollow, brown/ ? ? Hollow Hollow Hollow
white
No. of 2 at release ? 4 4 at release, ? 4 at release 4 at release 4 with
tentacles þ8 next day polyp
remnant
Nematocysts Adradial rows ? Irregular warts ? ? Spherical Vertical Numerous
of 4 large warts holotrichs, rows on haphazard
microbasic exumbrella warts
euryteles
Colour Brown ? Clear, with ? ? Ochre Ochre Red
zooxanthellae
Main references are noted numerically after species and are summarised in the succeeding text.
References: 1 Studebaker (1972), 2 Cutress and Studebaker (1973), 3 Stangl et al. (2002), 4 Straehler-Pohl and Jarms (2005), 5 Okada (1927), 6 Straehler-Pohl and Jarms
(2011), 7 Werner et al. (1971), 8 Werner (1983), 9 Hartwick (1991a), 10 Arneson (1976), 11 Arneson and Cutress (1976), 12 Yamaguchi and Hartwick (1980), 13 Hartwick
(1991b), Appendix A.
effects. In fact, most of the apparent island hot-spots in the Great Barrier
Reef region occur off the southwest portion of islands or rocky outcrops,
which are in the lee of the easterly winds (Figure 1.16). Similarly, Alatina
moseri in Hawaii aggregates on the leeward side of the island. These obser-
vations would appear to favour the retention hypothesis, but nonetheless do
not rule out the possibility that these leeward habitats are more favourable for
polyps and therefore also act as breeding grounds. Whether these patterns are
true for Irukandji at other localities has not been tested.
2.3.2 Metamorphosis induction

Triggers for natural onset of metamorphosis from polyp to medusa are
poorly understood and are likely to differ among species. In captivity, meta-
morphosis is reliable for some cubozoans and unpredictable for others. For
example, in the non-Irukandji Caribbean Carybdea xaymacana (often errone-
ously called Carybdea marsupialis), metamorphosis is reliably induced by
shifting the temperature from 20 to 28 C (Stangl et al., 2002), but could
not be induced in Carybdea morandinii (Straehler-Pohl and Jarms, 2011).
Statolith ring analyses have shown that natural metamorphosis corre-
sponds to semilunar cycles (Ueno et al., 1997). In particular, statolith forma-
tion commences in the last stage of medusa formation near the time of
liberation. In wild-caught medusae, initiation of statolith formation was
back-calculated to occur within 2 days before or after a spring tide in
86% of the statoliths studied. Moreover, one or more of the daily growth
rings are darker, better developed, and more conspicuous than others and
often occur at 2-week intervals; 70% of these darker rings correspond with
a period 3 days before or after neap tide. These darker rings were inferred to
potentially correspond to spawning cycles.
While metamorphosis has not yet been observed in carukiid Irukandji,
in captive Caribbean Alatina sp., metamorphosis commenced spontaneously
within 2–3 days after the polyp reached the definitive 16-tentacle stage
(Arneson and Cutress, 1976).
2.3.3 Ontogenetic changes in toxicity

The larger, more virulent multi-tentacled box jellyfish Chironex fleckeri
changes its cnidome ratio as it grows to become more toxic (Carrette
et al., 2002; Oba et al., 2004), but it is unclear whether the same is true
for Irukandji. Media claims of a similar process with Carukia barnesi
(Bateman, 2010b) are unsubstantiated (Underwood and Seymour, 2007).
In one recent study, gel electrophoresis of specimens pooled into imma-

ture and mature size classes found distinct differences in protein banding of
tentacular venom proteins (Underwood and Seymour, 2007). The actual
potency of the venom at different stages was not assessed, but ontogenetic
shifting seems likely, given that the venom profiles correlate strongly with
a change in prey type as the animal grows. The study further found that bell
venom had a different protein profile than tentacular venom in mature ani-
mals; ontogeny of bell venom was not studied.
The Hawaiian Irukandji species Alatina moseri presents an interesting
question. Vast numbers occur periodically in inshore waters (Thomas
et al., 2001), but it appears that only a small percentage actually cause Irukandji
syndrome (Yoshimoto and Yanagihara, 2002). Whether this is due to imma-
turity of specimens or some other factor is unknown. However, a similarly
low percentage of illness relative to stings is anecdotally observed for the
Australian Alatina mordens (R. Hore, unpublished data) and for the
Japanese Irukandji syndrome-producing hydromedusa Gonionemus oshoro
(Otsuru et al., 1974). It also therefore seems plausible that many more carukiid
Irukandji stings not resulting in illness occur than are recorded.
Irukandji polyps possess completely different cnidomes than their
medusa counterparts (Gershwin, 2006a). Whether the polyps also cause
Irukandji syndrome is unknown but seems unlikely.
2.3.4 Lifespan and natural mortality

Cubozoans are inherently difficult to monitor in nature or raise in captivity;
therefore, little reliable information on their lifespan is available. In general,
most jellyfish are assumed to die at the end of the summer. However,
Carybdea rastonii in southern Australia, the California Carybdea, and Alatina
spp. are found throughout the year, suggesting that such a die-off does not
always occur (Gershwin, 2005c; Matsumoto, 1995; Thomas et al., 2001).
Only scant evidence is available regarding the lifespan and senescence of
Carukia barnesi. In the summer of 2003–2004, one of us (LG) raised wild-
caught specimens in a laboratory. Small, young specimens generally took
about 2 weeks to grow to sexual maturity (LG, unpublished data). In the
laboratory, medusae raised from young began to degrade within a few days
of reaching full size and gonad maturity. Senescence was observed as ulcers
on the bell, loss of tentacles, and refusal to take food. Whether this fast
growth and short lifespan is typical of natural cycles is unconfirmed. Larger
Irukandji species have proven more difficult to keep in captivity; no infor-
mation is available about their longevity.
Statolith studies on other species demonstrate the presence of daily

growth rings (Gordon and Seymour, 2012; Gordon et al., 2004;
Kawamura et al., 2003; Ueno et al., 1995, 1997). These rings have been used
to infer the age of the medusae at the time of capture, but have not yet been
used to show or estimate maximum ages.
2.4. Eyes and vision

Cubozoans have long been a source of intrigue, possessing well-developed
eyes but lacking a comparably complex brain. The literature indicates that
they are highly visual and capable of sophisticated behaviours and some form
of decision making (Table 1.5). Therefore, no discourse on their biology and
ecology would be complete without discussion of their vision and eyes. Per-
haps more so than for any other feature, most of this information is only avail-
able for non-Irukandji cubozoans; however, by understanding the range of
visual apparatus and function, hypotheses can be developed to better under-
stand where Irukandji species are likely to fall on this spectrum.
2.4.1 Physical properties of the eyes

Cubozoans are extraordinary among the jellyfish, and indeed among most
invertebrates, in having complex eyes. Whether these complex eyes have
the physical capacity to resolve images has been debated for many years.
Arguments supporting image formation are generally based on observed
behaviour and are expanded in the succeeding text, whereas some argu-
ments examining the physical properties of the eyes conclude that they
are unlikely to form images. That cubozoans use their vision to navigate
their environment and find prey and mates is clear; what is less clear is
whether the eyes form images in ways that we do not yet understand or
whether the animals simply ‘make do’ with blurry or indistinct pictures.
Generally all cubozoans have 24 eyes clustered into four groups on each
rhopalium (Figure 1.9). Along the midline of the rhopalium are two com-
plex eyes, each with a lens, retina, and cornea. Along the sides of the lensed
eyes are two pairs of simple pigment-cup ocelli: one pair of slit eyes between
the two lensed eyes and one pair of pit eyes next to the upper lensed eyes.
Some Irukandji, however, have modified eyes. Species in the genus Malo
have only the median complex eyes and lack the lateral eye spots
(Gershwin, 2005b), and in several species of Alatina, the distal lensed eye
is greatly enlarged (Gershwin, 2005c).
The four types of eyes have different structural features and different func-
tions (Nilsson et al., 2005; O’Connor et al., 2009; Yamasu and Yoshida, 1976).
Table 1.5 Visual capabilities of cubozoans

Visual capability Details References
Phototaxis Strongly attracted to light 1–9
Colour perception Blue, green, and UV-sensing opsins suggest 8, 10–12
colour perception, as do behavioural studies;
colour blindness has also been argued
Obstacle avoidance Clearly and consistently moves away from 4, 5, 10,
dark objects and toward light-coloured 13–19
objects, possibly using colour or contrast
Terrestrial navigation Use visually guided cues above the water to 20, 21
manoeuvre to, around, and through complex
habitats
Sexual dimorphism Dark spots develop on the female velarium 14, 22, 23
and mate recognition when she is ready to mate, thought to offer a
visual signal to males
Courtship and Sophisticated mating behaviours appear to be 5, 14, 22,
copulation visually driven 24
References: 1 Barnes (1966), 2 Studebaker (1972), 3 Arneson and Cutress (1976), 4 Matsumoto (1995),
5
Stewart (1996), 6 Gershwin (2005b), 7 Gershwin (2005c), 8 Gershwin and Dawes (2008), 9 Kingsford
et al. (2012), 10 Martin (2004), 11 Coates et al. (2006), 12 Garm et al. (2007a), 13 Barnes in Kinsey (1986),
14
Hartwick (1991a), 15 Hamner et al. (1995), 16 Stewart (1997), 17 Ueno et al. (2000), 18 Buskey (2003),
19
Garm et al. (2007b), 20 Garm et al. (2011), 21 Garm et al. (2012), 22 Lewis and Long (2005), 23 Lewis
et al. (2008), 24 Werner (1973).
The two median eyes are camera-type eyes, each with a spherical or ellipsoid,
cellular fisheye-like lens, a retina, and cornea. There are about 11,000 sensory
cells in the cubozoan eye (Pearse and Pearse, 1978). The retina is composed of
four layers: a sensory layer, a pigmented layer, a nuclear layer, and a layer of
nerve fibres (Berger, 1900; Pearse and Pearse, 1978). The lens is separated from
the retina by a thin cellular space. The pigment layer covering the outside of
the retina forms an iris around the lens. The pupil of the lower eye can respond
to changing light intensity by changing the aperture in less than a minute;
however, the pupil of the upper eye is immobile.
The upper lensed eye is orientated straight up regardless of the position of
the jellyfish and has been demonstrated to be used in terrestrial navigation by
the non-Irukandji mangrove-inhabiting Tripedalia, as described in the
succeeding text. This eye has a nearly circular field of view with a width
of 95–100 , closely matching Snell’s window (the 97 circular visual field
through which the entire 180 of the terrestrial world is visible to an
Figure 1.9 Cubozoan eyes. (A) Anatomy of typical cubozoan eye (from Chiropsalmus).
(B) Malo: note the lack of lateral pit and slit eyes. (C) Alatina: note the greatly enlarged
lower lensed eye. All images copyright L. Gershwin.
underwater observer, compressed by refraction as light passes through the

air/water interface) (Garm et al., 2011). The lower main lensed eye is ori-
entated obliquely downward, with a much broader visual field than the
upper eye.
The lateral pit and slit eyes lack lenses and have different structural prop-
erties (Berger, 1900; Garm et al., 2008; Laska and Hündgen, 1982; Martin,
2004; Satterlie, 2002). The pit eyes have only a single-cell type, namely,
pigmented photoreceptors, and are thought to function only as light metres
without any spatial resolution. The slit eyes are made of four cell types,
including a canoe-shaped group of vitreous cells forming a lens-like struc-
ture over the retina; this vitreous group has a lobed surface and it is thought
that it may act as a UV filter. The slit eyes appear to have the potential for
spatial resolution and most likely detect vertical movement, but this is not
well understood.
The pit eyes and upper lensed eyes point directly upward, whereas the slit
eyes and main lower lensed eyes point obliquely downward; the heavy crys-
talline statolith keeps them orientated vertically, even when the animal is
upside down (Garm et al., 2011). In this way, some eyes are orientated
for looking up through the water surface at celestial or terrestrial cues,
and other eyes are orientated for looking downward at underwater structures
and shadows.
2.4.2 Visual ecology

The anatomy and histology of cubozoan eyes were studied in detail more
than a century ago by Conant (Berger, 1900; Conant, 1898), who speculated
that the eyes might ‘see’. Since that time, numerous studies have added to
our knowledge but not to our understanding. Many studies have convinc-
ingly described complex visual behaviours; others have argued why they
cannot be so based on the animals’ visual hardware. We are left with the
odd impression that cubozoans see, but without the physical basis to do so.
Experimental studies indicate that the complex eyes can form images and
that cubozoans are able to sense various stimuli in their surroundings such as
shapes, shades, and colours of light and react to them, often predictably.
Moreover, sophisticated behaviours such as hunting, evasion, navigation,
courtship, and copulation appear to involve sight and some manner of cog-
nitive processing. As noted by Martin (2004), cubozoans are commonly
found in nearshore habitats such as sandy beaches, kelp forests, mangrove
thickets, and coral reefs, and they use their vision to navigate these tricky
habitats, a particularly important survival strategy for soft-bodied animals
easily damaged by crashing waves and collisions with barriers. Coates
(2003) provides a good literature review on the visual ecology and relevant
functional morphology of cubozoans.
It has been proposed that different tasks are associated with different eye
types (Garm et al., 2008). Garm and his colleagues (2012) erroneously
asserted that all cubozoans have the same four eye types and that their visual
system varies only marginally. In fact, Irukandji are the exception to the rule,
with several species having unusual modifications to their visual apparatus.
For example, Malo lacks lateral eyes (Gershwin, 2007), which are thought to
aid the lensed eyes in peripheral filtering of information in other species. It is
unclear therefore whether Malo simply has less visual ability or has somehow
overcome the need for lateral eyes. Moreover, in Alatina, the lower lensed
eye is characteristically about twice the size of the corresponding eye of other
species and medusae are typically observed to be active at night (Gershwin,
2005c). It seems plausible that their large eyes are an adaptation to a noctur-
nal lifestyle, for example, sensing bioluminescence and possibly lunar syn-
chronisation of their monthly spawning aggregations.
2.4.3 Visual evolution

The Cubozoa offer insight into the early evolution of vision. While the slit and
pit eyes may provide visual information that the lensed eyes cannot, the lensed
eyes nonetheless receive far more light and provide better spatial perception
than the slit and pit eyes (Garm et al., 2008). And even though apparently out of
focus, blurry images are better than no images (Nilsson et al., 2005). Garm and
his colleagues (2011) proposed that having different eye types specialised
for different visual tasks might require less neural processing than if the infor-
mation for multiple behaviours were to pass through one eye.
Cubozoan behaviours (discussed in the succeeding text) suggest that at
least some species are able to perceive colour, suggesting that the Cubozoa
might represent early development of colour vision. O’Connor and her
colleagues (2010) thought that colour vision can eliminate the brightness
noise of flickering from surface ripple. Whether colour vision has allowed
these animals to move into flickering coastal habitats, or whether living in
coastal habitats selected for improved visual perception, is unclear.
2.5. Behaviour
2.5.1 Phototaxis
The propensity of cubozoans to be attracted to light has been noted many
times. For example, Barnes (1966) reported that in full daylight, surface and
sub-surface light intensities seem to have little effect, but in semidarkness,
these animals “are very markedly phototaxic. The light of a match is detected
at distances up to 5 ft and . . . [they] show a remarkable accuracy in turning
towards the light source, even though the latter be extinguished before the
turning movement is completed” (p. 322).
Although we have only a chequered understanding of the biology and
ecology of most Irukandji species, the one thing that seems consistent is that
they are easily caught by light attraction. For example, Barnes reported that
‘pseudo-Irukandji’ in Queensland (later-named Malo kingi) were ‘irresistibly
attracted’ to a submerged car headlight light held at the water surface
(Kinsey, 1988). Similarly, Gershwin (2005b) collected two new species of
Irukandji (Carukia shinju and Malo maxima) by attracting them to powerful
lights at the back of a ship. Gershwin (2005c) noted that Alatina mordens is
often encountered by scuba divers at night, where the divers swim up into
the light halo at the back of dive boats where the jellyfish are swarming; so
too, one of us (RH) has conducted monthly research on this species since
2002, using above-water lights to attract them (see Appendix B).
This hardwired attraction of cubozoans to light has potentially strong
implications for safe management of night-time activities where lights shine
into the water for prolonged periods, including recreational scuba diving,
port and marina facilities, fishing and night-snorkelling jetties, marine con-
struction work, and tourism resorts.
3. ECOLOGY OF IRUKANDJI
We know surprisingly little about the ecological patterns of Irukandji
species in general. But the scattered information we do have suggests that
while some species have similar ecologies, others are quite different, partic-
ularly at the levels of genus and family. Species differ not only in bloom strat-
egies, but also in seasonality and cross-shelf distribution.
3.1. Diet and feeding

The natural prey preferences of Carukia barnesi were recently quantified for
the first time (Underwood and Seymour, 2007). Stomach contents of
37 individuals of four size classes were examined: <4 mm, 4–6 mm,
6–8 mm, and >8 mm (interpedalial distance1). The authors found a signif-
icant difference in the relative proportion of crustaceans versus larval fish in
stomachs of medusae of different sizes, with a general trend toward an
increasing proportion of larval fish with increasing predator body size.
100% of the smallest size class of medusae had only crustacean prey, whereas
100% of the largest size class had only larval fish. The number of medusae in
each category was not specified nor was the percentage of individuals with-
out prey in the gut.
A similar ontogenetic shift in diet was noted for the larger multitentacled
Chironex fleckeri, but not for the smaller multitentacled Chiropsella bronzie (as
Chiropsalmus sp.) (Carrette et al., 2002). Therefore, such a shift does not
appear to be universal in the Cubozoa, but may well correlate with toxic
species or at least with their toxicity.
For Chironex and Carukia, the shift in prey type is accompanied by mor-
phological change. Chironex changes its cnidome ratio, whereas Carukia
develops peculiar banding on its tentacles (Figure 1.4). Barnes noted that
tentacles of Carukia, which he described as like a ‘cobweb with dewdrops
on it’, are invisible in water except for the tailed bands (Kinsey, 1988).
Two experimental prey-capture events have been observed: in each case,
the larval fish was attached head-on to one of the ‘tails’ of the modified nem-
atocyst bands, leading the authors to conclude that the beaded effect of the
bands and the jerking motion of the extended tentacles attracted larval fish
by mimicking the movements of their prey (Underwood and Seymour,
1
Interpedalial distance is generally not used because it is like measuring the distance between elbows; bell
height or interrhopalial distances are considered more reliable.
2007). These authors further remarked on the ecological advantage of

minimising energy expenditure in a small oceanic species that is able to
attract and envenom highly mobile larval fish.
Although it may be tempting to fascinate on the ‘tailed’ bands as a sophis-
ticated means of lure and capture, it must be borne in mind that juvenile
Carukia do not have the ‘tailed’ bands nor do other Irukandji species
(Figure 1.4). Based on the energetic needs of adult medusae and the onto-
genetic diet patterns of cubozoan species, it seems likely that adult Irukandji
of other genera also prey on fish, albeit apparently without lures.
A particularly interesting question lies in the halo-like bands of some spec-
imens of Malo kingi, that is, whether this is an unrecognised species difference
or another example of ontogenetic shift.
Very young juveniles, in contrast, have not yet developed their tentacles
and appear to rely on the bell for food capture. Newly metamorphosed
Alatina medusae (inaccurately identified as the Atlantic Carybdea alata) were
observed to envenom prey with the bell nematocysts and to then pass the
prey across the bell warts to the manubrium on the underside of the bell
(Underwood and Seymour, 2007). Additional notes on the feeding behav-
iour of laboratory-reared Carukia barnesi are given in Appendix A.
3.2. Geographic distribution

Determining the distribution of Irukandji species and Irukandji syndrome is
muddled by the lack of resolution in syndrome variation and lack of data
from specimen studies. We are currently presented with a riddle consisting
of sting events that we do not know how they correspond with species, and
species that we do not know how they correspond with stings, and some
species known to cause Irukandji syndrome that are not even in the
Cubozoa. Clearly, much more work needs to be done on species identifi-
cation and elucidation of species-syndrome linkages.
3.2.1 Global distribution

While Irukandji jellyfish are often associated with tropical Australia, the
numerous substantiated reports from far reaches of the globe make it clear
that Irukandji syndrome-producing jellyfish occur throughout the oceans
and seas of the world from at least 53 N to 38 S (Figure 1.10) and have done
so for many decades. In most cases outside tropical Australia, species are not
yet identified.
There are large numbers of Irukandji stings on the Great Barrier Reef
(e.g. Cairns and Whitsundays), Australia’s North West Shelf (e.g. Broome
Figure 1.10 Worldwide Irukandji sting distribution. Size of circles qualitatively indicates
relative numbers of stings. Only two fatalities have been confirmed, with four others
unresolved. Irukandji stings usually leave no mark and nothing to test postmortem,
so it is widely believed that additional fatalities have occurred.
and Exmouth), Hawaii (e.g. Waikiki Beach), Thailand (e.g. Phuket),

Malaysia (e.g. Langkawi), and the Caribbean (e.g. Stingray City and Florida
Keys) (Anonymous, 2011b; Fenner and Harrison, 2000; Fenner et al., 2010;
Grady and Burnett, 2003; Kinsey, 1988; Le May, 2013; Lippmann et al.,
2011; Macrokanis et al., 2004; Thomas et al., 2001).
Versions of Irukandji syndrome have been reported from many islands
throughout the Pacific (Table 1.2), including Fiji (Flecker, 1957a,b) and
Papua New Guinea (Barnes, 1964; Tyson, 1957), as well as Vanuatu, Tahiti,
Samoa, and New Caledonia (Williamson et al., 1996). These islands coin-
cide with the distribution pattern of Alatina (Gershwin, 2005c; Kramp,
1961), and it is possible that many of these stings are attributable to species
in this genus.
In Australian waters where Irukandji species are the most well known, it
is evident that species often have localised distributions (Figure 1.11). It
therefore seems probable that many more species of Irukandji jellyfish
remain to be discovered around the world.
In some cases, Irukandji syndrome is believed to result from species other
than cubozoans (Table 1.2). For example, symptoms consistent with
Irukandji syndrome have been reported from the Chinese giant rhizostome
jellyfish Nemopilema nomurai (Mingliang Zhang in Williamson et al., 1996,
Figure 1.11 Irukandji species distribution in Australia: confirmed localities are indicated
by coloured dots. Data were gathered from original descriptions of these species and
museum specimens around Australia.
p. 215). So too, Irukandji syndrome in Japan has been experimentally dem-

onstrated to result from the sting of the hydromedusa Gonionemus oshoro
(Otsuru et al., 1974). Curiously, the closely related and widely distributed
Gonionemus vertens is not known to be toxic throughout most of the world,
but gives a version of Irukandji syndrome when in high densities in Russia
and Cape Cod, Massachusetts (Evans, 2010; Yakovlev and Vaskovsky,
1993). In the Philippines, at least two different common species have been
blamed for systemic syndromes (Chrysaora quinquecirrha and Lobonema smithii)
(Light, 1914; Mayer, 1910); it is probable that these stings are more accu-
rately attributable to less visible Malo or Morbakka or some other species
of Irukandji.
3.2.2 Cross-shelf distribution

For many years, it was widely believed that Australian Irukandji were only a
problem on the coast and not on reefs and islands. These notions have been cat-
egorically disproven. In fact, the general pattern appears to be that as one travels
further offshore the virulence of the Irukandji species found increases, as does
distance from medical care (Gershwin, 2005b; Gershwin, 2007).
The majority of Irukandji specimens caught along beaches, in approxi-
mately waist-deep water, has been Carukia barnesi. Similarly, the majority of
coastal stings match the pattern for classic Irukandji syndrome, with
20–30 min onset, pain subsiding with morphine, and low or no hyperten-
sion or pulmonary oedema. Therefore, from both sting and specimen data, it
would appear that the dominant Irukandji along Queensland coastlines is
Carukia barnesi.
A study of trends among 62 stings over 1 year in the Cairns region found
the following: 47 (76%) patients were stung at coastal locations, 7 (11%)
were stung on the reef, and 5 (8%) were stung at the nearby islands
(Little and Mulcahy, 1998). Of the 34 patients seen in December 1996,
30 (88%) were stung at coastal locations, compared with 17 of 26 (65%)
for the period from January to May. Thirty-nine patients (63%) were stung
while swimming inside stinger net enclosures on the beaches. As with earlier
studies by Barnes (Kinsey, 1988), they found that the most frequent location
to be stung was Palm Cove (17/62; 27%), a beach about 25 km north of
Cairns.
Interestingly, however, stings over the last decade in the Cairns region
have shifted to being more common offshore on the reefs and islands com-
pared to the beaches, steadily trending from 88% beach stings in 2001 to 75%
offshore stings in 2007 (Sando et al., 2010). The reasons for this shift are not
yet clear and beg further investigation. Perhaps the most obvious explana-
tion is that management has improved at the beaches but the offshore
regions have yet to follow. This is an attractive hypothesis given the amount
of effort that lifeguards put into safety management but, if true, would call
for significant action by reef and island operators. Another possibility may
be greater use of offshore regions compared to beaches, as the reefs and
islands have become more accessible and desirable tourism destinations. Still
another possibility is that the jellyfish may have actually shifted their centre
of distribution.
Occasionally, other genera such as Malo and Morbakka are also found in
coastal areas (Gershwin, 2007, 2008). In Central Queensland waters, partic-
ularly in the Mackay/Sarina region, Morbakka is most often taken either
beached or in tidal fishnets. In northern and southern Queensland waters,
Morbakka is most often found swimming in marinas or shallow bays, partic-
ularly in the Port Douglas (far north) and Redcliffe (far south) regions. Why
these regions are particularly favoured by these species is not known, but the
patterns are so predictable as to be worth further investigation.
Stings are common in midshelf waters throughout the Great Barrier Reef
(Fenner and Carney, 2001; Little and Mulcahy, 1998), but specimens are
rarely taken, most probably due to lack of sampling. Midshelf stings are most
frequently of the Carukia barnesi type, that is, slow syndrome onset and low
incidence of hypertension or life-threatening complications.
Some midshelf stings are notably more severe, particularly in the popular
dive region of the SS Yongala wreck off Townsville (about 450 km south of
Cairns) and on the midshelf islands and reefs. These more severe syndromes
often onset rapidly (e.g. 5 min), the pain is severe and unresponsive to opi-
ates, and hypertension may be severe, leading to pulmonary oedema (Fenner
and Carney, 2001; Fenner and Hadok, 2002; Fenner and Lewin, 2003;
Fenner et al., 1988). The culprit species responsible for these severe midshelf
stings are not well studied but do not appear to be attributable to Carukia.
Scant evidence implicates Malo and Morbakka (Gershwin, 2007, 2008;
Huynh et al., 2003; Little et al., 2001, 2003).
Further offshore, for example, outer reef and Coral Sea localities, the
dominant Irukandji appears to be Alatina mordens (Gershwin, 2005c;
Appendix B); however, a case may be made that it is the easiest one to
see. Most specimens of Alatina mordens have been collected from dive sites
such as Moore Reef and Osprey Reef. Species-syndrome linkages have been
established on the basis that Alatina mordens was observed in light halos on
night dives of some sting events. The syndrome of Alatina mordens appears
to be typically fast onset (e.g. 5 min) and severe in both pain and
hypertension.
The cross-shelf distribution of Irukandji species elsewhere is less clear. In
Western Australia, Carukia shinju has been caught only a few times: once
offshore in the pearling grounds and the remaining times coastally around
Broome (Gershwin, 2005b). Malo maxima is encountered in large numbers
by pearl divers who fish many kilometres offshore, but has also been caught
occasionally closer to shore (Gershwin, 2005b). Therefore, segregation by
depth seems less clear in these species than in their Pacific counterparts. Sim-
ilarly, an undescribed species of Malo is known from the islands off Exmouth,
and an undescribed species of Alatina has been caught and photographed
numerous times off the Kimberley coast and at Ningaloo Reef
(Gershwin, 2005b,c). Neither species is sufficiently well known to infer pat-
terns of distribution, but Alatina does seem to occur closer to shore in the
west than in the east.
A species of Morbakka is known from Japan (Bentlage et al., 2010), but no
information exists on its stings other than as indicated by its name, Morbakka
virulenta. Similarly, a species of Malo and an unidentified Morbakka are
known from the Philippines (Bentlage et al., 2010), without information
on their stings or symptoms. Irukandji syndrome is known from both of
these regions, but specific linkages with these species or other yet-to-
be-identified species are unclear.
Southeast Asian and Caribbean species remain to be identified, and as yet
no information is available on their distribution other than the few stings
opportunistically reported. Fenner and his colleagues (2010) reported three
Irukandji stings in Thai waters, and the following year, Lippmann and his
colleagues (2011) reported three more from Malaysia. Both reports are
believed to dramatically underestimate the true scale of the problem. Clus-
ters of three Irukandji stings in the Florida Keys (Grady and Burnett, 2003)
and 25 in Stingray City in Grand Cayman (Anonymous, 2011a) are both
thought to have been caused by Alatina sp., while a single sting in Guade-
loupe (Pommier et al., 2005) remains unattributed to species and virtually no
information is available on other stings nearby.
All these regions are notable for having oligotrophic shelf habitats that are
occasionally flooded by oceanic intrusions, triggering vast salp blooms.
Many are likewise notable for having Irukandji infestations accompanied
by large numbers of salps.
In contrast, the other ‘hot-spot’ for Irukandji, namely, Waikiki Beach in
Hawaii, is a completely different mid-ocean volcanic island habitat and is
home to the more oceanic Alatina moseri (Thomas et al., 2001).
3.3. Vertical distribution

It is generally accepted that Australian Irukandji swim mostly near the surface.
While this has never been formally tested, at least for Carukia barnesi it does
appear to be fairly reliable. When Barnes famously caught the first Irukandji
specimen on 10 December 1961, he did so by concentrating his attention on
the top 50 cm of the water column. This tendency for Carukia barnesi to swim
near the surface has been noted by many workers (Barnes, 1964, 1966;
Cleland and Southcott, 1965; Fenner et al., 1988; Gershwin and Dabinett,
2009; Kinsey, 1988; Southcott, 1959; Williamson et al., 1996).
Numerous independent lines of evidence also support this surface-
swimming tendency. First, Southcott and Powys (1944) observed that the
majority of Irukandji stings occur “on the body or arms while swimming or
standing in the sea” (Figure 1.12A). Second, Kinsey (1988) provided a detailed
account of where stings occurred on the body and the depth at the time of the
sting, concluding that there was reasonable evidence for Barnes’s belief that Car-
ukia was most likely to be found in the top 0.5 m of water (Figure 1.12B). Third,
Fenner and Harrison (2000) found that of 377 Irukandji stings with body-site
information, almost half were stung on the arms, whereas less than one third
were stung on the legs. Fourth, a widely distributed public safety education fig-
ure plots stings reputedly from the Cairns region in 2001–2002; more than 70%
were on the upper half of the body (Figure 1.12C). Given that upper and lower
parts of the body are exposed as people enter and leave the water, and people
stand and float at different depths, the strong bias toward the upper body, arm,
neck, and facial stings strongly suggests that Carukia barnesi is primarily encoun-
tered near the surface.
Our understanding of where other species of Irukandji swim is less clear.
Malo maxima is most often observed by pearl divers while hanging at nine
metres on their decompression stop (Gershwin, 2005b). Whether this depth
is common for Malo, or merely an artefact of the divers’ spare time to observe
their surroundings, is unknown. Similarly, Alatina mordens is typically
encountered in surface swarms at the back of dive boats in the light halo
at night (Gershwin, 2005c).
Arneson and Cutress (1976) noted for the Caribbean Alatina sp. (as
Carybdea alata) that “The medusae are strong swimmers yet avoid choppy
surface conditions. Unless the sea is calm, they remain almost motionless
Figure 1.12 Location of Irukandji stings on the body, demonstrating that most stings
occur near the top of the water column. All data from Cairns region. (A) 1942–1943,
redrawn from Southcott and Powys (unpublished 1944). (B) 1960s–1970s, redrawn from
Kinsey (1988). (C) Believed to be from 2001–2002, from public domain safety education
materials. In (C), numbers denote stings on different body regions; black clothing indi-
cates the parts of the body that would have been protected by wearing of a full-body
lycra ‘stinger suit’ or equivalent.
near the bottom. With the usual abatement of wind at night, the medusae
rise to the surface to feed”. So too, Grady and Burnett (2003) noted that a
series of Irukandji stings in divers off Key West, Florida, occurred while they
were swimming close to a sandy, grassy bottom at 3–5 m at night without
lights, suggesting that this was the normal habitat for this species. A similar
pattern has been noted for many non-Irukandji species as well, so living near
the bottom does appear to be a common cubozoan behaviour (Berger, 1900;
Hartwick, 1991a; Kinsey, 1986; Larson, 1976; Martin, 2004; Matsumoto,
1995; Studebaker, 1972; Yatsu, 1917).
3.3.1 Shallow stings

An interesting corollary to the surface-swimming behaviour of Irukandji is
that they are often found right up to the water’s edge and sometimes even
stranded by the tide on the beach. Many authors have noted that there is a
disproportionately high percentage of Irukandji stings inside stinger-resistant
enclosures.
For example, Fenner (1988) wrote, “On Christmas Day 1985, the casu-
alty room of the Cairns Base Hospital looked like a battleground. Approx-
imately 40 people, many of whom had severe symptoms, needed treatment
following stings by Irukandji. All were stung in the stinger-resistant enclo-
sures!”. Analysis of 30 Cairns region Irukandji stings in December 1996 rev-
ealed that 67% of the stings that month had occurred within the enclosures
(Mulcahy and Little, 1997). In looking at the whole of 1996, Little and
Mulcahy (1998) found that 63% of Cairns region stings occurred inside these
enclosures. Notably, they also found that six (10%) stings that year occurred
at the water’s edge, suggesting that the coast itself may have some concen-
trating effect.
Whether the higher-than-expected rate of stings inside the nets is
because of the clustering effect of swimming in these areas or because of
some eddying effect of the enclosures has not been investigated. It is impor-
tant to note that the nets were designed to protect against the larger and more
dangerous Chironex fleckeri and have proven effective in this respect.
3.3.2 Vertical migration

Vertical migration in Irukandji has not been investigated. However, vertical
migration could be important for Irukandji to maintain their position
inshore and form blooms in tidal environments. For example, the distantly
related scyphozoan Aurelia typically spends most of its time near the bottom
or randomly distributed through the water column and aggregates at the
surface once or twice a day (Mackie et al., 1981; Malej et al., 2007; Yasuda,
1973). It is thought that vertical migration in Aurelia is a means of avoiding
tidal dispersion and that aggregation enhances survival by keeping the medu-
sae in an environment that facilitates the meeting of gametes, improves the
survival of larvae and juveniles, increases the capture rate of motile prey such
as copepods, and reduces the effects of predation by medusivores (Albert,
2007; Purcell et al., 2000).
3.4. Temporal changes

The Australian ‘stinger season’ is generally regarded as being November to
May. Indeed, experience and local lore suggest that stings are far more prev-
alent during the warmer months, but in fact, stings and specimens are known
from all months of the year (Goggin et al., 2004). However, stings occur in
brief epidemics, with generally two primary peaks, one almost invariably in
late December or early January and the other often around March or April
(Figures 1.13 and 1.14).
Many have questioned whether the observed pattern of stings might be
an artefact of more people in the water during these holiday periods. How-
ever, while certainly a logical concern, numerous streams of evidence have
demonstrated that jellyfish peak at these times independent of whether peo-
ple are in the water. In fact, this has been recognised at least since the 1940s,
“The occurrence of these stingings in December and January corresponds
with the experience of local inhabitants—the lack of cases during the
remainder of the year is certainly not entirely due to the smaller numbers
of people bathing” (Southcott and Powys, 1944).
So too, later workers in Cairns have noted the prevalence of coastal stings
in the height of summer. Little and Mulcahy (1998) analysed Cairns sting
data from 1996. They found that of 62 total stings that year, 35 (56%) were
stung between 30 November and 19 December, and of those, 30 (88%)
occurred at coastal locations. In comparison, for the period January to
May, only 17 of 26 (65%) of patients were stung at coastal locations. The
authors speculated that the observed swarm period may be due to the species
breeding or feeding patterns: “There is a higher proportion of people stung
on the Reef between January and May (9/26; 33%) compared with October
to December (3/37; 8%). We believe the ‘swarm’ occurs because the
Irukandji are either breeding or pursuing food, before moving to open water
later in the season” (Little and Mulcahy, 1998, p. 640). It is also possible that
they overlooked species differences and that their sampling design con-
founded their results by using a calendar year.
Figure 1.13 Australian Irukandji stings by time of day (A) and by east (B)and west
(C) coast seasonality. Data from the Australian Irukandji sting database, comprising
1629 Australian Irukandji sting records from January 1893 to June 2013, obtained from
Surf Life Saving, hospital and ambulance records, and media, and curated by a succession
of researchers since the 1950s; requests for access to the database can be made through
the senior author.
The tight clustering of Irukandji infestations is well illustrated by collec-

tion data from a single summer. During the summer of 1999–2000, two of us
(LG and RH) made standardised daily collections for 80 days at Palm Cove, a
popular beach north of Cairns (6 December–24 February) (Fenner, 2000).
During this period, Carukia barnesi were only found in two separate infesta-
tion events, 3 specimens in one of six samples on 14 December and then 270
specimens in a 4-day cluster as follows: 29 December, 1 specimen;
30 December, 22 specimens; 31 December, 206 specimens; and 1 January,
41 specimens.
Routine daily beach monitoring by lifeguards over the last decade also
suggests that Irukandji are not present all the time, but rather, they come
and go according to conditions. In particular, since 2003, Australian beach
safety protocol mandates closure of the beach when Irukandji are found or
Figure 1.14 Queensland Irukandji stings by location and season. (A) Location of stings.
(B) Seasonality of beach stings. (C) Seasonality of island stings. (D) Seasonality of reef
stings. Data from Australian Irukandji sting database.
when stings occur (Dawes et al., 2006). Given that most of the patrolled
swimming beaches are open and visited by tourists most days, even without
the ability to analyse data, we can reasonably conclude that Irukandji are not
present most days.
For other species, even less information is available. In Queensland,
Alatina is typically found at outer reef locations during its monthly swarm
events. Morbakka appears to be diffusely scattered along the coast throughout
the warmer months of the year, but one particularly severe sting event was
attributed to Morbakka on the reef (Gershwin, 2008; Little et al., 2006). Malo
is more complicated. Specimens have been taken coastally throughout the
northern and central regions, but its nematocysts were identified from a fatal
reef sting (Gershwin, 2007; Huynh et al., 2003), and numerous similar
severe stings at midshelf locations suggest that it is more abundant there.
Curiously, its coastal occurrence appears to peak around March-April in the

central region but around late December to early January in the north.
In the NT, stings in different regions correspond to prevailing offshore
winds in those regions, that is, October in Gove (East Arnhem Land) and May
farther west in Darwin. Different versions of the syndrome are reported, but
only one species is so far known (Gershwin and Alderslade, 2005).
Elsewhere in the world, even less is known about Irukandji seasonality.
In the Gulf of Thailand, especially around the Koh Samui area, Morbakka is
most frequently sighted from November to February, as shown by photo-
graphs and reports provided to Divers Alert Network Asia-Pacific. Photog-
raphers have usually been local who dive the area year-round. In Langkawi,
Malaysia, the main reports of Irukandji stings are from May to July. In Grand
Cayman, media reports following a cluster of 26 stings during the morning
of 27 April 2011 indicated that these jellyfish were typically present in late
spring or early summer and believed to be washed in by deep sea currents
(Fuller, 2011).
While the marked seasonal prevalence of Irukandji stings in different
regions is generally accepted by most workers (Figures 1.13 and 1.14), it
has yet to be formally studied or explained. Due to the species diversity
of Irukandji (Figure 1.3 and Table 1.2), it seems likely that much of what
we perceive as seasonal anomalies will eventually be explained by taxonomy.
3.4.1 Bimodal distribution in space and time

Several interesting examples exist where nearby regions have different peaks
on the calendar correlated with higher incidences of stings. In the far north
of Western Australia, the quiet town of Broome is the main location for
Irukandji stings in Western Australia, and may become a Rosetta Stone
for understanding Irukandji ecology. Here, Irukandji stings generally occur
inside the sheltered Roebuck Bay early in the summer (generally October
through December), with later season stings (generally March through June)
occurring on the more exposed Cable Beach facing the Timor Sea
(Macrokanis et al., 2004). The pearl divers operating offshore somewhat
to the south of Broome are also plagued by Irukandji during this late season
period (Gershwin, 2005b).
So too, the Irukandji season in the Northern Territory (NT) has two
peaks. In the eastern-facing region of Gove (East Arnhem Land), the sting sea-
son peaks in October, whereas the peak in the more northerly or westerly
facing Darwin is in May (Nickson et al., 2009). These peaks coincide with
the cusps of the monsoon; the ecological significance of this has not yet been
studied. Different versions of the syndrome are reported, but only one species,
Gerongia rifkinae, is currently known (Gershwin and Alderslade, 2005).
Similarly, in the Great Barrier Reef region of tropical eastern Australia,
where sting demographics are better-studied, peak sting times are dissimilar
north to south and east to west (Gershwin, 2005c; Kinsey, 1988). The primary
peak, generally in late December, occurs in the northern, central, and south-
ern beach regions. The secondary peak appears to be stronger in the central
region than in the north, as well as offshore.
These cases of bimodality do seem to be genuine jellyfish patterns rather
than human swim patterns, because people use the water throughout the year
in these localities. The extent to which these geographical shift patterns may
represent different species is not yet clear, but late season, more southerly stings
in Queensland tend to have a higher rate of serious illness, lending support to the
‘different species’ hypothesis (Fenner and Hadok, 2002). The environmental
stimuli and biological responses driving these spatio-temporal patterns are
not yet clear, but should be a high priority for study.
3.4.2 Lunar periodicity

The Hawaiian oceanic Irukandji, Alatina moseri, forms reproductive swarms
in nearshore waters along Oahu’s leeward coast about 8–12 days after the full
moon every month (Thomas et al., 2001), and subsequently washes ashore
in large numbers (Crow et al., 2010). Monthly counts since August 1994
suggest little seasonal pattern, but stronger annual variation. For example,
the total annual count for 2001 was more than 10,000, while the total for
2005 was just one-quarter of that. Curiously, anecdotal evidence suggests
that these monthly swarms increased in the early 1980s, and by the end
of that decade, recreational activity at Waikiki Beach was regularly affected
by stings, some of which produced Irukandji syndrome (Yoshimoto and
Yanagihara, 2002).
The closely related Australian oceanic Irukandji, Alatina mordens, appears
to swarm at a similar time of the month (R. Hore, unpublished data; Appen-
dix B). However, Alatina moseri presents a health hazard when swarming in
shallow waters during the day, whereas Alatina mordens is most commonly
encountered over the reef at night.
3.4.3 Diurnal patterns

At least some species of cubozoans are found on or near the bottom during
daylight hours and are more active in the water column during the dimmer
parts of the day or at night. For example, the Caribbean Carybdea xaymacana
rests on the bottom during the day and is most active in the mornings and
evenings (Berger, 1900; Larson, 1976; Studebaker, 1972). The Japanese
Carybdea mora was noted to have a similar pattern (Yatsu, 1917), and the
Australian Carybdea rastonii and the Californian Carybdea spend most of
the day foraging near the bottom and rise to the surface in the early morning
or on overcast days (Martin, 2004; Matsumoto, 1995). The Caribbean
Alatina sp. spends most of the day almost motionless near the bottom and
rises to the surface to feed at night (Arneson and Cutress, 1976). Barnes
noted that in the mid- to late afternoon, Chironex would sometimes rest
close to the bottom with the bell down and the tentacles retracted into or
near the bell (Kinsey, 1986, p. 27). In most cases, the distinction between
resting and epibenthic foraging is unclear. Specimen evidence and sting evi-
dence both indicate that Irukandji are more common in the afternoon
(Kinsey, 1988; Macrokanis et al., 2004; Nickson et al., 2009; Figure 1.13)
raising the question of whether these species respond differentially to differ-
ent levels of light.
Hartwick (1991a) noted that all parts of the life cycle of Copula sivickisi are
benthic and that the medusae intriguingly spend the day attached to benthic
structures but swim actively in the water column at night. In contrast,
Tripedalia cystophora, which is in the same family, has the opposite pattern;
it is active near the surface during the day and swims near the muddy bottom
at night (Garm et al., 2012). While the physiological and ecological bases for
the apparent diurnal rhythms of most cubozoans are not well understood,
Garm and his colleagues concluded that these behaviours in Tripedalia and
Copula were an adaptation to the activity patterns of their prey. Whether
this explains the afternoon activity peak for some Irukandji or the daytime
or night-time peak for others is worthy of investigation.
It is also possible that for most species in most regions, these morning and
evening peaks coincide with periods where low wind turbulence overlaps
with adequate daylight for hunting. In general, Irukandji are found in highest
abundance during periods of lowest turbulence (Gershwin et al., 2013a;
Kinsey, 1988).
3.4.4 El Niño/La Niña influence

The question of whether Irukandji occurrence patterns are affected by El
Niño–Southern Oscillation (ENSO) cycles is unresolved. On the one hand,
the weather conditions that best correspond with Irukandji infestations
include above-average temperatures, lack of recent rain, clear skies, and tem-
porary subsidence of the alongshore winds (Table 1.6). These hot, dry
Table 1.6 Summary of ecological conditions linked with Irukandji stings
Wind Wind Water
Source Locality speed direction temperature Rainfall Sunlight Tide Time Salps
Barnes (1964) Cairns QLD Low Northerly ND ND ND ND ND Swarms
Kinsey (1988) Cairns QLD Low NE–N ND ND ND ND Afternoon Swarms
Little and Cairns QLD <avg NNW– >avg <avg >avg ND ND ND
Mulcahy (1998) NNE
Fenner and QLD and NT No or Northerly Air temp None No or little Ebbing, moon ND ND
Harrison (2000) low wind mean cloud cover last ¼
31.2 C
Nickson et al. NT Still or Offshore Median None No or little High (also > Noon to ND
(2009) slight 29.9 C cloud cover or <) 2:59 pm
Gershwin Broome, WA ND ND >26 C ND Clear sky <Slack, neap Night Swarms
(2005b)
Thomas et al. Waikiki, ND ND ND ND Daytime 9–10 days after 1 h before ND
(2001) Hawaii full moon high tide
Gershwin Great Barrier ND ND ND ND ND 8–10 days after Night ND
(2005c) Reef, QLD full moon
Grady and Florida Keys ND ND Warm ND ND ND Night ND
Burnett (2003)
Macrokanis Broome WA >15 km/ NC >28.3 C NC ND High Afternoon ND
et al. (2004) h
Fenner et al. Thailand Low Onshore Warm ND ND ND ND Swarms
(2010)
NC, no correlation; ND, no data available. Australian states: QLD, Queensland; NT, Northern Territory; WA, Western Australia.
conditions are also often associated with El Niño in Australia. On the other
hand, a direct link has yet to be demonstrated.
3.4.5 Climate change influence

Recent media reports have suggested that the Irukandji sting season has length-
ened from about 1 month 40 years ago to about 6 months now (McKechnie,
2010) and have used this as evidence of global warming effects. These obser-
vations appear to be skewed. While there is no doubt that sting records have
increased over the last century (Figure 1.15), there could be multiple reasons
for it. Beach tourism has increased several-fold since that time (Harriott,
2002). Moreover, data from the 1960s to 1970s were primarily from the coastal
Cairns region because the reef tourism industry was nearly non-existent com-
pared with today and Cairns was the centre of Irukandji awareness and
reporting (Barnes, 1964). However, we now know that stings generally occur
later in the summer and autumn off Central Queensland and out on the reefs
and islands than along the Cairns beaches (Figure 1.14) and that these later sea-
son stings are often more virulent (Fenner and Hadok, 2002). Of course, it is also
possible that some fundamental change to the season or species has occurred
Figure 1.15 Interannual variability of Irukandji stings in Australia, 1920–2012. Low num-
bers of records pre-1960s and 1970s–1980s are believed to be due to low reporting
effort; low numbers in late 2000s are believed to be due to improved management
at the beaches. Data from Australian Irukandji sting database.
since Barnes’ time, but cannot be determined simply by taking the available data
at face value.
Curiously, two anomalous and remarkable high-latitude infestation events
occurred in the summer/autumn of 2013. Irukandji stings only rarely occur at
Fraser Island in southern Queensland, but in late December and early January,
a cluster of seven stings in 8 days occurred (Fraser Coast Chronicle, 2013).
Similarly, Irukandji stings rarely occur at Ningaloo Reef off central Western
Australia, but from April to June, at least 23 people were taken to hospital with
Irukandji syndrome, with nine occurring in less than a week (Le May, 2013).
In both of these high-latitude infestations, the number of stings was far higher
than for the more typical low-latitude stings for the season, suggesting some
sort of productivity shift. The physical and biological context for these infes-
tations remains unclear but is a high priority for urgent study.
It might be tempting to look at these events and conclude, as some have
done, that Irukandji must be moving toward the more populated temperate
regions. However, occasional cases of Irukandji syndrome have occurred in
higher latitudes for many decades (Cleland and Southcott, 1965; Gershwin
et al., 2009; Williamson et al., 1996). In truth, there is currently no evidence
to inform us as to the ecological circumstances that would be required for
tropical Irukandji species to migrate and flourish in southern coastal waters.
But one might imagine that it would involve ecosystem migration, not just a
medusa or two.
3.5. Movements and aggregations

Carukia barnesi blooms in large swarms, whereas Morbakka and Malo appear
to be more solitary. However, occasionally, clusters of Morbakka have been
found (Gershwin, 2008), and large numbers of Malo have been captured on
both the east and west coasts of Australia (Gershwin, 2005b, 2007; Kinsey,
1988). Similarly, the type series of Gerongia comprises many specimens cau-
ght together, but subsequent findings have been sparse (Gershwin and
Alderslade, 2005; Williamson et al., 1996). In contrast, Carukia does seem
to be a genuinely blooming species, with more than a thousand specimens
taken in one bloom event (Anonymous, 2002) and hundreds taken several
other times (AAP, 2005; Bateman, 2010a; Bester, 2012; Fenner, 2000).
Alatina mordens is only rarely found, but like its Hawaiian cousin Alatina
moseri, it appears to be more prevalent on the 8th, 9th, or 10th nights after
the full moon (Gershwin, 2005c; Appendix B). Studies have examined a
range of ecological and behavioural variables, but most have associated these
variables anecdotally and without statistical rigour.
3.5.1 Effects of wind

Onshore winds have long been regarded as the primary indicator heralding
the arrival of an Irukandji infestation. Indeed, the coincidence of Irukandji
stings and onshore breezes is so strongly linked that it has been noted by
almost every major worker on Irukandji (Barnes, 1964; Fenner and
Harrison, 2000; Flecker, 1957a; Gershwin, 2005a; Gershwin et al., 2009;
Kinsey, 1988; Little and Mulcahy, 1998; Southcott and Powys, 1944;
Williamson et al., 1996).
In popular local lore, a gentle onshore breeze (5–10 knots) sustained over
several days produces the highest risk conditions in tropical Australia
(Parsons, 2013; Roberts, 2002; http://www.cairnsvisitorcentre.com/faq).
Local lore also holds that the first couple of days after the breeze stops are
also high risk, supposedly because the Irukandji are thought to be ‘heading
back the other way’. Paradoxically, however, despite the large number of
these observations, this suggestion has rarely been tested rigorously.
The first effort at quantifying the link between wind and stings was
made by Kinsey (1988), who mapped Barnes’ Cairns region sting records
that contained wind information. Kinsey found that 25 stings occurred on
winds from the north, 23 on winds from the northeast, and 6 on south-
easterlies. Later, Little and Mulcahy (1998) analysed 62 Irukandji stings
from around Cairns in 1996 and found that 47 (76%) patients were stung
on days when the wind blew from the north, despite these winds only
being prevailent on 27% of days in 1996. Fenner and Harrison (2000)
examined 544 Irukandji stings in Queensland and the Northern Territory
and found that 73% occurred on 0-knot or light-wind days. Most recently,
Gershwin et al. (2013a), using a time series of stings over the past 30 years,
found that the subsidence of the southeasterly trade winds offered a mech-
anism for early prediction: as the dominant alongshore winds subside, the
onshore northeasterly sea breeze becomes more obvious and, along with
sub-surface intrusions, serves to drive the Irukandji conditions shoreward.
The phenomenon of Irukandji influx on an onshore breeze gives rise to a
long-standing hypothesis that Irukandji swarms are most prevalent on
exposed beaches facing into the breeze. However, the opposite seems to
be true more often. In particular, of 14 common island sting ‘hot spots’
in the Great Barrier Reef, 12 are near the southwestern portion of the island
or southwest of a rocky headland, whereas only two are along the open
northeast (Figure 1.16).
In contrast to the gentle onshore breezes heralding the arrival of
Irukandji on the east coast of Australia, Macrokanis et al. (2004) found that
Figure 1.16 Island Irukandji sting hot-spots in the Great Barrier Reef. Red dots indicate
hot-spots leeward of islands or headlands during northeasterly winds; yellow dots indi-
cate hot-spots in the direct path of northeasterlies. Data from Australian Irukandji sting
database. Maps from Google Earth.
higher sting probability on the west coast correlated with wind speeds
greater than 15 km/h. However, this does not appear to be universally true.
The large cluster of stings in the autumn of 2013 near Exmouth, Western
Australia, was accompanied by low wind speeds (Peter Barnes, Dept Envi-
ronment and Conservation, pers. comm., May 2013).
In Australia’s Northern Territory, it is the offshore wind rather than
the onshore wind that corresponds with Irukandji stings (Nickson et al.,
2009). Specifically, the other Australian regions discussed in the preceding
text (see bimodal distribution, section 3.4.1) peak during prevailing local
offshore wind periods. The ecological reason for this discrepancy is not
understood.
3.5.2 Infestations
For as long as Irukandji stings have been known, they have typically
occurred in occasional brief epidemics. For example, 36 stings occurred
on Christmas Day 1985 (Martin and Audley, 1990) and 50–70 in 1 day when
life-savers entered the water to haul in an enclosure net that was deployed to
keep swimmers safe (Kinsey, 1988). Barnes described seeing three truckloads
of ‘writhing carcasses’ driving past his house one day; they were taking
40–50 sting victims to the hospital (Kinsey, 1988).
Barnes (1966) described well the ephemeral nature of these infestations,
“Irukandji stings characteristically occur in localised outbreaks, claiming as
many as forty victims on a single beach within a period of a few hours. At the
same time, neighbouring beaches may remain stinger-free. Each visitation is
brief, rarely lasting more than 2 days, but the invasion may be repeated sev-
eral times within one season” (p. 309).
These mass sting events capture the imagination of the public and the
media, particularly in decades past or still today in regions where the cause
is poorly understood. Newspaper reports from Western Australia such as
Forty Swimmers Stung by Sea Snakes are thought to refer to Irukandji stings;
even though people did not see any snakes, these were the only thing imag-
inable that could cause such discomfort, so people assumed there were a lot
of invisible snakes doing the stinging (Kinsey, 1988).
Curiously, even though Carukia and Malo both occur coastally and off-
shore on the eastern and western Australian coasts, Carukia is well under-
stood to be the primary constituent of blooms in the east (Kinsey, 1988),
whereas Malo appears to be the primary bloomer in the west (Gershwin,
2005b). Whether these infestation events represent true swarming in the
active sense or are merely passive aggregations is not yet clear.
However, species in the Irukandji syndrome-causing genus Alatina are
believed to actually swarm in the true ethological sense. Thomas et al.
(2001) suggested that the monthly influxes of Alatina moseri in Hawaii were
spawning aggregations, with mature spawning males arriving at the shore
approximately 1 h before the high tide and mature spawning females arriv-
ing 1 h later. Hundreds of people are stung during these influxes. For exam-
ple, more than 800 people were stung on 29 July 1997 (Kreifels, 1997), some
developing Irukandji syndrome (Yoshimoto and Yanagihara, 2002). Why
this monthly Irukandji swarming phenomenon occurs only on the leeward
shore of Oahu remains mysterious, but may be simply a matter of the jellyfish
preferring calm conditions or habitats.
So too, Arneson and Cutress (1976) reported night-time spawning
aggregations of several hundred Alatina (as Carybdea alata) from Puerto Rico.
These aggregations occurred on 23 July 1973 and 12 August 1974, but did
not occur at other times; both of these dates coincide with the ninth night
after the full moon. The authors noted that the water was calm on both
nights, but no other environmental factors could be identified.
Elsewhere, we have less information on the species, but the epidemic

nature of the stings is similar. In Malaysia, for example, in addition to several
confirmed reports (Lippmann et al., 2011), in 2010, Divers Alert Network
Asia-Pacific received a report of around 150 people receiving treatment in
hospital for Irukandji-like symptoms sustained during aquatic activities in
Langkawi, Malaysia, between May and July that year. Similarly in Grand
Cayman, an area known as the Sandbar near the popular Stingray City
was shut down following a cluster of 26 stings on the morning of 27 April
2011, with eight being hospitalised (Fuller, 2011); this bloom was said to be
‘fairly typical’ for this time of year in this area.
The tendency for Irukandji to swarm and only occur periodically makes
safety management easier than if they were always present or problematic at
low densities. However, early forecasting of when and where the different
species are likely to occur is still in many ways the Holy Grail of Irukandji
research.
3.5.3 Swimming behaviour

Swimming studies have not been performed on Irukandji species, but the
California Carybdea has been recorded at 80–100 pulsations per minute
(Satterlie, 1979), and large Chironex fleckeri has been clocked at speeds of
4–5 knots (Barnes, 1960; Kinsey, 1986). Large Irukandji species such as
Morbakka and Alatina are very agile and powerful swimmers, and it is prob-
able that these species have similar swimming speeds and are able to swim
against a current. Even medium-sized species such as Gerongia and Malo
are quite powerful.
While larger species are quite strong swimmers, the more diminutive
Carukia is able to orient itself in the water column but cannot fight a cur-
rent. Even in a low-flow aquarium environment, it spends most of its time
drifting motionless with its tentacles streaming out, presumably fishing
(LG pers. obs.).
3.5.4 Effect of temperature

The associations between warm temperature and Irukandji infestations
seems fairly clear; however, whether thermal increase is a trigger for blooms
has not yet been investigated.
In a year-long study of northern Great Barrier Reef stings, 92% (57
patients) were stung on days hotter than the average for the month when
the sting occurred (Little and Mulcahy, 1998). Similarly, a study over
2.5 years in northern Western Australia found a higher probability of beach
stings when the water was greater than the yearly median of 28.3 C
(Macrokanis et al., 2004). Offshore in the same region, stings are anecdot-
ally believed to be most virulent when the water is above 26 C
(Gershwin, 2005b). Moreover, in an 18-year study of 87 cases in
Australia’s Northern Territory, water temperature was known for 77 cases;
the median was 29.9 C (range 25–32.3 C) (Nickson et al., 2009), most
well above the yearly average of 27 C.
3.6. Environmental variables

Many workers have found a suite of anomalous conditions associated with
higher incidence of Irukandji stings (Table 1.6). In general, periods with low
wind, unusually hot weather, less-than-average rainfall, clear skies, and thick
blooms of salps tend to coincide with Irukandji infestations.
3.6.1 Effect of tide

Tides are often invoked as a causal agent in coastal Irukandji infestations but
have yet to be demonstrated. For example, Great Barrier Reef stings are
anecdotally thought to be more prevalent on days with an afternoon high
tide, and this was also observed by Macrokanis et al. (2004).
Malo maxima was observed over the course of several nights around the
neap tides off the coast of northern Western Australia in autumn of 2004
(Gershwin, 2005a). The species was most often caught during the penulti-
mate hour before slack tide, with greater abundance on a falling tide than on
a rising tide. Approximately 1.5–2 h before slack tide, medusae began arriv-
ing in the halo under powerful flood lights. The medusae steadily increased
in numbers, with more than 10 simultaneously visible much of the time
despite being caught and removed when spotted; their attraction to the light
seemed undeterred by fish and squids that were also swarming under
the light.
About 30–60 min before slack tide, the arrival of medusae ended
abruptly. Some nights, they came for both slack tides but were more abun-
dant on the earlier slack, whereas other nights, they only came for the first
slack tide. These results may have been biased by the collecting trip being
limited to the neap period, during which the earlier evening tide was pre-
dominantly the low tide. In contrast to the large number of medusae
observed at night, divers caught approximately five specimens and saw some
several dozen during the day throughout the 9-day neap period.
Nickson and his colleagues (2009) found that more stings occurred at
high tide than any other time and that together high, incoming and outgoing
tides accounted for 86% of stings. Fenner and Harrison (2000) found that
more than 70% of the stings for which they had tidal information occurred
on an ebbing tide and that half of those with moon phase data occurred dur-
ing the moon’s last quarter. The majority of stings studied by Fenner and
Harrison were attributable to Carukia barnesi. Therefore, this peak of stings
during the last quarter moon is particularly intriguing, given that this is the
same time period as the monthly influx of Alatina spp. in Australia and
Hawaii (Gershwin, 2005c; Thomas et al., 2001).
3.6.2 Effect of sunlight

Little and Mulcahy (1998) noted that 69% of patients in their study were
stung on days with more hours of sunshine than average. Similarly,
Fenner and Harrison (2000) noted that more than 40% of Irukandji stings
occurred when cloud cover was less than or equal to two-eighths, and
Nickson et al. (2009) found that 73% of stings in their study occurred when
the weather was fine.
3.6.3 Effect of rainfall

Little and Mulcahy (1998) found a strong link between low rainfall and
Queensland Irukandji stings, with 87% of stings occurring on days with
5 mm or less of rain and 76% occurring when less than the average amount
of rain had fallen in the past week. Similar conclusions were drawn by two
other studies in Queensland and the Northern Territory (Fenner and
Harrison, 2000; Nickson et al., 2009). However, no correlation was observed
between rainfall and stings in Western Australia (Macrokanis et al., 2004).
4. TOXINS
Venoms and toxins occur abundantly across the animal kingdom facil-
itating not only prey capture and digestion but also to avoid predation and
for some sessile marine organisms, as a defense against infection. As cnidar-
ians have succeeded in persisting in highly competitive habitats for hundreds
of millions of years, it is not surprising to find that they exhibit numerous
sophisticated cellular inventions and innovations. These include cnidocyst
and venom composition variation and specialisation.
Bioactive components have been identified in all cnidarian classes
throughout the entire organism and not simply confined to the nematocyst
(Aneiros and Garateix, 2004; Ovchinnikova et al., 2006). Nevertheless this
review will focus on Irukandji nematocyst venoms. Their chemical arsenal is
an intricate mixture of pharmacologically active substances. These include

cytolysins, neurotoxins and lipases (Talvinen and Nevalainen, 2002), pepti-
dases (Gusmani et al., 1997), protease inhibitors (Delfı́n et al., 1994), and
antimicrobials (Morales-Landa et al., 2007).
The nature of the ‘Irukandji’ venom, its evolution and ecological signif-
icance, remains poorly described. Progress was minimal until, in the early
2000s, multidisciplinary Australian teams began a long-term effort to map
the species involved, the nature and action of their nematocyst toxins,
and to clone the DNA encoding the key molecules. This was driven, in large
part, by the need to address a growing public health problem that lacked a
specific treatment. In parallel, these and other investigators have also begun
to address the broader phylogenetic questions through complementary cni-
darian genome studies. Additionally, progress has recently been made in
mapping the nematocyst proteomes from other cnidarian species, providing
data that will ultimately assist in accelerating future understanding of the
toxins involved in this enigmatic syndrome.
Although some preliminary biochemical data and the initial results of
pharmacological studies using Carukia barnesi venom extract were reported
in 2000 (Tibballs et al., 2000; Wiltshire et al., 2000; Winkel et al., 2000), the
first major papers addressing the pathophysiology of Irukandji syndrome
were published more recently (summarised in Table 1.7; Li et al., 2011;
Ramasamy et al., 2005; Winkel et al., 2005; Winter et al., 2008). Major
reviews in the late 1990s (Burnett et al., 1996, 1998) had speculated on
the resemblance of the syndrome to cases of adrenal medullary or catechol-
amine excess, such as seen in cases of phaeochromocytoma and scorpion or
funnel-web spider envenomation.
As initially suspected from its clinical features, experimental studies con-
firmed that the syndrome is essentially one of excessive circulating catechol-
amines, notably noradrenaline and its methylation product, adrenaline
(Table 1.7). This appears to be secondary to venom-induced modulation
of Tetrodotoxin-sensitive prejunctional neuronal sodium channels in
peripheral postganglionic sympathetic sites and, possibly, splanchnic nerve
innervations and the adrenal medulla (Winkel et al., 2005). This results in
the systemic and pulmonary hypertension and increased cardiac output.
Although some variation in venom potency has been described, with Car-
ukia barnesi being apparently more potent than either Malo maxima or Alatina
mordens, all three species exhibited evidence of sympathetic activation in
experimental studies. Note that no intrinsic sympathomimetic activity, such
as from endogenous catecholamines, has been yet identified in these
Table 1.7 Summary of key studies and findings related to Irukandji jellyfish venom,
toxins, and genomics
Irukandji Summary of findings
venom study
Winkel et al. Investigated the cardiovascular pharmacology of the crude venom
(2005) extract (CVE) from Carukia barnesi, in rat, guinea pig, and human
isolated tissues and anaesthetised piglets. It was concluded that
venom may contain a neural sodium channel modulator (blocked by
TTX) that, in isolated atrial tissue (and in vivo), causes the release of
transmitter (and circulating) catecholamines. Both sympathetic and
parasympathetic nervous system effects observed. Venom may also
contain a ‘direct’ vasoconstrictor component. No biochemical data
provided. No studies of sensory nerve contributions
Ramasamy Investigated in vivo cardiovascular effects of Carukia barnesi venom
et al. (2005) and a tentacle extract (devoid of nematocysts). Findings consistent
with effects of catecholamine release. Also showed, for the first time,
that tentacle extract, free of nematocyst material, produces
cardiovascular effects distinct from those caused by venom derived
from isolated nematocysts
Winter et al. This study characterised the in vitro and in vivo effects of Alatina
(2008) mordens venom and indicated cardiovascular effects are at least
partially mediated by endogenous catecholamine release. Reported
a lower potency of venom compared with Carukia barnesi. Sodium
dodecyl sulphate polyacrylamide gel electrophoresis (SDS-PAGE)
profile of Alatina mordens venom showed that the venom is
composed of multiple protein bands ranging from 10 to 200 kDa.
Western blot analysis using CSL box jellyfish antivenom indicated
several antigenic proteins in Alatina mordens venom; however, it did
not detect all proteins present in the venom
Underwood Venom ontogeny, diet, and morphology in Carukia barnesi were
and Seymour assessed. SDS gel electrophoresis revealed differences in protein
(2007) banding of tentacular venom between immature and mature
animals. This was associated with a change in diet from invertebrate
prey in immature Carukia barnesi medusae to vertebrate prey in
mature medusae. Unlike other cubozoan studies, a change in venom
did not equate to a change in nematocyst types or their relative
frequencies
Ávila-Soria This Ph.D. thesis reported success with the development of both Malo
(2009) kingi and Carukia barnesi cDNA libraries. This allowed the establishment
of an EST resource from which were identified novel transcripts, several
serine and zinc proteinases and their inhibitors, two neurotoxin-like
genes, and two apparent cytolysins. RNA in situ hybridisation studies
revealed restricted expression of these putative neurotoxins, in adult
Carukia barnesi, to tentacular nematocyst batteries
Table 1.7 Summary of key studies and findings related to Irukandji jellyfish venom,
toxins, and genomics—cont'd
Irukandji Summary of findings
venom study
Li et al. The in vitro cardiac and vascular pharmacology of Malo maxima was
(2011) investigated in rat tissues. Malo maxima CVE appeared to activate
the sympathetic, but not parasympathetic, nervous system and to
stimulate sensory nerve CGRP release in the left atria and resistance
arteries. Effects are consistent with the catecholamine excess
thought to cause Irukandji syndrome, with additional actions of
CGRP release. Reported a lower potency of venom compared with
Carukia barnesi. SDS-PAGE profile of Malo maxima venom showed
most toxins to reside between 20 and 100 kDa molecular weight
venoms, although DOPA (dihydroxyphenylalanine), a precursor to

norandrenaline that has no pressor action, was detected in Malo maxima
venom extracts (Li et al., 2011). This pattern of venom action is quite dis-
tinct compared to that reported from non-Irukandji cubozoans such as
Chironex fleckeri (Hughes et al., 2012). This archetypal chirodropid venom
does not appear to involve autonomic nerves, postsynaptic adrenoceptors,
or muscarinic or sensory neural peptide calcitonin gene-related peptide
(CGRP) receptors, but may occur through direct effects on the cardiac
and vascular muscle (Hughes et al., 2012).
Further experimental variation in venom action has been identified
between these species. Specifically, minimal parasympathetic effects were
observed with Malo maxima venom in vitro, whereas Carukia barnesi venom
exhibited definite parasympathetic effects in isolated atrial tissues (Li et al.,
2011; Winkel et al., 2005). Hence, the relative significance of sympathetic
versus parasympathetic contributions to the dysautonomia (nervous system
dysfunction) manifest in the syndrome, as caused by different species,
remains to be determined. In addition, recent work on Malo maxima venom
has revealed a direct action of this venom on sensory nerves. The role of
sensory nerve effects has not been examined for the two other species.
While Malo venom action involves the release of the CGRP from sen-
sory nerves, it might also involve neuropeptide Y (Li et al., 2011). This pos-
sibility, and the possible role of other afferent pain pathways in the
syndrome, requires further investigation. For example, although some cni-
darian venoms (Chironex fleckeri, Aiptasia pulchella, Cyanea capillata, and
Physalia physalis) appear to activate TRPV-1 (Cuypers et al., 2006), a
nonselective cation channel expressed in nociceptive neurones, it is unclear

whether these channels are implicated in Irukandji syndrome. Although
Irukandji stings may cause a variable degree of local pain, the characteristic
severe muscular pain of delayed onset cannot be explained by the involve-
ment of local nociceptive effects alone. Indeed, compared to the pro-
nounced local and immediate pain associated with those jellyfish venoms
tested (Cuypers et al., 2006), Irukandji syndrome pain is very different.
Hence, a distinct mechanism would be predicted (Tibballs et al., 2012).
As these pharmacological studies progressed, the first details of the
biochemistry of ‘Irukandji’ toxins were discovered/found (Table 1.7).
Although the first description of the nature of cubozoan toxins began with
Wiener’s studies of Chironex fleckeri in the late 1950s (Southcott and
Kingston, 1959), no Irukandji species were subject to such assessment until
significant numbers of specimens became available in the late 1990s. It
appears that these venoms contain a minimum of tens of proteins, most
of which reside between 20 and 100 kDa molecular weight, but with some
higher weight entities noted in all three species examined. Based on extrap-
olation from the Chironex fleckeri proteome, many of these proteins are
likely to be posttranslationally modified by glycosylation (Brinkman
et al., 2012). Further, ontogenetic studies of Carukia barnesi venom profiles
suggest that the venom protein complement changes as the organism
matures, coincident with a transition from crustacean-targeting immature
forms to adult stages preferring larval fish (Underwood and Seymour,
2007). Note that this change in venom proteome did not equate to a
change in nematocyst types or their relative frequencies. Whether the
venom of mature adults is actually more toxic to vertebrates, including
humans, requires further research.
This emergent pattern is consistent with general trends evident in a series
of newly published medusozoan nematocyst proteomes. For example, the
screening, using high-throughput protein analysis, of nematocysts from
two hydrozoans, Hydra magnipapillata and Olindias sambaquiensis, and one
cubozoan, Chironex fleckeri, has begun to reveal the evolutionary history
of this organelle, one characteristic of the cnidarians, a group that is arguably
the most ancient of all venomous animals (Balasubramanian et al., 2012;
Brinkman et al., 2012; Weston et al., 2013). The former study reported a
complex secretome of 410 proteins with venomous and lytic but also adhe-
sive or fibrous properties (Balasubramanian et al., 2012). The authors con-
cluded that extracellular matrix motif proteins may have provided the
evolutionary origin of nematocyst venoms.
The second hydrozoan proteome (O. sambaquiensis) contained tens of

potential toxins homologous to most of the important superfamilies of
venom peptides reported from higher organisms. This includes cytolysins,
neurotoxins, phospholipases, and toxic peptidases (Weston et al., 2013).
These findings were consistent with an earlier study of an anthozoan met-
aproteome that revealed a complex mix of diverse toxins, including ion-
channel-modulating peptides and cytolytic enzymes (Weston et al.,
2012). Such findings argue that the development of these toxin types may
represent very early and basal eumetazoan innovations (Weston et al.,
2013), consistent with the antiquity of this group of venomous animals.
The closest published nematocyst proteome to that of the Irukandji group,
representing the first from a cubozoan, is that of Chironex fleckeri (Brinkman
et al., 2012). This recent analysis identified 61 proteins included both toxins
and proteins important for both nematocyte development and nematocyst
formation. The most abundant of these putative toxins identified were
isoforms of potent cnidarian cytolysins.
Due to the shortage of animals to provide sufficient material for conven-
tional bioassay-guided protein purification, it would seem logical to prioritise
genomic strategies to accelerate understanding of Irukandji toxins. However,
few genomic studies of cnidarian, let alone cubozoan or Irukandji, toxin fam-
ilies have been published. A draft genome of the sea anemone Nematostella
vectensis revealed surprising complexity and unexpected affinities with
higher-order bilaterians, notably vertebrates (Putnam et al., 2007). Neverthe-
less, the first complete mitochondrial genome sequence from a cubozoan,
Alatina moseri, confirmed the significant deviation of medusozoan mitochon-
drial DNAs from that of other animals (Smith et al., 2012). Subsequently, a
comprehensive cubozoan phylogeny, based on ribosomal genes, was publi-
shed (Bentlage et al., 2010). This latter paper proposed that the last common
ancestor of Carybdeida probably possessed the mechanism(s) underlying
Irukandji syndrome. This has strengthened the case for applying molecular
cloning strategies to elucidate the nature of toxin genes.
Preliminary success has been reported with the development of both
Malo kingi and Carukia barnesi cDNA libraries (Ávila-Soria, 2009). The
former allowed the establishment of an EST resource from which were
identified novel transcripts, several serine and zinc proteinases and their
inhibitors, two neurotoxin-like genes, and two apparent cytolysins homol-
ogous to those previously reported from other cnidarians. Further, RNA
in situ hybridisation studies revealed restricted expression of these putative
neurotoxins, in adult Carukia barnesi, to tentacular nematocyst batteries.
Finally, after successful expression of one of these putative Carukia barnesi

neurotoxin genes, pilot studies confirmed their neurotoxic potential in
the form of lethal paralysis after injection into cockroaches (Ávila-
Soria, 2009).
4.1. Which part of the animal is toxic?

Although we have yet to resolve whether the tentacles, or the bell, or both
carry the toxic fraction that produces Irukandji syndrome, there are logical
arguments on both sides. Jellyfish tentacular nematocysts are the most var-
iable and diagnostic between species (Figure 1.6; Gershwin, 2006a), and
therefore, logically, special types would provide a substantial functional
advantage to their owners. Moreover, the type of nematocyst that carries
the lethal fraction in Chironex, called a mastigophore, is confined to the ten-
tacles of Irukandji (Endean and Rifkin, 1975; Gershwin, 2006a).
However, on the unusual occasions that a sting mark is observed, it is
generally blobular rather than linear, leading to a hypothesis that the bell
is responsible for the sting. For example, a bell-shaped sting mark was evi-
dent in a case from the Northern Territory in which bell nematocysts were
recovered (Williamson et al., 1996, pl. 5.5). But then, it is equally plausible
that the tentacles attached to the bell inject venom without leaving a mark,
particularly in the smaller Irukandji species with fine tentacles.
Perhaps a more rigorous approach to test whether the Irukandji
syndrome-producing toxin (ISPT) is carried in the bell nematocysts lies
in the nematocysts themselves. Types of tentacular nematocysts are variable
among species, including even the presence or absence of mastigophores;
however, all species of syndrome-producing cubozoans share the same type
of bell nematocyst, called spherical isorhizas, and these are also found in blue
bottles (Physalia spp.), at least one of which causes Irukandji syndrome.
However, non-syndrome-producing species of cubozoans and Physalia also
have isorhizas, leading us to question this hypothesis. Nonetheless, a switch
of presence/absence of syndrome-producing venom in one type of nema-
tocyst would be more parsimonious than similar switches in cnidomes
peculiar to each species.
Even species in the genus Carybdea, long considered safe compared to
their more toxic cousins Carukia and Chironex, have spherical isorhizas on
the bell. And there is some suggestion that Carybdea may be capable of caus-
ing systemic symptoms consistent with Irukandji syndrome (Fenner, 2006;
Gershwin, 2006b; Little et al., 2006).
4.2. Evolution of Irukandji toxins

Combined nuclear large subunit, small subunit, and mitochondrial 16S anal-
ysis led Bentlage et al. (2010) to conclude that the carybdeid family
Alatinidae is ancestral to other carybdeid families, and therefore, the ISPTs
were likely to be present in the ancestral carybdeids and subsequently lost in
some groups. It may thus be reasonably hypothesised that ISPTs may be at
least 300 million years old.
A host of interesting questions arise in discussions about ISPTs. Perhaps
the most frequently asked is, “Why would a jellyfish need toxins that cause
such powerful systemic effects?”. Typical hypotheses include the following:
The delicate body must neutralise prey rapidly or risk damage, highly motile
prey such as fish must be quickly subdued in order to get a meal, and a soft
gelatinous body requires powerful defence.
However, the apparent ancient origin of ISPTs may predate fish. The
oldest putative bony fish is the approximately 500-million-year-old
armoured and jawless Cambrian species Anaspis. Similar to the modern-
day jawless hagfish and lampreys, these early ancestral forms were almost
certainly bottom dwellers and therefore probably had little contact with
jellyfish. Most fish diversification took place in the Silurian and Devonian
(ca. 440–360 mya), the latter of which is often referred to as the ‘Age of
Fishes’. However, it appears that all extant marine actinopterygians are
derived from a freshwater ancestor (Carrete Vega and Wiens, 2012).
Irukandji do not survive in freshwater nor is there any reason to believe that
they ever did. It therefore seems plausible that ISPTs either evolved inde-
pendently of fish or coevolved in the context of fish predator/prey dynamics
that are no longer extant. It is possible that the powerful toxic effect on
humans and at least some other vertebrates may be purely coincidental.
5. STINGER MANAGEMENT
Today, management of the Irukandji problem primarily falls into four
broad categories with a somewhat sequential relationship:
• Prediction of infestations to identify when and where they are likely
to occur
• Detection of the animals before stings occur
• Prevention of stings when the animals are present
• Treatment of symptoms when stings occur
5.1. Prediction
Decades ago, Barnes (1964) recognised the association between Irukandji
and onshore winds. However, it was not until 2012 that a plausible mech-
anism was identified, which now appears to be the subsidence of alongshore
winds (Gershwin et al., 2013a). In the coastal Cairns region, occasional pro-
longed subsidence of the southeast trade winds corresponds with days on
which stings have occurred (Figure 1.17), allowing for early forecasting
of heightened risk conditions. On these days, subsidence of the alongshore
winds reduces the turbulence and turbidity, creating conditions more
favourable for these delicate animals. Simultaneously, release from wind-
influenced downwelling pressure results in intrusions of oceanic water onto
the shelf, bringing in the oceanic hydromedusae and stimulating the salps
that are often observed with Irukandji infestations. Sub-surface intrusions
and internal waves may further enhance transport of this Irukandji water
mass closer to shore. This hypothesised mechanism has not yet been tested
in other locations, but the principles may be applicable to numerous other
habitats around the world.
Figure 1.17 Alongshore and cross-shore wind components around the time of three
stings in the Cairns region (the first sting corresponded to the 9th January 2007). Most
stings coincide with a drop in the alongshore wind (red), allowing the onshore sea-
breeze (blue) to dominate. Following such events, high sting rates can persist for up
to a week.
The habitats in which most Irukandji occur globally are similar in several
key features, while the specific infestation conditions are anomalous overall.
Namely, Irukandji habitats include an oligotrophic shelf system with occa-
sional salp blooms; they also share the feature of dominant alongshore winds,
where the sea breezes occasionally appear dominant as the alongshore winds
subside. Therefore, because of these similar anomalous conditions, predicting
when and where Irukandji infestations will occur should be feasible.
5.2. Detection
5.2.1 Bioindicators
A strong association between Irukandji and salps has been used effectively by
Surf Life Saving Queensland since 2005 to better estimate the relative risk of
Irukandji. In particular, because Irukandji can be hard to see but swarms of
salps are hard to miss, the presence of salps can be used as an indicator that
Irukandji jellyfish are likely to be present. Typical densities are on the order
of 2–4 l of salps in a 5–10 min hand-towed net drag in waist-deep water;
typically just a few, but sometimes dozens, of Irukandji are found in each
of these salp samples (Gershwin, unpublished data; Surf Life Saving Queens-
land, unpublished data). The days with the highest numbers of Irukandji
caught generally coincide with a band of salps and hydromedusae washed
up at the tideline.
Irukandji infestations have been known for decades to co-occur under an
anomalous set of conditions, that is, a thick bloom of salps, a variety of
hydromedusae including oceanic species such as Narcomedusae and Liriope,
and cool, clear, oceanic water. Barnes and others vividly described this
unusual set of conditions (Barnes, 1964, 1966; Cleland and Southcott,
1965; Kinsey, 1988). Even early workers such as Stenning (1928) and
Southcott and Powys (1944) noted that Irukandji stings occurred when a
large amount of gelatinous zooplankton was in the water.
For example, Barnes (1964) noted that during prolonged northerly
weather, “Under these conditions there is, about a half mile off shore, a
south-going stream of clear oceanic water; near the coast the water is murky,
warmer, and also moving south, but at a slower rate . . . It is interesting that
in the past, during periods of Irukandji infestation, life-savers have com-
mented on ‘drops of solid water’ (salps and small hydromedusae) on their
skins, and other observers have noted ‘jelly buttons’ (discoid medusae) cast
up by the waves. These correlations provided a valuable method of forecast-
ing the likelihood of Irukandji stings, and greatly reduced their incidence.
Collection of current-borne marine life was facilitated, but the very
plenitude of this life proved an embarrassment. Fine-mesh nets became

clogged with compacted jellies within a few minutes, and detailed examina-
tion of the catch was impracticable” (pp. 899–900).
The strong anecdotal link between Irukandji jellyfish and salps seems
persuasive, at least for Carukia barnesi, despite having never been formally
quantified or scientifically tested. It seems safe to say that every worker
who has studied Carukia barnesi or its stings in the field has observed the prev-
alence of salps and ‘sea lice’ during times of infestation. While the term ‘sea
lice’ can mean different things in different regions, these Australian ‘sea lice’
are not actually lice, or even arthropods; they are a large mass and diversity of
small hydromedusae and tentacle fragments that give the skin a feeling of tiny
pinpricks all over. These sea lice are not dangerous and they do not cause
Irukandji syndrome.
The relationship between salps and Irukandji does not appear to be equally
applicable across all species. So far, Carukia barnesi and Malo maxima have been
confirmed to co-occur with salps (Barnes, 1964; Gershwin, 2005b), whereas
Alatina and Morbakka appear not to. No information indicating an association
is available for Gerongia or other species of Carukia and Malo.
The reason for the association between salps, sea lice, and Irukandji has
not yet been resolved. However, dense aggregations of other types of gelat-
inous zooplankton have been studied and are believed to have adaptive sig-
nificance (Gershwin, 2013). It is possible that Irukandji need these dense
blooms of salps and hydromedusae where competition and predation are
minimal but biomass protection is maximised.
5.3. Prevention
The most effective method of in-water protection is a full-body lycra
‘stinger suit’ (Dawes et al., 2006; Gershwin et al., 2009; Figure 1.12).
The efficacy of different types of fabrics was tested by Gershwin and
Dabinett (2009), who found that smooth fabrics with a tight weave provided
the best protection. These tests used Carukia barnesi, which has the finest ten-
tacles of any known Irukandji species; stings from other species with heavier
tentacles are likely to be even more successfully prevented.
5.4. Treatment
Neither a vaccine nor an antivenom currently exists for Irukandji syndrome.
Treatment is largely symptom-based, that is, symptoms are treated as they arise.
In 2003, intravenous magnesium sulphate was first used to treat the

hypertension (high blood pressure) associated with some cases of Irukandji
syndrome (Corkeron, 2003). Unexpectedly, it relieved all symptoms, not
just the hypertension. Since that time, much debate has ensued regarding
the efficacy of magnesium, with some workers reporting total resolution
of symptoms (Corkeron et al., 2004; Rathbone et al., 2013), while others
find that it does not work for all stings (Little, 2005; McCullagh et al., 2012).
These studies have typically not taken species differences, phylogeny,
distribution, seasonality, or ontogeny into consideration. However, as with
snakes and spiders, these biological and ecological factors are highly likely to
govern the relative toxicity of the species we are trying to understand.
Treating all species and growth stages as a uniform entity is a cumbersome
and antiquated approach; far less painful and more elegant outcomes are
likely to be achieved through zoological understanding.
Conversely to the magnesium treatment, Hawaiian Irukandji stings are
routinely treated with hot water showers (Thomas et al., 2001). Two poten-
tially life-threatening problems arise from this. First, freshwater causes dis-
charge of remaining nematocysts by osmotic action (Glaser and Sparrow,
1909; Grosvenor, 1903). Second, heat dilates capillaries (Jaszczak, 1988),
theoretically inviting in more venom faster. Regardless of the efficacy of
pain relief, hot water treatment requires further research before it can be
confidently considered standard safe treatment (Gershwin et al., 2013b).
6. RESEARCH GAPS
Research on jellyfish in general, and Irukandjis in particular, has been
stymied by the relatively small amount of money available (Gibbons and
Richardson, 2013). Quantifying the magnitude of socio-economic impacts
of blooms will provide the impetus for more directed research into Irukandji
dynamics and prediction. This should be the major research priority, as it
contextualizes the Irukandji problem, encourages industry and government
funding and participation in research, and allows for the prioritization of
research questions. Obtaining this information requires innovative collabo-
rations among ecologists, economists, medical practitioners and social scien-
tists. It also requires the use of unconventional data sources, including
questionnaires to key stakeholder groups and meta-analyses of newspaper
articles to estimate the scale of the problem, and analysis of hospitalization
records to estimate health costs. Cost-benefit analysis of different mitigation
options will be needed to identify the best management practices
economically and environmentally. Currently, estimates of the cost of

Irukandji to coastal economies are sparse and qualitative, although one esti-
mate of losses to the tourism industry in 2002 in North Queensland due to
negative publicity is around AU$65 million (Williams, 2004 in Gershwin
et al., 2009).
The other major gap hampering our understanding of Irukandji blooms is
the lack of data. Few time series of Irukandji exist, and none of co-occurrence
with indicator organisms such as salps. To better identify the environmental
conditions responsible for blooms and when and where they will occur, time
series and spatial surveys of Irukandji abundance are needed. Despite more
than 70 years of study, our understanding of Irukandji jellyfish is still in its
infancy. We have synthesised the available information on their biology
and ecology, but in many ways, this raises more questions than it answers:
it is certainly an interesting and wide-open field of study for the curious
student of marine biology, ecology, toxinology, and taxonomy. In Table 1.8,
we summarise the major gaps, questions and issues, and techniques in the
hope of stimulating hypotheses for further study into these most remarkable
creatures and their dramatic interface with humans worldwide.
Table 1.8 Summary of the major gaps and issues in Irukandji jellyfish studies
Major discipline Gaps, questions, and issues
Taxonomy Development of regional taxonomic expertise
Systematic collecting in regions with unattributed stings
Potential for use of statoliths for gut contents and fossil IDs
First-aid research Does vinegar inactivate all Irukandji nematocysts?
Define the venom dose – syndrome severity relationship
Medical research Defining the links between different species and syndromes, for
improved management
Define the molecular mechanism/s underlying the various
features of the syndrome
Define and sequence the responsible venom toxins, and clone
and express the relevant genes in vitro
Develop a specific antivenom to neutralize the relevant toxin/s
across the various responsible genera
Better define the biomarkers predictive of syndrome severity
Table 1.8 Summary of the major gaps and issues in Irukandji jellyfish studies—cont'd
Major discipline Gaps, questions, and issues
Biology and Breeding grounds of polyps in the wild
ecology
Seasonal conditions that trigger metamorphosis
Potential response to climate change
Quantify the relationship between Irukandji and salps
Coordination of vision without a brain
Age and growth Robust studies on growth rates and longevity
Ontogenetic changes in morphology and physiology
Venom changes with ontogeny
Ontogenetic changes in food preference
Genetics Population genetics, species boundaries, and connectivity
Better understanding of evolutionary history, age of group
Development of tools for rapid identification
Why are mitochondria linear rather than circular, and how do
they duplicate?
Trophic Predator/prey behavioural dynamics
relationships
Fatty acid and stable isotope analyses
Bloom prediction Time series of abundance and spatial surveys of key sites
Environmental conditions that cause infestations
Socioeconomic Quantifying the magnitude of socio-economic impacts of both
impacts stings and the public fear of stings
ACKNOWLEDGEMENTS
We gratefully acknowledge the many collectors, research assistants, funding bodies, and
people and organisations through the years who have given us specimens, notes, data, and
literature relating to Irukandji, without whose help, most of the research would not have
been possible. In particular, we humbly thank James Angus, Natalia Aponte, Brad
Armstrong, the Australian Biological Resources Study, the Australian Institute of Marine
Science, Dave Barker, Paul Barker, the family of Jack Barnes, Nick Barnes, Peter Barnes,
Broome Shire Council, Machael Carlson, Michael Corkeron, the CRC Reef Research,
Bart Currie, Karen Dabinett, Ian Day, Department of Parks and Wildlife (WA), Marty
Durkan, Ben Eales, the Great Barrier Reef Research Foundation, Dean Harrison, Bill
Horsford, James Cook University, David Kain, Ebony Keating, Mike Kingsford, Deb
Lewis, Ran Li, Lions Foundation, Col McKenzie, Dale Mengel, John Menico, Kim Moss,
Paspaley Pearling Company and its divers and skippers, Pearl Producers Association, Robert
King Memorial Foundation, Ron Pollard, Kathryn Porch, Victor Hugo Beltran Ramirez,
John Rathbone, Mark Ross-Smith, Jamie Seymour, Grant Small, the family of Ron
Southcott, Surf Life Saving, James Tibballs, Tim Trew, Heather Walling, Kathryn Walsh,
John Williamson, Carolyn Wiltshire, Christine Wright, and Angel Yanagihara. The
AVRU also gratefully acknowledges funding support from the Australian Government
Department of Health and Ageing as well as from the National Health and Medical
Research Council and Sutherland Trust.
APPENDIX A: NOTES ON REARING AND LIFE CYCLE

OF CARUKIA BARNESI
Neither the methods nor the early life cycle stages of Irukandji have
previously been described. One of us (LG) has had extensive experience
collecting all stages of medusae from the wild over 10 summers and rearing
Carukia barnesi in the laboratory. The following is a summary of these
unpublished findings. The aquaria used as rearing chambers were plastic
hamster cages with fine nylon mesh screening off the outflow in one-third
of the tank; a slow but steady fall of water from small airline tubing was used
to drive the circulation in the other two-thirds.
Life cycle notes

The youngest medusa specimens have the appearance of tiny strawberries.
They are about 1–2 mm in diameter, pyramidal to globular in shape, and
dark red. The pedalia and rhopalial niches are not yet formed; four stubby
tentacles mark the corners and the rhopalia are external. The reddish colour
is presumed to come from the dense concentration of nematocyst batteries
on the bell, which spread out as the animal grows. A few of the smallest spec-
imens each year are caught with their ‘umbilical cord’ still attached: this is a
portion of the polyp that remains still attached to the apex of the bell for the
first few hours after liberation. By the time these specimens are processed
some hours later, they invariably have lost this structure. Laboratory rearing
of other cubozoan species has revealed that the umbilical cord is typically
resorbed within 2–12 h but may take up to several days (Arneson, 1976;
Arneson and Cutress, 1976; Cutress and Studebaker, 1973; Horita, 1992;
Stangl et al., 2002; Straehler-Pohl and Jarms, 2005, 2011; Studebaker,
1972). Therefore, assuming that Carukia barnesi is typical within this resorp-
tion range, the species must be breeding near the shore and essentially being
picked up by currents and transported the short distance shoreward.
Hand-fed medusae change and grow rapidly. The juvenile strawberry

appearance is lost within a few days, and the animals become more evenly
dome-shaped and golden; the pedalia form, the tentacles lengthen, and the
rhopalial niches are fully formed within a week. In this time, the animals
have tripled to quadrupled in body size. Over the next several days, animals
continue to grow rapidly, taking on a more transparent and sculpted appear-
ance; the tentacles develop the handkerchief banding and grow at an
astounding rate of about 2.5 cm per day (relaxed length). By 2 weeks, the
tentacles can relax to about 100 cm in length and the animals have fully
mature gonads. Mature specimens range in size from about 8 mm bell height
to 14 mm, with the most common specimens in this size range being about
9–11 mm. After a day or two of spawning and senescing, most specimens do
not survive longer than 2 weeks.
Medusae were not observed to spawn. In field-collected specimens, ripe
gonads are full and broad; after spawning, the gonads of both males and
females are narrow. Brooding embryos have not been observed; thus, it
appears that Carukia barnesi is a broadcast spawner. Planula larvae were
not observed in captive cultures. Cubozoan polyps were observed simulta-
neously in eight aquaria on a closed system and both inflow and outflow UV
sterilisation; therefore, the polyps were assumed to come from the Carukia
barnesi specimens in the aquaria.
The first polyps were observed while medusae were still alive in the
aquaria and colonised rapidly. Within a couple of months, polyp density
was estimated at 500–1000 per 24 cm2 hanging acrylic plate. Polyps readily
colonised all substrates: plastic aquarium sides and bottom, hanging acrylic
plates, shells, terracotta chips, glass petri dishes, and PVC connectors. Many
polyps were also found adhering to the algal films and flocculants that
covered most of the surfaces and fish scales on the bottom.
Polyps were whitish and extremely small, to 0.6 mm in diameter. The
polyp was divided into three main parts: an aboral stalk with an adhesive
basal disc; a short, stocky body; and a huge conical hypostome with a ter-
minal round mouth, with the margin between the body and hypostome
bearing up to 20 solid tentacles. The hypostome was quite plastic in form,
as often the polyps were observed either with the mouth raised like a smooth
bell curve or with the oral disc quite flat. The oral disc was evenly smooth
and glistened from a heavy speckling of nematocysts.
The number of tentacles increased with body size: The smallest polyps
(0.1 mm diameter) had four tentacles, whereas the largest (0.65 mm
diameter) had 19–20. The tentacles were evenly spaced around the disc
margin, each elongate–triangular in shape with a single large nematocyst

embedded in the tip. Most of the time, the polyps lay in ‘fishing mode’ with
the disc flat and the tentacles radiating out. When prey particles were caught,
they were rapidly ‘slam-dunked’ into the mouth. Then the tentacle was
quickly returned to fishing mode and the single terminal nematocyst was rep-
laced in about 2 h by migration from the body. In the non-Irukandji
cubopolyp of Carybdea, restoration of the terminal nematocyst took about
4 h (Maniura et al., 2001).
Creeping polyps appeared without their development being observed.
These polyps were considerably longer and larger than the sedentary polyps,
up to 2 mm long. The oral disc was broadly conical with a flattened top. It
bore six evenly spaced cylindrical tentacles, which were about twice the
diameter of the oral disc in length. Each tentacle had a single large nematocyst
in its distal end.
Feeding notes
In another study involving laboratory rearing of Carukia barnesi, specimens of
all sizes would accept fish and prawn food particles touched to the tentacles;
however, these were eventually discarded and never ingested. Food particles
offered straight to the lips on a probe were readily accepted and rapidly
ingested. However, younger specimens tended to spit out fish more often than
prawn and thus grow more slowly. By contrast, older specimens tended to spit
out food less often but grow more rapidly and maintain a healthy appearance
on fish (Gershwin, unpublished notes).
When fed, laboratory specimens would typically remain fairly inactive for a
brief time, either on the bottom or drifting passively. If disturbed, they would
usually expel their food. Undisturbed, prawn-meat particles equal in size to
about one-quarter of the stomach took about 2 h to digest, and fish sections
of the same size took about two to four. After about 20–30 min, the jellyfish
would begin expelling the scales through the mouth in a sparse mucous stream.
Between feedings, medusae exhibited what was interpreted as foraging
behaviour. Medusae hung nearly motionless several centimetres below the
surface with the tentacles relaxed as a loose tangle of fine threads through
the water column. Pulsation was slow and irregular. A variety of suitably sized
prey items were observed to be envenomed upon contact, made apparent by
the struggling movements of the prey. However, in this captive environment,
food was never observed to be ingested, but rather, the medusae continued
in fishing mode and occasionally food items were ensnared by more than
one jellyfish simultaneously. In all cases, food was eventually discarded dead.
APPENDIX B: NOTES ON AUSTRALIAN ALATINA

MORDENS OCCURRENCE
Research from long-term monitoring in Hawaii during the 1990s sug-
gests that an aggregation occurs on coral reefs where oceanic Irukandji
(Alatina moseri) appear 8–12 days after the full moon each month
(Thomas et al., 2001). Some of these jellyfish remain behind in the lagoon
and can potentially cause significant stings (Yoshimoto and Yanagihara,
2002). A review of marine sting reports from a marine operator in far north
Queensland from 1996 to 2002 suggested that there was a similar, but
milder, pattern with Irukandji.
A collaborative research programme involving the CRC Reef Research,
James Cook University, Australian Venom Research Unit, and Reef
Biosearch began in 2002. Metal halide flood lights were positioned over
the side of a research vessel at night with plankton nets used to retrieve spec-
imens. Attempts were made to sample in open water in front of reef systems,
but conditions were generally untenable, so to maximise catch efforts, a deci-
sion was made early to consistently sample on the leeward side of the reef.
Specimens caught were identified to at least genus level, bagged, and
snap frozen. These specimens were then sent to other research institutes
for genetic and venom analysis and taxonomy purposes.
Specimens were caught during this lunar period over most months of the
year, with a larger prevalence over the summer months (December to April),
but with a surprising mild spike during August to September during
some years.
Several species of Irukandji were collected in all weather conditions (from
0 to 40 knots), but best results were during 5–10 knot southeasterly condi-
tions, and highest yield per night was over 70 specimens. Some specimens
were caught during extreme conditions, such as an unnamed new species
of Carukia caught during a cyclone, with 40 knot northwesterly winds.
Irukandji appeared to be highly photopositive, actively moving into illu-
minated areas, regardless of the presence or absence of prey items. Medusae
attracted to light sources were nearly always at the surface of the water, espe-
cially Alatina mordens (the most common species encountered).
Alatina mordens sting

Most stings from Alatina moseri in Hawaii do not produce Irukandji syn-
drome, but some do (Yoshimoto and Yanagihara, 2002). Similarly, only
about 5% of stings from Alatina mordens in Australia produce systemic illness;

more often, the sting produced is merely painful and localised (R. Hore,
unpublished data). Some cases attributed to this species have required life
support (Gershwin, 2005c). Because of the possibility of life-threatening
stings in rare instances, this species should be treated with great care.
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CHAPTER TWO
Marine Invasions and Parasite

Escape: Updates and New
Perspectives
April M.H. Blakeslee*,†,1, Amy E. Fowler†,{, Carolyn L. Keogh}
*Biology Department, Long Island University-Post, Brookville, New York, USA
†
Marine Invasions Laboratory, Smithsonian Environmental Research Center, Edgewater, Maryland, USA
{
Marine Resources Research Institute, South Carolina Department of Natural Resources, Charleston,
South Carolina, USA
}
Odum School of Ecology, University of Georgia, Athens, Georgia, USA
1
Corresponding author: e-mail address: april.blakeslee@liu.edu
Contents
1. Introduction 88
1.1 The enemy release hypothesis 90
1.2 Parasite escape and release in marine systems, and the influence of invasion
pathway 91
1.3 Marine parasite escape: updates and new perspectives 96
2. Methods 108
2.1 Data sources 108
2.2 Data extraction 109
2.3 Data analysis 112
3. Results 113
3.1 Metadata based on studies from literature search 113
3.2 Parasite species richness, abundance, and escape across investigations 114
3.3 Mechanistic factors influencing parasite escape 118
3.4 Multivariate analyses 137
3.5 Evidence of parasite release 138
4. Discussion 138
4.1 Parasite taxa 140
4.2 Host–parasite geography 144
4.3 Time since introduction 146
4.4 Vector and vector strength 147
4.5 Host taxa 150
4.6 Parasite release 151
4.7 Case studies of noteworthy host species 153
4.8 Parasite escape in the context of marine parasite invasion 157
4.9 Study limitations 158
5. Conclusions 160
References 161

http://dx.doi.org/10.1016/B978-0-12-408096-6.00002-X
88 April M.H. Blakeslee et al.
Abstract
Marine invasions have risen over time with enhanced globalization, and so has the intro-
duction of non-native hosts and their parasites. An important and well-supported par-
adigm of invasion biology is the significant loss of parasites that hosts enjoy in
introduced regions compared to native regions (i.e. parasite escape), yet less is known
about the factors that influence parasite escape in marine systems. Here, we compile an
up-to-date review of marine parasite invasions and test several hypotheses related to
host invasion pathway that we suspected could influence parasite escape across the
31 host–parasite systems included in our investigation. In general, we continued to
show significant support for parasite escape; however, escape varied among parasite
taxa, with most taxa demonstrating moderate levels of escape and a few showing com-
plete or no escape. Moreover, we revealed several important factors related to host taxa,
geography, time, and vector of introduction that influenced parasite escape, and in
some cases demonstrated significant interactions, revealing the complexity of the inva-
sion pathway in filtering parasites from native to introduced regions. In some (but not
all) cases, there was also evidence of invasive host advantages due to parasite escape,
but more evidence is required to demonstrate clear support for the enemy release
hypothesis. In general, our study revealed the need for further research across systems,
especially in understudied regions of the world.
Keywords: Marine, Invasion, Biogeography, Parasite, Trematode, Parasite
escape, Enemy release, Introduction vector
1. INTRODUCTION
As globalization has escalated over the past two centuries, so has the
rate at which non-native species have been intentionally or unintentionally
introduced to areas outside their natural ranges (Brawley et al., 2009; Levine
and D’Antonio, 2003; Ruiz et al., 2000; Cohen and Carlton, 1998). When
introduced species become established in new habitats and spread, they can
have far-reaching impacts on recipient communities (Simberloff et al.,
2013). In fact, species invasions have been ranked second only to habitat loss
as a force of ecological disturbance (Crowl et al., 2008; Vitousek et al.,
1997). While physical disturbances via abiotic or anthropogenic sources
can open up niche ‘space’ or alter community dynamics thus providing a
mechanism for invasion (Byers, 2002; Cohen and Carlton, 1998), invasive
populations can also act as a type of biotic disturbance themselves, paving the
way for subsequent invasions by other species (Grosholz, 2005; Simberloff,
2006; Simberloff and von Holle, 1999).
New Perspectives of Marine Parasite Escape 89
A prominent example of the effect multiple species invasions can have on

recipient communities is San Francisco Bay (Grosholz, 2002). Arguably the
most invaded estuary in the world (Cohen and Carlton, 1998), San Francisco
Bay has seen a steady increase in successful invasions over the past few
decades, and in many communities, the number and biomass of invasive spe-
cies can contribute the vast majority (97% and 99%, respectively) of its biota.
It is remarkable, in fact, that this estuary has continued to accumulate so
many invaders over time with its inherent constraints for niche availability
and space. This enigma may be the consequence of a complicated process
of invader-induced positive feedback loops and high levels of anthropo-
genic disturbance, transforming the bay from a coevolution-structured
community into an invasion-structured community (Rummell and
Roughgarden, 1985), whereby natural community dynamics become
perturbed, leading to a contraction of niche space separation and the poten-
tial for more species to exist under the same resource distribution
(Byers, 2009).
This oft-noted dominance of invaded communities by non-native rather
than native fauna (e.g. San Francisco Bay) is in some ways surprising, given
that the probability for establishment and spread of founding populations is
expected to be relatively small. For example, the prominent hypothesis, ‘the
rule of tens’, estimates only a 10% chance of transition between each phase of
the invasion process, resulting in invasive status for just a fraction of those
species reaching a new location (Williamson and Fitter, 1996). However,
even with such low success rates, those populations that do become invasive
typically demonstrate considerable ecological success, often reaching high
population densities and larger individual sizes than conspecifics in native
ranges and even outperforming native species (Blossey and Notzold,
1995a,b; Mitchell and Power, 2003; Torchin and Mitchell, 2004;
Torchin et al., 2001)—underscoring one of the most fundamental questions
in invasion biology: why do some invasive species fare so well in novel envi-
ronments, sometimes even ‘better’ than phylogenetically similar natives in
the same environment?
The answer to this question involves a highly complex, often context-
dependent, scenario played out across source community, invasion pathway
(including introduction vector), and recipient community for each specific
introduction ‘attempt’. In particular, Lonsdale (1999) described three char-
acteristics that might affect a species’ ability to invade a novel ecosystem, including
(1) the properties of the recipient ecosystem—such as its potential for invasion
resistance, its current level of disturbance, its environmental stochasticity,
and its ability to support the particular invader (i.e. environment matching);
(2) the propagule pressure of the invader to the novel ecosystem—which is heavily
influenced by anthropogenic introduction vectors, which may be inten-
tional/accidental, selective/unselective, occur frequently/infrequently, or
in areas of high species abundance—all of which will impact the likelihood
of colonization and establishment success; and (3) the properties of the biota in
the ecosystem, which could influence an ecosystem’s resistance to invasion or
enhance invasion success.
Once a species has successfully established in a non-native range, the inva-
sion process itself may influence the exotic’s ability to spread and exert dominance over
native species. One hypothesis for this is that the invasion process mirrors
selective evolutionary processes, providing the invader with an ‘edge’
(e.g. competitive, predatory, and physiological) over natives. Depending
on the type of introduction vector and invasion pathway, there could be
multiple physical and/or biological factors (e.g. transit time, temperature
and salinity fluctuations, and human handling) that impact a species during
the process, possibly eliminating the most sensitive individuals. Those geno-
types that survive and reproduce will be the ones passed down to subsequent
generations, potentially resulting in a highly ‘fit’ population that can establish
and spread in the new environment and may even possess enhanced fitness
and survival compared to natives (e.g. Lavergne and Molofsky, 2007;
Saltonstall, 2002; Simberloff, 2009). Yet another (non-mutually exclusive)
hypothesis for the potential ‘edge’ an invader may have over natives is that
the invasion process can filter out natural enemies (predators, competitors,
and parasites), thus providing invaders with fewer enemies to contend with
in their exotic range (Keane and Crawley, 2002; Torchin et al., 2001, 2002,
2003). This enemy release hypothesis is a well-developed and well-explored
hypothesis in numerous systems around the globe; however, there is much
still to be learned regarding its implications for invasive communities, espe-
cially in marine systems. In the subsequent text, we briefly summarize the
current evidence for the enemy release hypothesis and focus on a particular
type of enemy escape: parasite escape in marine systems.
1.1. The enemy release hypothesis

One of the most commonly cited explanations for the high degree of
demographic success that invaders can exhibit in their recipient communi-
ties is the enemy release hypothesis, whereby a loss of predators and parasites
enhances an invasive species’ biological and/or physiological performance
in their exotic populations compared to native conspecifics (Keane and

Crawley, 2002; Torchin et al., 2001, 2003). Most of our understanding
of the processes and consequences of enemy release comes from studies
of plants, where experiments have tested implications of documented escape
on invader performance. For example, Wolfe et al. (2004) found that North
American individuals of the invasive perennial weed Silene latifolia were
17 times less likely to be damaged by natural enemies than native European
populations (Wolfe, 2002). In another example, Liu and Stilling (2006)
found invasive plants to show significantly lower numbers of insect species
feeding on them in their introduced versus native ranges, as well as a reduc-
tion in the number of specialist insects in invasive populations. Among ani-
mal systems, a prominent example comes from the US west coast, where a
non-native snail, Batillaria attramentaria (¼cumingi), has displaced a native
snail, Cerithidea californica, in many of their overlapping populations through
exploitative competition; moreover, the invader is parasitized by many
fewer castrating trematode species than the native, and this almost complete
elimination of the top-down influence of parasitism may be another reason
for Batillaria’s dominance over Cerithidea (Byers, 2000; Byers and
Goldwasser, 2001; Torchin et al., 2005). This last example demonstrates
the importance of parasite release on an exotic species’ success in invasive
populations, which we further explore later.
1.2. Parasite escape and release in marine systems, and the

influence of invasion pathway
In the seminal work, “Introduced species and their missing parasites”,
Torchin et al. (2003) clearly demonstrated the significant loss in parasite
diversity that occurs in non-natives versus natives across taxa worldwide.
In particular, they found introduced hosts to possess roughly half the number
of parasites as natives, with the greatest losses coming from freshwater sys-
tems, followed by marine systems, and finally terrestrial systems (Torchin
and Lafferty, 2009). How this loss of parasites (¼parasite escape) translates
into enemy release (i.e. demonstrating a clear benefit to released hosts com-
pared to unreleased conspecifics) is less clear in many systems (see Colautti
et al., 2004); however, there are several examples of individual or
population-level benefits that have been attributed to parasite escape
(Torchin and Mitchell, 2004). For example, Mitchell and Power (2003)
noted that the most highly damaging plant invaders introduced to the
United States from Europe were those that had also seen the most release
from plant pathogens; moreover, Torchin et al. (2001) found that invasive
populations of the European green crab (Carcinus maenas) were larger and
exhibited greater biomass than native populations, correlating with signifi-
cantly lower parasite diversity in non-native crab populations and escape
from a particularly harmful parasite group, namely, castrating barnacles.
Specific to marine communities, Torchin et al. (2002) documented a
clear reduction in parasite diversity in non-native versus native hosts; yet
much remains to be learned regarding the role of parasite escape in marine
systems, especially given the increase in studies in this area over the last
decade. In particular, while parasite escape is a signature of invasion
irrespective of host or biome (Torchin and Mitchell, 2004; Torchin
et al., 2003), there is apparent variability from host to host in the extent
of that escape and its root causes. In general, variability in parasite escape
may be influenced by a combination of properties of the host and parasite
fauna, as well as particular aspects of the invasion process. In other words,
a host’s escape from parasites will be controlled not only by the rate it accu-
mulates parasites in its exotic range [that is, the number introduced with the
host plus those it picks up in the invaded range (Torchin and Mitchell,
2004)], but also the properties of an invasion that influence the strength
and duration of escape for a given host, for example, host and parasite geo-
graphic range, host introduction vector and vector strength, and the time
elapsed since introduction. In the succeeding text, we describe each of these
factors and their potential for influencing parasite escape in marine systems.
1.2.1 Host–parasite geography

There are several ways in which the geographic range and location of a
host, its parasites, and source and recipient communities can influence parasite
escape. Probably the most intuitive geographic influence on parasite escape is
the degree of isolation of the recipient range with respect to the source region.
If the distance between the source and recipient regions is short, the ranges are
likely to experience more frequent connectivity by vectors, to share more
phylogenetically similar taxa, and to allow a greater proportion of entrained
hosts and parasites that survive the journey, thus reducing the invasive hosts’
chances of losing parasites (e.g. Drake and Lodge, 2004). In general, geo-
graphic constraints on invasion are largely determined via the introduction
vector (i.e., mechanism of introduction), as well as the durability of the inva-
sive propagules. Moreover, a positive relationship between geographic
distance and the stress experienced by propagules during transport may also
contribute to a greater filtering out of individuals with increased distance
between ports (Miller and Ruiz, 2009). Because parasitized hosts may be more
susceptible to stress (e.g. Jokela et al., 2005; Thieltges, 2006), they may be even
less likely to survive long transport times, thereby reducing the probability of
parasite introduction.
Other biogeographic relationships, aside from distance, might also con-
tribute to parasite escape. Lafferty et al. (2010) explored the relative contri-
bution of latitude, land mass, and site of origin (native or introduced) on
parasite species richness across 26 taxa, including herpetofauna, mammals,
birds, and fish. For native species (both parasites and free living), latitudinal
diversity gradients predicted that diversity decreased with increasing lati-
tude. However, an increase in parasite richness with increasing latitude
was found for introduced populations, supporting the hypothesis that par-
asite escape influences parasite richness more strongly than geographic
effects operating independently.
1.2.2 Introduction vector and vector strength

Mechanisms of introduction play an important role in determining the like-
lihood of establishment and spread of an invading host, as well as the degree
of parasite escape that the invading host will experience. In marine systems,
invasion vectors are highly variable and include a number of anthropogenic
categories including shipping, aquaculture, live trade, biocontrol, and canals,
among others (Ruiz et al., 2000). Introduction vectors are also variable in
their frequency, targeting, transport time, and transfer of specific host life
stages. These interacting variables determine ‘vector strength’, which in
our investigation is specific to marine parasites. For example, those introduc-
tion vectors with high vector strength often include multiple, frequent
movements between source and recipient regions, which may serve to (a)
increase host population size to the threshold necessary to support parasites,
(b) introduce additional species that serve as hosts in the parasite’s life cycle,
or (c) introduce sufficient propagules of the parasite to allow infection to
establish (Torchin and Lafferty, 2009). Such aspects are also related to the
‘propagule pressure’ associated with a particular vector and the likelihood
for successful establishment and spread of propagules entrained within it.
Both theoretical and empirical studies point to propagule pressure as a
key predictor of invasion success (Colautti et al., 2006; Drake and Lodge,
2006; Grevstad, 1999; Hopper and Roush, 1993; Kolar and Lodge, 2001;
Miller et al., 2007); however, typical levels of propagule pressure associated
with certain vectors, and thus their vector strengths, could be substantially
different among free-living organisms compared to parasites. For example,
in free-living species, ship-based transportation of goods between ports and
across oceans has likely served as the dominant vector of introduction via
the entrainment of larvae within ballast tanks (Briski et al., 2012; Carlton,
1985), but this same vector would be expected to have much lower vector
strength for introducing parasites because it would lack (or have in very
low abundance) the necessary infective life stages of hosts, which are typ-
ically adults (Rohde, 2005; Torchin and Lafferty, 2009). In contrast, inten-
tional introductions associated with aquaculture have been shown to result
in the establishment of not only targeted species but also whole associated
assemblages, including parasites. For example, Miller et al. (2007) examined
predictors of success and failure in molluscan invasions associated with
Eastern oysters (Crassostrea virginica) transplanted by the millions to the
U.S. Pacific coast in the late 1800s through the mid-1900s (Carlton,
1979; Miller et al., 2007) and found that a species’ abundance in the region
from which it was introduced was the strongest predictor of whether or
not it became invasive on the Pacific coast. This trend was in fact mirrored
in a snail–parasite system of an associated mudsnail (Ilyanassa obsoleta)
introduced to the Pacific coast with eastern oysters, in that the introduction
of several of the snail’s native parasite species to the Pacific came from
some of its highest infected sites along the U.S. East coast (Blakeslee
et al., 2012).
1.2.3 Time since introduction

Time since introduction may emerge as a predictor of parasite escape when
time interacts with vector strength, geography, and host and parasite taxa to
influence the probability of the introduction of parasites from the native
range or the accumulation of new generalist parasites from the invaded
range. Parasite escape signals are likely to be most apparent in the earliest
stages of invasion, where a strong differential between invasive and native
populations may exist; however, this differential may decrease over time
due to subsequent invasions of infected hosts or parasite invasions via other
hosts (Blakeslee et al., 2009, 2012; Gendron et al., 2012; Prenter et al.,
2004). For example, time since introduction has been implicated in the
greater parasite escape experienced by the more recently established Asian
shore crab (Hemigrapsus sanguineus) on the east coast of North America, com-
pared to sympatric invasive populations of Carcinus maenas, which have been
in residence in some parts of eastern North America for 200 years
(Blakeslee et al., 2009). Carcinus maenas provides an additional example of
time since introduction and parasite escape, as shown by a linear relationship
between the timing of the crab host’s introduction and the number of par-
asite species that infect it in several of its introduced populations worldwide
(Torchin and Lafferty, 2009). Finally, Gendron et al. (2012) describe
populations of the invasive round goby (Neogobius menalostomus) in the Great
Lakes-St. Lawrence Basin that have similar levels of parasite infection as

native fish after just 15 years of residence, while newer introductions to
the region demonstrate significant declines in parasite infection compared
to source populations, as well as to native Canadian fish.
1.2.4 Host and parasite taxa

Host and parasite taxa are also likely to be influential factors of parasite escape
across host–parasite systems and could potentially also interact with many of
the factors described earlier. Specific to host taxa, some taxa entrained in
introduction vectors may be more likely to introduce parasites than others.
For example, in a recent review, Karatayev et al. (2009) found that molluscs
and crustaceans constituted 50.7% and 37.8% of the invasive taxa in North
America, respectively (but only accounted for 4.4% and 6.5% of native bio-
diversity in the continent). Moreover, Ruiz et al. (2000) found that molluscs
and crustaceans also constituted the majority of organisms transported via
marine introduction vectors, being more than twice as numerous as other
taxonomic groups. Not only are these taxa the most common invaders in
marine introduction vectors, but they are also the most common host taxa
to have escaped parasites around the globe (Torchin and Lafferty, 2009;
Torchin et al., 2002).
Specific to parasite taxa, the composition of parasite fauna in the native
range and the probability for introduction into the host’s invasive range are
important determinants of the magnitude and persistence of the introduced
hosts’ experience of parasite escape. In particular, the complexity of parasite
life cycles can differ considerably across parasite groups, and this might be
expected to impact a parasite’s invasion success (Torchin and Mitchell,
2004; Torchin and Lafferty, 2009). Directly transmitted parasites with simple
one-host life cycles might be more likely to accompany their host to the inva-
sive range than parasites that require multiple hosts to compete life cycles. Even
still, directly transmitted parasites may fail to invade if their transmission
dynamics are density-dependent, i.e. they would have difficulties establishing
if their host population falls below a critical threshold. As such, small host pop-
ulation size during the establishment phase of invasions may serve to filter out
some directly transmitted parasites (Lloyd-Smith et al., 2005). In contrast,
other parasite life cycles can be highly complex, requiring multiple species
from multiple trophic levels for life cycle completion. Parasites with complex
life cycles (involving more than one-host species) may have difficulties invad-
ing if they are highly specific to hosts in their life cycle and/or if any of the
hosts required for their development are missing or present in insufficient
densities in the novel range (Torchin and Lafferty, 2009). Many multihost par-
asites have differing degrees of host specificity in their life cycles, allowing for
some flexibility in the requirement that all hosts from their native range be
present.
One particular parasite group that has been well explored in marine sys-
tems (and a group we focus on here) is trematode parasites, which are char-
acterized by life cycle complexity. Trematodes are trophically transmitted
parasites with a multihost life cycle, involving a molluscan (typically gastro-
pod) first-intermediate host that becomes castrated during infection. Within
its snail host, the trematode reproduces asexually, releasing free-swimming
larval stages that seek out a second-intermediate host, often a mollusk, crus-
tacean, or fish, in which the larvae encysts. The life cycle is completed when
the second-intermediate host is preyed upon by a vertebrate definitive host
(often a bird or fish) and the encysted trematode is trophically transmitted to
the gut of the definitive host where it matures and sexually reproduces (Esch
et al., 2001). Trematode parasites have been found to dramatically influence
their first-intermediate hosts, where castration eliminates further reproduc-
tion, may influence host growth, and in some cases could influence behav-
iour (Granovitch and Maximovich, 2013; Wood et al., 2007). While the
first-intermediate stage is typically an obligate relationship, specificity is usu-
ally lower for the second-intermediate and definitive stages, which is an
important consideration for parasite escape in this group and other trophi-
cally transmitted parasites.
1.3. Marine parasite escape: updates and new perspectives

As described, parasite escape in introduced populations has been demon-
strated across numerous systems worldwide, including those in marine
environments (e.g. Torchin et al., 2003). Exploration of marine parasite
escape has continued to grow over time; however, as of yet, there has
been no formal, comprehensive analysis of works completed over the past
decade, following the seminal papers by Torchin et al. (2002, 2003).
Here, we explore parasite escape in marine systems over the past two
decades (prior to and following Torchin et al., 2002); yet our study does
not simply emulate the prior work, but instead focuses extensive analysis
on the invasion pathway to look for possible explanations across host–
parasite systems. Moreover, we generated six hypotheses that we tested
using the database we constructed from our exploration of the literature
(Table 2.1) and the potential mechanistic factors associated with invasion
pathways and host–parasite taxa. In particular, we hypothesized:
Table 2.1 Studies including marine parasite invasions and species richness information
Distance
(km) # Intro- Index of
between # Native duced parasite # Native # Intro Index of
native and Type of parasites Decade parasite parasite escape parasite parasite parasite
Source (native) Recipient introduced in study (N), (I), of intro taxa (all taxa (all (all taxa taxa escape Evidence of
Host species Abbr Host taxa range (introduced) range range (N,I) Vector type (host) parasites) parasites) parasites) (trem) (trem) (trem) parasite release Citation source(s)
Alosa AS Fish Eastern North Western North 4076 Cestoda (N), Deliberate 1870 26 2 0.92 N/A N/A N/A Unknown Hogans et al.
sapidissima (Osteichthyes) America America (Alaska Crustacea (N), introduction (1993), Shields
(American (southern to San Francisco Copepoda (N), et al. (2002), and
shad) Labrador to Bay, California: Hirudinea (N), Hershberger
northern Florida: 59 N–37 N); Monogenea (N), et al. (2010)
48 N–29 N); lat. median: Nematoda (N, I),
lat. median: 48 N; lon. and Protozoa (N, I),
39 N; lon. and median: 124 W Trematoda (N)
median: 74 W
Apollonia AM Fish Black Sea Gulf of Gdansk, 1641 Acanthocephala Ballast 1990 71 24 0.66 36.00 6.00 0.83 Low parasite Pronin et al.
melanostoma (Osteichthyes) (47 N–39 N; Baltic Sea, (N, I), Bivalvia water/hull loads in (1997) and
(¼Neogobius 41 E–26 E); lat. Poland; lat. (N), Cestoda (N, fouling introduced Kvach and Skora
melanostomus) median: 43 N; median: 54 N; I), Ciliophora locations may (2007)
(round goby) lon. and median: lon. and median: (N, I), Copepoda suggest enemy
34 E 19 E (N, I), release
Microspora (N),
Monogenea (N),
Myxozoa (N),
Nematoda (N, I),
Trematoda (N, I)
Asterias AA Sea star Asia (Japan; Southern coast of 9598 Ciliophora (N), Ballast 1990 2 0 1.00 N/A N/A N/A Unknown Torchin et al.
amurensis (Asteroidea) Russia; North Australia (37 S– Copepoda (N) water/hull (2002)
(Northern China; Korea: 43 S); lat. fouling
Pacific seastar) 60 N–31 N); median: 40 S;
lat. median: lon. and median:
46 N; lon. and 146 E
median: 137 E
Continued
Table 2.1 Studies including marine parasite invasions and species richness information—cont'd
Distance
Batillaria BC Snail Asia (Japan; Western North 11,093 Trematoda (N, I) Oysters 1920 15 3 0.80 15 3 0.80 Exploitative Byers (2000),
attramentaria (Gastropoda) Hong Kong: America (British competition Torchin et al.
(¼cumingi) 40 N–0 N); lat. Columbia; with Cerithidea (2002), Torchin
(Asian median: 20 N; Washington; californica, which et al. (2005),
hornsnail) lon. and median: Elkhorn Slough, has high Hechinger
110 E California: infection rates (2007), and
50 N–36 N); and many more Lafferty and
lat. median: parasite species; Kuris (2009)
43 N; lon. and loss of parasites
median: 124 W could contribute
Batillaria BA Snail Southeastern West Australia 3469 Trematoda (N, I) Ballast 1950 8 3 0.63 8 3 0.63 Some evidence Thomsen et al.
australis (Gastropoda) Australia (Swan River water/hull of a population- (2010)
(Whitsunday estuary and fouling level effect
Islands, Cockburn
Queensland; Sound:
southwards to 31 S–32 S); lat.
Victoria and median: 32 S;
Tasmania: 20 S– lon. and median:
43 S); lat. 115 E
median: 32 S;
lon. and median:
152 E
Carcinus CMJAP Crab Europe (Norway Japan 9263 Acanthocephala Ballast 1980 10 0 1.00 2 0 1.00 Unknown Torchin et al.
maenas (Crustacea) to Mediterranean (45 N–30 N); (N), Cestoda water/hull (2001)
(European green Sea: Tokyo lat./lon.: (N), Copepoda fouling
crab)/C. 70 N–35 N); 35 N/139 E (N), Fecampida
aestuarii lat. median: (N), Isopoda (N),
(Mediterranean 53 N; lon. and Nematoda (N),
green crab) median: 5 E Nemertea (N),
Rhizocephala
(N), Trematoda
(N)
Carcinus CMSA Crab Europe (Norway South Africa 9749 Acanthocephala Ballast 1980 10 0 1.00 2 0 1.00 In Torchin et al. Torchin et al.
maenas (Crustacea) to Mediterranean (Cape Peninsula, (N), Cestoda water/hull (2001): mostly an (2001) and
(European green Sea: Cape Town, S. (N), Copepoda fouling effect of release Zetlmeisl et al.
crab)/C. 70 N–35 N); Africa: (N), Fecampida from parasitic (2011)
aestuarii lat. median: 33 S–34 S); lat. (N), Isopoda (N), castrators. In
(Mediterranean 53 N; lon. and median: 34 S; Nematoda (N), Zetlmeisl et al.
green crab) median: 5 E lon. and median: Nemertea (N), 2011: testes
18 E Rhizocephala weight tested,
(N), Trematoda but no overall
(N) effect of parasites,
unless infected
by Sacculina,
which castrates
Carcinus CMWNA Crab Europe (Norway Western North 8050 Acanthocephala Live trade 1990 10 2 0.80 2 0 1.00 In Torchin et al. Torchin et al.
maenas (Crustacea) to Portugal: America (British (N), Cestoda (N, (algal packing (2001): mostly an (2001) and
(European 70 N–37 N); Columbia to San I), Copepoda materials) effect of release Torchin et al.
green crab) lat. median: Francisco Bay, (N), Fecampida from parasitic (2002)
54 N; lon. and California: (N), Isopoda (N), castrators
median: 5 E 50 N–37 N); Nematoda (N),
lat. median: Nemertea (N, I),
44 N; lon. and Rhizocephala
median: 123 W (N), Trematoda
(N)
Carcinus CMENA Crab Europe (Norway Eastern North 5459 Acanthocephala Dry ballast 1810 10 3 0.70 2 1 0.50 From Torchin Torchin et al.
maenas (Crustacea) to Portugal: America (N, I), Cestoda (original et al. (2001): (2001), Torchin
(European 70 N–37 N); (Newfoundland (N), Copepoda intro); Ballast crabs were larger et al. (2002), and
green crab) lat. median: to North (N), Fecampida water/hull and greater Blakeslee et al.
54 N; lon. and Carolina: (N), Isopoda (N), fouling (later biomass than in (2009)
median: 5 E 49 N–34 N); Nematoda (N, I), intro) native regions
lat. median: Nemertea (N), (where size and
42 N; lon. and Rhizocephala biomass are
median: 70 W (N), Trematoda negatively
(N, I) correlated with
parasitic
castrators)
Continued
Distance
Carcinus CMAUS Crab Europe (Norway Australia 16,504 Acanthocephala Dry ballast 1900 10 2 0.80 2 0 1.00 In Torchin et al. Torchin et al.
maenas (Crustacea) to Portugal: (Victoria; (N), Cestoda (N, (original (2001): mostly an (2001) and
(European 70 N–37 N); Tasmania: I), Copepoda intro); Ballast effect of release Zetlmeisl et al.
green crab) lat. median: 43 S–33 S); lat. (N), Fecampida water/hull from parasitic (2011)
54 N; lon. and median: 38 S; (N), Isopoda (N), fouling/ castrators. In
median: 5 E lon. and median: Nematoda (N, I), Oysters (later Z 2010: testes
145 E Nemertea (N), intro) weight tested,
Rhizocephala but no overall
(N), Trematoda effect of parasites,
(N) unless infected
by Sacculina,
which castrates
Cephalopholis CA Fish French Polynesia Hawaiian 4182 Monogenea (N), Aquaculture 1950 10 3 0.70 N/A N/A N/A The fish show Vignon et al.
argus (peacock (Osteichthyes) (17 S); lat. Archipelago Cestoda (N, I), significant (2009a)
grouper) median: 17 S; (22 N–18 N); Copepoda (N), reductions in
lon. and median: lat. median: Isopoda (N), richness and
149 W 20 N; lon. and Hirudinea (N), prevalence of
median: 156 W Nematoda (N, I) parasites in
Hawaii, but fish
condition indices
are not
significantly
different
between native
and recipient
regions;
therefore, more
evidence is
needed to
demonstrate
enemy release
Charybdis CL Crab Red Sea (30 N– Mediterranean 1366 Rhizocephala Suez canal 1950 >1? 1 N/A N/A N/A N/A Originally crab Innocenti and
longicollis (Crustacea) 12 N); lat. Sea (Turkey; (N, I) was released Galil (2007) and
(swimming median: 21 N; Israel: from parasites, Innocenti et al.
crab)* lon. and median: 36 N–30 N); but a few decades (2003), 2009
38 E lat. median: after original
33 N; lon. and introduction
median: 35 E (1992), a
rhizocephalan
parasite was
introduced
through same
vector, and
prevalence of
infection in the
crab was very
high in some
places; crab
populations
appeared to
remain stable
after parasite
introduction;
therefore, no
suggestion of
release detected
Crassostrea CGWNA Oyster Asia (Russia; east Western North 7596 Copepoda (N, I), Oysters 1900 4 1 0.75 2 0 1.00 Unknown Mann et al.
gigas (Pacific (bivalve) coast of China; America Nematoda (N), (1991)
oyster) Korea; Japan: (southern Alaska Trematoda (N),
59 N–22 N); to Humboldt Turbellaria (N)
lat. median: Bay, California:
41 N; lon. and 40 N–60 N);
median: 129 E lat. median:
50 N; lon. and
median: 125 W
Continued
Distance
Crassostrea CGEUR Oyster Asia (Russia; east Western Europe 7964 Copepoda (N, I), Oysters 1960 4 6 0.50 2 2 0.00 Seems to be little Mann et al.
gigas (Pacific (bivalve) coast of China; (Exe Estuary, Nematoda (N), suggestion of (1991),
oyster) Korea; Japan: Great Britain; Polychaeta (I), overall parasite Aguierre-
59 N–22 N); Wadden Sea; Trematoda (N, release given Macedo and
lat. median: France; I), Turbellaria many ‘native’ Kennedy (1999),
41 N; lon. and Netherlands; (N, I) parasites that also Krakau et al.
median: 129 E Belgium; infect it in its (2006), Troost
Germany; introduced (2010), Elsner
Denmark; regions et al. (2011), and
Sweden; Thieltges et al.
Norway: (2012)
65 N–44 N);
lat. median:
55 N; lon. and
median: 8 E
Crassostrea CGNZ Oyster Asia (Russia; east New Zealand 10,129 Copepoda (N, I), Ballast 1950 4 4 0.00 2 0 1.00 Unknown Dinamami
gigas (Pacific (bivalve) coast of China; (46 S–34 S); lat. Nematoda (N, I), water/hull (1987)

oyster) Korea; Japan: median: 40 S; Trematoda (N), fouling
59 N–22 N); lon. and median: Turbellaria (N, I)
lat. median: 175 E
41 N; lon. and
median: 129 E
Crepidula CF Snail Eastern North Europe (Norway 5947 None in native Oysters 1870 0 0 N/A N/A N/A N/A N/A Pechenik et al.
fornicata (Gastropoda) America to and introduced (2001) and
(common (Newfoundland Mediterranean: Thieltges et al.
slipper shell)* to Gulf of 60 N–36 N); (2006)
Mexico: lat. median:
48 N–25 N); 48 N; lon. and
lat. median: median: 1 W
37 N; lon. and
median: 75 W
Cyclope neritea CN Snail Iberian Bay of Biscay, 782 Trematoda (N, I) Oysters 1970 6 3 0.50 6 3 0.50 Suggestion the Bachelet et al.
(Gastropoda) Peninsula; France (48 N– snail has a greater (2004)

Mediterranean 43 N); lat. ability to acquire
(42 N–36 N); median: 46 N; food than the
lat. median: lon. and median: native mudsnail
39 N; lon. and 1 W with which it
median: 0 W competes
(exploitative
competition)
Ensis EA Clam Eastern North Northern 5530 Trematoda (N, I) Ballast 1970 >1? 4 N/A >1? 4 N/A Unknown Thieltges et al.
americanus (bivalve) America Europe water/hull (2006), Krakau
(¼directus) (Labrador to (northern fouling et al. (1986), and
(Atlantic razor South Carolina: Wadden Sea; Armonies and
clam)* 53 N–32 N); North Sea; Sylt, Reise (1999)
lat. median: Germany:
43 N; lon. and 57 N–53 N);
median: 70 W lat. median:
55 N; lon. and
median: 8 E
Fistularia FC Fish Red Sea Mediterranean 2768 Cestoda (I), Suez canal 2000 8 5 0.38 6 2 0.67 Unknown Pais et al. (2007)
commersonii (Osteichthyes) (30 N–12 N); Sea Isopoda (I),
(bluespotted lat. median: (44 N–30 N); Nematoda (I),
cornet fish) 21 N; lon. and lat. median: Trematoda (N, I)
median: 38 E 37 N; lon. and
median: 16 E
Haminoea HJ Snail Asia (Japan; Western North 9552 Trematoda (I); Oysters 1990 ? 1 N/A ? 1 N/A Unknown Brant et al.
japonica (Gastropoda) Korea; Thailand: America cannot find any (2010)
(Japanese 45 N–13 N); (Washington; record of studies
bubble snail)* lat. median: San Francisco on native
29 N; lon. and Bay, California: parasites
median: 122 E 48 N–37 N);
lat. median:
43 N; lon. and
median: 124 W
Continued
Distance
Hemigrapsus HS Crab Asia (Japan; Eastern North 10,167 Acanthocephala Ballast 1980 8 2 0.75 5 0 1.00 Suggestion that Blakeslee et al.
sanguineus (Crustacea) Russia: America (Maine (I), Nematoda water/hull parasite escape (2009),
(Asian shore 60 N–30 N); to Carolinas: (I), Microspora fouling may make it a Christiansen
crab) lat. median: 44 N–33 N); (N), better et al. (2009), and
45 N; lon. and lat. median: Rhizocephala competitor; McDermott
median: 137 E 39 N; lon. and (N), Trematoda however, no (2011)
median: 74 W (N) empirical
evidence
Ilyanassa IO Snail Eastern North Western North 4024 Trematoda (N, I) Oysters 1900 9 5 0.44 9 5 0.44 Unknown Curtis (1997) and
obsoleta (Gastropoda) America (Saint America Blakeslee et al.
(Eastern Lawrence, (Boundary Bay, (2012)
mudsnail) Canada to British
Georgia: Columbia;
48 N–29 N); Willapa Bay,
lat. median: Washington; San
39 N; lon. and Francisco Bay,
median: 74 W California:
49 N–37 N);
lat. median:
46 N; lon. and
median: 123 W
Littorina LLENA Snail Europe (White Eastern North 5144 Trematoda (N, I) Dry ballast 1840 11 5 0.55 11 5 0.55 Suggestions of Blakeslee and
littorea (Gastropoda) Sea, Russia to America exploitative Byers (2008)
(common Portugal: (Labrador to competition
periwinkle) 70 N–40 N); Delaware Bay: with native
lat. median: 51 N–38 N); periwinkles and
55 N; lon. and lat. median: other native
median: 8 E 45 N; lon. and snails
median: 66 W
Littorina LLWNA Snail Europe (White Western North 8728 Trematoda (N, I) Deliberate 1960 11 1 0.91 11 1 0.91 Unknown Chang et al.
littorea (Gastropoda) Sea, Russia to America (San introduction (2011) and
(common Portugal: Francisco Bay, Blakeslee,
periwinkle) 70 N–40 N); California); lat. unpublished
lat. median: median: 37 N;
55 N; lon. and lon. and median:
median: 8 E 122 W
Littorina LS Snail Northeastern Western North 4678 Trematoda (N, I) Live trade 1990 14 3 0.79 14 3 0.79 Unknown Blakeslee et al.
saxatilis (Gastropoda) N. America America (San (algal packing (2012)
(rough (Labrador to Francisco Bay, materials)
periwinkle) Long Island, California:
New York; 37 N); lat.
64 N–40 N); median: 37 N;
lat. median: lon. and median:
52 N; lon. and 122 W
median: 65 W
Lutjanus fulvus LF Fish French Polynesia Hawaiian 4182 Acanthocephala Aquaculture 1950 27 16 0.41 4 1 0.75 Possible Vignon et al.
(blacktail (Osteichthyes) (17 S); lat. Archipelago (N), Cestoda (N, individual and (2009b)
snapper) median: 17 S;
(22 N–18 N); I), Copepoda (N, population-level
lon. and median: lat. median: I), Hirudinea effects
149 W 20 N; lon. and (N), Isopoda (N),
median: 156 W Monogenea (N,
I), Nematoda (N,
I), Trematoda
(N, I)
Lutjanus LK Fish French Polynesia Hawaiian 4182 Cestoda (N, I), Aquaculture 1950 19 16 0.16 2 1 0.50 Possible Vignon et al.
kasmira (Osteichthyes) (17 S); lat. Archipelago Copepoda (N, I), individual and (2009)
(common median: 17 S; (22 N–18 N); Hirudinea (N), population-level
bluestripe lon. and median: lat. median: Isopoda (N, I), effects
snapper) 149 W 20 N; lon. and Monogenea (N,
median: 156 W I), Nematoda (N,
I), Trematoda
(N, I)
Metacarcinus MN Crab New Zealand southern 2588 Trematoda (N) Oysters 1880 1 0 1.00 1 0 1.00 Unknown Kuris and
novaezelandiae (Crustacea) (46 S–34 S); lat. Australia & Gurney (1997) in
(Pie crust median: 40 S;
Tasmania (43 S– Torchin et al.
crab) lon. and median: 33 S); lat. (2002) and
175 E median: 38 S; Torchin and
lon. and median: Lafferty (2009)
145 E
Mnemiopsis ML Ctenophore Eastern North Black Sea; 9027 Amphipoda (N), Ballast 1980 4 2 0.50 1 0 1.00 Unknown Torchin et al.
leidyi (Atlantic (Tentaculata) America (New Mediterranean Cnidaria (N, I), water/hull (2002) and
ctenophore) York to Florida: Sea; Baltic Sea; Nematoda (N, I), fouling Selandar et al.
40 N–26 N); North Sea Trematoda (N) (2010)
lat. median: (57 N–31 N);
33 N; lon. and lat. median:
median: 78 W 44 N; lon. and
median: 34 E
Continued
Distance
Musculista MS Mussel Asia (Russia; New Zealand 9651 Copepoda (N, I) Aquaculture/ 1980 3 1 0.67 N/A N/A N/A Unknown Miller et al.
senhousia (bivalve) Korea; Japan; (46 S–34 S); lat. Oysters (2008)
(Asian date China; median: 40 S;
mussel) Singapore: lon. and median:
60 N–1 N); lat. 175 E
median: 31 N;
lon. and median:
121 E
Mya arenaria MA Clam Eastern North Europe 5530 Copepoda (N), Vikings? 1240 4 4 0.00 3 3 0.00 Unknown Thieltges et al.
(soft shell (bivalve) America (northern Nematoda (I), (2006)
clam) (Labrador to Wadden Sea: Trematoda (N,
South Carolina: 57 N–53 N); I), Turbellaria (I)
54 N–32 N); lat. median:
lat. median: 55 N; lon. and
43 N; lon. and median: 8 E
median: 70 W
Paralithodes PC Crab North Pacific; Barents Sea 5696 Acanthocephala Deliberate 1960 8 5 0.38 N/A N/A N/A Unknown Hawkes et al.
camtschaticus (Crustacea) Alaska (71 N– (76 N–67 N); (N, I), Bivalvia introduction (1986), Sparks
(Red king 34 N); lat. lat. median: (I), Copepoda and Morado
crab) median: 53 N; 72 N; lon. and (N, I), Nemertea (1987), Kuris
lon. and median: median: 24 E (N, I), Isopoda et al. (1991),
160 E (N), Jansen et al.
Rhizocephala (1998), and
(N), Turbellaria Hemmingsen
(I) et al. (2005)
Poecilia PL Fish Atlantic and Gulf Global (New N/A Copepoda (N), Aquarium 1950 19 1 0.95 15 1 0.93 Unknown Torchin et al.
latipinna (Osteichthyes) Coast drainages Zealand; Isopoda (N), releases, (2002)
(Sailfin molly) (Cape Fear, Western North Monogenea (N), biocontrol
North Carolina America; Nematoda (N),
to Veracruz, Hawaii; Trematoda (N, I)
Mexico: Philippines;
35 N–19 N); Singapore;
lat. median: Australia; Puerto
27 N; lon. and Rico)
median: 87 W
Ruditapes RP Clam Indo-Pacific Europe (France: 9894 Trematodes (N, Oysters 1970 10 4 0.60 10 4 0.60 Dang et al. Rybakov (1983),
philippinarum (bivalve) (40 N–1 N); lat. 48 N–43 N); I) (2009) suggest Rybakov and
(Manila clam) median: 21 N; lat. median: little evidence for Mamaev (1987),
lon. and median: 45 N; lon. and enemy release; Hua (1989), Mei
110E median: 1 W however, not a (1994), Lee et al.
clear (2001), Park et al.
understanding of (2008), Dang
native trematode et al. (2009), and
loads Yanagida et al.
(2009)
Siganus SR Fish Red Sea (30 N– Mediterranean 2768 Acanthocephala Suez canal 1920 23 8 0.65 6 0 1.00 Suggestion that Dang et al.
rivulatus (Osteichthyes) 12 N); lat. Sea (44 N– (N), Amoebida release from (1999) and
(Rabbitfish) median: 21 N; 30 N); lat. (N, I), parasitism has Torchin and
lon. and median: median: 37 N; Ciliophora resulted in high Lafferty (2009)
38 E lon. and median: (N, I), abundance in
16 E Diplomonadida Mediterranean
(N, I),
Microspora (N,
I), Monogenea
(N, I), Myxozoa
(N, I), Nematoda
(N), Trematoda
(N)
The papers listed in this table were ones that included information on marine host and metazoan parasite invasion and also included information for taxonomic richness of parasites; in some cases, there was insufficient information in either the source or the
founding populations to perform statistical analyses on parasite escape—those studies are noted with an*. In the first column, the host species is listed, followed by host abbreviation (abbr) in the second column, and then host taxa in the third column; in the
fourth column is the known native (source) range (host and parasite) including latitude range, latitude median, and longitude and latitude median (see Section 2); in the fifth column is the known introduced (founding) range (host and parasite) including
latitude range, latitude median, and longitude and latitude median; next the distance (km) between native and introduced range in the sixth column; the parasite taxa and whether it is reported in the native range only (N), the introduced range only, or both
native and introduced ranges (N, I) in the seventh column; the vector type (host and parasite) in the eighth column; the decade of introduction (host) in the ninth column; the number of native parasite taxa (all parasites) in the tenth column; the number of
introduced parasite taxa (all parasites) in the eleventh column; the index of parasite escape (all parasites) in the twelfth column; the number of native parasite taxa (trematodes) in the thirteenth column; the number of introduced parasite taxa (trematodes) in the
fourteenth column; the index of parasite escape (trematodes only) in the fifteenth column; evidence of parasite release (if applicable) in the sixteenth column; and citation sources in the seventeenth column.
1. that we would continue to detect a significant effect of parasite escape

across host taxa in marine systems but that some parasite groups would
be more likely to contribute to that escape than others;
2. that we would find some geographic factors to influence parasite escape,
especially distance between source and recipient regions;
3. that parasite escape would correlate with time since introduction;
4. that some introduction vectors would promote higher levels of parasite
escape than others, and this would be influenced by their vector
strength;
5. that the degree of parasite escape may be correlated with host taxa, given
association of some host taxa with pathways of invasion that may result in
higher versus lower escape;
6. that we would observe interactions among these factors, given the com-
plex nature of invasion pathways and their numerous variables.
Below, we describe our data collection methodologies and analyses, includ-
ing potential mechanistic factors that may help explain parasite escape based
on our hypotheses. Moreover, we briefly evaluate evidence for parasite
release in the studies in our database, though our primary emphasis is on sig-
natures of parasite escape.
2. METHODS
2.1. Data sources
To assess parasite escape and release in marine and estuarine hosts, we
searched the Web of Science, Google Scholar, Springer, PubMed, and JSTOR
for publications by using the following key search terms: invas*, intro*,
marine*, estuarine*, and parasit*. Where appropriate, we also reviewed lit-
erature citations for any relevant papers not identified in our online database
searches. Collectively, this search identified 52 relevant publications
addressing parasite escape and/or parasite release for 34 marine and estuarine
host–parasite systems. We then further culled publications by focusing on
those that provided information on metazoan parasite taxonomic richness
(to lowest taxonomic level) from native and introduced ranges of host spe-
cies. In some cases, this information was in the same publication; in other
cases, we had to do additional research to obtain parasite taxonomic richness
in both ranges (typically this was required for the native range). This step
reduced our relevant list to 31 host–parasite systems from around the globe;
however, in some of these cases, there were repeated species that invaded
different regions around the globe (e.g. Carcinus maenas’ multiple
introductions including Atlantic and Pacific North America, South

Africa, Japan, and Australia; Littorina littorea introductions to Atlantic and
Pacific North America; and Crassostrea gigas introductions to Pacific North
America, western Europe, and New Zealand; see Table 2.1). Altogether,
there were 24 unique hosts included in our study.
Though we attempted to be as exhaustive in our search as possible, we
recognize that accidental omissions of other relevant studies are possible, and
that our search was partially limited by the restriction to studies published in
and/or translated into English. Altogether, we believe we captured the bulk
of the studies that presently exist on the subject, and thus, our work should
provide a good representation of marine parasite escape across systems
worldwide.
2.2. Data extraction

For each host–parasite system, we extracted the following information from
the publications, online databases (e.g. Encyclopedia of Life, the USGS
Nonindigenous Aquatic Species database, the Global Invasive Species Database,
FishBase, the National Exotic Marine and Estuarine Species Information System),
or regional websites that report biogeographic information:
• Host and parasite identification to lowest taxonomic level: For hosts, species
were identified in publications; for parasites, we focused on metazoans
identified to the lowest taxonomic level.
• Host and parasite taxa: Larger taxonomic groups of hosts and parasites. For
hosts, we used the class level of classification; for parasites, we used the
classification (often to class or order level) provided in published works.
• Native and introduced region and latitude and longitude: Median whole num-
ber latitude was calculated from the most northern and southern extents
of the host’s native and invasive ranges, and longitude was classified at the
median latitude point or, if within an enclosed sea, the median longitude
point within that sea.
• Distance (km) between source (native) and recipient (introduced) regions: Using
median whole number latitude and longitude values, we calculated dis-
tance between source and recipient ranges using NOAA’s latitude/
longitude distance calculator (http://www.nhc.noaa.gov/gccalc.shtml).
• Introduction vector: Hosts were categorized into the following bins based
on their vector type:
• APM—association with algal packing materials for live bait
and trade.
• AQC—introductions associated with nonoyster aquaculture

• BWF—ballast water and/or hull fouling associated with ballast water
carrying vessels
• CANAL—accidental introduction following the creation of a canal,
connecting two previously unconnected bodies of water
• DEL—deliberate introductions not associated with aquaculture (eg.
research or biocontrol).
• DBF—dry ballast and/or fouling associated with dry/rock ballast-
carrying vessels
• OYS—introductions associated with oyster transplantation. We sep-
arated out oyster aquaculture as its own grouping because of the
numerous introductions that have been specifically associated with
oyster transplantation around the world (e.g. Cohen and Carlton,
1995; Ruesink et al., 2005).
• Vector strength: Table 2.2 provides detail on how we defined ‘vector
strength’ for each vector, providing us with a rough characterization
of the entrainment, transport, and establishment likelihood (i.e. compo-
nents of the invasion process; Kolar and Lodge, 2001; Ruiz and Carlton,
2003) of hitchhiking parasite species for each host–parasite system in our
study. In particular, we assessed vector strength based on the following
categories: (a) whether a vector transports adults and/or juveniles and/or
larvae; (b) whether introduction ‘attempts’ would be considered fre-
quent and numerous, moderately numerous, or infrequent and few;
(c) whether the selectivity and transport of hosts entrained in a vector
would be targeted and contain numerous propagules, moderately
targeted with some propagules, or untargeted and few propagules; and
(d) whether transport time for a vector would be short, moderate, or
long. We populated Table 2.2 based on our understanding of these vec-
tor attributes from numerous studies in the literature (e.g. Colautti et al.,
2006; Johnston et al., 2009; Kolar and Lodge, 2001; Miller and Ruiz,
2009; Ruiz and Carlton, 2003), though we acknowledge that these
values are intrinsically qualitative and only provide a ‘rough’ and general
characterization of vector strength. Moreover, we based our assessments
of these various attributes with parasite introduction in mind, and some
may differ from what would be attributed to free-living species. Alto-
gether, assigning values to each of these attributes allowed us to calculate
a whole number vector strength value (ranging from 1 to 3) for each vec-
tor, which we used as an independent categorical variable in our
analyses.
Table 2.2 The seven main marine introduction vectors identified in our investigation and the various attributes of those vectors that
influence vector strength and likelihood for successful entrainment, transport, and establishment of hitchhiking parasites in novel marine
environments
Targeted/numerous
propagules (3),
Adults, juveniles, and larvae Frequent and numerous moderately
(3); adults and juveniles (3); attempts (3), moderately targeted/some Vector transport
adults (3); juveniles (2); numerous attempts (2), propagules (2), time: short (3), Average
Juveniles and larvae (2); infrequent and few untargeted/few moderate (2), across Vector
Vector larvae (1) attempts (1) propagules (1) long (1) attribute strength
APM Adults and juveniles (3) Moderate (2) Untargeted (1) Short (3) 2.25 2
AQC Adults and juveniles (3) Frequent (3) Targeted (3) Moderate (2) 2.75 3
BWF Larvae (1) Moderate (2) Untargeted (1) Moderate (2) 1.5 1
CANAL Adults, juveniles, and Moderate (2) Moderately targeted (2) Moderate (2) 2.25 2
larvae (3)
DEL Adults and juveniles (3) Frequent (3) Targeted (3) Moderate (2) 2.75 3
DBF Adults and juveniles (3) Moderate (2) Moderately targeted (2) Long (1) 2 2
OYS Adults and juveniles (3) Frequent (3) Targeted (3) Moderate (2) 2.75 3
Assigned values range from 1 to 3, where 1 ¼ low strength; 2 ¼ moderate strength; 3 ¼ high strength. The first column provides the acronym for the vector (see Section 2).
The second column assigns a numerical value (1–3) depending on whether the vector carries primarily adults and/or juveniles and/or larvae. Because parasites are typ-
ically introduced via adult hosts, we considered vectors that introduce adults to have high strength for that attribute (3) versus those that carry larvae to have low strength
(1). The third column assesses frequent and numerous introduction ‘attempts’ via the vector as high strength (3), moderate numbers of introduction ‘attempts’ as mod-
erate strength (2), and infrequent and few introduction ‘attempts’ as low strength (1). The fourth column assesses selectivity of the vector in transporting host organisms,
and those vectors that are targeted and contain numerous propagules had high strength (3), those that are moderately targeted and contain some propagules have moderate
strength (2), and those that are untargeted with few propagules have low strength (1). The fifth column assesses vector transport time with short durations as high strength
(3), moderate durations as moderate strength (2), and long durations as low strength (1). The sixth column averages across the four prior columns, and vector strength as a
whole number is provided in the last column.
• Decade of host introduction: If multiple dates were listed, we used the earliest
recorded date and then rounded down to the decade (e.g. 1922 ¼ decade
of 1920). For this variable, we made the assumption that the host intro-
duction date equals the parasite introduction date. In some cases, this may
not be correct, especially if the host was introduced on multiple occasions
and the parasite arrived in a later introduction event; however, actual
introduction dates for the parasites themselves are typically not available
or even known. We therefore used the host’s introduction date as the best
possible understanding of introduction timing for their parasites. Intro-
duction time was explored not only as a continuous independent variable
but also as a categorical independent variable—in that, we divided intro-
duction time into three major periods: (1) prior to 1900, (2) 1900–1950,
and (3) 1950 to present. We used those categorical dates because before
1900, species invasions would have been primarily associated with older
shipping and transfer vectors (e.g. solid ballast and some oyster transloca-
tions); between 1900 and 1950, ballast water use in shipping became
more prevalent and transport processes became faster and more efficient;
and in the 1950s onwards, there was a large increase in globalization and
worldwide transport via ballast-carrying vessels (Carlton, 1992; Ruiz
et al., 2000).
• Accidental versus intentional introduction vectors: This allowed for a more
general assessment of vectors based upon whether they are accidental
(i.e. unintentional movements of species from source to recipient loca-
tions) or intentional (i.e. targeted movements of species from source to
recipient regions).
• Parasite richness for each host species in native and introduced ranges: Parasite
richness was defined as the total number of parasite taxa reported in
each range.
2.3. Data analysis

We obtained parasite richness in specific host species for both the hosts’
native (N) and introduced (I) ranges using published accounts. Using the
formula [(N I)/N], we assessed the index of parasite escape for hosts in
introduced ranges (Torchin et al., 2003). Because trematodes were the most
highly studied and common parasite group in our investigation (see
Figure 2.2), we calculated the index of parasite escape for this particular tax-
onomic parasite group as well and ran the same analyses for trematodes
(¼‘trematodes only’) as we did for all parasite groups (¼‘all parasites’). With
these two parasite groups as dependent variables, we ran numerous analyses

on our dataset using continuous mechanisms as independent variables to
produce regressions and categorical mechanisms as independent variables
in ANOVAs (see Table 2.1). We also grouped our categorical variables in
regression analyses to look for more specific correlations (e.g. grouping
by ‘host taxa’ and producing separate regression lines for each host class).
Finally, we investigated two synergistic approaches of multiple factors that
might work together to explain parasite escape, including a multiple regres-
sion analysis and a generalized linear model (GLM). We classified signifi-
cance in three categories: nonsignificant (p > 0.10), nearly significant
(0.10 < p > 0.05), and significant (p < 0.05).
3. RESULTS
3.1. Metadata based on studies from literature search
Table 2.1 details the results of our investigation of peer-reviewed literature
exploring marine parasite escape over two decades prior to (1992–2002) and
following (2003–2013) Torchin and Lafferty (2002)’s “Parasites and Marine
Invasions” (Note: there are a couple of studies that precede the last two
decades, but the vast majority fall within this time period). The table includes
several descriptors of the invasion pathway for each host–parasite as outlined
in Section 2. Overall, we identified 35 marine host–parasite invasions that
explicitly investigated parasite richness in introduced regions. Of these,
31 also included an understanding of parasite richness in the native region
such that we were able to measure parasite escape; 26 of these were also
analysed for trematode specific escape (Table 2.1).
The host taxa in our 31 studies included 6 classes [Asteroidea (sea star)
(3%), Bivalvia (bivalve) (19%), Crustacea (specifically crabs) (26%), Gas-
tropoda (snail) (23%), Osteichthyes (bony fish) (26%), and Tentaculata
(ctenophore) (3%) (Figure 2.1)]. The parasite taxa represented a total of
20 different taxonomic groups (see Table 2.3), which we proportionally
ranked in terms of the number of reports of the parasite group across all
investigations (also see Figure 2.2A–C). The four most common parasite
taxa in both native and introduced regions were Trematoda, Nematoda,
Copepoda, and Cestoda (Table 2.3; Figure 2.2). However, other taxa exem-
plified differences in their rankings between native and introduced regions;
for example, Isopoda were more common in native regions than introduced
Figure 2.1 Frequency of host taxa by class across all investigations that have intro-
duced parasites to various regions. They are ordered from highest to lowest based
on their proportion among all hosts. Fish, crabs, snails, and bivalves made up the major-
ity of host taxa that have introduced marine parasites globally.
regions, while turbellarians were reported more often in introduced than

native regions (Figure 2.2).
The studies included numerous source and recipient regions of parasite
invasion; however, the majority were from four continents: North America,
Europe, Asia, and Australia. Only one study included data from Africa, and
none from South America or Antarctica. In order of frequency, 38% came
from Asia, 31% came from Europe, 24% came from North America, and 7%
came from Australia (Figure 2.3A). Of the recipient regions, 36% were to
North America, 32% to Europe, 21% to Australia, 7% to Asia, and 4% to
South Africa (Figure 2.3B).
3.2. Parasite species richness, abundance, and escape across

investigations
Among the 31 host–parasite investigations, there was a significant reduction
in average parasite richness in the introduced regions compared to the native
regions. When including total counts, introduced regions only made up 32%
of all reported parasites (native, 139/204; introduced, 65/204; Figure 2.4A),
and when averaged across parasite taxa, the difference between native and
introduced was significantly different (p ¼ 0.050; Figure 2.4B).
When exploring individual parasite taxa, we also observed a reduction in
parasite abundance in introduced versus native regions, whereby introduced
regions demonstrated a profound reduction for many of the parasite taxa,
including dominant taxa, such as acanthocephalans, cestodes, isopods, nem-
atodes, and trematodes. Some taxa were completely absent in introduced
Table 2.3 Parasite taxa (n ¼ 20) included in the 31 investigations on parasite escape
Native Introduced Total Percentage Ranking Percentage Ranking Percentage Ranking
(N) (I) (N þ I) (N) (N) (I) (I) (N þ I) (N þ I)
Trematoda 27 16 43 19.42 1 24.62 1 21.08 1
Nematoda 19 11 30 13.67 2 16.92 2 14.71 2
Copepoda 18 9 27 12.95 3 13.85 3 13.24 3
Cestoda 10 7 17 7.19 4 10.77 4 8.33 4
Acanthocephala 9 4 13 6.47 6 6.15 5 6.37 5
Isopoda 10 2 12 7.19 4 3.08 8 5.88 6
Monogenea 7 3 10 5.04 7 4.62 7 4.90 7
Turbellaria 5 4 9 3.60 10 6.15 5 4.41 8
Nemertea 6 2 8 4.32 9 3.08 8 3.92 9
Rhizocephala 7 0 7 5.04 7 0.00 n/a 3.43 10
Ciliophora 3 2 5 2.16 13 3.08 8 2.45 11
Fecampida 5 0 5 3.60 10 0.00 n/a 2.45 11
Hirudinea 4 0 4 2.88 12 0.00 n/a 1.96 13
Microspora 3 1 4 2.16 13 1.54 11 1.96 13
Myxozoa 2 1 3 1.44 15 1.54 11 1.47 15
Amoeboidae 1 1 2 0.72 16 1.54 11 0.98 16
Continued
Table 2.3 Parasite taxa (n ¼ 20) included in the 31 investigations on parasite escape—cont'd
Native Introduced Total Percentage Ranking Percentage Ranking Percentage Ranking
(N) (I) (N þ I) (N) (N) (I) (I) (N þ I) (N þ I)
Cnidaria 1 1 2 0.72 16 1.54 11 0.98 16
Amphipoda 1 0 1 0.72 16 0.00 n/a 0.49 18
Crustacea 1 0 1 0.72 16 0.00 n/a 0.49 18
Polychaeta 0 1 1 0.00 n/a 1.54 11 0.49 18
Here, the number of reports for each taxa across all 31 investigations is listed for native regions only (N), introduced regions only (I), and the total for N þ I. Then the
percentage out of the whole for each taxa and its ranking based on that percentage is listed for native only (N), introduced only (I), and both native and introduced (N þ I).
The rankings are the same for the first four dominant parasite taxa, but they change for the later rankings for native only and introduced only, especially for the latter
where several groups are not represented. Of the 20 parasite taxa for N þ I, 19 of those 20 are represented in the native regions, while just 15 of the 20 are in the introduced
regions.
Figure 2.2 Proportion of parasite taxa across all investigations for (A) both native and
introduced, (B) just native regions, and (C) just introduced regions. There is little change
for the first four parasite taxa among (A–C); however, the remainder of the taxa show
differences in proportion in native versus introduced regions.
Figure 2.3 Proportion of host–parasites (A) introduced from specific source continents
and (B) introduced to specific recipient continents across all investigations. NA ¼ North
America, EUR ¼ Europe, ASIA ¼ Asia, AUS ¼ Australia, and SA ¼ Africa (in particular, South
Africa). Asia is the continent where most parasites came from, while North America is the
continent where most parasites were reported introduced to.
Figure 2.4 Native and introduced parasite abundance recorded in 31 host–parasite

investigations for (A) the proportion of parasite taxa from all studies and (B) the average
parasite richness across investigations. In (A), the native region had many more
recorded parasites than the introduced region, and in (B), there was a significant reduc-
tion in parasite richness in the introduced regions compared to the native regions
(p<0.05).
regions, such as rhizocephalans. Overall, most hosts exhibited >50% escape

across parasite taxa, but there was some variability across parasite taxa; that is,
some showed much less escape than others (e.g. cestodes and turbellarians),
while others showed complete escape (e.g. hirudinids and rhizocephalans)
(Figure 2.5A and B). When parasite escape was averaged across all taxa,
the index of parasite escape for all hosts was 0.575 (standard error ¼ 0.074).
3.3. Mechanistic factors influencing parasite escape

In our study, we investigated several potential mechanisms that might
explain differences in parasite escape. Each analysis is distinguished by a spe-
cific subheading in the succeeding text; within each subheading, we report
numerous results of these various analyses but focus in particular on those
that demonstrated interesting and/or significant trends. Analyses are orga-
nized within Table 2.4, which lists each analysis explored; R2 values
Figure 2.5 Parasite taxa from 31 host–parasite investigations for (A) total reported num-
bers of parasites among taxa across investigation in native and introduced regions and
(B) host–parasite escape for specific parasite taxa. For almost all species, there was a
large reduction in reported numbers in the introduced region compared to the native
region, and for some taxa, no reports exist in introduced regions, which is also exem-
plified in (B) where complete escape exists for some parasite taxa.
Table 2.4 Data analyses and statistical results

Nonsignificant,
nearly significant,
Analyses R2 p significant Figure
Parasite richness/abundance (general)
Source (native) richness–recipient 0.05 Significant 2.4B
(introduced) richness
Geographic explorations (general)
Source (native) latitude–parasite 0.002 0.784 Nonsignificant 2.6A
escape (‘all parasites’)
Source (native) latitude–parasite 0.00008 0.888 Nonsignificant 2.6C
escape (‘trematodes only’)
Source (native) longitude–parasite 0.0003 0.949 Nonsignificant 2.6B
Source (native) longitude–parasite 0.024 0.447 Nonsignificant 2.6D
Recipient (introduced) latitude– 0.064 0.177 Nonsignificant 2.6E
parasite escape (‘all parasites’)
Recipient (introduced) latitude– 0.153 0.053 Nearly significant 2.6G
parasite escape (‘trematodes only’)
Recipient (introduced) longitude– 0.0001 0.931 Nonsignificant 2.6F
Recipient (introduced) longitude– 0.033 0.384 Nonsignificant 2.6H
Distance between source and 0.02 0.453 Nonsignificant n/a
recipient regions (km)–parasite
Distance between source and 0.102 0.120 Nonsignificant n/a
recipient regions (km)–parasite
Time (general)
Decade of introduction and 0.006 0.683 Nonsignificant n/a
Decade of introduction and 0.03 0.404 Nonsignificant n/a
Categorical introduction time and n/a 0.830 Nonsignificant 2.7A
Table 2.4 Data analyses and statistical results—cont'd

Nonsignificant,
nearly significant,
Categorical introduction time and n/a 0.206 Nonsignificant 2.7B
Significant and nearly significant
post-hoc pairwise comparisons
(host taxa, ‘trematodes only’):
<1900–1900–1950 n/a 0.096 Nearly significant 2.7B
Host taxa (general and specific)
Host taxa–parasite escape (‘all n/a 0.040 Significant 2.8A
parasites’)
(host taxa, ‘all parasites’):
Bivalve–crab n/a 0.002 Significant 2.8A
Bivalve–snail n/a 0.022 Significant 2.8A
Bivalve–fish n/a 0.040 Significant 2.8A
Host taxa–parasite escape n/a 0.125 Nonsignificant 2.8B
(‘trematodes only’)
(host taxa, ‘trematodes only’):
Bivalve–crab n/a 0.019 Significant 2.8B
Snail–crab n/a 0.081 Nearly significant 2.8B
Regressions, grouped by host taxa,
of distance between source and
recipient regions and parasite
escape (‘all parasites’):
Bivalve 0.081 0.585 Nonsignificant 2.9A
Crab 0.01 0.811 Nonsignificant 2.9A
Fish 0.016 0.785 Nonsignificant 2.9A
Snail 0.537 0.061 Nearly significant 2.9A
Continued

Nonsignificant,
nearly significant,
of distance between source and
escape (‘trematodes only’):
Bivalve 0.366 0.280 Nonsignificant 2.9B
Crab 0.117 0.452 Nonsignificant 2.9B
Fish 0.305 0.335 Nonsignificant 2.9B
Snail 0.537 0.061 Nearly significant 2.9B
of time and parasite escape
(‘trematodes only’):
Bivalve 0.321 0.433 Nonsignificant 2.9C
Crab 0.596 0.042 Significant 2.9C
Fish 0.141 0.464 Nonsignificant 2.9C
Snail 0.189 0.329 Nonsignificant 2.9C
Introduction vector (general and
specific)
Vector–parasite escape n/a 0.488 Nonsignificant 2.11A
(‘all parasites’)
Vector–parasite escape (‘trematodes n/a 0.041 Significant 2.11B
only’)
Significant and nearly significant n/a
(vector, ‘trematodes only’):
BWF–OYS n/a 0.014 Significant 2.11B
Regressions, grouped by vector, of
recipient latitude and parasite
AQC 0.75 0.333 Nonsignificant 2.12A
BWF 0.03 0.710 Nonsignificant 2.12A
DBF 0.985 0.078 Nearly significant 2.12A
OYS 0.519 0.107 Nonsignificant 2.12A

Nonsignificant,
nearly significant,
distance between source and
AQC 0.75 0.330 Nonsignificant 2.12B
BWF 0.714 0.018 Significant 2.12B
DBF 0.987 0.073 Nearly significant 2.12B
OYS 0.008 0.860 Nonsignificant 2.12B
time and parasite escape (‘all
parasites’):
AQC 0.353 0.405 Nonsignificant 2.12C
BWF 0.443 0.072 Nearly significant 2.12C
DBF 0.318 0.619 Nonsignificant 2.12C
OYS 0.148 0.390 Nonsignificant 2.12C
Vector strength, accidental versus intentional introduction vectors (general and
specific)
Vector strength–parasite escape n/a 0.721 Nonsignificant 2.13A
(‘all parasites’)
Vector strength–parasite escape n/a 0.154 Nonsignificant 2.13B
(Vector strength, ‘trematodes
only’):
1 (low)–3 (high) n/a 0.056 Nearly significant 2.13B
Regressions, grouped by vector
strength, of distance between
source and recipient regions and
parasite escape (‘trematodes only’):
1 (low) 0.968 0.0004 Significant 2.14A
2 (moderate) 0.188 0.322 Nonsignificant 2.14A
3 (high) 0.00005 0.983 Nonsignificant 2.14A
Continued

Nonsignificant,
nearly significant,
Regressions, grouped by vector
strength, of time and parasite
escape (‘all parasites’):
1 (low) 0.541 0.060 Nearly significant 2.14B
2 (moderate) 0.0007 0.954 Nonsignificant 2.14B
3 (high) 0.116 0.196 Nonsignificant 2.14B
Accidental/intentional–parasite n/a 0.122 Nonsignificant 2.15A
Accidental/intentional–parasite n/a 0.175 Nonsignificant 2.15B
Regressions, grouped by
accidental/intentional, of recipient
latitude and parasite escape (‘all
parasites’):
Accidental 0.228 0.084 Nearly significant 2.16A
Intentional 0.008 0.756 Nonsignificant 2.16A
accidental/intentional, of recipient
latitude and parasite escape
(‘trematodes only’):
Accidental 0.017 0.675 Nonsignificant 2.16B
Intentional 0.305 0.078 Nearly significant 2.16B
accidental/intentional, of distance
and parasite escape (‘all parasites’):
Accidental 0.272 0.056 Nearly significant 2.16C
Intentional 0.013 0.689 Nonsignificant 2.16C
accidental/intentional, of distance
and parasite escape (‘trematodes
only’):
Accidental 0.305 0.050 Significant 2.16D
Intentional 0.032 0.596 Nonsignificant 2.16D

Nonsignificant,
nearly significant,
accidental/intentional, of time and
parasite escape (‘trematodes only’):
Accidental 0.319 0.044 Significant 2.16E
Intentional 0.128 0.254 Nonsignificant 2.16E
Multiple stepwise regression
Distance between source and recipient 0.195 0.013 Significant n/a
regions–decade of introduction–host
taxa–introduction vector–vector
strength (‘all parasites’)
Host taxa (crabs and snails and fish– n/a 0.013 Significant n/a
bivalves)
Recipient latitude–distance between 0.412 0.003 Significant n/a
source and recipient regions–decade of
introduction–host taxa–introduction
vector–vector strength (‘trematodes
only’)
Vector (AQC&DBF&OYS-BWF) n/a 0.009 Significant n/a
Host taxa (bivalves and snails and n/a 0.036 Significant n/a
fish–crabs)
Generalized linear model
Significant and nearly significant interactions:
Decade of introduction vector (‘all n/a 0.089 Nearly significant n/a
parasites’)
Decade of introduction vector n/a 0.027 Significant n/a
strength (‘all parasites’)
Decade of introduction accidental/ n/a 0.048 Significant n/a
intentional vectors (‘all parasites’)
Decade of introduction vector n/a 0.011 Significant n/a
Decade of introduction host taxa n/a 0.036 Significant n/a
Decade of introduction accidental/ n/a 0.033 Significant n/a
intentional vectors (‘trematodes only’)
Continued

Nonsignificant,
nearly significant,
Vector host taxa (‘trematodes only’) n/a 0.022 Significant n/a
Decade of introduction vector host n/a 0.083 Nearly significant n/a
taxa (‘trematodes only’)
Distance between source and recipient n/a 0.070 Nearly significant n/a
regions host taxa (‘trematodes only’)
The first column lists the specific analyses that were run, the R2 for regressions, the p value of the statistical
test, and whether it was considered nonsignificant (when p is greater than 0.10), nearly significant (when p
was greater than 0.05 and less than 0.10), and significant (when p was less than 0.05). We also list the
corresponding figure for each analysis (if applicable).
(if applicable); p value; whether results were statistically nonsignificant,

nearly significant, or significant; and the corresponding figure (if applicable).
3.3.1 Host–parasite geography

The following data regress parasite escape for ‘all parasites’ and ‘trematodes only’
with geographic measures to look for general patterns across host–parasite inves-
tigations. Specifically, we constructed regressions of parasite escape for both
source (native) region latitude and longitude (Figure 2.6A–D), as well as recip-
ient (introduced) region latitude and longitude (Figure 2.6E–H). For source
regions, we found neither a latitudinal nor longitudinal correlation with parasite
escape for ‘all parasites’ nor for ‘trematodes only’ (Table 2.4). For recipient
regions, we found no correlation between latitude/longitude and parasite escape
for ‘all parasites’ nor for ‘trematode only’ longitude (Table 2.4), except for a
slight and nearly significant negative trend with latitude for the ‘trematode
only’ parasite escape regression (R2 ¼ 0.153, p ¼ 0.053). Finally, we explored
whether parasite escape might be affected by distance between source and
recipient regions and found no correlation among ‘all parasites’ nor ‘trematodes
only’ (Table 2.4).
3.3.2 Time since introduction

We used time (decade of host introduction) as a continuous variable and also as a
categorical variable (<1900, 1900–1949, 1950 to present; refer to Section 2) for
‘all parasites’ and ‘trematodes only’. In our regression of time and parasite
escape, there were no apparent trends for either ‘all parasites’ or ‘trematodes
only’. When we explored time in a categorical sense, neither ‘all parasites’
Figure 2.6 Latitudinal (A, C, E, and G) and longitudinal (B, D, F, and H) explorations of
parasite escape for all parasites (A, B, E, and F) and trematodes only (C, D, G, and H) from
source (native) and recipient (introduced) regions. Latitude moves from south to north,
and longitude moves from west to east. There is no latitudinal nor longitudinal corre-
lation with parasite escape in source regions, and there was little to no correlation
between recipient latitude and longitude and parasite escape for all parasites and trem-
atodes, except for trematode escape and latitude, where there was a nearly significant
negative trend between latitude and parasite escape.
Figure 2.7 Parasite escape for (A) ‘all parasites’ (B) trematodes by categorical date of
introduction (earlier than 1900, <1900; between 1900 and 1949; and from 1950 to pre-
sent). There was no overall significant effect in either (A) or (B); however, in post-hoc
tests, there was a nearly significant pairwise comparison between <1900 and
1900–1950 for ‘trematodes only’ (represented by *).
nor ‘trematodes only’ showed a significant trend; however, in pairwise Stu-

dent’s post-hoc comparisons, <1900 exemplified a nearly significant decline
in parasite escape compared to 1900–1950 (p ¼ 0.096; Figure 2.7; Table 2.4).
3.3.3 Host taxa

Overall, there were six classes of host taxa that were reported to have intro-
duced parasites (Figure 2.8); however, only four of them were dominant:
Bivalvia (bivalves), Crustacea (specifically crabs), Gastropoda (snails), and
Osteichthyes (bony fish). In general, host taxa had a significant influence
on parasite escape for ‘all parasites’ ( p ¼ 0.040), but not for ‘trematodes only’
(p ¼ 0.125). In pairwise post-hoc analyses (Student’s t), bivalves showed
Figure 2.8 The influence of host taxa on parasite escape for (A) ‘all parasites’ and (B)
‘trematodes only’. For ‘all parasites’, bivalves showed significantly lower parasite escape
than other host taxa (crabs, fish, and snails). In ‘trematodes only’, bivalves were signif-
icantly lower than crabs, and there was a nearly significant difference between crabs
and snails, represented by the *.
significantly lower parasite escape than all other host taxa for ‘all parasites’, but
just significantly lower than crabs in the trematode only investigation
(Figure 2.8A and B).
When we grouped by host taxa and regressed source and recipient lati-
tude/longitude with parasite escape, we revealed no significant correlations
(data not reported). However, explorations with distance for both ‘all
parasites’ and ‘trematodes only’ revealed a couple interesting trends
(Figure 2.9A and B). In particular, snails demonstrated a nearly significant pos-
itive relationship between parasite escape and distance for ‘all parasites’
(R2 ¼ 0.537, p ¼ 0.061) and ‘trematodes only’ (R2 ¼ 0.537, p ¼ 0.061) with
no significant correlations for the other three taxa. Moreover, investigations
of time for ‘trematodes only’ demonstrated a significant positive correlation
between decade of introduction and trematode parasite escape for crabs
(R2 ¼ 0.596, p ¼ 0.042), but not the other host taxa (Table 2.4; Figure 2.9C).
Figure 2.9 The influence of host taxa on parasite escape and distance between source
and recipient regions for (A) ‘all parasites’ and (B) ‘trematodes only’, and (C) decade of
introduction for ‘trematodes only’. The red line represents bivalves; green ¼ crustacean;
blue ¼ fish; and purple ¼ gastropod. None of the regressions grouped by host taxa
showed a significant correlation, except for snails, which demonstrated a nearly signif-
icant positive relationship between parasite escape and distance for both (A) and (B).
For the time regressions (C), only crustaceans showed a significant positive correlation
between decade of introduction and escape from trematode parasites.
3.3.4 Vector of introduction/vector strength/accidental versus

intentional vectors
We recognized seven distinct vectors of introduction for the host–parasite
systems in our study as outlined in Section 2. Here, we describe the results
of our analyses that were based on these seven vectors and also our charac-
terization of vector strength and accidental versus intentional vectors.
3.3.4.1 Introduction vector

Overall, we found BWF and OYS to be the most prominent vectors of
introduction in our study for both ‘all parasites’ and ‘trematodes only’.
AQC was also an important host introduction vector, while the other four
vectors of introduction were less important for introducing hosts
Figure 2.10 The proportion of vectors introducing hosts for (A) ‘all parasites’ and (B)
‘trematodes only’. In both cases, the greatest proportion of introduced hosts was
through BWF, followed by OYS and AQC. For ‘all parasites’, this was then followed by
DEL, DBF, CANAL, and APM. For ‘trematodes only’, it was DBF, DEL, and APM.
(Figure 2.10). In our analyses exploring vector and parasite escape, we found
no significant associations of any vector for ‘all parasites’ ( p ¼ 0.488;
Figure 2.11A). However, for ‘trematodes only’, there was a significant asso-
ciation of vector with parasite escape ( p ¼ 0.041; Figure 2.11B), which
appeared to be mostly driven by two vectors: oysters and ballast water. In
pairwise post-hoc tests, oyster vectors had significantly lower parasite escape
than ballast water (p ¼ 0.014) (Table 2.4).
We also explored potential associations between vector on parasite
escape and recipient latitude. For ‘all parasites’, there were no significant
correlations; however, for ‘trematodes only’, though nonsignificant, three
vectors displayed high R2 values: AQC (R2 ¼ 0.750, p ¼ 0.333), DBF
(R2 ¼ 0.985, p ¼ 0.078), and OYS (R2 ¼ 0.519, p ¼ 0.107) (Figure 2.12A).
Explorations of associations of vector on parasite escape and distance
between source and recipient regions for all parasites revealed no significant
regressions. However, trematodes moved via BWF and DBF showed signif-
icant (R2 ¼ 0.714, p ¼ 0.018) and nearly significant (R2 ¼ 0.987, p ¼ 0.073)
positive relationships, respectively, with the index of parasite escape increas-
ing with increasing distance between source and introduced regions
(Figure 2.12B). Finally, in investigations of parasite escape and time grouped
Figure 2.11 The influence of vector of introduction on parasite escape for (A) ‘all para-
sites’ and (B) ‘trematodes only’. Blue ¼ BWF; yellow¼ APM; orange¼ DBF;
brown ¼ CANAL; and shades of red represent DEL, AQC, and OYS. For ‘all parasites’, there
was no overall significant influence of vector on parasite escape; however, for ‘trematodes
only’, there was a significant association of vector with parasite escape, which appeared to
be mostly strongly driven by the oyster and ballast water vectors, where oysters were sig-
nificantly lower than ballast water.
by vector (Figure 2.12C), we found a nearly significant correlation for BWF

for ‘all parasites’ (R2 ¼ 0.443, p ¼ 0.072), but no correlations for the other
vectors of introduction (Table 2.4). For ‘trematodes only’, there were no
significant correlations among the grouped vectors (data not shown).
3.3.4.2 Vector strength

Vector strength [1 (low), 2 (moderate), and 3 (high)] was assessed using a
semiqualitative method averaging across five attributes of a vector that we
deemed would be important in manifesting strength (Table 2.2). From low
to high, BWF averaged as 1.5 and we rounded down to a value of 1; DBF aver-
aged as 2.0; CANAL averaged as 2.25 and was rounded down to a value of 2;
APM also averaged as 2.25 and was rounded down to a value of 2; DEL averaged
as 2.75 and was rounded up to 3; AQC averaged as 2.75 and was rounded up to
3; and OYS averaged as 2.75 and was rounded up to 3.
Figure 2.12 The influence of introduction vector on parasite escape and (A) latitude in
recipient populations for ‘trematodes only’, (B) distance between source and recipient
regions for ‘trematodes only’, and (C) decade of introduction for ‘all parasites’. The green
line represents AQC; blue ¼ BWF; teal ¼ DBF; and yellow ¼ OYS. For (A), none of the
regressions grouped by vector demonstrated a significant correlation; however, AQC,
DBF, and OYS demonstrated a tight fit for their regressions (negative trends for DBF
and OYS and a positive trend for AQC); in addition, DBF represented a nearly significant
correlation. In (B), BWF demonstrated a significant positive correlation, while DBF
showed a nearly significant positive correlation between distance and parasite escape.
For (C), BWF was the only vector to demonstrate a nearly significant positive correlation
for parasite escape and time since introduction.
In our analyses of parasite escape and vector strength (Figure 2.13A and B),
neither ‘all parasites’ nor ‘trematodes only’ demonstrated significant relation-
ships (Table 2.4); however, they did both show trends for parasite escape to
decrease as vector strength increased, and post-hoc analyses revealed a nearly
significant difference in low (1) versus high (3) vector strength in the ‘trematode
only’ investigation (p ¼ 0.056). In regression analyses where we grouped by
vector strength, there was a highly significant effect for the lowest strength
(1) with distance between source and recipient regions for ‘trematodes only’,
whereby parasite escape increased with increasing distance (R2 ¼ 0.968,
p ¼ 0.0004; Figure 2.14A). In addition, for ‘all parasites’, there was a nearly
Figure 2.13 The effect of vector strength (1–3: low, moderate, and high) and parasite
escape for (A) ‘all parasites’ and (B) ‘trematodes only’. Overall, neither show a significant
relationship between parasite escape and vector strength, though both demonstrate a
decreasing trend in parasite escape as vector strength increases, and post-hoc analyses
revealed a nearly significant difference in low versus high vector strength in the ‘trem-
atodes only’ investigation, represented with the *.
Figure 2.14 The influence of vector strength on parasite escape and (A) distance
between source and recipient regions for ‘trematodes only’ and (B) decade of introduc-
tion for ‘all parasites’. For (A), the lowest vector strength (1) demonstrated a significant
relationship with distance and parasite escape, and for (B), there was a nearly significant
trend for the lowest vector strength (1), whereby parasite escape increased with time.
significant positive correlation between time and parasite escape for the lowest
vector strength (R2 ¼ 0.541, p ¼ 0.060, Figure 2.14B).
3.3.4.3 Accidental versus intentional introduction vectors

For analyses of accidental versus intentional introduction vectors, there was
no significant relationship for parasite escape in ‘all parasites’ or ‘trematodes
only’; however, both showed a trend for lower parasite escape in intentional
vectors compared to accidental vectors (Table 2.4; Figure 2.16A and B). The
effect of accidental versus intentional vectors on regressions of parasite
escape and recipient latitude demonstrated nearly significant correlations
for ‘all parasites’ and ‘trematodes only’ in that accidental vectors showed a
decline in parasite escape with increasing latitude for ‘all parasites’
(R2 ¼ 0.228, p ¼ 0.084; Figure 2.15A), while intentional vectors showed a
decline in parasite escape with increasing latitudes for ‘trematodes only’
(R2 ¼ 0.305, p ¼ 0.078; Figure 2.15B). Moreover, accidental vectors dem-
onstrated a nearly significant increase in parasite escape with increasing
Figure 2.15 The effect of accidental versus intentional vectors and parasite escape for
(A) ‘all parasites’ and (B) ‘trematodes only’. Overall, neither showed a significant relation-
ship, though they demonstrate a trend for lower parasite escape with intentional
vectors.
Figure 2.16 The influence of accidental versus intentional vectors on parasite escape for
(A) recipient (introduced) latitude in ‘all parasites’, (B) recipient (introduced) latitude in
‘trematodes only’, (C) distance between source and recipient regions in ‘all parasites’, (D)
distance between source and recipient regions in ‘trematodes only’, and (E) decade of intro-
duction for ‘trematodes only’. Blue line ¼ accidental introductions; red line ¼ intentional
introductions. For (A), there was a nearly significant negative correlation for accidental
introductions, whereby parasite escape in ‘all parasites’ decreased with increasing latitude;
in contrast, for (B), there was a nearly significant negative correlation for intentional intro-
ductions, whereby parasite escape in ‘trematodes only’ declined with increasing latitudes.
In (C), there was a nearly significant correlation of distance and escape of ‘all parasites’ for
accidental introductions, and in (D) this same relationship was significant for ‘trematodes
only’. Finally in (E), accidental introductions again showed a significant correlation with time
for ‘trematodes only’, whereby parasite escape increased with time.
distance between source and recipient regions for ‘all parasites’ (R2 ¼ 0.272,
p ¼ 0.056; Figure 2.16C), and in ‘trematodes only’, this same relationship
was significant (R2 ¼ 0.305, p ¼ 0.050; Figure 2.16D). Finally, for ‘trema-
todes only’, accidental introductions demonstrated a significant positive cor-
relation between parasite escape and introduction time (R2 ¼ 0.305,
p ¼ 0.050; Figure 2.16E).
3.4. Multivariate analyses

3.4.1 Stepwise multiple regression
When we included the factors that we found to be most important in the
earlier analyses in a multiple stepwise regression (i.e. distance between
source and recipient regions, decade of introduction, host taxa, introduction
vector, and vector strength), the most influential factor explaining parasite
escape for ‘all parasites’ was host taxa (p ¼ 0.013). This was driven by
bivalves, which displayed significantly lower parasite escape than the other
taxa. For ‘trematodes only’, two mechanistic factors were significant in
explaining parasite escape: vector (p ¼ 0.009) and host taxa (p ¼ 0.036).
For the latter, bivalves once again showed low parasite escape but were
not different from fish or snails, but all three taxa were different from crabs,
which demonstrated high levels of escape. For introduction vector, BWF
was distinct from several other vectors, including DBF, AQC, and OYS.
3.4.2 Generalized linear model

We also ran GLM analyses on our data (using parasite escape as our depen-
dent variable) to determine if there were interactions among our
various independent variables (including distance between source and
recipient regions, decade of introduction, introduction vector, host taxa,
vector strength, and accidental/intentional vectors). We found several sig-
nificant and nearly significant interactions, which we report here (we do
not report nonsignificant results). For ‘all parasites’, these included
decade of introduction vector (p ¼ 0.089), decade of introduction
vector strength (p ¼ 0.027), and decade of introduction accidental/
intentional vectors (p ¼ 0.048). For ‘trematodes only’, these included
decade of introduction vector (p ¼ 0.011), decade of introduction
host taxa (p ¼ 0.0364), decade of introduction accidental/intentional
vectors (p ¼ 0.033), vector host taxa (p ¼ 0.022), decade of introduction
vector host taxa (p ¼ 0.083), and distance between source and recipient
regions host taxa (p ¼ 0.070).
3.5. Evidence of parasite release

Of the 31 host–parasite investigations, 16 reported some evidence or sugges-
tion of parasite release (or lack thereof ) in their host–parasite system. Of
these, 13 (81%) suggested the possibility for parasite release, while three
suggested little evidence of parasite release in their system. However, of
these, only five presented empirical evidence of increased performance,
reproduction, or population abundance directly related to an escape from
parasites or, alternatively, a demonstrated lack of such benefits. In general,
the most common suggested possible effect (typically based on observational
data) was at the individual and population level, with occasional discussion of
community-wide influences of parasite loss in invasive hosts (Table 2.1).
4. DISCUSSION
In 2003, Torchin et al. synthesized what was then known regarding
escape from parasites across taxa and system (terrestrial and aquatic), and
in Torchin et al. (2002), parasite escape specific to marine environments
was reported. Over the last decade, several papers have been published that
continue to support those seminal works (see Table 2.1), and in our inves-
tigation here, we combined those new works with what was reported in the
previous decade by Torchin et al. (2002, 2003), along with a few additional
studies in Torchin and Lafferty (2009), thus updating and expanding what is
currently known about marine parasite escape over the past two decades and
adding more than 20 new marine host–parasite systems to the original Tor-
chin et al. studies. In addition, we extracted pertinent data regarding the
invasion pathways of these host–parasite systems to test our hypotheses based
on parasite escape. These independent variables included geography, time
since introduction, host and parasite taxa, and introduction vector.
Here, we recap our main results in the context of our six hypotheses. We
briefly describe what analyses were significant or showed nearly significant
trends and whether there was evidence based on our analyses to support our
hypotheses. We then expand discussion of these results and their implica-
tions in subheaded sections in the subsequent text.
1. We would continue to detect a significant effect of parasite escape in general across
host taxa in marine systems, but that some parasite groups would be more likely
to contribute to that escape than others. Overall, this hypothesis was
well supported: when all host–parasite systems were included, there
was a >50% reduction in the parasite richness in introduced versus
native regions. Therefore, most hosts demonstrated a clear signature

of parasite escape in their non-native regions. We also observed that
in some cases, it did depend on the parasite taxa—there were a few taxa
that demonstrated complete escape, while others exhibited little to
no escape.
2. We would find some geographic factors to influence parasite escape, especially dis-
tance between source and recipient regions. We found little correlation
between geographic factors and parasite escape across host–parasite
investigations; moreover, our hypothesis for parasite escape to be
influenced by distance between source and recipient regions was gener-
ally unsupported. However, we did find some support for distance as an
important factor when some categorical variables were grouped; these
included host taxa, particularly snails; introduction vector, particularly
BWF and DBF; vector strength, particularly the lowest value; and acci-
dental introduction vectors. For latitude and longitude, we found only
one general trend for parasite escape in ‘trematodes only’: a negative cor-
relation between parasite escape and recipient (introduced) latitude.
However, in our grouping analysis, latitude was important for introduc-
tion vector, particularly AQC, DBF, and OYS; and accidental/inten-
tional introduction vectors.
3. Parasite escape would correlate with time since introduction. Parasite escape may
be expected to decline with time as invasive hosts acquire new parasites;
therefore, we hypothesized that older invasions would exhibit lower par-
asite escape than newer invasions. Generally, this hypothesis was not
upheld; however, when grouped by categorical variables, time was
important for host taxa, particularly crabs; vector, particularly ballast
water; vector strength, particularly the lowest value; and accidental
introduction vectors. Moreover, when we explored time as a categorical
variable, we found differences between the time periods prior to 1900
and for 1900–50 for ‘trematodes only’.
4. Some introduction vectors would exhibit higher levels of parasite escape than
others, and this would be influenced by vector strength. We found seven intro-
duction vectors to contribute to the spread of marine parasites with their
hosts to locations around the world, and there was some support that
vector and vector strength were mechanistic factors influencing parasite
escape. In particular, our categorical analysis of vector and parasite escape
demonstrated vector to be a significant effect in the ‘trematodes only’
analysis, and in post-hoc tests, BWF had significantly higher escape
than OYS.
5. Parasite escape may be correlated with certain host taxa. The host taxa in our
study were primarily from four taxonomic classes, which were also the
most commonly transported organisms in marine invasion vectors and
the most commonly utilized hosts of marine parasites. In our categorical
analysis of host taxa and parasite escape, we found a significant effect of
taxa on escape for ‘all parasites’, and post-hoc analyses suggested bivalves
to have significantly lower escape than crabs, snails, or fish. For ‘trema-
todes only’ bivalves had significantly reduced escape compared to crabs
and nearly significant compared to snails.
6. We would observe interactions among these factors, given the complex nature of
invasion pathways. We found several significant and nearly significant
interactions among our variables, and these included introduction
timing vector, introduction timing vector strength, introduction
timing accidental/intentional vectors, introduction timing host taxa,
vector host taxa, introduction timing vector host taxa, and
distance host taxa.
On the whole, many of our hypotheses were supported or partially
supported by our data, especially when explored at a finer scale, where cer-
tain groups were analysed independently. Altogether, several categorical
variables were important across analyses, including host taxa and introduc-
tion vector/vector strength, while our continuous variables demonstrated
limited support except when grouped by specific categorical variables. This
result, along with our GLM analyses showing multiple significant interac-
tions among variables, demonstrates the complexity of the invasion pathway
for parasite introductions, especially given differences in parasite propagule
pressure and life history (Torchin and Lafferty, 2009). The following sec-
tions expand the discussion of these results and provide possible explanations
regarding their influences on parasite escape. In addition, although it is not a
primary goal of this chapter, we also include some analysis and discussion of
parasite release in the studies included here. We also explore four case studies
from our investigation that highlight many of the discussion points in the
subsequent text. Finally, we take a broader perspective of our work in
the context of emerging compilations of marine parasite invasions and
how our investigation informs the increasingly emerging awareness of the
importance of parasites in global marine introductions.
4.1. Parasite taxa

In general, our hypothesis for marine parasite escape in introduced
populations was supported in the majority of the host–parasite systems
included in our investigation, but there were some differences among par-
asite taxa. In some cases, this was simply due to sample size; e.g. those parasite
taxa reported as Amoeboidae, Amphipoda, Cnidaria, Crustacea, and Poly-
chaeta had two or fewer reported records and thus are suspect and do little to
inform our data when broken into parasite taxa. However, for the other par-
asite taxa included in our study with sufficient reported records, there were
some that showed complete escape (100% escape) across hosts, including
Fecampidae, Hirundinidae, and Rhizocephala, while others exhibited little
escape (<35% escape), such as Cestoda, Ciliophora, and Turbellaria. The
rest demonstrated moderate to high levels of escape (ranging from 40% to
80% escape). While the influence of parasite traits on parasite biodiversity
patterns is ‘hard to isolate’ (Poulin and Morand, 2000, 2004), there may
be several separate factors at play.
Parasite diversity has been shown to increase with increasing host body
size, host population density, and host geographical range (George-
Nascimento et al., 2004; Poulin, 1997; Poulin and Morand, 2000, 2004),
but this can differ between ecto- (living outside the host) and endoparasites
(living in the host), as ectoparasite diversity has been found to show a pos-
itive correlation with increasing body size (due to direct transmission onto
increased surface areas), while there is less of a correlation for endoparasites
(since many have indirect transmission vectors) (e.g. Munoz et al., 2007). As
a result, depending on the invasion pathway, larger hosts may be few or
absent, and this could impact the successful transmission of ecto- versus
endoparasites. While some of the parasite taxa in our review are ectoparasites
(e.g. Hirudinea), the majority are endoparasites, and therefore, the body
size of hosts may be less of a factor for these parasites—except for the notable
correlation between size and age and that infectivity often requires adult life
stages for successful infection in endoparasites (Lafferty and Kuris, 1996;
Torchin and Lafferty, 2009). Moreover, ectoparasites could be more prone
to human handling during the invasion process than endoparasites—in that
they are more easily visible and could be culled prior to movement (e.g. fish
aquaculture), or alternatively, if vector conditions are harsh, ectoparasites
may fall off their hosts (which would be impossible for endoparasites).
Finally, some parasite taxa may be more prone to temperature/salinity fluc-
tuations (e.g. rhizocepahalans) that could occur during vector transport,
which could impact successful introduction to new locations (Hines
et al., 1997; Kashenko and Korn, 2002; Tolley et al., 2006).
Host specificity would also be expected to impact introductions of
marine parasites. In particular, direct-transmission parasites may show less
specificity than trophically transmitted parasites that often have highly spe-
cific infection stages, including those that are obligate (Torchin and Lafferty,
2009). In our investigation, however, we did not observe any clear trends for
greater parasite escape in trophically transmitted versus direct-transmission
parasites. Trematodes represent an example of trophically transmitted para-
sites that have an obligate first-intermediate host stage but decreased speci-
ficity in second-intermediate and definitive hosts. In our analysis, trematodes
demonstrated moderate levels of escape across all hosts included in our study,
which could be partly explained by their ability to hitchhike with their first-
intermediate gastropod hosts (the obligate stage) and then utilize other, less
specific hosts to complete life cycles. For example, the first-intermediate
host, I. obsoleta (Eastern mudsnail), transported 55% of its native parasite
fauna from the Atlantic to the Pacific coast of North America, and these
trematodes were able to utilize native Pacific second-intermediate and
definitive hosts to complete life cycles, many of which were already familiar
to those trematodes (i.e. cosmopolitan distributions or previously intro-
duced to the region) (Blakeslee et al., 2012). Moreover, one of its trematodes
(Austrobilharzia variglandis) has become fairly prevalent on the Pacific coast
(Grodhaus and Keh, 1958), and it only requires two animal hosts,
I. obsoleta (first-intermediate) and a wide array of marine birds (as definitive
host); instead of utilizing a second-intermediate host, Austrobilharzia var-
iglandis encysts on firm surfaces, like shell and algae, which are readily avail-
able in its new environment. The invasion of this trematode has even
resulted in public awareness, due to outbreaks of ‘swimmer’s itch’ on the
Pacific coast, which are rarely reported in its native east coast range
(Blakeslee et al., 2012; Brant et al., 2010).
It is well known that parasites can have larger ecosystem-level impacts by
directly or indirectly driving host population dynamics and overall biomass
(Irvine, 2006; Kuris et al., 2008; Torchin et al., 2003) and influencing tro-
phic interactions, food web structure, competition, biodiversity, and key-
stone species (Britton, 2013; Lafferty and Kuris, 2009; Lafferty et al.,
2006, 2008; Lessios, 1988). However, for introduced parasites, these effects
may be limited in novel environments due to various traits of the parasite
itself, such as lifecycle complexity and host diversity (Hechinger and
Lafferty, 2005; Keesing et al., 2006), ability to use native hosts in the intro-
duced range, and environmental tolerance ranges (Britton, 2013). Those
introduced parasites able to take advantage of a multitude of host species
(e.g. generalists) may be able to add new host species in novel environ-
ments (i.e. via host switching; Gozlan et al., 2006; Norton et al., 2005;
Peeler et al., 2011), thus increasing the overall biodiversity in introduced

regions, and also the potential for “parasite spillback,” where competent
invasive hosts could influence disease dynamics in natives (e.g., Kelly
et al., 2009). Moreover, the introduction of novel parasites to marine
systems may result in host behavioural or physiological changes that could
increase the likelihood of transmission to other hosts (e.g. Johnson et al.,
1999; Lafferty and Morris, 1996; Poulin et al., 2005; Rohde, 2005). In addi-
tion, they may impact various aspects of host physiology, functioning as
keystone species (e.g. Mitchell and Power, 2003; Price et al., 1986;
Wood et al., 2007)—an important consideration in realizing the potential
impacts of parasite escape in invasive communities of marine hosts.
4.1.1 ‘All parasites’ versus ‘trematodes only’

Related to our two parasite groups, ‘all parasites’ and ‘trematodes only’, it is
interesting that in several cases, we found stronger correlations in our ‘trem-
atodes only’ analyses compared to ‘all parasites’. We suggest a couple possibil-
ities for this result. (1) Because the ‘trematodes only’ analysis was focused on
one taxonomic group, it may have allowed for more precise detection of par-
asite species richness in native and introduced hosts rather than in the ‘all par-
asites’ analysis, which included broad taxonomic categories that were
inconsistent across studies (ranging from species to class level, though mostly
at the family level and lower). (2) Trematodes are known to have highly com-
plex life cycles, typically involving 2–4 hosts, some of which are obligate.
Therefore, it may be that the effects of parasite escape are more apparent in
this parasite group because a trematode’s life cycle can be highly specific; thus,
the invasion process could disrupt successful transmission throughout the cycle
(i.e. especially if a necessary host is absent in the new range), resulting in fewer
trematode species that can establish and maintain viable populations in an
invasive range (Torchin and Mitchell, 2004). Moreover, parasite escape inher-
ently explores the number of parasite species included in a host’s native range,
minus the number of species it leaves behind during the invasion process, plus
the number it acquires in the invasive range (Torchin and Lafferty, 2009);
thus, a parasite group’s host specificity could be a large factor in whether or
not hosts demonstrate high levels of parasite escape. For trematodes, higher
host specificity may preclude native trematodes from recognizing new
invaders as possible hosts, eliminating that third part of the parasite escape
equation (i.e. the number of parasites a host acquires in its new range). In con-
trast, our ‘all parasites’ analysis includes parasites with varying levels of host
specificity, and in fact, we have clear evidence that some hosts have acquired
new parasites in their invasive range (e.g. Crassostrea gigas; Thieltges et al.,
2012); therefore, this varying host specificity among parasites included in
our ‘all parasites’ investigation could be a reason why it shows slightly weaker
support for parasite escape in some of our statistical analyses compared to our
‘trematodes only’ investigations.
4.2. Host–parasite geography

When comparing the source and recipient geographic regions of marine
parasite escape on a global scale, the majority of peer-reviewed literature
focused on four regions: North America, Europe, Asia, and Australia. Nota-
bly, there was a lack of data from South America and Africa, probably
due to a lack of investigations in those continents, rather than an actual
lack of marine host/parasite introductions there. Asia was the most often
cited source region for marine parasites, which corresponds with the finding
that Southeast Asia is a hot spot for marine biodiversity (Rohde, 2010);
in contrast, North America was the most often cited recipient region;
however, this result could be partly due to a sampling effect, given the
amount of research that has occurred in this region. Such a likelihood
is in fact supported by a global study by Pyšek et al. (2008), which
clearly demonstrates sampling biases in invasion ecology research across
continents, presenting (in decreasing order) the regions where invasions
have been well studied as North America > Europe > Australia > South
America > Asia > Africa. With the exception of South America, these trends
mirror our own data in terms of parasite invasions in recipient regions,
where North America > Europe > Australia > Asia > Africa (Figure 2.3).
Based on this evidence, sampling bias is likely playing a role in the frequency
of marine parasite invasions in source and recipient regions that we compiled
from our literature review.
While we predicted that increasing distance between source and recip-
ient regions may positively correlate with parasite escape, that is, due to
increasing transport time and increasing dissimilarity between source
and recipient environments (Carlton, 1996; Lafferty et al., 2010), we found
little support for that hypothesis, except when we grouped by categorical
variables; important results included host taxa (snails) and accidental
introduction vectors for ‘all parasites’; and host taxa (snails), introduction
vector (BWF and DBF), and vector strength (the lowest value) for ‘trema-
todes only’.
Particular to snail hosts, the trend for lower parasite escape with increas-
ing distance was driven by trematodes, which were the dominant parasite
taxa infecting snails. It is possible that longer transport times (i.e. with inher-
ently enhanced stress) resulted in higher mortality among infected snails,
reducing the number of trematode species that successfully invaded distant
locations. In fact, stress-induced mortality has been demonstrated in several
snail–trematode systems (e.g. Lauckner, 1987a,b; Mouritsen and
Poulin, 2002).
Related to introduction vector, those vectors showing positive trends
between distance and escape were the two shipping vectors (BWF and
DBF), and these were also the vectors with the lowest vector strengths
(Table 2.2) and thus less likely to introduce infective stages of parasites, espe-
cially during long transport times. Moreover, when these two ‘accidental’
vectors were combined with the other two accidental vectors (APM and
CANAL), we saw positive trends between time and parasite escape, com-
pared to intentional vectors, which showed no correlation. Accidental vec-
tors may be more likely to demonstrate an effect of distance than intentional
vectors because intentional vectors target species for introduction, which are
purposefully kept healthy during transport (thus enhancing likelihood for
survival of associated parasites), whereas accidental vectors possess
untargeted individuals that may be more influenced by mortality with
increasing distance.
For our explorations of latitude and longitude, we found no correlations
with longitude; however, there were a few significant correlations with lat-
itude, including one general trend for parasite escape to decline with lower
latitudes for ‘trematodes only’. It is possible that this trend may exist because
3 out of the 5 studies including trematodes in southern latitudes were intro-
ductions originating from northern latitudes (i.e. long separation between
source and recipient populations), and in each of the three cases, parasite
escape was 100%. However, these are very small sampling numbers, and
it is probable that sampling bias has had a strong influence on this ‘trend’
due to the paucity of studies that exist in southern versus northern latitudes.
There were also a few interesting trends with latitude and escape when
categorical variables were grouped, including introduction vector, where
three vectors—AQC, DBF, and OYS—each showed strong correlative
values with recipient latitude for ‘trematodes only’; and accidental/inten-
tional introduction vectors, where accidental vectors demonstrated a nearly
significant negative correlation with recipient latitude for ‘all parasites’, and
intentional vectors showed a nearly significant negative correlation with
recipient latitude for ‘trematodes only’. These trends are less intuitive, but
it may relate once again to the limited numbers of studies in southern lati-
tudes as recipient regions—the majority of which came from Australia and
New Zealand with a complete lack of studies from South America and
only one from Africa.
4.3. Time since introduction

In their invasive range, introduced hosts may be expected to accumulate
novel parasites over time because (1) native parasites may eventually recog-
nize an invasive organism as a viable host especially if they have invaded an
area with phylogenetically related or evolutionarily similar hosts to them-
selves and (2) multiple introductions may transport new parasites to the inva-
sive region (Torchin and Mitchell, 2004). Even still, Torchin and Mitchell
(2004) suggest that though introduced organisms may accumulate new par-
asite species from the introduced range, those new infections may not be
sufficient to replace the parasites they escaped in their native range. As a
result, though parasite richness may increase with time, it will likely never
reach the same level as in the native range.
Time since introduction has been found to be an important factor in a few
individual cases of marine host invaders (e.g. in Carcinus maenas, Torchin et al.,
2002), where a linear correlation between time and parasite richness has been
detected in the invasive region. However, in our investigation of 31 host–
parasite systems, we found little evidence for a correlation between parasite
escape and time since introduction for either our ‘all parasites’ or ‘trematodes
only’ analyses in general. Yet, when grouped by specific categorical variables,
time was found to correlate with parasite escape in several cases, including host
taxa (crabs), vector (BWF), vector strength (1), and accidental introduction
vectors, and we also found several significant and nearly significant interactions
with time in our GLM analyses for both ‘all parasites’ and ‘trematodes only’,
including vector, host taxa, vector strength, and accidental/intentional intro-
ductions, and one instance of a three-way interaction for ‘trematodes only’
among time vector host taxa. Thus, it is clear in our investigation that time
since introduction is a complicated variable and appears not only to be case
dependent but also to interact with other important invasion pathway variables
in its effect on parasite escape.
Interestingly, our investigation detected ‘crabs’ as a host group demon-
strating a significant and tight linear correlation between parasite escape and
time since introduction, and this corroborates the linear relationship Torchin
and Lafferty (2009, Figure 11.3) found specifically for Carcinus maenas. While
five of the crab systems in our study included Carcinus maenas (Table 2.1), par-
asite richness from three other crab species was also included in our analysis,
and among these four total crab species, time demonstrated a positive linear
correlation with parasite escape. Moreover, we also detected three vector-
related significant or nearly significant correlations between time and escape.
All three of these were strongly driven by one introduction vector, BWF,
which possesses the lowest vector strength for introducing metazoan parasites
and may be more likely to show an apparent link between time and escape
compared to higher vector strengths. This is because high strength vectors
have the potential to introduce numerous parasite species in initial introduc-
tion ‘attempts’ (i.e. time zero), rather than slowly accumulating parasites over
time, as expected in accidental and low-strength introduction vectors.
4.4. Vector and vector strength

We found the vectors BWF and OYS to be the most common vectors of
introduction in our study for both ‘all parasites’ and ‘trematodes only’, which
corroborates other studies of marine introduction vectors (e.g. Ruiz et al.,
2000), demonstrating these to be two of the most important vectors involved
in introducing marine species worldwide. However, less represented vectors,
like APM and CANAL, may actually suffer from sampling limitations, con-
sidering they are both currently active vectors responsible for the introduction
of several marine invaders, including infamous ones (like Carcinus maenas to
Pacific North America via APM). The Suez Canal, in particular, has been
responsible for introducing more than 300 species between the Red and Med-
iterranean Seas (World Ocean Review, http://worldoceanreview.com/en/
wor-1/marine-ecosystem/invasive-species/); yet in our investigation, we
could only find records for three invaders through the canal that were assessed
for parasites. Finally, the historical vector, DBF, is no longer operating, but
records of species movements via this vector are poor, and it remains probable
that more hosts and parasites were moved via dry ballast shipping that cannot
be accounted for (Carlton, 1995).
In our explorations regarding the influence of vector and vector strength
on parasite escape, we found parasite escape to be significantly higher for BWF
compared to OYS for ‘trematodes only’, and vector strength demonstrated a
trend for decreasing parasite escape with higher vector strength. Moreover,
our multiple regression analysis also revealed vector as an important factor
in explaining parasite escape for ‘trematodes only’—specifically, BWF had
significantly higher escape compared to OYS, AQC, and DBF. Here, we

describe each vector included in our analysis in detail to help explain these
results in terms of their vector attributes and vector strengths.
Ballast water (BWF) had the lowest vector strength for introducing par-
asites in our analysis, which we evaluated based on four vector attributes:
first, the vector primarily transports larvae in its ballast tanks, which may then
be released into recipient ports at the end of the voyage. We considered this
transport of primarily larvae to have low strength because though larval hosts
can carry parasites, “they are often lost post-recruitment and are typically not
the same types of parasites that infect adult populations” (Rohde, 2005);
moreover, per Torchin and Lafferty (2009): “the introduction of uninfected
larval stages, such as those introduced by ballast water will exclude parasites
from transferring to novel location”, and as such, “ballast water introduction
may be a particularly potent means for marine species to escape parasites”.
Moreover, we judged BWF to have moderately numerous introduction
‘attempts’ because transport between/among regions will be variable and
ballast water uptake will result in variable species composition and abun-
dance (Verling et al., 2005). Furthermore, the uptake of organisms in ballast
water is untargeted and may not include host species (or the necessary life
stages) likely to introduce parasites, while transport time is likely to be mod-
erate. On the whole, these attributes help explain why BWF has significantly
higher parasite escape than other vectors.
In contrast, the oyster (OYS) vector would be expected to have a greater
potential for introducing parasite species, and thus, its vector attributes would
manifest as high vector strength. In particular, hosts associated with oysters
would primarily include juvenile and adult life history stages, the latter of
which is more likely to harbour metazoan parasites that could successfully
establish in the non-native range (Torchin and Lafferty, 2009). Moreover,
the frequency of introduction ‘attempts’ and the number of propagules
entrained in the vector would likely be quite high because oyster transplan-
tation has typically been carried out on a massive scale, often sustained over
numerous years, and was implemented in such a manner as to ensure high
survivability, thus resulting in a strong potential for numerous propagules
of associated hosts (including parasitized ones) to be transported via the vec-
tor (Carlton, 1979; Miller, 2000). For these reasons, it is not surprising that
we detected significantly lower parasite escape among introduced hosts asso-
ciated with OYS compared to BWF. While the other two vectors with high
vector strength, aquaculture (AQC) and deliberate introductions (DEL), might
also be expected to show a similar trend as OYS (given many similarities
among vector attributes), our data do not support such an expectation,

although AQC did demonstrate a difference from ballast water in our mul-
tiple regression analysis, and also when both AQC and DEL were grouped
with oysters in ‘vector strength’, there was a trend for lower parasite escape.
Our final three vectors of interest are dry ballast/fouling (DBF), canals
(CANAL), and algal packing materials (APM). DBF is no longer an active vec-
tor (i.e. it is historical), and when it was operational, it carried primarily bal-
last rock collected from the intertidal zone in the source region (likely
covered in algae and other organisms), which were then discarded at the
recipient port (Brawley et al., 2009; Carlton, 1987). DBF likely included
both juvenile and adult organisms, and its frequency of introduction
‘attempts’ would likely be considered moderate given that vessels moving
between Europe and North America at the time were fairly numerous as
a result of the lumber trade (Brawley et al., 2009); moreover, it was mod-
erately targeted because the rocks often used as ballast were collected from
locations where host organisms could be fairly abundant. Transit time would
have been long. On the whole, we found few patterns associated with DBF
except for a nearly significant correlation with distance (as discussed earlier)
and a significant difference from BWF in our multiple regression analysis.
The movement of species through the vector CANAL and particularly
the opening of the Suez Canal (a still operating means of introduction
between Asia/Africa and the Middle East and Europe) has been shown to
be another vector of host introduction with moderate vector strength. In par-
ticular, this vector allows for the transit of all waterborne life stages of hosts,
including larvae, juveniles, and adults, and per earlier, adults are the primary
means of transporting infective stages of parasites (Torchin and Lafferty,
2009). The frequency of introduction ‘attempts’ in this vector is likely
moderate, considering not all organisms would have the capacity to success-
fully migrate through the canal (e.g., physically and/or physiologically); in
addition, most movements would be accidental, though some human vectors
(e.g. shipping) could assist in that movement. Finally, transit time is probably
moderate given that natural movements of organisms would be expected to
be slower than human-aided movements. While canals are an important vec-
tor for introducing species into previously disconnected bodies of water, our
data did not find any trends for parasite escape associated with hosts transported
through canals, though, as mentioned earlier, sample size is very low in our
investigation.
Our last vector is APM, associated with live bait and trade. This vector
remains active and is principally involved in the transfer of small adults and
juveniles (Cohen et al., 2001; Cohen et al., 2012; Haska et al., 2011; Yarish
et al., 2009). It also has a short transit time (almost always shipped via over-
night mail), and care is taken to ensure the target organisms (bait or live
seafood) arrive in good condition (hence the use of algae as a means of
cushioning and moisture), also ensuring greater survivability of hitchhiking
organisms in the algae (Carlton and Cohen, 1998). We classified the vector
as moderate strength because the frequency of introduction ‘attempts’ would
be moderately numerous given the worldwide shipments of bait and algae,
which may then be randomly discarded in numerous locations across
the globe; however, the number of host propagules associated with the vec-
tor are often fairly low (Fowler, Blakeslee, pers. obs.) especially because
the infective stages of many parasite species are adults (Torchin and
Lafferty, 2009). When explored for patterns associated with parasite escape,
this vector also demonstrated little effect; however, sample size was once
again low.
4.5. Host taxa

In a review of 892 species, Pyšek et al. (2008) determined that numerous
host taxa have been transported and introduced to locations worldwide,
the majority of which were plants and insects. Of marine organisms, the spe-
cies that were most frequently reported were crustaceans, molluscs, and fish.
Similarly, Ruiz et al. (2000) found molluscs and crustaceans to dominate
North American marine invaders. It is noteworthy that parasite diversity
often concentrates in these same taxa: crustaceans, molluscs, and fish. Marine
invertebrates, especially molluscs and crustaceans, are often utilized as inter-
mediate hosts of parasites with multihost strategies and sometimes also as
hosts for direct-transmission parasites (e.g. Lauckner, 1987a,b;
Marcogliese, 2002; Torchin et al., 2002). Moreover, Poulin and Morand
(2000) demonstrate fish as one of the most common vertebrate hosts of par-
asites, especially for trematodes, and marine fish in particular have been
shown in numerous studies to host a vast number of parasites—for example,
the two species of snapper (Lutjanus spp.) included in our study were found
to host upwards of 20 different parasite species (Vignon et al., 2009), and
the round goby (Apollonia melanostoma) has been shown to possess over
70 different parasite species in its native location (Kvach and Skora, 2007;
Pronin et al., 1997). Therefore, it is some of the most commonly transported
marine taxa via anthropogenic vectors that are also some of the most com-
mon hosts of marine metazoan parasites.
In our study, molluscs, crustaceans, and fish were also identified as the
most common host taxa. In particular, we found bivalves and snails (both
molluscs), crabs, and fish to be fairly equitable as far as their proportion of
the total number of host–parasite invasions. When we included host taxa
as a possible mechanistic factor for parasite escape, we found that one group,
bivalves, possessed significantly lower parasite escape than the other three
groups for ‘all parasites’ and it was significantly lower than crabs and nearly
significantly lower than snails for ‘trematodes only’. Moreover, when we ran
our multiple regression analysis, host taxa turned up as one of the most
important factors explaining parasite escape, and this was again largely driven
by significantly lower escape in bivalves. We suspect a reason for this is that
one of the most prominent bivalves in our analysis is Crassostrea gigas, which
is not only a vector for the transmission of hitchhiking parasites but also a
highly important introduction vector for the movement of other free-living,
hitchhiking organisms (e.g. Ruesink et al., 2005). As discussed in the pre-
vious section, we ranked oysters as an introduction vector possessing high
vector strength for introducing parasites compared to other vectors. In fact,
our data here support this, given that oysters as a host taxa demonstrate sig-
nificantly lower parasite escape than other host taxa and, additionally, oysters
as a vector possessed the lowest parasite escape value of all the other vectors.
Given the careful manner in which oysters are transported to ensure survival
and enhance establishment (Carlton, 1979; Carlton, 1992; Miller, 2000), it is
perhaps not surprising that they have transported numerous parasites and
thus parasite escape in these taxa is relatively low.
Finally, it is noteworthy that the global understanding of marine parasite
invasions has been dominated by marine invertebrates as study organisms, and
prior to recent endeavours, little was available regarding source and recipient
richness of parasites in marine fishes. According to Torchin and Lafferty in
2009, “although limited, studies examining parasitism in introduced and
native populations of marine and estuarine fishes are beginning to emerge. . .”.
In fact, several recent studies have continued that trend, and the way has been
paved for an even better understanding of parasite escape in this important
group, among other host taxa that have currently limited information but
may be important contributors to marine invasions worldwide.
4.6. Parasite release

Our global investigation of parasite escape in marine systems over the last
two decades continues to show strong support for a significant reduction
in parasite taxonomic richness in introduced compared to native regions.

Though it was not a primary goal of our work, we also explored any evi-
dence or suggestion of parasite (¼enemy) release via increased performance,
reproduction, or abundance in hosts included in our study. We found that
the majority of those studies that examined parasite release demonstrated or
suggested that it was, or could be, occurring in their system. However, most
studies based that assessment on observational rather than experimental evi-
dence (or simply on speculation), again pointing to the fact that more exper-
imental work is needed to demonstrate that invasive marine hosts benefit (or
do not benefit) from their often highly significant escapes from parasites. In
addition, there was sometimes conflicting evidence for parasite release in the
studies that explored it in our database. For example, two studies (Torchin
et al., 2001; Zeitlmeisl et al., 2011) investigated whether Carcinus maenas’
highly significant escape from parasites (in some cases 100% escape) in its
invasive locations has resulted in a physiological and/or ecological benefit
for the crab compared to native conspecifics. In particular, Torchin et al.
(2001) examined crabs in four of Carcinus maenas’ invasive ranges (eastern
North America, western North America, Australia, and South Africa) com-
pared to native European populations and found a loss of parasites to corre-
late with increased performance in non-native crabs—that is, individuals
were larger and populations were at a greater biomass than native conspe-
cifics, although limb loss (an indirect measure of predation pressure) was
not lower in introduced locations. Such enhanced size and biomass were
believed at least partly attributable to the crab’s escape from parasitic barna-
cles (Sacculina spp.), which castrate the crab in native regions and result in a
significant impact on its fitness there—that is, escaping such castrators might
be expected to confer a fitness advantage to non-native individuals and
populations. However, Zeitlmeisl et al. (2011) examined the influence of
parasitism on reproduction in Carcinus maenas and did not find evidence
for a difference in testes weight in native versus introduced crabs, concluding
that there was not clear support for a fitness advantage in introduced loca-
tions. Therefore, results of enemy release have been somewhat conflicting in
this particular species; however, there is much still to be learned regarding
the potential for enemy release in Carcinus maenas, especially spanning its
numerous introduced regions worldwide.
Over the past few decades, enemy release has been a leading biological
hypothesis, receiving considerable attention in the literature and tested in
numerous systems worldwide (e.g. a Google Scholar search for ‘enemy
release’ resulted in 269,000 results, although this includes any mention
of enemy release in an article; when restricting to title only, it resulted in 112

total results). A recent review by Jeschke et al. (2012) exemplifies the con-
siderable interest in these (and five other) prominent theories in invasion
biology research and whether support for each hypothesis has declined over
time (‘decline effect’) with the inclusion of new model systems, long-term
data, and greater experimental work. They found that though some hypoth-
eses have in fact demonstrated a significant decline in support over time, the
support for enemy release has largely remained unchanged with time, and
marine studies in particular have shown the strongest support (close to
80%) compared to terrestrial (close to 50%) and freshwater (close to 60%)
systems (although sample sizes were almost seven times higher in terrestrial
versus marine systems). The Jeschke et al. (2012) review is therefore sugges-
tive that studies of enemy release have provided consistent evidence over the
past few decades that non-native organisms may benefit from escaping their
enemies, especially in marine systems. However, other studies have found
conflicting or little evidence of a significant benefit of enemy release on
invasion success. For example, Colautti et al. (2004) reviewed the global lit-
erature of invasion biology and enemy release and argued that instead of ter-
ming the loss of natural enemies as a ‘release’, it would be more appropriate
to call that loss an enemy ‘reduction’ since invasive species are not
completely devoid of potential enemies in non-native locations; moreover,
this reduction is situation-dependent—that is, invasion processes are highly
complex and therefore may not all fit under the same umbrella. The com-
plex nature of invasion biology and enemy release was also very apparent in
our investigation here of global marine host–parasite systems in native and
non-native locations—given the numerous factors (ecological and anthro-
pogenic) involved in each invasion pathway.
4.7. Case studies of noteworthy host species

Here, we describe four cases studies from Table 2.1 that exemplify some of
the interesting aspects discussed earlier. The first is Carcinus maenas, the
European green crab, which has been accidentally introduced via numerous
introduction vectors and which demonstrates differential parasite escape
among its introduced regions. The second is Crassostrea gigas, the Pacific oys-
ter which is not only an introduced host but also an introduction vector and
which has been intentionally introduced as a food source to numerous loca-
tions worldwide, and in a few of these locations, parasite species richness and
disease have been assessed. The third is Littorina littorea, the common
periwinkle snail, which is a species that was once considered cryptogenic in

its highly abundant introduced range, but through the signatures of parasite
escape, was determined to be non-native. Finally, we discuss the story of
Charybdis longicollis, the swimming crab, which is a species that invaded
the Mediterranean through the Suez Canal and at first appeared parasite-free
but was later followed by a castrating parasite from its native range.
4.7.1 Carcinus maenas: An accidentally introduced host to numerous

locations worldwide
Carcinus maenas, the European green crab, is a truly global invader, being
present on almost every continent worldwide but only native to one
(Europe). It has been named one of the “100 of the World’s Worst Invasive
Alien Species” (http://www.issg.org/database/species/search.asp?st¼100ss)
due to its highly successful invasions in numerous populations globally, its
predatory impacts on native species, and its competitive interactions with
natives (Cohen et al., 1995; Grosholz et al., 2000; Walton et al., 2002).
Moreover, it has been transported via numerous introduction vectors,
including older vectors like DBF, and currently active ones including
APM and BWF (Carlton and Cohen, 2003). In its native range, Carcinus
maenas is host to ten parasite species (Blakeslee et al., 2009; Torchin
et al., 2002), and in its various invasive populations worldwide, it has shown
a clear reduction in parasite species richness and often high levels of parasite
escape (Torchin et al., 2001). In its oldest introduced location (Atlantic
North America), Carcinus maenas is infected by 3 parasite species and has
a parasite escape value of 0.70; in its next oldest introduced location
(Australia), it is infected by 2 parasite species, escape ¼ 0.80; in the next
two introduced locations (South Africa and Japan), it is infected by 0 parasite
species, escape ¼ 1.0 (although of note is that these two latter introductions
could have been hybridizations between Carcinus maenas and a closely related
congener Carcinus aestuarii); finally, in its most recent introduced location
where parasite information is available (Pacific North America), Carcinus
maenas is infected by 2 parasite species, escape ¼ 0.80 (Torchin et al.,
2001; Zeitlmeisl et al., 2011). As noted previously, Torchin and Lafferty
(2009) recognized this as a linear relationship of parasite diversity with time,
although it is interesting that the most recently reported parasite introduc-
tion possesses lower escape than the two prior ones. Vector of introduction
may be playing a role, considering the South African and Japanese invasions
are believed due to BWF (low vector strength), while the Pacific North
American introduction is probably the result of entrainment in APM
(moderate vector strength). Carcinus maenas has been recently introduced to

other worldwide locations, including South America, other areas of Asia,
and recently to Newfoundland; however, at present, nothing is known
regarding the parasite richness in those populations.
4.7.2 Crassotrea gigas: An intentionally introduced host to numerous

locations worldwide
Crassostrea gigas, the Pacific oyster, is an interesting case because it not only
hosts hitchhiking parasites but also serves as an introduction vector for the
movement of free-living hitchhikers (Ruesink et al., 2005). Similar to
Carcinus maenas, the global movement of Crassostrea gigas and associated par-
asites has been documented in a few populations including western Europe,
the Pacific Northwest, and New Zealand (e.g. Dinamami, 1987; Mann et al,
1991; Thieltges et al., 2012), but there are numerous other populations in
which the oyster has been translocated (Ruesink et al., 2005) where parasite
richness is presently unknown. As such, there is still much to be understood
regarding parasite movements as a result of intentional introductions of
Crassostrea gigas. Moreover, though our investigation focused on metazoan
parasites, Crassostrea gigas translocation has also resulted in the movement of a
few virulent diseases, including the haplosporidian parasite Haplosporidium
nelsoni (likely introduced with spat and adult oysters from Japan and British
Columbia; Peeler et al., 2011); the oyster herpes virus (OsHV-1) (Garcia
et al., 2011); a recently detected fungus, Ostracoblabe implexa (Thieltges
et al., 2012); and a gram-negative bacteria, Vibrio spp. (Thieltges et al.,
2012). Crassostrea gigas translocations have originated not only from native
populations in Asia but also from secondary sources like Canada, and as a
result, micro- and macroparasites accumulated in secondary sources like
North America could be transported to other global populations. For exam-
ple, Thieltges et al. (2012) note the recent appearance of the virulent OsHV-1
herpes virus in populations of Crassostrea gigas in New Zealand and Australia
following a massive spread of the virus throughout oyster culture areas of
Europe. These cosmopolitan movements could be yet another reason why
bivalves like Crassostrea gigas have much lower parasite escape than other host
taxa since parasites could be being moved from not only native sources but
also secondary sources, where the host may accumulate local parasites. This
particular host is therefore one in which further research on parasite loads
is sorely needed across its global populations, especially considering its com-
mercial value and potential for spreading diseases globally.
4.7.3 Littorina littorea: Parasite escape used as a tool for resolving

cryptogenic status
Littorina littorea, the common periwinkle snail, is highly abundant on both
coasts of the North Atlantic, but its presence in eastern North America
was the subject of a 100-year debate (starting in the late 1800s) because
of conflicting archaeological, ecological, and molecular records, which
suggested both native and non-native status; as such, it was classified as a
cryptogenic species in North America (see references in Blakeslee, 2007).
Presently, the snail is believed to be non-native in eastern North America
based on multiple lines of evidence (e.g., Chapman et al., 2007; Blakeslee
et al., 2008; Brawley et al., 2009), in part due to a parasite richness study
(Blakeslee and Byers, 2008) that used the well-supported signatures of parasite
escape (e.g. Torchin et al., 2002) in reverse to provide further evidence to
resolve its cryptogenic status. In particular, L. littorea is infected by 11 different
species of trematodes in its native range (James, 1968a,b), and through exten-
sive sampling of eastern North America (Labrador to Delaware Bay),
Blakeslee and Byers (2008) discovered only five trematodes infecting the snail
throughout North America with two being extremely rare (each only 0.02%
out of 8210 surveyed snails). Moreover, when they compared the results for
L. littorea to known native North Atlantic periwinkles (L. obtusata, smooth
periwinkle, and L. saxatilis, rough periwinkle), they found L. littorea to dem-
onstrate a significant reduction in parasite species richness in eastern North
America versus Europe when compared to the two native snails. The study
concluded that L. littorea displayed clear signatures of parasite escape, while
its two native congeners did not. Interestingly, four of the snail’s native trem-
atodes in Europe were found infecting congeners, L. obtusata and L. saxatilis,
in North America; thus, L. littorea did not escape those four trematodes
physically, but likely evolutionarily/physiologically, either because the
North American trematode species are phylogenetically divergent from their
European counterparts or because of the long-term separation from their native
European host (L. littorea) in North America (i.e. L. saxatilis, which hosts the
four trematodes, has been present in North America for an extensive period
of time, much longer than the last glacial maximum; Panova et al., 2011), which
has resulted in an incompatibility between host and parasite species. In either
case, it is noteworthy that for L. littorea, parasite escape has occurred in sympatry
for four of its parasite species and not as the result of a large ocean barrier.
4.7.4 Charybdis longicollis: Suez Canal invader

Charybdis longicollis, the swimming crab, is one of the highlighted species in
Table 2.1 that includes parasite richness information in the introduced range,
but there is insufficient evidence from its native range. The crab was intro-
duced from the Red Sea to the Mediterranean Sea in the 1950s through
the Suez Canal, which is documented as the dominating invasion vector
in Europe (24.5% of introduced taxa have come to Europe via this route;
Gollasch, 2006). When Charybdis longicollis was first noted in the Mediter-
ranean, it appeared to be relatively parasite-free and had escaped a damag-
ing castrating barnacle that infects it in its native range of the Red Sea, East
Africa, and the Persian Gulf. However, in 1992, its native castrating bar-
nacle also invaded the Mediterranean through the Suez Canal and began
infecting the crab, sometimes in high prevalences. Even with this possible
threat on the crab’s reproduction and population abundance, Charybdis
longicollis’ (and its parasite’s) densities remained relatively stable over
time, and thus, a release effect was deemed unlikely in the crab (although
behavioural differences between infected and uninfected individuals were
detected) (Innocenti and Galil, 2007; Innocenti et al., 2003, 2009). Unfor-
tunately, because the crab is not a commercially important species, little is
known regarding its parasite richness and prevalence in its native range
(Galil, pers. comm.); thus, it is impossible to ascertain the level of escape
and/or release the crab has experienced. This story once more points to
the fact that more research is required in this system and in the numerous
other Suez Canal invaders, where knowledge of parasite fauna is very
limited.
4.8. Parasite escape in the context of marine parasite invasion

Since the publication of Torchin et al.’s (2002) paper, calling attention to the
relative lack of knowledge regarding the importance of parasite release in inva-
sion ecology in marine systems (i.e. only 10 introduced host–parasite relation-
ships were documented in 2002), there have been an increasing number of
publications that have attempted to describe and find commonalities between
systems and host–parasite relationships (e.g. Dunn, 2009; Prenter et al., 2004;
Roy et al., 2011; Tompkins et al., 2010). Our manuscript is the most recent in a
line of current publications that highlight the role of parasites in invasions
(e.g. “Invasions and Infections” special feature in Functional Ecology 2012).
While terrestrial and aquatic introduced parasites have been relatively well
documented, there is a lack of comparable information on introduced parasites
in marine systems (e.g. those specific to fish: Vignon and Sasal, 2010). However,
our meta-analysis of 31 host–parasite invasions in the marine biome enabled us
to specifically explore the host invasion pathway and its potential role (via a
number of mechanisms) in a host’s ability to escape parasites in its introduced
region. Many studies have reported the direct or indirect impacts of introduced
parasites on ecosystem function (e.g. Dunn et al., 2012), whereas our analysis
examines the various physical and biological factors that may influence parasite
invasion success. For example, vector type and strength have been suggested in
several studies to play an important role in differential invasion success (e.g.
Colautti et al., 2004; Miura et al., 2006; Prenter et al., 2004), which we were
able to test and demonstrate some support for in our investigation. Colautti et al.
(2004) have also suggested that invasion success may vary dramatically between
accidental and intentional introductions, with survival dependent on anthro-
pogenic treatment, and we were also able to show some support for this, in
regards to parasite escape. Altogether, our work provides updated, as well as
new, perspectives on the well-supported phenomenon of marine parasite
escape, not only continuing to support the theories postulated in Torchin
et al. (2003) but also finding new and interesting connections among our data
that move forward our understanding of marine parasite invasions.
4.9. Study limitations

In our investigation, we attempted to make our dataset as comprehensive
and consistent as possible, and in several cases, we eliminated host–parasite
systems that fell short of our criteria for inclusion in the database. Even still,
our study has several limitations that may have impacted our attempt at a
comprehensive (as possible) understanding of parasite escape in marine
systems, including the following:
1. Although parasites are common in many systems, they can be easily over-
looked and poorly understood regarding their detection, identification,
and reporting (Poulin and Leung, 2010), which may be the result of sev-
eral factors, including taxonomic biases—that is, a poorer understanding
of taxonomy/phylogeny in parasites compared to their hosts, a lack of
parasite experts that can identify and record parasite species, and difficul-
ties in understanding and predicting the movement of parasites between
ecosystems and correctly identifying them. As such, taxonomic issues are
certainly a consideration, especially as some species may have been
lumped under a larger taxonomic grouping, possibly underestimating
species richness in a region.
2. In our review of the literature, we uncovered several cases where the
invasive range was better understood than the native range, especially
for some source regions (e.g. Asia). A good example of this issue is
the parasitic bopyrid isopod, Orthione griffenis, which was first described
and named based on coastal collections in the Pacific northwest

(Washington, USA), even though the parasite is in actuality a recent
invader to North America from Asia (Chapman et al., 2011). Therefore,
more analysis on parasite diversity needs to be conducted over the
entire native and introduced ranges of host species to adequately describe
parasite fauna and more accurately calculate parasite escape.
3. We attempted to understand parasite taxonomic richness in the host’s full
range; however, records may have been incomplete in some places, and
we could not completely account for the particular range that was
included in a study; for example, some studies may have explored
broader geographic ranges and therefore uncovered more parasite species
than other studies. In addition, it is possible ‘propagule bias’ may have
occurred in some cases when cumulative numbers overestimate parasite
diversity of a source region; as such, it would be more appropriate to
compare introduced populations with the most likely source host
populations (Colautti et al., 2004). However, for many of the host–
parasite systems, it was impossible to pinpoint exact source locations
for introduced host populations.
4. For some studies, the focus was on a single parasite rather than a host’s full
complement of parasites (e.g. Charybdis longicollis, as described earlier),
which eliminated some potential host–parasite systems from our study.
On the whole, we attempted to ensure we were including the best
understanding of parasite diversity in both native and introduced ranges,
and in many cases, we conducted extensive additional research of the lit-
erature to uncover hosts that may not have been reported in particular
studies comparing invasive versus host parasites.
5. Our study focused specifically on parasite richness and thus did not
include parasite abundance or prevalence. Because source region parasite
prevalence would be expected to dictate recipient region parasite prev-
alence, those parasites with high prevalences in source regions would be
more likely to be associated with introduced host populations that may
then become established and potentially achieve high prevalences in
introduced regions as well (Miura et al., 2006; Torchin et al., 2003).
While our focus on parasite richness provides a measure of parasite
escape, it does not impart the full understanding of the parasite propagule
pressure of the native region, since it lacks knowledge of the abundance
of a particular parasite in the native or introduced populations, which
may help predict the success of that particular species in introduced
ranges (Blakeslee et al., 2012; Torchin and Mitchell, 2004).
6. Finally, there are several limitations to our understanding of introduction

timing of parasites that may influence or mask possible trends in our dataset.
For one, we based introduction timing on the host’s introduction timing,
given that in virtually all cases there is no information on when parasites
were actually introduced. Moreover, the introduction timing of the para-
sites would largely depend on the invasion pathway of the host, as well as the
ability of the parasite to successfully reproduce and expand in the introduced
range. In this sense, we have very little understanding of the historical nature
of parasitism in many of these hosts. Second, the parasite escape values used
in our study represent a snapshot of parasite richness in native and intro-
duced regions taken within the last two decades, and therefore, we cannot
be certain if those values are entirely reflective. However, there is some evi-
dence (e.g. Blakeslee and Byers, 2008; Blakeslee et al., 2012; Kube et al.,
2002) that parasite richness is more robust to annual fluctuations/
stochasticity than other variables. Even still, these limitations are likely to
have influenced our understanding of the potential link between time since
introduction and parasite escape across marine systems and point to the need
for better historical information (if it exists) and better temporal monitoring
of current invasions for parasite species richness.
Even with these limitations, our data still uncovered significant patterns of
parasite escape across host–parasite systems globally—particularly for our
more focused analysis of trematode parasites. Clearly, enhanced datasets will
resolve some of the questions that still remain and will also eliminate some of
the potential sampling biases that exist. We therefore encourage more
detailed, as well as temporal, exploration of the systems included here, as
well as those that remain to be investigated. Moreover, further experimental
evidence is needed to ascertain the actual impact that parasite escape is hav-
ing on introduced hosts, in as far as the potential for enemy release and asso-
ciated benefits, when compared to native individuals.
5. CONCLUSIONS
Parasite escape is a global phenomenon that has garnered increasing
awareness over the past two decades. Our work here has added to the current
research, providing greater understanding of the multiple variables that interact
to influence parasite escape across parasite taxa, host taxa, introduction vector,
time, and geography. We uncovered several significant mechanistic factors,
most notably related to introduction vector/strength and host taxa, as well as
the importance of categorical grouping on regressions of continuous variables

in revealing specific attributes that drive significant patterns.
Our study therefore enhances the baseline knowledge that currently
exists regarding the outcomes of marine invasions on hosts and parasites;
yet much still needs to be learned, especially the consequences of parasite
escape and release not only on individuals and populations but also on com-
munity dynamics. For example, there is evidence for parasite-mediated
competition in two Pacific North American snail species, B. attramentaria
(invader) and Cereithidea californica (native), which has resulted in the replace-
ment of the native’s parasite fauna with that of the invader’s (Lafferty and
Kuris, 2009; Miura et al., 2005) and the potential for cascading effects in
the community (Rohde, 2005; Torchin et al., 2005), thereby demonstrating
the significant influence of parasites in marine ecosystems and how marine
invasions can disrupt or enhance infection cycles, either through the
removal or addition of parasites as a result of invasion processes
(Rohde, 2005).
Finally, we return to the question originally posed in the introduction,
why do some invasive species fare so well in novel environments, sometimes even ‘bet-
ter’ than natives in the same environment? While much still needs to be learned
in order to answer this question, our research here does provide more evi-
dence towards its resolution, in that we have further supported the case for
parasite escape as a likely significant force in affording some invasive hosts an
advantage over natives. As more studies are completed, however, it remains
to be seen what further evidence is revealed and how strong the relationship
is between parasite escape and enemy release.
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CHAPTER THREE
Echinoderm Responses
to Variation in Salinity
Michael P. Russell1
Biology Department, Villanova University, Villanova, Pennsylvania, USA
1
Corresponding author: e-mail address: michael.russell@villanova.edu
Contents
1. Introduction 172
1.1 Echinoderm distribution and diversity 172
1.2 The relevance and brief history of salinity measures 173
2. Salinity Tolerance and Response 175
2.1 Field reports 175
2.2 Biogeographic patterns 182
2.3 Experimental studies of tolerance and response 183
3. Biologically Important Ions 193
4. S. droebachiensis and Hyposalinity 194
4.1 Juvenile acclimation study 195
4.2 Adult acclimation limits study 198
5. Future Prospects and Aquaculture Implications 203
Acknowledgements 204
References 204
Abstract
Although Echinodermata is one of the only stenohaline phyla in the animal kingdom,
several species show remarkable abilities to acclimate and survive in euryhaline habitats.
The last comprehensive review of this topic was over 25 years ago and much work has
been published since. These recent studies expand the field reports of species living in
hyposaline environments and detail experimental research on the responses, physiolog-
ical range, and limits of echinoderms to salinity challenges. I provide a brief review of the
historical concepts and measures of salinity and relate this overview to the physiological
and ecological studies on echinoderms. Many marine biologists are not aware that
chemical oceanographers advocate abandoning today’s commonly used measure of
salinity, ‘PSU’, in favour of absolute salinity (SA)—a return to the ppt (%) metric. The lit-
erature survey reveals only one euryhaline-tolerant species in the Southern Hemisphere
(there are 42 in the North) and more euryhaline species in the geologically older, brack-
ish seas. The green sea urchin, Strongylocentrotus droebachiensis, is one of the most tol-
erant echinoids to hyposalinity. Different source populations have varying levels of
acclimation and tolerance to hyposalinity. Experiments show that green urchins
Advances in Marine Biology, Volume 66 #2013 Elsevier Ltd 171

http://dx.doi.org/10.1016/B978-0-12-408096-6.00003-1
172 Michael P. Russell
previously unexposed to hyposalinity experience a clear decrease in growth rates; how-

ever, this adverse effect is short lived. Green urchins already acclimated to hyposalinity
can endure intense and repeated bouts and grow at the same rate of urchins not
exposed. Promising future work on the physiological and cellular mechanisms of
hyposalinity acclimation includes comparative studies of the role of heat shock proteins
in the response to changing salinities.
Keywords: Echinoderms, Sea urchins, Salinity, Stressors, Hyposalinity, HSP,
Acclimation, Strongylocentrotus droebachiensis
1. INTRODUCTION
1.1. Echinoderm distribution and diversity
In her classic treatise, The Invertebrates, Hyman (1955) described the phy-
lum Echinodermata as “exclusively marine [and] among the most common
and widely spread of marine animals. They occur in all seas and at all latitudes
and at all depths from the intertidal zone to the ocean depths” (p. 6). The
approximate 6500–7000 species (Pawson, 2007; Pearse et al., 1987;
Ruppert et al., 2004) are in five extant classes: 30% in Ophiuroidea (brittle
stars), 27% in Asteroidea (sea stars), 19% in Holothuroidea (sea cucumbers),
14% in Echinoidea (sea urchins and sand dollars), and 10% in Crinoidea (sea
lilies and feather stars). Sea stars and sea urchins can have significant top-
down effects on benthic community structure through their foraging and
grazing activities (Estes et al., 1998, 2011; Harrold and Pearse, 1987;
Paine, 1969; Uthicke et al., 2009; Watanabe and Harrold, 1991) and sea
cucumbers and sea urchins are important fisheries (Andrew et al., 2002;
Purcell et al., 2012). Exploring the effects of salinity fluctuations on echino-
derms will elucidate one of the most important abiotic factors that influences
their distribution patterns in nearshore communities and may help
policymakers craft sustainable strategies for managing these valuable and lim-
ited resources (Anderson et al., 2011; Micael et al., 2009).
In identical phrases, Hyman (1955) described both asteroids (p. 383) and
echinoids (p. 564) as having ‘practically no power of osmotic regulation’.
Although echinoderms lack dedicated excretory–osmoregulatory organs,
some excretory functions have been assigned to peristomal gills in echinoids
(Cobb and Sneddon, 1977; Santos-Gouvea and Freire, 2007) and the rectal
caeca in asteroids, holothuroids, and echinoids (Warnau and Jangoux, 1999;
Warnau et al., 1998). Brusca and Brusca (2003) also considered echinoderms
“strictly marine, stenohaline creatures” and attributed their absence from
Echinoderms and Salinity 173
freshwater habitats to “their cutaneous gas exchange methods and their lack
of excretory–osmoregulatory structures”; however, they concede “a num-
ber of species have been reported from brackish water [and that] some mech-
anism allows them to survive in these low salinities”.
Echinoderms encounter hyposaline conditions in coastal areas where
freshwater outflow from rivers and rainfall, or melting ice, mixes with sea
water. These areas are far more common and widely distributed than
basins that have hypersaline conditions, for example, the Persian Gulf and
Gulf of Suez. Although representatives of all classes except crinoids
have been reported in both hyper- and hyposaline environments, there
are many more field reports and laboratory studies of echinoderms in
brackish and hyposaline waters (see Tolerance and Response sections 2.1
and 2.3).
1.2. The relevance and brief history of salinity measures

Salinity, and variation in salinity, affects marine organisms from cellular
(homeostatic responses) to community and ecosystem levels (distribution
and dispersion patterns). The ionic gradients that salinity fluxes establish
at the membrane level present a myriad of physiological challenges. Salinity
is second only to temperature among abiotic factors in determining abun-
dance and distribution patterns (Kinne, 1964).
The evolution of techniques and metrics to quantify salinity in the last
50 years has been driven primarily by the needs of physical and chemical
oceanographers to characterize the thermodynamic properties of sea water
(Millero, 2010). Accurate and precise estimates of salinity are crucial in
their efforts as salinity affects density and, together with temperature, drive
large-scale, deep-water circulation and much of the Earth’s climate cycle.
Recent evidence suggests climate change-induced salinity alterations may
have important effects on this global cycle (Curry et al., 2003; Curry and
Mauritzen, 2005; Helm et al., 2010; Zhang and Wu, 2012).
The concept of salinity is simple and straightforward—it is a measure of
the grams of solute in a kilogram of water (Table 3.1).
The symbol % can be used to report salinity and indicates parts per thou-
sand (ppt) or g kg1. However, accurately quantifying salinity is not as sim-
ple as defining it. If one could evaporate all the water from a sample and
weigh the remaining dried solutes, then you would have an accurate mea-
sure of salinity. The problem is the extremely high temperatures (500 C)
required to liberate all the water would result in the loss of volatile solutes
Table 3.1 Major ions in sea water at 35% (Chester and Jickells, 2012)
Ion g kg1 %
Cl 19.3540 55.29
þ
Na 10.77 30.77
SO2
4 2.712 7.75
2þ
Mg 1.290 3.69
2þ
Ca 0.4121 1.18
þ
K 0.399 1.14

Br 0.0673 0.19
and the release of CO2 and HCl gas from the reaction and decomposition of
other solutes (Emerson and Hedges, 2008). This problem is partially resolved
because the relative proportions of the major ions in sea water are the same
regardless of total concentration—quantifying one solute yields an accurate
estimate of all the solutes and total salinity (Table 3.1).
Nineteenth-century workers established this concept of constancy of
composition, which was summarized by Marcet (1819, p. 194): “. . .with
the exception of the Dead Sea, and the Lake Ourmia, which are mere salt
ponds, perfectly unconnected with the ocean, all the specimens of sea water
which I have examined, however different in their strength, contain the
same ingredients all over the world, these bearing very nearly the same
proportions to each other; so that they differ only as to the total amount
of their saline contents.” This ‘first law of chemical oceanography’
(Millero, 2010) is also known as Marcet’s principle, Forchhammer’s princi-
ple of constant proportions, or simply the principle of constant proportions
(Millero et al., 2008). Early workers could accurately measure the chloride,
iodides, and bromides in sea water using titration with silver nitrate. This
method led to the ‘chlorinity’ metric of salinity and it was used into the
mid-twentieth century (Chester and Jickells, 2012) and some echinoderm
studies reported salinity as ‘chlorinity’ as late as 1972 (Por, 1972).
Other methods of quantifying salinity in terms of ppt using hydrometers
and refractometers became more available to marine biologists in the mid-
twentieth century. The level of accuracy of these devices was limited (1 part
in 50 for hydrometers and 1 part in 70–700 for refractometers) relative to titra-
tion (1 part in 3000–8000) methods (Pilson, 2012); however, these devices
were more convenient and efficient and provided adequate resolution for
most ecological and physiological investigations. Following the development

and refinement of salinometers that used temperature-calibrated conductivity
measures to quantify salinity, oceanographers moved away from chlorinity to
salinity–conductivity estimates and introduced the practical salinity scale (S—
Lewis, 1982; Lewis and Perkin, 1978). S is a conductivity ratio of a sample to
standard sea water of known ionic composition and therefore has no units. It
was calibrated carefully to yield a value of 35.000 for standard sea water when
the conductivity ratio was 1 at 15 C and one atmosphere. The practical salin-
ity scale and measures of salinity based on density (%) are the same for coastal
and marine environments and within 0.05 units for very dilute estuarine
waters (Millero, 1984). Since the development of S, many publications
reporting salinity use the erroneous notation ‘psu’ or ‘PSU’ (practical salinity
units) but this is clearly not what oceanographers intended (Millero, 1993,
2010) and unfortunately this mistake is perpetuated in many marine biology
textbooks (e.g. Levinton, 2009).
The most recent change to estimating salinity is at the heart of TEOS-10,
the Thermodynamic Equation Of Seawater—2010 (Pawlowicz, 2010). This
standard for quantifying sea water properties was adopted jointly by the Sci-
entific Committee on Oceanic Research (SCOR), the International Asso-
ciation for the Physical Sciences of the Oceans (IAPSO), and the
Intergovernmental Oceanographic Commission (IOC). They advocate
abandoning the practical salinity scale and instead using ‘absolute salinity’
or SA. This shift represents a return to using ppt because they define SA
as having units of g kg1. The necessary tools, programmes, and information
for implementing this change are available at www.teos-10.org and Millero
(2010) provided an engaging and personal account of the development of
the concepts of salinity and their relation to the current metrics of
quantifying it.
2. SALINITY TOLERANCE AND RESPONSE

In this section I build upon the earlier work from two excellent
reviews. Binyon (1966) provided the first in a chapter from the classic syn-
thesis ‘Physiology of Echinodermata’ and two decades later Stickle and
Diehl (1987) updated and expanded on this work.
2.1. Field reports

Table 3.2 provides a review of field reports of echinoderms in hyposaline
and hypersaline environments. It refines and adds to the previous two
Table 3.2 Echinoderms reported in both hyposaline and hypersaline environments

Tolerated
Species Site (%) References
HYPOSALINE
Asteroidea
Asterias forbesi East coast N. 14 Gosner (1971)
America
Long Island Sound 18 Loosanoff (1945)
Asterias rubens Loch Etive, United 16 Binyon (1976)
Kingdom
Baltic Sea 8 Brattström (1941)—in
German, cited in
Binyon (1966) and
Stickle and Diehl (1987)
(Reported as Asterias East coast N. 18 Gosner (1971)
vulgaris) America
Baltic Sea 8 Schlieper (1957)
The Netherlands 18 Wolff (1968)
Baltic Sea 11.1 Gulliksen (1977)
(Reported as Asterias Narraguagus Bay, 27.4 Topping and Fuller
vulgaris) Maine (1942)
Astropecten articulatus San Carlos Bay, 23.0–32.9 Gunter and Hall (1965)
Florida
Crossaster papposus Cape Shelagsk, 24 Dyakonov (1955) (in
(reported as Solaster Russia Russian)
papposus)
Echinaster sentus San Carlos Bay, 23.0–35.0 Gunter and Hall (1965)
Florida
Evasterias troscheli Lynn Canal, Alaska 11 Stickle and Demoux
(reported as Evasterias (1976)
troschelii)
Leptasterias hexactis Lynn Canal, Alaska 13 Stickle and Diehl
(1987)
Leptasterias polaris Gulf of St. 9.6 Drouin et al. (1985)
Lawrence
Table 3.2 Echinoderms reported in both hyposaline and hypersaline

environments—cont'd
Tolerated
Luidia clathrata Tampa Bay, Florida 18 Lawrence (1973)
Tampa Bay, Florida 22 Watts and Lawrence
(1986)
Marthasterias glacialis Black Sea 18 Tortonese and Demir
(1960)
Patiriella regularis Doubtful Sound, 3.7 Barker and Russell
New Zealand (2008)
Urasterias lincki East coast N. 15 Gosner (1971)
America
(Reported as Asterias White Sea 28 Zenkevitch (1963)
lincki)
Echinoidea
Echinocardium cordatum The Netherlands 27 Wolff (1968)
Echinocyamus pusillus Sado Estuary, 14.8 Monteiro-Marques
Portugal (1982)
Echinometra lucunter San Carlos Bay, 23.0–25.6 Gunter and Hall (1965)
(reported as Echinometra Florida
lacunter)
Lytechinus variegatus San Carlos Bay, 23.0–32.9 Gunter and Hall (1965)
Florida
Mellita quinquiesperforata San Carlos Bay, 24.5–30.8 Gunter and Hall (1965)
(reported as Mellita Florida
quinquesperforata)
Psammechinus miliaris The Netherlands 27 Wolff, 1968
Sado Estuary, 26.3 Monteiro-Marques
Portugal (1982)
Strongylocentrotus Lynn Canal, Alaska 14.1 Stickle and Demoux
droebachiensis (1976)
Gulf of St. 9.6 Drouin et al. (1985)
Lawrence
Continued

Tolerated
Holothuroidea
Cucumaria kirschbergii Sado Estuary, 29 Monteiro-Marques
Portugal (1982)
Cucumaria miniata Lynn Canal, Alaska 18 Stickle and Diehl (1987)
(reported as Cucumaria
mineata)
Cucumaria vega Lynn Canal, Alaska 13.5 Stickle and Demoux
(1976)
Eupentacta quinquesemita Lynn Canal, Alaska 17.8 Stickle and Demoux
(1976)
Leptosynapta inhaerens Black Sea 18.46 Bacesco and
Margineanu (1959)
Oestergrenia digitata Black Sea 18 Zenkevitch (1963)
Black Sea 18 Tortonese and Demir
(1960)
Stereoderma kirchsbergii Black Sea 15–18 Cherbonnier (1960)
(reported as Stereoderma
kirschbergi)
Sclerodactyla briareus Woods Hole, 50% sea Pearse (1908)
(reported as Thyone Massachusetts water
briareus)
Synapta hispida Black Sea 18 Zenkevitch (1963)
Ophiuroidea
Amphipholis squamata Sado Estuary, 23.5 Monteiro-Marques
Portugal (1982)
Amphiura chiajei Sado Estuary, 14.8 Monteiro-Marques
Portugal (1982)
Scotland 20.7 Pagett (1980b)
Black Sea 18 Tortonese and Demir
(1960)
(Reported as Amphiura Black Sea 18 Zenkevitch (1963)
florifera)

Tolerated
Amphiura filiformis Sado Estuary, 25.5 Monteiro-Marques
Portugal (1982)
Black Sea 8.9 Sezgin and Dağlı
(2009)
Ophiocten sericeum Chukotsk Sea 28 Dyakonov (1955)
Ophiocten sp. Cape Shelagsk, 25 Dyakonov (1955)
Russia
Ophioderma brevispina San Carlos Bay, 21.4–34.2 Gunter and Hall (1965)
Florida
Ophiolepis elegans San Carlos Bay, 22.3–35.0 Gunter and Hall (1965)
Florida
Ophiopholis aculeata Gulf of St. 9.6 Drouin et al. (1985)
Lawrence
White Sea 28 Zenkevitch (1963)
Ophiothrix angulata Cedar Key, Florida 16 Stancyk and Shaffer
(1977)
Ophiophragmus Whitewater Bay, 7.7 Thomas (1961)
filograneus Florida
Ophiothrix fragilis The Netherlands 27 Wolff (1968)
Ophiura albida Scotland 20.7 Pagett (1980b)
Ophiura ophiura The Netherlands 27 Wolff (1968)
(reported as Ophiura
texturata)
Ophiura robusta Gulf of St. 9.6 Drouin et al. (1985)
Lawrence
Stegophiura nodosa Chukotsk Sea 28 Dyakonov (1955)
HYPERSALINE
Asteroidea
Aquilonastra burtoni Al-Uqair, Persian 60 Price (1982)
(reported as Asterina Gulf
burtoni)
Continued

Tolerated
Astropecten hemprichi Dammam, Persian 43 Price (1982)
Gulf
Astropecten monacanthus Dammam, Persian 43 Price (1982)
Gulf
Astropecten polyacanthus Dammam, Persian 60 Price (1982)
phragmorus Gulf
Linckia multifora Dammam, Persian 43 Price (1982)
Gulf
Luidia maculata Dammam, Persian 43 Price (1982)
Gulf
Echinoidea
Clypeaster humilis Dammam, Persian 43 Price (1982)
Gulf
Echinodiscus auritus Dammam, Persian 43 Price (1982)
Gulf
Echinometra mathaei Dammam, Persian 43 Price (1982)
Gulf
Nudechinus scotiopremnus Bitter Lake, Suez 45 Por (1972)
Canal
Temnopleurus Dammam, Persian 43 Price (1982)
toreumaticus Gulf
Holothuroidea
Holothuria leucospilota Dammam, Persian 43 Price (1982)
Gulf
Leptosynapta chela Al Qurayyah, 55 Price (1982)
Persian Gulf
Synaptula reciprocans Bitter Lake, Suez 45 Por (1972)
Canal
Ophiuroidea
Amphipholis squamata Al Qurayyah, 55 Price (1982)
Persian Gulf

Tolerated
Amphiura fasciata Al Qurayyah, 55 Price (1982)
Persian Gulf
Ophiothrix savignyi Persian Gulf 43 Price (1982)
All species names checked on the World Register of Marine Species (WoRMS—www.marinespecies.
org) for taxonomic status (accepted). The name originally reported is also listed if different from the cur-
rent accepted taxonomy. The salinity levels, tolerated (%), are the values reported in the References.
For species listed by Wolff (1968) and Por (1972)—Cl (chlorinity) levels converted to salinity (%) using
the formula (% ¼ 0.03 þ 1.805Cl; Millero, 2010); Topping and Fuller (1942) salinity calculated from
reported freezing points (www.csgnetwork.com/h2ofreezecalc.html) and percentage of freshwater/sea
water mix. This table is modelled after the reviews of Binyon (1966; Table 15.1) and Stickle and Diehl
(1987; Table 1). There are several corrections and edits to the data reported in their tables based on exam-
ination of the original references: Segerstråle (1949) did not report Asterias rubens or Ophiura albida in the
Baltic Sea; Zenkevitch (1963) did not report Cucumaria orientalis (no records of this species in WoRMS),
Ophiothrix fragilis, or Ophiura texturata (accepted name ¼ Ophiura ophiura) in the Black Sea; Tortonese and
Demir (1960) did not report Echinus acutus (accepted name ¼ Gracilechinus acutus) or Amphipholis squamata
in the Black Sea. Dyakonov (1955—in Russian but species names in English) lists Solaster papposus
(accepted name ¼ Crossaster papposus) not Solaster sp.; and several additional records not reported in
the tables of Binyon (1966) or Stickle and Diehl (1987) but found in the original references are included.
seminal reviews. The names of all 60 species were verified in WoRMS

(World Register of Marine Species www.marinespecies.org) and the refer-
ences were thoroughly reviewed for location and reported levels of salinity.
When possible, conversions were calculated when salinity was not reported
originally as % (Table 3.2).
After taking into account edits and taxonomic changes, Binyon (1966) cat-
alogued 18 species from hyposaline environments (4 asteroids, 5 holothurians,
and 9 ophiuroids). Stickle and Diehl (1987) reported 34 species from hyposaline
environments (9 asteroids, 4 echinoids, 9 holothurians, and 12 ophiuroids) and
16 species from hypersaline environments (5 asteroids, 5 echinoids, 3 holothu-
rians, and 3 ophiuroids). The current accounting (Table 3.2) shows 43 species
from hyposaline environments (12 asteroids, 7 echinoids, 9 holothurians, and
15 ophiuroids) and 17 species from hypersaline environments (6 asteroids, 5
echinoids, 3 holothurians, and 3 ophiuroids). Although some species of crinoids
occur in shallow-water habitats, none have been reported in the field from
either hypo- or hypersaline environments.
The lowest published salinity level (Table 3.2) observed in the field is for the
small cushion star, Patiriella regularis (Barker and Russell, 2008), at 3.7% in
Doubtful Sound, New Zealand. This sea star is common in the shallow subtidal of
Fiordland where unique weather patterns (as much as 7 m of rainfall per year) and
hydrographic conditions produce a low-salinity layer (LSL) that is nearly fresh-
water for extended periods (Gibbs, 2001; Gibbs et al., 2000). The depth and range
of the LSL varies with rainfall patterns and tidal fluctuation, and P. regularis can be
exposed to near-freshwater conditions for days at a time in the LSL.
The highest published salinity levels (Table 3.2) observed in the field
are for the asteroids Aquilonastra burtoni (from Al-Uqair) and Astropecten
polyacanthus phragmorus (from Dammam Channel), at 60% in the Western
Persian Gulf (Price, 1982). Two ophiuroids, Amphipholis squamata and
Amphiura fasciata, and one asteroid, Leptosynapta chela, (all from Al Qurayyah)
have been reported at 55% (Price, 1982). High summer temperatures
(45–50 C) combined with limited input from rivers result in high evapo-
ration rates producing these extreme hypersaline conditions. Price (1982)
stated that salinity levels as high as 70% occur south of these sites and that
in ‘hypersaline lagoons salinities may exceed 200%’ (although no echino-
derms are reported from these areas). He also suggested that these hyper-
saline conditions may cause dwarfism and presented data comparing the
smaller sizes of Aquilonastra burtoni and Astropecten polyacanthus phragmorus
from sites with a salinity range of 52–60% to larger sizes from sites with
salinity ranging from 40% to 43%.
2.2. Biogeographic patterns

Interesting global distribution patterns emerge from the survey summarized in
Table 3.2. There is only one field report of a hyposaline occurrence from the
Southern Hemisphere (P. regularis from Doubtful Sound (Barker and Russell,
2008)), whereas the other 42 instances are restricted to the Northern Hemi-
sphere. There are no reports of echinoderms from hypersaline environments
in the Southern Hemisphere and all 17 instances in the north occur in the Persian
Gulf or Bitter Lakes, which is north of the Gulf of Suez (Por, 1972; Price, 1982).
The Gulf of Mexico is the region with the highest number of species
(n ¼ 10) and includes all the sites listed in Florida (Table 3.2). However, this
high number must be viewed cautiously as 7 of these occurrences from
Gunter and Hall (1965) are from a single site (San Carlos Bay). Their report
includes a range of salinities for all 7 species and it is not clear if they were found
at the low end of the range. Two mutually exclusive sets of 8 species occur in the
western and eastern Atlantic. In the eastern Atlantic, there are three species from
Loch Etive in Scotland (Binyon, 1976; Pagett, 1980b) and five species from
Sado Estuary in Portugal (Monteiro-Marques, 1982). The western Atlantic
includes four species from the Gulf of St. Lawrence (Drouin et al., 1985),
one from the Woods Hole area (Pearse, 1908), one from Narraguagus Bay
in the Gulf of Maine (Topping and Fuller, 1942), and one from Long Island
Sound (Loosanoff, 1945); the remaining species (Urasterias lincki) was reported
by Gosner (1971) as occurring at sites with ‘a salinity as low as 15%’.
Two of the largest brackish seas have very different echinoderm diversi-
ties. The Black Sea has 7 species, whereas the Baltic Sea has only one (Asterias
rubens). This difference is probably the result of the very disparate ages of these
two bodies of water. Geologically, the Baltic Sea is relatively young at
10,000–15,000 years (Ojaveer et al., 2010). In stark contrast, estimates of
the age of the Black Sea exceed 50 million years (Kazmin et al., 2007).
The remaining areas with reports of echinoderms found in hyposaline
environments are the North Sea with 5 species (Wolff, 1968), the Pacific
Northwest with 6 species (Stickle and Demoux, 1976; Stickle and Diehl,
1987), and the seas of northern Russia with 5 species (Dyakonov, 1955;
Zenkevitch, 1963).
2.3. Experimental studies of tolerance and response

Table 3.3 provides a review of studies evaluating the tolerance and survival
of postmetamorphic (juveniles and adult) and premetamorphic (larvae and
gametes) echinoderms in hyposaline and hypersaline treatments. It refines
and adds to the previous two seminal reviews of Binyon (1966) and
Stickle and Diehl (1987). The names of all 55 species were verified in
WoRMS and the references were thoroughly reviewed for treatment (range
of salinities), survival, and mortality levels. Some studies reported only sur-
vival data, others tolerance levels, and still others both. The duration of
exposures varies from a few hours to weeks.
After taking into account edits and taxonomic changes, Binyon (1966)
reported 8 studies evaluating 7 species: 2 asteroids, 1 crinoid, and 3 echinoids;
there were no studies of holothurians or ophiuroids. Stickle and Diehl (1987)
raised the number to 25 studies of 29 taxa: 8 asteroids, 1 crinoid (the same one),
11echinoids, 1 holothurian, and 8 ophiuroids. The 90 studies reviewed in
Table 3.3 include the reports from the previous two reviews and nearly double
the number of species to 55 since the study of Stickle in Diehl 26 years ago.
There are 19 asteroid species (17 adult and juvenile and 7 larvae—5 common
Table 3.3 Echinoderms, both postmetamorphic (adults and juveniles) and

premetamorphic (larvae), tested in hyposaline and hypersaline conditions
Range
examined
Low High Tolerated Mortality
Species (%) (%) (%) (%) References
ADULTS AND JUVENILES
Asteroidea
Asterias amurensis 6 32 22 20 Kashenko (2003)
Asterias forbesi 0 30 18 16 Wells (1961)
7.5 20 16–18 14 Loosanoff (1945)
15 42.5 16–34 White Sea Sarantchova (2001)
20–40 Barentz Sea
Asterias rubens 25 18 Binyon (1961)
16 32 26 Shumway (1977)
(Reported as 22 32.7 27.4 22 Topping and Fuller
Asterias vulgaris) (1942)
(Reported as 5.7 27.5 14 12 Smith (1940)
Asterias vulgaris)
Asterina gibbosa 14 70 14 Emson (1979)
Asterina phylactica 14 70 18/44 14/53 Emson (1979)
Astropecten 16 32 26 Shumway (1977)
irregularis
Crossaster 16 32 26 Shumway (1977)
papposus
(reported as
Solaster papposus)
Cryptasterina sp. 26 34 26/34 Chen and Chen (1993)
(reported as
Patiriella
pseudoexigua)
Henricia 16 32 26 Shumway (1977)
sanguinolenta
Leptasterias 10 30 15 10 Shirley and Stickle
hexactis (1982)

premetamorphic (larvae), tested in hyposaline and hypersaline conditions—cont'd
Range
examined
Luidia clathrata 17 27 17 Forcucci and
Lawrence (1986)
16 26 16 Watts and Lawrence
(1990)
20 30 20 Kaack and Pomory
(2011)
16 27 16 Ellington and
Lawrence (1974)
16 22 16 Watts and Lawrence
(1986)
15 35 15 Diehl and Lawrence
(1985)
Odontaster validus 50% Full 50% Pearse (1967)
strength
Patiria pectinifera 6 32 18 16 Kashenko (2003)
Patiriella exigua 20 25 20 Binyon (1977)
(reported as
Asterina exigua)
Patiriella 0 34 25 15 Barker and Russell
mortenseni (2008)
Patiriella regularis 0 34 5 0 Barker and Russell
(2008)
Pisaster ochraceus 15 30 15 Stickle and Ahokas
(1974)
Held and Harley
(2009)
15 30 20 15 Bamfield population
15 30 15 Vancouver population
22 32 22 Pia et al. (2012)
Continued

Range
examined
Crinoidea
Tropiometra 75% 120% 75%/ 120% Clark (1917)
carinata 110%
Echinoidea
Arbacia lixula 25 35 25 Vidolin et al.
(2007)
15 45 21 15 Santos et al.
(2013)
20–22 26 Petersen and Almeida
(1976)
Arbacia 0 30 20 18 Wells (1961)
punctulata
Echinarachnius 10 32 20 Allen and Pechenik
parma (2010)
Echinocardium 20 33 28 24 Kashenko (2006b)
cordatum
Echinometra 25 45 25 45 Freire et al. (2011)
lucunter
15 45 21 15 Santos et al. (2013)
25 45 25 45 Santos-Gouvea and
Freire (2007)
Evechinus 5 35 27 <25 Antonie (2003)
chloroticus
Heliocidaris 25 33.5 25 Lau et al. (2009)
crassispina
(reported as
Anthocidaris
crassispina)
(Reported as 5 45 25–35 <15/40 Kang et al. (1993)
Anthocidaris
crassispina)

Range
examined
Lytechinus 20 35 25 Bishop et al. (1994)
variegatus
25 35 25 Vidolin et al. (2007)
15 45 24 18 Santos et al. (2013)
20–22 26 Petersen and Almeida
(1976)
0 30 24 22 Wells (1961)
18 Stickle and Diehl
(1987)
25 40 25/40 Lawrence (1975)
2 36 18 2 Irlandi et al. (1997)
Psammechinus 15 Gezelius (1963)
miliaris (Z form)
Scaphechinus 12 34 14 12 Kashenko (2008)
mirabilis
Strongylocentrotus Himmelman et al.
14 30 14 St. Lawrence Estuary
14 30 16 14 Nova Scotia
12 30 15 12 Sabourin and Stickle
(1981)
21.5 32.5 21.5 Campbell and Russell
(2004)
21.5 23.3 21.5 Lange (1964)
12.5 30 15 12.5 Roller and Stickle
(1994)
15 30 15 Stickle and Ahokas
(1974)
17.5 35 17.5 Emerson (1969)
10 30 13 Stickle et al. (1990)
Continued

Range
examined
Strongylocentrotus 12.5 30 25 21 Roller and Stickle
pallidus (1994)
10 30 21.5 Stickle et al. (1990)
Strongylocentrotus 30% 170% 30–70% Giese and
purpuratus and Farmanfarmaian
120–170% (1963)
17 32.5 20.9 17 Burnett et al. (2002)
Holothuroidea
Apostichopus 20 40 25/40 20 Dong et al. (2008)
japonicus
22 36 22 Yuan et al. (2010)
22 38 22/38 Zhang et al. (2012)
20 30 20 Meng et al. (2011)
9 51 13/47 11/51 Hu et al. (2010)
Cucumaria 15 30 15 Stickle and Ahokas
miniata (1974)
Eupentacta 12 30 15 12 Sabourin and Stickle
quinquesemita (1981)
17.5 35 17.5 Emerson (1969)
Holothuria 15 40 30 25 Asha and Muthiah
spinifera (2005)
Isostichopus 20 48 20 48 Foglietta and Herrera
badionotus (1996)
Sclerodactyla 0% ¼ 59% 33% 25 % Pearse (1908)
briareus (reported fresh
as Thyone
briareus)
Ophiuroidea
Amphipholis 14 52 22–52 14–54 Emson and Foote
squamata (1980)

Range
examined
Amphiura chiajei 13.8 27.6 20.7 Pagett (1980b)
Ophiocomina 13.8 27.6 27.6 Pagett (1980b)
nigra
Ophioderma 15 30 15 Stickle et al. (1982)
brevispina
(reported as
Ophioderma
brevispinum)
Ophiophragmus 16 30 16 Talbot and Lawrence
filograneus (2002)
8 24 10 8 Turner (2007)
10 42 10/42 Turner and Meyer
(1980)
Ophiothrix 23 38 23 Donachy and Watabe
angulata (1986)
12 30 16 14 Stancyk and Shaffer
(1977)
Ophiura albida 13.8 27.6 20.7 Pagett (1980b)
LARVAE
Asteroidea
Acanthaster planci 22 35 26 22 Lucas (1973)
Asterias amurensis 8 32 22 18 Kashenko (2005)
3 70 15 Sagara and Ino (1954)
Asterias rubens 21 35 27 Sameoto and Metaxas
(2008b)
18 35 24–27 Sameoto and Metaxas
(2008a)
8 45 12 8 Saranchova et al.
(2006)
Continued

Range
examined
Echinaster sp. 25 39 25 Watts et al. (1983)
25 39 32 Watts et al. (1982)
Luidia clathrata 25 35 25/35 Hintz and Lawrence
(1994)
Patiria pectinifera 12 34 18 16 Kashenko (2006a)
Pisaster ochraceus 20 30 20 Roller and Stickle
(1985)
Echinoidea
Arbacia lixula 22 42 26 Petersen and Almeida
(1976)
Dendraster 11 21 15 11 Arellano et al. (2012)
excentricus
15 32 15 George and Walker
(2007)
Echinocardium 22 36 20 Kashenko (2007)
cordatum
Echinometra 22 42 26 Petersen and Almeida
lucunter (1976)
15 33 21 short 27 long Metaxas (1998)
term term
Evechinus 5 35 27 <25 Antonie (2003)
chloroticus
Heliocidaris 20 45 25–40 20/45 Kang et al. (1993)
crassispina
(reported as
Anthocidaris
crassispina)
Lytechinus 22 42 26 Petersen and Almeida
variegatus (1976)
Mellita isometra 25 32 32 Schioupu and George
(2004)

Range
examined
Parechinus 10 41 20 Greenwood and
angulosus Bennett (1981)
Psammechinus Gezelius (1963)
miliaris
20 40 20–32 Shallow form (Z)
20 40 26–38 Deep form (S)
Scaphechinus 12 36 18 Kashenko (2009)
mirabilis
Sterechinus 30 34 30 Cowart et al. (2009)
neumayeri
Strongylocentrotus 20 30 20 Roller and Stickle
21 35 24 Sameoto and Metaxas,
2008b
15 35 24–27 Sameoto and Metaxas
(2008a)
Strongylocentrotus 11 33 20 Yaroslavtseva et al.
intermedius (2002)
pallidus (1985)
purpuratus (1985)
Parechinus 10 41 20 Greenwood and
angulosus Bennett (1981)
Holothuroidea
Apostichopus 14 32 22 20 Kashenko (2000a)
japonicus
10 45 20 15 Li and Li (2010)
Continued

Range
examined
Eupentacta 20 32 22 20 Kashenko (2000b)
fraudatrix
Cucumaria 24 34 24 Hamel and Mercier
frondosa (1996)
Ophiuroidea
Amphioplus 5 40 25 15 Hendler (1977)
abditus
All species names checked on the World Register of Marine Species (WoRMS—www.marinespecies.org)
for taxonomic status (accepted). The name originally reported is also listed if different from the current ac-
cepted taxonomy. The low (%) and high (%) salinity values examined are reported although many studies
included intermediate levels. If more than half survived the tested level, then this salinity reported as tolerated
(%); if more than half perished at the tested level, then this salinity reported as mortality (%). Three studies
reported salinity as a dilution percentage of sea water rather than %. This table is modelled after the reviews of
Binyon (1966; Table 15.2) and Stickle and Diehl (1987; Table 2), and differences between these two reviews
and the information below include (i) the exclusion of Hemipholis elongata (nomen dubium in WoRMS) and
Amphiodia limbata (no record but Amphiodia bimbata is nomen dubium in WoRMS) and (ii) Fredericq
(1922) excluding and only reporting ‘fragment of integument’ surviving for two echinoids (more recent data
are now available for Sphaerechinus granularis and Strongylocentrotus lividus).
to both), 1 crinoid, 22 echinoids (16 adult and juvenile and 16 larvae—10 com-
mon to both), 5 holothurians (3 adult and juvenile and 3 larvae—1 common to
both), and 8 ophiuroids (7 adult and juvenile and 1 larvae).
The earliest published study was the work of Pearse (1908) from the
Woods Hole, MA, area on the sea cucumber, Sclerodactyla briareus (reported
as Thyone briareus), which can occur at the mouths of rivers where salinity
fluctuates. Pearse showed that this species tolerates reductions of 50% in
salinity for up to 24 h. The next published study by Clark (1917) evaluated
the reaction of the crinoid, Tropiometra carinata, to both temperature and
osmotic challenges and showed that it had a narrow range of tolerance to
both stressors. This species does not occur in euryhaline areas. More than
25 years passed until two studies on the salinity tolerance of asteroids were
published. Topping and Fuller (1942) showed that Asterias rubens (reported
as Asterias vulgaris) from the Gulf of Maine could tolerate salinity exposures
<28% and Loosanoff (1945) established that Asterias forbesi from Long Island
Sound could tolerate salinities as low as 16–18%.
Many of the studies summarized in Table 3.3 have a physiological focus,

for example, the effects of reduced salinities on excretion or growth rates and
ionic concentrations in tissues (n ¼ 21). Most studies are ecological (n ¼ 29)
and evaluate salinity effects on abundance and distribution (9 studies com-
bine both physiological and ecological components). In addition, recent
work (n ¼ 9) has focused on the applied consequences of the effects of
hypo- and hypersalinity on the aquaculture production of two species of
sea cucumbers, Apostichopus japonicus and Holothuria spinifera (Asha and
Muthiah, 2005; Dong et al., 2008; Hu et al., 2010; Li and Li, 2010;
Meng et al., 2011; Yuan et al., 2010; Zhang et al., 2012), and one species
of sea urchin, Heliocidaris crassispina (Kang et al., 1993; Lau et al., 2009).
3. BIOLOGICALLY IMPORTANT IONS

A detailed synthesis of the many excellent studies examining the
behaviour of biologically important ions (Naþ, Cl, Ca2þ, Kþ, and
Mg2þ) in response to osmotic challenges is beyond the scope of this chapter;
however, it would not be complete without mentioning some key findings
of some recent studies.
Although Shumway (1977) found no evidence for ionic or osmotic reg-
ulation in four species of asteroids, several species of echinoderms show at least
a limited capacity to regulate key ions when faced with either hyperosmotic or
hyposmotic conditions. For example, intracellular Kþ was ‘well regulated’ in
the sea cucumber Isostichopus badionotus when challenged with both hypo-
(20%) and hyper- (48%) osmotic conditions, but Naþ and Cl were isos-
motic (Foglietta and Herrera, 1996). Similarly, in the brittle star Ophiocomina
nigra, Naþ and Cl were isosmotic in hyposaline water, but Kþ levels were
maintained at higher levels (Pagett, 1980a). The sea urchin, Echinometra
lucuntur, ‘held gradients for Mg2þ, Ca2þ, and Kþ’ in the coelomic fluid, in
both hypo- (20%) and hyper- (48%) conditions (Freire et al., 2011).
Vidolin et al. (2007) found that the echinoid, Lytechinus variegatus, displayed
some ionic regulation of Naþ and Kþ, and Santos et al. (2013) demonstrated
varying degrees of osmoconforming gradients in Naþ, Mg2þ, and Kþ for
three species of echinoids (L. variegatus, E. lucuntur, and Arbacia lixula).
It is clear that species across classes differ in their abilities to regulate ions when
faced with osmotic challenges. Some species like L. variegatus, E. lucuntur, and
Strongylocentrotus droebachiensis have a greater capacity to tolerate hyposalinity
treatments (Table 3.3). This ability to acclimate to and tolerate these conditions
is at least partially due to their limited abilities to control key ions.
4. S. DROEBACHIENSIS AND HYPOSALINITY

Of the taxa reviewed in Tables 3.2 and 3.3, the green sea urchin,
S. droebachiensis, seems the ideal species to explore the range and limits for
physiological acclimation to hyposalinity. As postmetamorphic juveniles
and adults, they occur in habitats subjected to tidal and seasonal salinity var-
iation (Drouin et al., 1985; Stickle and Demoux, 1976) and in stenohaline
environments (subtidal areas removed from freshwater run-off ). Several
studies show different levels of tolerance and mortality for different
populations. For example, Himmelman et al. (1984) compared a population
from the Gulf of St. Lawrence that is periodically exposed to hyposaline con-
ditions to one in Nova Scotia that is not. The population from the Gulf of St.
Lawrence could tolerate salinities as low as 14%, whereas for a population
from Nova Scotia, these low salinities caused complete mortality. The range
of reported salinities that cause mortality varies from as low as 12% for a
population from the Pacific Northwest to 21.5% for a Norwegian popula-
tion (Table 3.3).
Most acclimation studies are on the order of days or weeks and evaluate
behaviour (righting time) or a host of metabolic responses. Only one study
assessed growth in the face of osmotic challenges. Although Shirley and
Stickle (1982) found that there was overall positive growth in the sea star,
Leptasterias hexactis, exposed to 20% for 3 weeks, growth was much less than
in the controls held at 30%. In addition, the exposure ran at a consistent
hyposaline level for the duration of the experiment, and there was no oppor-
tunity to demonstrate acclimation/recovery to repeated exposures.
A single osmotic challenge without a period to recover would not show
the acclimation potential to variable conditions that exist in the field on a
seasonal or tidal temporal cycle. Repeated exposures to hyposalinity with
ample time to recover would allow a more robust quantification of whole
organism acclimation. Complimentary experiments using two populations
of S. droebachiensis, juveniles (section 4.1) collected from a stenohaline
environment and adults (section 4.2) from an area subjected to seasonal
episodes of hyposalinity, are described to illustrate this point. The experi-
ment using juveniles ran for 5 months and the one using adults lasted 1 year.
These studies demonstrated that juveniles from a stenohaline environment
can acclimate to hyposaline conditions, but there is a single, short-term cost
in growth rate. Adults from the euryhaline environment have already ‘paid’
this cost and show no short-term growth effects from repeated hyposaline
exposures.
4.1. Juvenile acclimation study

In September of 2000, juveniles were collected (all <10 mm test diameter)
from Cape Neddick, Maine (Nubble Light—43 090 5800 N 70 350 3300 W),
from a depth of 5 m. This stenohaline, subtidal habitat is on the exposed
coast of the Gulf of Maine. The urchins were transported back to the lab-
oratory and kept in a filtered, recirculating, 1000 liter, sea water system at a
constant temperature of 10 C, salinity of 31.5% (when not exposed to
hyposaline conditions), and 12:12 light/dark cycle.
On 25 October 2000, the urchins were partitioned into 20 replicates of
10 urchins per replicate (Table 3.4) so the means and variances of test sizes
were as uniform as possible. Each replicate was a cylindrical, open-top PVC
cage (10 cm diameter and 12 cm tall) with a mesh (5 mm) bottom. The
cages were suspended in the sea water system so the tops of the cages were
2.5 cm above the water line; see Deming and Russell (1999) for an illus-
tration of the cage design. Each cage was aerated and had filtered sea water
pumped directly into the centre. The same food was supplied to each cage—
a mixture of kelps and diced mussels. The urchins attached to the inside walls
of the cages and had easy access to the ad libitum food supply.
Ten replicates each were assigned randomly to a control group and a
hyposalinity treatment group, on 4 December 2000 (Table 3.4). Beginning
this day and every 2 weeks until 27 February 2001, the following protocol
was followed for the 24 h hyposalinity exposure. All food was removed from
the cages, test diameters measured, and wet weights recorded. Two shallow
Table 3.4 Sizes (mm—test diameters) of juvenile green sea urchins at 5 time points
before starting hyposaline treatments
Oct 25 Nov 7 Nov 20 Nov 27 Dec 4
Ind Rep Ind Rep Ind Rep Ind Rep Ctrl S%
Mean 7.90 7.90 8.12 8.12 8.36 8.35 8.63 8.62 8.97 8.97
sd 1.08 0.12 1.07 0.17 1.16 0.27 1.16 0.30 0.38 0.36
Min 5.44 7.69 5.42 7.70 5.52 7.81 5.82 7.82 8.27 8.28
Max 9.99 8.24 10.86 8.42 10.95 8.84 11.32 9.08 9.52 9.49
N 200 20 190 20 169 20 166 20 10 10
Ten individual (Ind) urchins were systematically assigned to one of 20 replicates (Rep) to homogenize
size and variance at the outset. On 4 December 2000, the 20 replicates were divided into two groups of 10
each so means and variances were approximately equal. These two groups of 10 were randomly assigned
to control (Ctrl) and hyposalinity (S%) treatments. There were 79 individuals in the Ctrl group and 81 in
the S% group when the hyposaline treatments began on December 4. Over the next 3 months there were
eight hyposaline exposures and only four mortalities among the individuals in the Ctrl group and three in
the S% group.
tanks (0.18 m deep 2.44 m long 0.84 m wide) were partially filled with
sea water (31.5%) and the control cages suspended in one and the
hyposalinity cages in the other. All cages were aerated and submersible
pumps provided thorough mixing in each tank. De-ionized water was added
to the hyposalinity treatment tank every 10 min, for 2 h, to reduce the salin-
ity to 23% (every 10 min the reduction was 0.71%). An equal amount of
sea water was added at each 10 min interval to the control tank.
After 22 h, hypersaline water was added to the treatment tank every
10 min over a 2 h period to raise the salinity back to 31.5% at the 24 h mark
(simultaneously, an equal amount of sea water was added to the control
tank). At this point, the posthyposalinity treatment wet weights were
recorded. After the hyposalinity treatment, all replicates were supplied with
food and restored to the sea water system. There were a total of 8 hyposaline
exposures (every 2 weeks).
Each day during the experiment, food in the cages was replaced and the
aeration and water flow rates adjusted as needed. Several mortalities were
recorded during this maintenance and the remains of the urchins were mea-
sured and removed. The numbers of urchins per replicate stabilized, and by
the end of the experiment, 15 of the 20 replicates had 8 or more individuals
and only one replicate had a minimum of 5 urchins (Table 3.4).
The change in weight was recorded between the start of the 24 h
hyposalinity treatment and the end for each replicate. As predicted, the mean
weight change for the hyposalinity group was always greater than the con-
trol. In all but one of the exposures (15 December 2000), these differences
were significant at the 0.05 level (t-tests). Although body fluid osmolarity
was not measured, it is safe to infer from the positive weight change and pre-
vious studies (Bishop et al., 1994; Freire et al., 2011; Santos et al., 2013;
Stickle and Ahokas, 1974; Vidolin et al., 2007) that osmolarity in the peri-
visceral fluid and body tissues decreased in the hyposaline treatment group.
Figure 3.1 plots the mean test diameters of the replicates versus the time
course of the experiment. The slopes of the three lines plotted quantify
growth rates because they represent change in size (y-axis) over change in
time (x-axis). From 4 December 2000 to 8 January 2001, there were four
bouts of hyposalinity treatments. It is clear that the growth rate of the
hyposalinity group decreased during this 35 days interval relative to the con-
trol group. The slope of the hyposalinity treatment during this period
(0.028 mm day1) is significantly less than the slope of the control group
(0.045 mm day1; t ¼ 6.63, p < 0.001). Although the mean size of the control
group on 8 January is larger (10.43 0.53 mm vs. 10.00 0.45 mm [sd] for
the hyposaline group), there is no significant difference (t ¼ 1.11, p ¼ 0.28).
14
13
Mean diameter (mm) ± SE Control

12
(0.045)
11
(0.043)
10
Hyposalinity
9 (0.028)
7
Nov Dec Jan Feb Mar
Date (2000–2001)
Figure 3.1 Growth rates of green sea urchins in juvenile hyposalinity experiment. All
data points are mean test diameters standard error. Open circles (n ¼ 20) are prior
to low-salinity treatments, open triangles (n ¼ 10) are controls, and grey squares
(n ¼ 10) are hyposalinity treatments. The numbers are slopes (growth rates) of the three
plotted regressions: control (0.45, 4 December–27 February), hyposalinity before accli-
mation (0.28, 4 December–8 January), and hyposalinity postacclimation (0.43, 20
January–27 February).
There were four bouts of hyposalinity treatments after 8 January, from

20 January to 27 February (Figure 3.1). The growth rates of the hyposalinity
group clearly rebounded to the levels of the control group during this
period. There is no significant difference between the control slope and
the ‘postacclimation’ hyposalinity treatment slope (0.043 mm day1;
t ¼ 1.22 and p ¼ 0.33). Although there was no difference in growth rates
between the two groups, the control rate of growth was slightly greater than
the treatment and this difference combined with the effect of the dramati-
cally reduced growth rate during the acclimation period in the hyposaline
group resulted in a significant difference in sizes between the two groups
on the final day of the experiment (t ¼ 2.54 and p ¼ 0.02).
This experiment demonstrates several points. First, juveniles from steno-
haline habitats have the capacity to endure repeated exposures to low salin-
ities. However, there is a cost as measured in the reduction in growth rate
following the initial exposures. This cost is short term as the growth rate
rebounded to the levels of the control group. Qualitative observations of
the reaction of urchins to low salinity include increased activity of tube feet
movement, greater pedicellaria activity, and a reduced ability of the tube feet
to adhere to the substratum (it took less force to dislodge urchins from the
wall of the cage). Although this experiment demonstrates the capacity of

green urchins to acclimate to hyposalinity on a short-time scale, it does
not address the mechanism of that acclimation (see section 5 for future pros-
pects and directions). This experiment does lead to predictions about adult
green sea urchins in habitats that experience periodic episodes of
hyposalinity. These urchins should already be acclimated and not show
the cost in growth rate relative to a control group. But can they endure lon-
ger periods of more extreme hyposalinity? To test this prediction (already
acclimated) and answer these questions (the potential range and limits of
physiological acclimation), a second experiment was conducted on an adult
population of green sea urchins from a nearby site.
4.2. Adult acclimation limits study

Samples for the adult acclimation study were collected from Little Harbor, in
New Castle, New Hampshire (43 040 1300 N 70 430 3100 W). Although this
site is only 16 km southwest of Cape Neddick (the source of urchins for the
juvenile acclimation study on the exposed open coast), it is a very different
habitat. Little Harbor is a small, sheltered channel, in the Piscataqua River,
5 km from the open coast. Although there are no historical salinity records
from Little Harbor, data from the Coastal Marine Lab (University of New
Hampshire) are available, which is 2.5 km down-river near the open coast
in the mouth of the Piscataqua at Fort Constitution. Daily measures of salin-
ity at the laboratory provide a conservative historical record of euryhalinity
at the collection site because salinity decreases upriver.
Salinity records (1993–2000) from the Coastal Lab show a distinct sea-
sonal pattern with greater frequency and intensity of hyposaline events in the
spring (Figure 3.2). March and April have the lowest average salinities and
the greatest number of days recording salinities <26%. The lowest salinity
documented during this 8-year period was 15% on 27 March 1994 and the
lowest salinities of each year occurred from as early as 8 March (1999—21%)
to as late as 16 June (1998—16%). Sea urchins in this area regularly expe-
rience low-salinity conditions and adults should be acclimated to extended
bouts of hyposalinity.
In October of 2001, adult green sea urchins, collected from Little Harbor
at a depth of 5 m, were transported back to the laboratory and kept in the
same sea water system at a constant temperature of 10 C, salinity of 31.5%
(when not exposed to hyposaline conditions), and 12:12 light/dark cycle as
described earlier. The cages for the juvenile experiment were too small and
Mean salinity (‰)
Month
Figure 3.2 Summary of daily salinity records at the Coastal Marine Laboratory of the
University of New Hampshire at Fort Constitution, New Castle, New Hampshire (43
040 1900 N 70 420 3200 W), from 1993 to 2000. The plotted points are monthly
averages standard error. The values above the x-axis are the total number of days dur-
ing each month of the 8-year period that the salinity was <26 ppt.
individual cages for each urchin were not practical because of space con-
straints; so all urchins were kept in an open-top, rectangular plastic cage
(15 cm tall 50 cm wide 90 cm long) with a mesh (1 cm) bottom that
was suspended in the sea water system so the top of the cage was 4 cm
above the water line.
On 21 November 2001, each urchin was implanted (in the main body cav-
ity through the peristomal membrane, test diameter range 21.22–59.59 mm,
mean ¼ 37.85 mm 8.63 sd, and n ¼ 66) with a passive integrated transponder
(PIT) tag. These tags allowed identification of individuals held in a single tank
and have been used successfully in studies of sea urchins (Hagen, 1996; Shelton
et al., 2006). In a field study, Lauzon Guay and Scheibling (2008) cautioned that
PIT tags can have a detrimental effect on sea urchin performance; however, in
their experiment, they immediately placed urchins in the field posttagging
without a period of recovery (the large-gauge needle leaves a wound in the peri-
stomal membrane). In this study, 7 weeks’ recovery postimplantation was pro-
vided before beginning hyposalinity treatments. Even if the PIT tag affected the
urchins after the recovery, it would not influence the outcome or interpreta-
tions of the effects of salinity because all individual in both experimental groups
were tagged.
There were some key differences between the adult and juvenile
hyposalinity experiments. In the juvenile study, the replicate was mean size
of urchins in each cage; in the adult study, the individual urchin was the
replicate because each urchin was uniquely identified and all could be held
in the same cage between hyposalinity treatments. Hurlbert (1984) clearly
recognized that both experimental designs are not pseudoreplicated.
Growth rates of sea urchins decrease with size so to detect measurable
differences in larger individuals over natural variation and measurement
error, the adult experiment was longer (1 year) and the frequency of
exposures was every 3 weeks for a total of 15 versus 8 exposures. In the
adult experiment, the target hyposalinity treatment level was lower
(21% vs. 23%) and lasted 36 h instead of 24. The same size tanks were used
as in the juvenile experiment, but at the midpoint of a hyposalinity treatment
(18 h), the water was changed in each tank (21% for the treatment and
31.5% for the control).
At the outset of the experiment, the urchins were partitioned into two
groups so the range, means, and variances of test sizes were as uniform as
possible (Figure 3.3). One group was randomly assigned to the control
and the other to the treatment. Before each hyposalinity exposure, we
divided the urchins into the two groups by the PIT tag identification.
Control Hyposalinity
Test diameter (mm)
21 Nov 2001 30 Oct 2002

Date
Figure 3.3 Test diameters of (adult sea urchin control, n ¼ 34 and hyposalinity, n ¼ 32)
before (21 November 2001) and after (30 October 2002) the 15 (begun on 11 January
2002 and administered every 3 weeks), 36 h long hyposalinity treatments. The horizon-
tal line in the box is the median. The boundaries of the box are the 25th and 75th per-
centiles, the lines extending from the box are the 5th and 95th percentiles, and data
points beyond these percentiles are plotted. There are no significant differences
between the groups on either date.
After the first exposure, an individual that was supposed to be in the

hyposalinity group was mistakenly put in the control cage so it never expe-
rienced a hyposalinity treatment. During the subsequent 14 exposures, there
were no other misassignments and this single event accounts for the unequal
sample sizes (n ¼ 34 for control; n ¼ 32 for hyposalinity).
There were no significant differences in test diameters either at the outset
of the experiment on 11 January 2001 (t ¼ 0.286 and p ¼ 0.396) or on the
final day of measurements on 30 October 2002 (t ¼ 0.856 and p ¼ 0.776;
Figure 3.3). A more sensitive assessment for growth differences between
the control and hyposalinity groups is evaluating the regressions of individual
growth increments as a function of original size (Figure 3.4), and there were
no significant differences in either the slopes (t ¼ 0.441 and p ¼ 0.661) or
intercepts (t ¼ 0.808 and p ¼ 0.422) between the two groups.
Finally, on 5 December 2002, we dissected all urchins and recorded total
wet weights and gonad wet weights. Gonads not only serve the obvious role
of reproduction but also function as energy storage tissue in sea urchins, that
is, they have the capacity to resorb the energy reserves stored in the nutritive
phagocytes of the gonad (Giese, 1966; Lawrence and Lane, 1982; Russell,
1998; Walker, 1982). An energetic cost associated with repeated low-salinity
exposures could be reflected in less gonad tissue in the hyposalinity group—less
energy stored over the course of the year of repeated hyposalinity exposures.
Growth (mm)
Original test diameter (mm)

Figure 3.4 Growth increment of adult sea urchins from 21 November 2001 to 30
October 2002 of the control (open triangles, n ¼ 34, upper regression line) and
hyposalinity (grey squares, n ¼ 32, lower regression line) groups. There are no significant
differences in either the slopes or intercepts.
There was no significant difference in gonad wet weight between the

two groups (t ¼ 1.013 and p ¼ 0.158, one-tail test); however, gonad wet
weight was higher in the control group and there was a significant difference
in the gonad index (t ¼ 1.872 and p ¼ 0.033, one-tail test), which is the per-
cent body weight of the gonad (Figure 3.5).
This experiment demonstrates that adults from euryhaline habitats in the
field are acclimated to repeated bouts of low salinity as evidenced by the
growth rate data (Figures 3.3 and 3.4). Urchins exposed to low salinity every
3 weeks grow at the same rate and reach the same overall sizes as urchins not
exposed. There may be an energetic cost to the frequency and intensity of
exposures even in acclimated urchins (Figure 3.5). The average gonad index
for the control group is 0.33 0.04 sd and 0.31 0.05 sd for the hyposalinity
group at the conclusion of the experiment. However, the hyposalinity treat-
ments in this experiment were extreme: 15 exposures (36 h each) at 21%
over the course of 10 months. This level of exposure is equivalent to 27 days
in a single year. The daily salinity records from the Coastal Marine Labora-
tory only record an average of 3 days below 21% each year (and this value is
driven by the high of 11 days in 1993—2 years, 1995 and 1999 had no days
this low).
An interesting picture emerges from the results of the juvenile and adult
experiments. Initial exposure to low salinity is a stressor and results in a
growth rate reduction. However, in relatively short order (3 or 4 exposures
Control
Hyposalinity
Gonad index (%)

Figure 3.5 Gonad index (percent of the total wet body weight that is gonad) on 5
December 2002. Between the last hyposalinity treatment on 30 October and the dissec-
tion date, there were one mortality in the control group and four in the hyposalinity
group. Two PIT tags were lost during the dissection resulting in n ¼ 32 for the control
group and n ¼ 27 for the hyposalinity group. The vertical line in the box is the median.
The boundaries of the box are the 25th and 75th percentiles, the lines extending from
the box are the 5th and 95th percentiles, and data points beyond these percentiles are
plotted. There is a significant difference between the two groups (t ¼ 1.872, p ¼ 0.03—
one-tail t-test).
over 4–6 weeks), subsequent exposures do not produce adverse effects on

growth (Figure 3.1). Urchins in the field from euryhaline environments
appear to be acclimated to periodic hyposalinity events. When these urchins
are exposed to frequent and intense hyposalinity events (beyond the normal
levels recorded in these habitats), they show no significant adverse growth
responses. However, they may ‘pay’ an energetic cost in terms of slightly
lower gonad wet weights in dealing with these extreme levels.
These results demonstrate the flexible acclimation that green sea urchins
have to osmotic challenges. This species demonstrates a wide range and
extreme limits of their physiological acclimation abilities to euryhaline envi-
ronments. What these experiments fail to determine is the physiological
mechanism(s) that are triggered and seem to endure once ‘turned on’.
One promising avenue of future investigation is the potential role of heat
shock proteins (HSP), in the response to changes in salinity.
5. FUTURE PROSPECTS AND AQUACULTURE

IMPLICATIONS
Some echinoderms like the green sea urchin have the capacity to suc-
cessfully thrive in euryhaline environments and show an ability to acclimate
to these conditions. However, the physiological basis of both acclimation
and tolerance is unknown. Although we can expose these organisms to
extreme environmental challenges and measure their response, as yet we
do not understand the underlying processes they employ to deal with,
and rebound from, these stressors.
Many marine invertebrates respond to a variety of environmental
stressors by producing HSPs—in particular Hsp70 that is found in the purple
sea urchin, S. purpuratus (Hammond and Hofmann, 2010). These proteins
are expressed in response to a variety of environmental challenges, including
osmotic shock. They temporarily prevent the denaturation of other physi-
ologically essential proteins. Prolonged exposure to stress will eventually
result in diminished capacity to function and/or mortality. However, HSPs
provide a stopgap to allow organisms to survive prolonged environmental
challenges and enable them to recover from these challenges more quickly.
Recent work on the commercially harvested sea cucumber, Apostichopus
japonicas, has demonstrated that Hsp70 is produced in response to osmotic
challenges (Dong et al., 2008; Meng et al., 2011). However, the link
between salinity stress and HSP production has not been established in other
echinoderms. One promising future avenue of investigation is to quantify
HSP production in echinoids in response salinity challenges. This work lies

at the intersection of both basic and applied science because of the aquacul-
ture implications and potential value of understanding the physiological basis
of salinity acclimation and tolerance. Additionally, with the genomic
resources currently available, and continuing to increase, it should be pos-
sible to identify conserved genes or networks of genes involved in the
response to salinity from which detailed differential expression studies could
be carried out.
Three species of echinoids that occur in North America are excellent
candidates for a comparative study of salinity and HSP synthesis:
S. droebachiensis, S. purpuratus, and L. variegatus. The green sea urchin is com-
mercially harvested and there are efforts to augment wild populations with
aquaculture production. Both S. purpuratus and L. variegatus are important
model organisms and there is much interest in raising these sea urchins in
controlled laboratory settings.
The available studies of salinity tolerances (Table 3.3) show a gradient for
these three species: S. droebachiensis is the most tolerant and S. purpuratus is
the least. One prediction is that HSP expression would reflect this ranking
and show the potential physiological mechanism that some species use to
acclimate to euryhaline environments.
ACKNOWLEDGEMENTS
I thank Michael P. Lesser for constructive comments and the invitation to write this chapter.
Ms. Shellie Bryant provided editing and technical assistance. For the green sea urchin
experiments, Larry Harris provided lab and field support and his students, C. Sisson,
S. Chavanich, and T. Madigan, aided in the fieldwork. Jay Gingrich holds an aquaculture
lease at the Little Harbor and allowed sampling at this site. Noel Carlson provided salinity
data from the Coastal Marine Laboratory, University of New Hampshire. Joanne
Dougherty assisted with the lab experiments and supervised Villanova students: J. Beck,
J. Campbell, S. Fabian, C. Flannery, K. Parsley, A. Sewald, and A. Smolock, in the lab.
J. Navaratnam and C. Dumont assisted with sea urchin dissections. Constructive
comments were provided by V. Gibbs and the 2013 Russell Lab. Finally, the Villanova
Biology Department and US Department of Agriculture provided financial support.
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CHAPTER FOUR
The Coral Sea: Physical

Environment, Ecosystem Status
and Biodiversity Assets
Daniela M. Ceccarelli*,1, A. David McKinnon†, Serge Andréfouët{,
Valerie Allain}, Jock Young}, Daniel C. Gledhill}, Adrian Flynn||,
Nicholas J. Bax},||||, Robin Beaman#, Philippe Borsa**,
Richard Brinkman†, Rodrigo H. Bustamante††, Robert Campbell},
Mike Cappo†, Sophie Cravatte{{,}}, Stéphanie D’Agata{,
Catherine M. Dichmont††, Piers K. Dunstan}, Cécile Dupouy}},
Graham Edgar||||, Richard Farman##, Miles Furnas†, Claire Garrigue***,
Trevor Hutton††, Michel Kulbicki†††, Yves Letourneur{{{,
Dhugal Lindsay}}}, Christophe Menkes}}},||||||||, David Mouillot||||||,
Valeriano Parravicini†††, Claude Payri{, Bernard Pelletier###,
Bertrand Richer de Forges****, Ken Ridgway}, Martine Rodier}},††††,
Sarah Samadi****, David Schoeman{{{{, Tim Skewes††,
Steven Swearer}}}}, Laurent Vigliola{, Laurent Wantiez{{{,
Alan Williams}, Ashley Williams}, Anthony J. Richardson††,}}}}
*Marine Ecology Consultant, PO Box 215, Magnetic Island, Queensland, Australia
†
{
Institut de recherche pour le développement (IRD), LabEx-CORAIL, UR 227 ‘CoReUs’, BP A5, Noumea,
New Caledonia
}
Oceanic Fisheries Programme, Secretariat of the Pacific Community, BP D5, Noumea, New Caledonia
}
Wealth from Oceans Flagship, CSIRO Marine and Atmospheric Research, Castray Esplanade, Hobart,
Tasmania, Australia
||
Fathom Pacific Pty Ltd, Kensington, Victoria, Australia
#
School of Earth and Environmental Sciences, James Cook University, PO Box 6811, Cairns, Queensland,
Australia
**IRD-UR 227 ‘CoReUs’ c/o Universitas Udayana, Jl Sesetan Gang Markisa no.6, Denpasar, Indonesia
††
Wealth from Oceans Flagship, CSIRO Marine and Atmospheric Research, Ecosciences Precinct, GPO
Box 2583, Dutton Park 4001, Qld, Australia
{{
Institut de Recherche pour le Développement, LEGOS, Nouméa, New Caledonia
}}
LEGOS, Observatoire Midi-Pyrénées, Université de Toulouse/IRD/CNRS/CNES, Toulouse, France
}}
Mediterranean Institute of Oceanography, UMR CNRS/IRD/AMU/USTV 7294, 235, BP A5, Noumea,
New Caledonia
||||
Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 49, Hobart, Tasmania,
Australia
##
Aquarium des Lagons, BP 8185, Nouméa, New Caledonia
***Opération Cétacés, BP 12827, Noumea, New Caledonia
†††
IRD-UR 227 ‘CoReUs’, LABEX “Corail”, c/o Laboratoire Arago, BP 44, Banyuls-sur-mer, France
{{{
}}}
Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka
City, Kanagawa Prefecture, Japan

http://dx.doi.org/10.1016/B978-0-12-408096-6.00004-3
214 Daniela M. Ceccarelli et al.
}}}
UMR 7159 LOCEAN (IRD/CNRS/UPMC/MNHN), Université Pierre et Marie Curie, Case 100,
Paris, France
||||||
5119 ECOSYM (CNRS-UM2-IFREMER-IRD), Université Montpellier 2 cc 093,
Montpellier Cedex 5, France
###
UMR 7329 GEOAZUR (UNS-CNRS-IRD-OCA), BP A5, Noumea, New Caledonia
****Muséum National d’Histoire Naturelle, Département Systématique et Evolution, 57 rue Cuvier 75005
Paris Cedex 5, France
††††
UMR 241 EIO (IRD-Ifremer-UPF-ILM) BP 529, PK 3, 5 chemin de l’Arahiri, ARUE, Papeete, French
Polynesia
{{{{
Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Locked Bag 4,
Maroochydore DC, Queensland, Australia
}}}}
Department of Zoology, University of Melbourne, Melbourne, Victoria, Australia
}}}}
Centre for Applications in Natural Resource Mathematics, School of Mathematics and Physics, The
University of Queensland, St. Lucia, Queensland, Australia
||||||||
Institut de recherche pour le Développement-LOCEAN, Nouméa, New Caledonia
1
Corresponding author: e-mail address: dmcecca@gmail.com
Contents
1. Introduction 215
2. Research Trends 218
3. The Physical System 228
3.1 Tectonics and topography 228
3.2 Physical oceanography 229
3.3 Climate 231
4. Biological Oceanography 235
4.1 Nutrients and their supply 236
4.2 Phytoplankton and primary production 238
4.3 Meso- and macrozooplankton 240
4.4 Micronekton 241
5. Benthic Ecosystems 242
5.1 Coral reefs 243
5.2 Seamounts 245
5.3 Bathyal habitats 248
6. Fish Communities and Fisheries 248
6.1 Demersal fish 249
6.2 Deepwater fisheries 252
6.3 Pelagic fish 254
6.4 Pelagic fisheries 255
7. Iconic and Protected Species 258
7.1 Marine mammals 258
7.2 Seabirds 260
7.3 Turtles 261
7.4 Sea snakes 261
7.5 Elasmobranchs 262
7.6 Nautilus 263
8. Ecosystem Linkages and HotSpots in the Coral Sea 263
8.1 Northern Coral Sea 265
8.2 Central Coral Sea 266
8.3 Southern Coral Sea 267
The Coral Sea 215
9. Biogeography and Connectivity within and Beyond the Coral Sea 267
10. Research and Management Priorities 270
10.1 Species inventories 270
10.2 Movement, migration and connectivity 271
10.3 Temporal dynamics and ocean observation 271
10.4 Ecosystem modelling for a whole-of-system understanding 272
10.5 Human use and impacts 273
10.6 International collaboration on research and management 273
11. Conclusions 274
Acknowledgements 275
References 275
Abstract
The Coral Sea, located at the southwestern rim of the Pacific Ocean, is the only tropical
marginal sea where human impacts remain relatively minor. Patterns and processes
identified within the region have global relevance as a baseline for understanding
impacts in more disturbed tropical locations. Despite 70 years of documented research,
the Coral Sea has been relatively neglected, with a slower rate of increase in publications
over the past 20 years than total marine research globally. We review current knowledge
of the Coral Sea to provide an overview of regional geology, oceanography, ecology
and fisheries. Interactions between physical features and biological assemblages influ-
ence ecological processes and the direction and strength of connectivity among Coral
Sea ecosystems. To inform management effectively, we will need to fill some major
knowledge gaps, including geographic gaps in sampling and a lack of integration of
research themes, which hinder the understanding of most ecosystem processes.
Keywords: Tropical sea, Ecosystem function, Connectivity, Food web, Pristine
ecosystems, Collaborative research
1. INTRODUCTION
Anthropogenic pressures have altered marine ecosystems to the point
where they no longer represent baseline conditions (Butchart et al., 2010).
Even areas not directly affected by human activities are subject to climate
change and ocean acidification, and truly ‘pristine’ seas are a thing of the past
(Halpern et al., 2008). Approximately half of the global human population is
concentrated within 200 km of the world’s coastlines on 10% of the earth’s
land area, enhancing direct impacts on our oceans, such as exploitation of
marine resources (Foley, 2013), extraction of oil and minerals (UNEP-
WCMC, 2007) and the input of waste, pollutants and nutrients (Zirino
et al., 2013). This is especially true of tropical seas and their coastlines,
fringed by high-density and increasing human populations, which threaten
marine species, ecosystem functioning and food security (Burke et al., 2011).
This is a major concern, considering that tropical seas support a range of
environments characterised by high species diversity (coral reefs and sea-
mounts) or biomass (e.g. pelagic aggregations), despite being generally oli-
gotrophic (McKinnon et al., 2014).
The Coral Sea is among the 4% of the ocean relatively unaffected by
human impacts (Halpern et al., 2008). It is bounded by the Australian con-
tinental shelf to the west; the northern limit extends from southeastern
Papua New Guinea (PNG) to the southeastern Solomon Islands; the eastern
limit follows the Vanuatu archipelago, joining Pine Island to the south of
New Caledonia and Elizabeth and Middleton Reefs at its southeastern limit;
and the southern boundary is the parallel of 30 south (Figure 4.1A). The
Coral Sea covers 4,791,000 km2, making it the second-largest tropical
marginal sea after the Philippine Sea (McKinnon et al., 2014). It borders
the biodiversity hotspots of the Great Barrier Reef (GBR) and Coral
Triangle (Robert et al., 2002), as well as the highly productive Tasman Front
(Baird et al., 2008). The Coral Sea is generally oligotrophic, and has topo-
graphic and oceanographic features that support high biodiversity and iconic
megafauna, as well as underpinning pelagic fisheries and their associated
human livelihoods. Tuna fisheries in the Coral Sea and in adjacent seas
are an important economic resource to the countries with Coral Sea Exclu-
sive Economic Zones (EEZs) (Williams and Terawasi, 2012).
So far, pelagic fisheries are the only field where transboundary manage-
ment has been implemented in the Coral Sea. Spatial management planning
has not extended beyond Australia’s EEZ; marine protected areas (MPAs)
established by New Caledonia, Vanuatu, the Solomon Islands and PNG
are relatively small and largely restricted to coastal waters (Figure 4.1B).
Recently, Australia’s bioregional planning process resulted in the establish-
ment of a large no-take MPA in the eastern half of Australia’s Coral Sea,
covering 502,654 km2 of pelagic and deep-sea benthic habitats
(DSEWPaC, 2013), and New Caledonia pledged to declare its 1.4 million
km2 Coral Sea territory an MPA at the Pacific Islands Forum in September
2012 (Environment News Service, 2012). The importance of establishing
MPAs in deep-sea and pelagic ecosystems, including in international waters,
is increasingly discussed (Game et al., 2009), and there has been a rising num-
ber of large MPAs globally (90,000 to >1,000,000 km2).
The lack of coordination in scientific research programmes of the nations
with Coral Sea EEZs has led to incomplete and fragmented knowledge of
key ecosystems in the region. Without identifying and monitoring areas
A B 150o E 160o E 170 o E
Solomon Islands
10o S
Papua New Guinea
Australia
500
Vanuatu 500
20o S
0 0
−2000
New Caledonia −2000
Australia
30o S
−9000 −9000
C D PNG NGC Solomons

C
Islands SECC
Eastern Plateau
GPC Vanuatu
NVJ
NCJ
SVJ
Marion New
Plateau
Caledonia SFJ
So
Kenn
uth
Plateau SCJ
Australia
Loya
Fair
wa
lty
yB
Ba
sin
asin
SE rtades EAC STCC

NW Monsoon
Transient
Figure 4.1 (A) Boundaries of the Coral Sea set by the International Hydrographic Organization (black line) and EEZ boundaries (white line). This chapter
considered all marine areas >200 m depth or beyond the shelf break of continents and major islands. (B) Marine protected areas within the Coral Sea,
including those within territorial waters of each jurisdiction. (C) Major topographic features of the Coral Sea. (D) Oceanography of the Coral Sea, includ-
ing major surface currents and fronts. NGCC: New Guinea Coastal Current, mirroring the deeper New Guinea Coastal Undercurrent; GPC: Gulf of Papua
Current, including the North Queensland Current and Hiri Gyre; SECC: South Equatorial Countercurrent; Jets of the South Equatorial Current (SEC): NVJ:
North Vanuatu Jet; NCJ: North Caledonia Jet; SVJ: South Vanuatu Jet; SFJ: South Fiji Jet; SCJ: South Caledonia Jet; EAC: East Australian Current; STCC:
Subtropical Countercurrent.
of high conservation values and key drivers of ecosystem function that

underpin them, it will be difficult to maintain biodiversity assets into the
future. The collation and synthesis of existing information for the whole
Coral Sea are critical first steps toward the identification of globally impor-
tant and vulnerable areas. Understanding connectivity between habitats
within the Coral Sea and with the adjacent Coral Triangle, GBR, western
Pacific and temperate boundaries will shed light on the Coral Sea’s regional
role and importance (e.g. Hobday et al., 2011; Treml et al., 2008).
In a sister publication, we have reviewed the biodiversity, ecosystem
function and management issues facing tropical marginal seas globally
(McKinnon et al., 2014). Here, we concentrate on the Coral Sea specifically,
bringing together existing knowledge of Coral Sea ecosystems, identifying
the significance of the Coral Sea within the western Pacific region and
highlighting knowledge gaps (Table 4.1). The geographic scope of this
chapter excludes continental shelf habitats and associated features (e.g. the
GBR), and shallow waters of major islands (e.g. the New Caledonian barrier
reefs and lagoons and the islands of Vanuatu). We begin with an analysis of
research trends in the Coral Sea to distinguish research themes and regions
that are well studied from those that have been neglected. We then describe
various facets of the Coral Sea ecosystem, from physical drivers (tectonics,
geology and physical oceanography), through ecosystems (plankton com-
munities, benthic ecosystems and demersal and pelagic fish communities),
to species of human interest (fisheries and iconic and protected species
groups). Within each section, we present a summary of current knowledge
and knowledge gaps, and discuss links between physical drivers and ecosys-
tems. We then highlight key features and processes of the Coral Sea, focus-
ing on connectivity between habitats within and beyond the Coral Sea. We
conclude by discussing future research themes that would be most useful in
supporting regional management.
2. RESEARCH TRENDS
Research in the Coral Sea spans more than a century, beginning with
expeditions in the late 1800s, such as the HMAS Challenger oceanographic
expedition of 1873–1876. Much of this early work is no longer readily acces-
sible and has not been included in our analyses. We compiled a database of all
documents on the Coral Sea, based on ISI Web of Science searches, identi-
fication of research reports by the authors, and soliciting input from govern-
ment and nongovernment organisations and research institutions from all
nations surrounding the Coral Sea. Documents were classified by year,
Table 4.1 Major knowledge areas and gaps for the Coral Sea by research theme
Regional context/
Themes Key knowledge importance Connectivity Major knowledge gaps
Tectonics and Good maps, descriptions Geological and Combination of geological Fine-scale mapping (e.g. some
topography of developmental history evolutionary history are history and sea-level seamounts are unnamed).
of basin-scale topography. closely linked. fluctuations alternately A better understanding of
An understanding of Considered one of the creating dispersal barriers the links between geological
complex bathymetry. basal centres of speciation. and likely stepping stones history and evolution of
Good descriptions of Complex topography through time. species is needed.
tectonic activity on interacts with regional- Present-day Coral Sea
eastern edge. scale currents as major reefs may be stepping
History of Gondwanan driver of productivity stones connecting
fragmentation is known. patterns. western Pacific reefs and
the Great Barrier Reef.
Physical Broadscale mean Water masses that pass Major currents form links Vertical extent of currents is
oceanography circulation is well through the Coral Sea are (depending on depth) unresolved for most areas.
documented. redistributed poleward between the subtropical Variability of the currents and of
Effects of topographic and equatorward, and gyre and the southwest the water properties at seasonal,
features on the formation eventually join the eastern Pacific, Coral Triangle interannual and longer
of oceanic jets are partly equatorial region. and GBR and between timescales is poorly known.
known. tropical waters and Variability of connectivity
Some understanding of temperate Tasman Sea. pathways and of the
the relationship between Tropical waters and equatorward and poleward
currents and ENSO. equatorial band extend redistribution of waters is
through to the Solomon poorly known.
Sea. Connectivity between Pacific
and Indian Oceans through
northern Australia is unclear.
Continued
Table 4.1 Major knowledge areas and gaps for the Coral Sea by research theme—cont'd
Regional context/
Climate Dominant summer and Water masses that pass Climate drivers (especially Variability of regional
winter climate patterns through the Coral Sea ENSO) influence physical response to climate drivers
understood. influence global climate and biological (ENSO, PDO, and at longer
Patterns in SST and patterns. oceanography and linked timescales) in terms of
cyclogenesis related to Relationships exist ecological communities. temperature, precipitation and
differences between El between variations in cyclone activity is unknown.
Niño and La Niña. currents and climate in Lack of evidence of secular
eastern Australia and New change in temperature and
Zealand, and in the physical forcing.
equatorial thermocline
water properties.
Biological Oligotrophic character Ephemeral and/or seasonal Interactions between We need a better
oceanography dominated by aggregations feed large climate, physical understanding of topographic
picoplankton and microbial pelagics that sustain oceanography and controls on productivity.
processes. important recreational and topographic complexity The trophic fate of
Role of myctophids and commercial fisheries. drive ecological processes productivity needs to be
squid in top predator Hiri Gyre entrains larvae of and productivity in the explored.
aggregations. important species (rock pelagic realm. Zooplankton community
Importance of the ‘jelly lobsters and eels). Remote sources of iron, structure is unknown.
food web’ in the northern nutrients (volcanic Trophodynamics and
Coral Sea. plumes), N2 fixation with production are unknown.
drifting Trichodesmium Micronekton taxonomy,
blooms. distribution and abundance/
biomass are virtually
unknown.
Productivity regimes
supporting large biomasses are
unclear.
Population connectivity is
unknown.
Spatiotemporal variability and
relationships to predator
distributions need to be
resolved.
Benthic Steady progress toward Several distinct Complex gene flow, Biodiversity of benthic
ecosystems regional-scale seabed biogeographic realms showing dispersal from east invertebrates poorly known
mapping, with targeted within the Coral Sea. to west, from north to for many reefs, seamounts,
fine-scale mapping of key Different population south and across the Torres plateaux and deep sedimentary
features, e.g. coral reefs and structure between isolated Strait for different taxa and areas.
seamounts. reefs of the Coral Sea and species at a range of Intra- and interregional
Shallow (<20 m) reef large islands, for fish, algae timescales. connectivity is poorly
communities relatively and invertebrates. Low-dispersal species understood, including
well known (but see gaps). Endemism on coral reefs is evolve as isolated between reefs, between
Emerging knowledge of low but present according populations. seamounts and continental
deep systems, including to current sampling efforts Deep-sea cold-water corals slope, between depth zones
mesophotic reefs. Isolated oceanic reefs far with links to NZ and and between faunal groups
Coral reef communities from human disturbance Tasmanian coral with contrasting life histories.
are impacted by climate could provide long-term communities. Virtually no knowledge
change and are regularly refugia from human and of benthic ecological
impacted by Coral Sea climate impacts, including processes, including
cyclones. at mesophotic and greater benthopelagic coupling.
depths.
Continued
Regional context/
Complex patterns of Phylogeography and
biodiversity distribution biogeography of major reef
between seamounts and taxonomic groups remain to
bathyal domains. be studied in the Coral Sea and
A large reservoir of species adjacent regions.
new to science at bathyal Coupled biophysical processes
depths. of transport at mesoscale and
small scale remain unknown.
Demersal fish Described for many Some reefs still in good to May play a role in linking Assembly rules for reef fish at
shallow (<20 m) reef excellent condition, with GBR and New Caledonia the reef level unresolved.
communities. abundant and diverse fish to adjacent regions. Little knowledge of demersal
There is some knowledge communities. Historical importance as fish, especially in the north.
of deeper demersal fish in these reefs were emergent Intra- and interregional gene
the southern plateaux. during glaciations and were flow unknown.
North–south gradient in then important stepping Gene flow and migration
diversity and biomass for stones. between the seamount fauna
reef fish becoming clearer. and the continental slope
unknown.
Phylogeography and
biogeography at the regional
scale (Coral Sea and adjacent
regions) are unknown.
Pelagic fish Ecology and niche World’s only known Stock structure of some Need to establish population
segregation of commercial black marlin spawning pelagic fish indicates trans- connectivity and migration
top predators described. aggregation. Pacific stock structure and pathways between the Coral
Only known black marlin Coral Sea spawning migration. Sea and adjacent regions.
spawning ground grounds for a number Movements of some Relationship between
identified. of large pelagics. pelagics link basin-scale movement and
Increasing knowledge of regions, e.g. movements of oceanographic/climate drivers
neritic tunas. large fish and sharks is unresolved.
between western Pacific Little knowledge of unfished
islands and Australian shelf species.
and between temperate Some basic biological
Tasman and tropical Coral parameters for some species
Seas. (distribution, growth,
reproduction, etc.) are
poorly known.
Spatial extent of spawning
areas and residency times is
unknown.
Fisheries Invertebrate and Coral Sea may represent Stock structure of some Population connectivity and
ornamental fishing on most major source of pelagic fish indicates trans- migration pathways between
reefs well documented. recruitment of large Pacific connectivity. the Coral Sea and other
Low demersal fisheries pelagics to fisheries off Movements of some regions of the WCPO are
productivity (e.g. Eteline eastern Australia. pelagics link basin-scale unclear.
spp.). regions, e.g. movements of
Continued
Regional context/
Good catch records for large fish and sharks Better observer coverage on
most commercial pelagic between western Pacific pelagic fisheries is needed to
fleets. islands and Australian increase representativeness of
shelf and between the data in space and time and
temperate Tasman and acquire more information on
tropical Coral Seas. non-target species.
Need for better knowledge of

population genetic structure at
the regional scale (Coral Sea
and adjacent regions).
Poor catch records for game
fish industry.
Extent of illegal, unreported
and unregulated fishing is
poorly known.
Iconic and Population dynamics and Important nesting, resting Migrations and movements Occurrence, distribution and
protected nesting success known for and feeding areas for turtles of megafauna link terrestrial migration pathways for most
species some seabirds and sea and seabirds. and marine ecosystems, and species are unknown.
turtles from a few cays. Whale sharks attracted by continents (e.g. birds), and The mechanism behind the
Some knowledge of the myctophid aggregations. basin-scale regions (e.g. negative effect of ENSO on
genetic structure of sea Group V humpbacks and loggerheads). bird success is unknown.
turtle and humpback whale other cetaceans may breed Relationship/predation
populations. in the Coral Sea. between seabirds and marine
Detection of a decline in Migration pathways for fauna (fish and cephalopods)
sea snake populations. several species, including are not understood.
humpback whales
Data on the occurrence,
distribution and abundance,
population genetic structure,
connectivity, population
trends, growth, reproduction
of sea snakes are needed.
Connection between
humpback whales observed on
the Chesterfield Islands and
the migratory path or
reproductive area of substocks
Ei or Eii is not understood.
Connection of Indo-Pacific
bottlenose dolphin to
Australian or New Caledonian
population is not understood.
Phylogeography and
biogeography at the regional
scale (Coral Sea and adjacent
regions) are unknown for most
species.
discipline and EEZ; for ecological and biological studies, minimum and max-
imum geographic coordinates were also recorded. Between 1954 and 2012,
1434 scientific documents were published on the Coral Sea (Appendix 1; see
supplementary material in the web version of this chapter). Even though the
bulk of this published research was conducted in the past decade, surprisingly,
the Coral Sea has been relatively neglected; the rate of increase in publications
over the past 20 years has been slower than for total marine research globally
(Figure 4.2A). Much of the literature (41%) on the Coral Sea is from ‘grey’
literature, although the bulk is from peer-reviewed literature (59%); both types
of documents had a similar trajectory of increase (Figure 4.2A).
A
Cumulative number of Coral Sea papers
1000 200,000
Coral Sea: Peer-reviewed
number of marine papers globally

Coral Sea: Grey
800 Global: Marine
150,000
Cumulative
600
100,000
400
50,000
200
0 0
1960 1970 1980 1990 2000 2010
B 400 Geology and Geomorphology
Climate and Oceanography
Cumulative number of papers
Biology and Ecology

300 Fisheries
Management
200
100
0
1960 1970 1980 1990 2000 2010
Year
Figure 4.2 Research trends in the Coral Sea. Cumulative number of papers from 1960 to
2012. (A) For peer-reviewed and grey-literature Coral Sea research and peer-reviewed
global marine research trends. (B) For major scientific disciplines studied in the Coral Sea
(grey and peer-reviewed literature).
The Coral Sea 227
Ecological and biological studies were most common (31.5%), followed by

geology and geomorphology (27%), fisheries (20.5%), climate and oceanogra-
phy (19.1%), other disciplines (1.3%—including tourism, archaeology, sociol-
ogy, history and economics) and management (0.6%). Earliest studies were
reports of descriptive oceanographic cruises and taxonomic collections, with
a rise in geological, geomorphological and sedimentological studies in the mid-
1970s (Figure 4.2B). The past decade has seen a larger proportion of fisheries
and ecological studies and a number of cross-disciplinary studies that combine
ecological variables or fisheries catch rates with oceanographic or geological
data. Management studies have only increased in the past few years.
To examine the spatial distribution of research effort in the Coral Sea, we
included the central latitude and longitude and spatial extent of ecological
studies in our compiled database. Most research has been conducted within
Australian (31%) and New Caledonian (25.8%) waters. EEZs of PNG, the
Solomon Islands and Vanuatu accounted for 13.6%, 12.6% and 16.9% of
research, respectively. Ecological and biological studies have focused over-
whelmingly on the oceanic coral reefs of the Coral Sea, with less work
addressing seamounts, continental slopes, plateaux and the deep sea
(Figure 4.3). The greatest proportion of documented ecological research
comes from the Chesterfield Plateau, followed by the Loyalty Islands
Figure 4.3 Spatial distribution of the number of ecological research documents from
1954 to 2012.
and reefs of Australia’s Queensland Plateau (particularly Osprey Reef, the

Coringa–Herald complex and Lihou Reef; Figure 4.3).
3. THE PHYSICAL SYSTEM

A complex geological history interacts with present-day topography,
major currents and a tropical climate influenced by El Niño–Southern
Oscillation (ENSO) to set the foundation for the Coral Sea’s ecology.
Aspects of the region’s geology, oceanography and climate are well under-
stood and documented, allowing some inference of drivers of ecological
processes and likely pathways of connectivity.
3.1. Tectonics and topography

Between the Australian continental shelf to the west and the Solomon
Islands and Vanuatu island arcs to the east, the Coral Sea consists of a series
of basins interrupted by plateaux and rises (Collot et al., 2011; Pelletier,
2006; Figure 4.1C). Most of the major geological features of the Coral
Sea seabed are derived from the fragmentation of Gondwana during the
Cretaceous (Mortimer et al., 1998); the plateaux and rises to the east of Aus-
tralia (Lord Howe Rise, Norfolk/New Caledonia Rise) are continental in
origin. The deepest parts of the Coral Sea (the Coral Sea basin, the
d’Entrecasteaux and South and North Loyalty Basins) are made of oceanic
crust (Pelletier, 2006). The structure of other parts of the Coral Sea, such as
the Fairway and New Caledonia Basins, is still under debate, as it is unclear
whether they are also composed of oceanic crust (Auzende et al., 2000) or
thinned continental crust (Lafoy et al., 2005).
The basins formed through seafloor spreading or continental stretching
and crustal thinning, dominated by the oceanic accretion of the Tasman
(84–52 Mya) and Coral Sea basins (65–52 Mya); the stretching and thinning
of continental crust of the Fairway and New Caledonia Basins (70 Mya);
and the opening of the South Loyalty Basin (100–56 Mya), the
d’Entrecasteaux Basin (56–33 Mya) and the North Loyalty Basin
(45–35 Mya; Figure 4.1C). The region’s major subduction zone is at the
eastern dipping point of the North Loyalty Basin at the d’Entrecasteaux
Zone, a convergent zone that began 7 Mya. Currently, the Australian
plate moves in a NNE direction at 7 cm year1 and is subducted under
the Pacific Plate along the New Hebrides (or Vanuatu) and South Solomon
Trenches at 9–17 cm year1 (Calmant et al., 2003; Pelletier et al., 1998).
The Coral Sea 229
The Tasmantid and Lord Howe seamount chains are ancient volcanic
hot spots (McDougall and Duncan, 1988). Kenn Reef in the north is the
oldest seamount of the Tasmantid chain, with a predicted age of 38 My
(Exon et al., 2006). The Bellona and Chesterfield Reefs, on the northern
part of the Lord Howe seamount chain, are tentatively dated at 25 Mya
(Missegue and Collot, 1987).
The shallowest of the large plateaux are the Eastern, Queensland,
Marion, Mellish, Kenn and Chesterfield–Bellona Plateaux; the Lansdowne
Bank; the New Caledonia lagoons and d’Entrecasteaux reefs; and the Loy-
alty Rise, all of which host emergent reefs, cays and islands. Some of these are
among the world’s largest atolls, such as the Chesterfield and Lihou Reefs.
Sea-level variation controlled platform facies; rising and higher sea levels
promoted carbonate deposition, whereas falling and lower sea levels
restricted carbonate deposition, increased terrigenous input and in many
cases resulted in exposure of the platforms (Davies et al., 1989). Various stud-
ies of the palaeofauna suggest successive episodes of connection and isolation
between the Gondwanan supercontinent and its fragments (Collot et al.,
2011). Some reefs formed on natural high points of the plateaux, and the
structure of present-day reefs suggests that reef growth kept pace with pla-
teau subsidence and sea-level rise for the last 25 My (Davies et al., 1989).
3.2. Physical oceanography

The dominant feature of the circulation in the Coral Sea is the westward-
flowing South Equatorial Current (SEC) and its bifurcation at the Australian
continental margin (Ridgway and Dunn, 2003; Kessler and Cravatte, 2013a;
Figure 4.1D). The SEC redistributes South Pacific thermocline waters from
the subtropics to the equator and the Southern Ocean (Qu and Lindstrom,
2002). The southern arm of the bifurcation feeds the southward-flowing
East Australian Current (EAC), the major western boundary current of
the South Pacific Gyre, and the northern arm forms the Gulf of Papua Cur-
rent, which flows northward along the Queensland coast and turns eastward
along the southern rim of PNG (SPICE Community, 2012), and feeds into
the New Guinea Coastal Undercurrent that subsequently enters the Solo-
mon Sea. In 2005, the Southwest Pacific Circulation and Climate Experi-
ment (SPICE) was initiated to provide improved understanding of Coral Sea
circulation (Ganachaud et al., 2013).
Within the Coral Sea, the SEC comprises narrow filaments and jets cre-
ated by the complex island, reef, seamount and ridge topography (Couvelard
et al., 2008; Gourdeau et al., 2008). Major westward currents are the North
Vanuatu Jet, the North Caledonian Jet and the episodic South Caledonian
Jet (Figure 4.1D). Eastward countercurrents are also present in the lee of the
Vanuatu and Fiji islands (Kessler and Cravatte, 2013a). This interaction of
hydrodynamics and topography is an important influence on local mixing pro-
cesses. The Coral Sea transit of the waters advected by the SEC and bifurcating
equatorward is important because changes in the temperature or the water
transport toward the equator can modulate the ENSO cycle and trigger
Pacific-scale climate feedbacks (Ganachaud et al., 2013). South of the bifurca-
tion, EAC thermocline waters are important drivers of eastern Australian and
New Zealand climate; seasonal and interannual changes in advection influence
the air–sea heat flux and atmospheric conditions (Roemmich et al., 2005).
Current pathways depend on the depth of the relevant water masses
(Kessler and Cravatte, 2013a; Figure 4.4), linked to the vertical tilt of the
bifurcation latitude at the Australian coast: at the surface, the bifurcation is
at 15 S; at 500 m, it is at 23 S. Warm, low-salinity waters dominate at
the surface. A high-salinity and poorly oxygenated water mass, Subtropical
Lower Water, is subducted in the eastern subtropical Pacific (Donguy,
1994) and spreads westward into the Coral Sea through the North Vanuatu
Jet, appearing as a subsurface salinity maximum at 100–200 m (Kessler, 1999).
Subantarctic Mode Water and Antarctic Intermediate Water are formed
in the Southern Ocean and entrained into the anticyclonic South Pacific
Gyre, which projects them into the Coral Sea at a depth of between
400 m and 1000 m. These water masses are advected through the region
by the SEC following pathways dictated by the island groups (Maes et al.,
2007) and with components spreading poleward and equatorward following
the bifurcation. Underlying the intermediate waters throughout the South
Pacific, there is an oxygen minimum centred at 2000 m (Sokolov and
Rintoul, 2000). At even greater depths, the spreading of water masses is
increasingly constrained by topography. The Lower Circumpolar Deep
Water, identified by a weak salinity maximum, is found in the South Pacific
over a depth range of 2500–3000 m. Deep layers of the Coral Sea are fed by
components of Lower Circumpolar Deep Water from the east (via the SEC)
and, from the south, from the Tasman Abyssal basin through a narrow pas-
sage at 24 S (Sokolov and Rintoul, 2000). Whilst there are strong tidal cur-
rents through the shallow Torres Strait to the northwest (mostly <20 m), the
mean flow is small (0.1 m s1) and makes a negligible contribution to the
Coral Sea water mass structure (Saint-Cast and Condie, 2006). Circulation
features in the Coral Sea vary on seasonal to multidecadal timescales, but the
magnitude and drivers of this variability are not well understood.
The Coral Sea 231
Figure 4.4 Main currents for different water masses within the Coral Sea. (A) Surface
currents; (B) Upper thermocline currents; (C) Pathways of Antarctic Intermediate Water
(AAIW) (800–1200 m); and (D) Path of Circumpolar Deep Water (CDW) through the deep
channels in the region (<3500 m). NGCU: New Guinea Coastal Undercurrent; GPC: Gulf
of Papua Current; NVJ: North Vanuatu Jet; NCJ: North Caledonia Jet; NFJ: North Fiji Jet;
SFJ: South Fiji Jet; SCJ: South Caledonian Jet; EAC: East Australian Current. NGCC: New
Guinea Coastal Current; STCC: Subtropical Counter Current; SECC: South Equatorial
Counter Current; CSCC: Coral Sea Counter Current; FBCC: Fiji Basin Counter Current.
3.3. Climate
The most important driver of interannual climate and oceanographic con-
ditions in the Coral Sea is the ENSO pattern, with major changes in sea sur-
face temperature (SST) and sea level north of 15 S over 3–7 year cycles.
During El Niño events, waters in the northwestern Coral Sea cool and
sea level drops, and the SEC entering the Coral Sea north of Vanuatu swings
westward (Kessler and Cravatte, 2013b); the reverse pattern is true of La
Niña years. ENSO-related temperature anomalies can penetrate to the base
of the mixed layer (100 m; Holbrook et al., 2005). There has been a
quasidecadal change in ocean properties of the southwest Pacific Ocean over

the past 60 years, associated with a spin-up/spin-down cycle of the South
Pacific Gyre (Hill et al., 2011), which may be related to decadal variations
in ENSO (Holbrook et al., 2011). Over the past 50 years, the South Pacific
Gyre has intensified, due to a poleward shift in the circumpolar westerly
winds driven by the trend in the Southern Annular Mode (Cai and
Cowan, 2007). The EAC may have strengthened in the south (Ridgway,
2007), and modelling studies suggest a corresponding decrease in SEC
strength (Cai and Cowan, 2007) and an associated region of enhanced
warming off southeastern Australia (Ridgway, 2007).
There is also seasonal variability of the atmospheric conditions in the
Coral Sea. During winter, trade winds over the Coral Sea bring dry condi-
tions, with SST between 23 and 24 C around New Caledonia and
27–28 C in the Gulf of Papua (Figure 4.5). In summer, the South Pacific
Convergence Zone reaches its southernmost position, with heavy precipi-
tation in the Gulf of Papua, SST generally >28 C and trade winds converg-
ing from the south toward the South Pacific Convergence Zone
(Figure 4.5). Depending on prevailing conditions, cyclones are most likely
to develop in summer.
The Coral Sea experiences both an increased intensity of cyclones and
enhanced rainfall during La Niña events, with the opposite trend during
El Niño periods (Vincent et al., 2011). Potential drivers include a strength-
ening of the wind vertical shear between the upper troposphere and lower
troposphere and a weakened convective potential during El Niño and the
opposite pattern during La Niña (Menkes et al., 2012). Cyclones can be
highly damaging for shallow environments and coral reefs in particular
(Emanuel, 2005), but they can also supply the photic layer with enough
nutrients to support up to 15% of the annual mean new production in this
oligotrophic sea (Christophe Menkes, unpublished data).
Climate projections suggest a continuation of observed patterns, but
there will be minor changes in the currents south of 12 S (Ganachaud
et al., 2011). The strength of the SEC transport entering into the Coral
Sea and the Gulf of Papua Current transport toward the equator are expected
to increase (Sen Gupta et al., 2012). Warming is expected to continue, with
faster rates in the upper 100 m (Table 4.2). In the past decades, the rate of
warming in the Coral Sea has been closely aligned with global trends of SST
increase of 0.6 C within the upper 100–200 m, with a broadscale cooling at
greater depths extending to 25 S (Durack and Wijffels, 2010). These
changes have led to increased stratification, potentially limiting the vertical
A Precipitation + Wind DJFM B Precipitation + Wind JJAS
10° S 10° S
15° S 15° S
20° S 20° S
25° S 25° S
140° E 145° E 150° E 155° E 160° E 165° E 170° E 175° E 140° E 145° E 150° E 155° E 160° E 165° E 170° E 175° E
8 8
0 1 2 3 4 5 6 7 8 9 10 0 1 2 3 4 5 6 7 8 9 10
C SST DJFM D SST JJAS
10° S 10° S
15° S 15° S
20° S 20° S
25° S 25° S
140° E 145° E 150° E 155° E 160° E 165° E 170° E 175° E 140° E 145° E 150° E 155° E 160° E 165° E 170° E 175° E
20 21 22 23 24 25 26 27 28 29 30 20 21 22 23 24 25 26 27 28 29 30
1
Figure 4.5 (A) Contours of precipitation (mm day ) from GPCP data during summer (DJFM) with arrows from Qscat wind stress for the same
months. The GPCP climatology is computed for 1979–2010. The Qscat climatology is computed for 2000–2009. (B) Precipitation contours for
winter (JJAS). (C) SST from AVHRR during summer (DFJM), and (D) during winter. The AVHRR V4.1 climatology is computed for 1985–2010.
Table 4.2 Projected threats (vulnerabilities) of pelagic systems to climate change

Vulnerability of the
Variable Prediction pelagic system
Water To increase by 0.7–0.8 C by 2035 Low
temperature
Mixed layer To become shallower Moderate to high
depth
Changes in Dependent on location, upwelling may Low
upwelling increase or decrease
Solar and Increased cloud cover, rainfall but Low
ultraviolet potentially higher ultraviolet radiation
radiation
Dissolved To decrease by <5% by 2100 Low
oxygen
Ocean Aragonite saturation state to decline, Low
acidification potentially affect calcification rates
Summarised from Le Borgne et al. (2011).
exchange of nutrients, decreasing subsurface dissolved oxygen concentra-

tions (Stramma et al., 2008) and reducing oceanic pH in the region due
to increased absorption of CO2 (Bindoff et al., 2007). Projections suggest
that these patterns will intensify (Ganachaud et al., 2011).
To calculate average temperature change in the Coral Sea over the past
50 years, we used HadISST 1.1 data (http://badc.nerc.ac.uk/view/badc.
nerc.ac.uk__ATOM__dataent_hadisst). For future temperature projec-
tions, we used CSIRO-Mk3.6.0 data from the PCMDI5 (Program for Cli-
mate Model Diagnosis and Intercomparison) data archive, interpolated onto
a 1º grid. We extracted annual temperature anomalies for the four RCPs
(Representative Concentration Pathways) considered by IPCC AR5 (i.e.
RCP 2.6, RCP 4.5, RCP 6.0 and RCP 8.5) and used these to project
the HadISST data series forward to 2100. It must be noted that these results
are based on outputs from a single model, and further studies should assess
these in a multi-model framework. SST in the Coral Sea warmed by
0.089 C per decade between 1960 and 2009 (Figure 4.6). Projected warm-
ing in the future ranges from 0.85 C by 2100 for RCP 2.6 to 3.17 C for
RCP 8.5 (anomalies of 5-year means at the start and end of the time series).
RCP4.5 and RCP6.0 show intermediate increases of 1.17 and 1.51 C,
respectively, over the twenty-first century.
The Coral Sea 235
30 Sea surface temperature trajectories

HadISST 1.1
Linear trend for HadISST1.1
RCP 2.6
RCP 4.5
RCP 6.0
RCP 8.5
29
28
SST (°C)
27
26
1960 1980 2000 2020 2040 2060 2080 2100

Year
Figure 4.6 Sea surface temperatures for the Coral Sea over the period 1960–2100. His-
torical temperatures are taken from HadISST 1.1, whilst projections according to four
IPCC Representative Concentration Pathways were derived using anomalies from the
CSIRO-Mk3.6.0 data. A linear trend is fitted to the HadISST data to illustrate the historical
warming trend in the region.
4. BIOLOGICAL OCEANOGRAPHY
The ecology of pelagic habitats is closely linked to oceanography and
climate, especially in the upper oceanic layers where most research has
focused. The availability of inorganic and organic nutrients, influenced by
water movement, temperature, salinity and climatic conditions, sustains
phytoplankton assemblages that form the basis of pelagic food webs. Pelagic
production and community structure are also influenced by topographic fea-
tures. Here, we summarise current knowledge of nutrients, phytoplankton,
zooplankton and micronekton in the Coral Sea.
4.1. Nutrients and their supply

The water column of the Coral Sea is characterised by low nutrient concen-
trations in the surface mixed layer, whilst nutrient concentrations increase
and temperatures cool below the thermocline (Figure 4.7). Mixed layer
depths offshore vary from 25 to 125 m, depending on the location, season,
wind-stress history and regional dynamics (Furnas and Mitchell, 1996).
‘New’ nutrients are episodically introduced into the surface layer by atmo-
spheric forcing of the ocean surface in the form of momentum, heat, fresh-
water fluxes and cyclones; ENSO-driven climate variability can therefore
influence nutrient availability. Strong rotational forces associated with eddies
deflect ocean density, either lifting nutrients into surface waters (cyclonic
rotation) or depressing surface waters (anticyclonic rotation). On top of this
direct effect, impacts of eddies on the ecosystem are expected on the sides of
the eddies due to localised geostrophic and ageostrophic processes (e.g.
Dandonneau et al., 2003). In the Coral Sea, eddies associated with the
EAC are most pronounced and therefore the most likely areas of localised
elevated nutrient content. Other weaker eddy activity also originates from
the instabilities of the SEC currents further to the east (Chelton et al., 2011).
Spatial variations in wind forcing lead to divergent and convergent currents,
resulting in regions of upwelling and downwelling, respectively. Interac-
tions of large-scale current features with island, reef and seamount topogra-
phy produce wakes or vortices on the lee side of the obstacle, which dissipate
energy and trap suspended and floating material and particles (Couvelard
et al., 2008). This was observed around Cato Island (Suthers et al., 2004),
and probably applies to islands throughout the region. Internal waves or ver-
tical perturbations of density surfaces generated by the interaction of the
barotropic tide with the shelf break or other topographic features drive
the nutricline toward the surface during the passage of wave crests. Leaching
of guano from seabird rookeries can also cause local enrichment near cays
and islands (McCauley et al., 2012).
Micronutrients, most commonly iron, often limit the productivity of
ocean environments. Though there are relatively few studies, concentra-
tions of iron appear to vary regionally, with the northern Coral Sea more
The Coral Sea 237
Figure 4.7 Vertical profiles of temperature, salinity, nitrite plus nitrate, silicate, chloro-
phyll a, total dissolvable iron in the northern Coral Sea and the adjacent western
Pacific Ocean. From Obata et al. (2008).
iron-deficient than the western Pacific Ocean (Figure 4.7; Obata et al.,
2008). Several groups of microorganisms living in surface layers of the Coral
Sea have the ability to fix atmospheric N2 (diazotrophy; Moisander et al.,
2010). Recent work indicates that nitrogen fixation by heterotrophs may
exceed that of autotrophs in the open ocean (Halm et al., 2012).

The importance of nitrogen fixation in the world’s oceans is poorly under-
stood but is likely to be significant (Karl et al., 2002); this is especially true of
the Coral Sea, where surface rafts of Trichodesmium are common (Dupouy
et al., 2011; McKinna et al., 2011).
4.2. Phytoplankton and primary production

Coral Sea circulation maintains a deep thermocline and nutricline reaching
110 m in the central Coral Sea, whilst other processes maintain higher pro-
duction at its edges and near islands (Figure 4.8). Low nutrient concentra-
tions in the surface waters of the Coral Sea lead to low surface phytoplankton
biomass (<0.2 mg chl L1) and slow rates of production, although this can
vary with ENSO (Condie and Dunn, 2006). There is a deep chlorophyll
maximum (nutricline) near the top of the thermocline, where concentra-
tions can double (Figure 4.7; Furnas and Mitchell, 1996).
Figure 4.8 Average primary production estimates from satellite data for the period
1998–2007, VGPM: http://www.science.oregonstate.edu/ocean.productivity/ (Behrenfeld
and Falkowski, 1997), in mg C m2 h1. Areas deeper than 200 m have been masked.
The mean depth (m) of the 1 mM L1 nitrate isopleth is extracted from the CARS 2009
climatology—http://www.marine.csiro.au/dunn/cars2009/ (Ridgway et al., 2002).
Vectors: mean 0–150 m total geostrophic currents.
The Coral Sea 239
At most oceanic sites within the Coral Sea, light penetrates deeply into
the water column, producing a deep euphotic zone (Iz >0.1% I0) up to
100 m deep. Fastest rates of primary production are in the well-lit
(20–50% I0) near-surface layer (20–30 m). Nutrients to support primary pro-
duction within the near-surface zone are largely supplied by in situ
mineralisation of organic N and P by bacteria and microbial grazers, but
ratios of dissolved inorganic N (NH4 þ NO2 þ NO3): P (PO4) in the mixed
layer indicate chronic nitrogen limitation of phytoplankton and bacterial
biomass production (e.g. Furnas, 1991). Ellwood et al. (2013) found that
phytoplankton north of the Tasman Front were primarily limited by N,
but further north iron availability probably limits primary production.
Picoplankton (<2 mm) are the largest component of phytoplankton
biomass and primary production, contributing 39–82% of total chlorophyll
in the oceanic Coral Sea (Furnas and Mitchell, 1996). Greatest contributors
to this size class are the cyanobacteria Synechococcus spp. and Prochlorococcus
spp. and, to a lesser extent, small eukaryotic algae. Nanoplankton
(2–20 mm in size and comprising mostly diatoms, dinoflagellates and flagel-
lates) are an important component of phytoplankton biomass under certain
conditions (Furnas and Mitchell, 1996; Tenório, 2006). Populations of
the diazotrophs UCYN-A (<1 mm, photoheterotrophic) and cyanobacteria
Crocosphaera watsonii (3–8 mm, photosynthetic) and Trichodesmium
(Campbell et al., 2005; Moisander et al., 2010) have distinct vertical and
horizontal distribution within the Coral Sea, owing to their temperature
and light preferences and requirements for phosphate and iron (Dupouy
et al., 2004; Campbell et al., 2005). Large phytoplankton (>10mm, e.g.
Trichodesmium) can fix the bulk of available nitrogen at very high rates
(up to 1.8nmol l1 h1). Elevated 15 nitrogen accumulation (up to 0.83nmol
l1 h1) was always observed in the <10 mm fraction, representing a mean of
3120% of total nitrogen fixation, up to 98% at the oceanic DIAPAZON
sampling site in the Loyalty Channel (21 S, 165 E, Garcia et al., 2007;
Masotti et al., 2007). A new Trichodesmium ecotype adapted to low light
was discovered at depth in the Coral Sea (Neveux et al., 2006, 2008).
Jitts (1965) divided the Coral Sea into two regions based on their produc-
tivity, with a boundary at 20 S; the central Coral Sea (15 mg C m2 h1)
and the more oligotrophic southern Coral Sea (11 mg C m2 h1). These
hourly rates are at the low end of those reported from margins of the
Coral Sea by Furnas and Mitchell (1996), which ranged from 16 to
58 mg C m2 h1. At the eastern entrance of the Coral Sea, in situ measure-
ments made during the Pandora cruise in 2011 found primary production
Table 4.3 Means and ranges of primary production rates measured in the Coral Sea
region
Mean primary
production
Region mg C m2 day1 Range Reference
Gulf of Papua 159 210 2–693 Robertson et al. (1993,
(estuarine) 1998)
Gulf of Papua (shelf ) 318 225 134–942 Robertson et al. (1993,
1998)
Central Coral Sea 243 74 117–330 Furnas and Mitchell (1988)
(1985)
Central Coral Sea 431 211 21–462 Furnas and Mitchell (1988)
(1988)
Solomon Sea 491 277 106–701 Furnas and Mitchell (1988)
Papuan Barrier Reef 989 956 247–3030 Furnas and Mitchell (1988)
boundary
Great Barrier Reef 493 297 189–944 Furnas and Mitchell (1988)
boundary (East and Furnas (unpublished)
Australian Current)
Great Barrier Reef 680 Furnas and Mitchell (1988)
shelf and Furnas (unpublished)
New Caledonia lagoon 460 165 Clavier et al. (1995)
ranges from 8 to 33 mg C m2 h1. Changes in methodology may account for

the higher productivities observed in later studies, but a robust estimate of in
situ primary production is hindered by the paucity of data. Nevertheless, some
trends are apparent: more productive sites at the margins of the Coral Sea have
shallower surface mixed layers and a greater proportion of larger (>10 mm)
phytoplankton (Table 4.3). These primary production values can be comple-
mented by indirect estimates from satellites in noncoastal regions (Figure 4.8),
which suggest higher production at the edges of the Coral Sea south of 17 S
and lower production north of 17 S.
4.3. Meso- and macrozooplankton
All published studies on Coral Sea zooplankton are from the epipelagic zone
and used comparatively coarse plankton nets (i.e. >200 mm) that do not
quantitatively sample the most numerous, but small, zooplankton in tropical
seas. Sampling has therefore only glimpsed the top of the mesopelagic zone,
The Coral Sea 241
and the bathypelagic and abyssal zones remain unsampled. Additionally,

sampling has been confined to margins of the Coral Sea, such as coastal areas
of New Caledonia (Le Borgne et al., 2011) and of the GBR (McKinnon
et al., 2005). The only plankton research in the Australian sector of the Coral
Sea has concerned zooplankton biomass in the island wake around Cato
Reef (e.g. Suthers et al., 2006). However, the Coral Sea shares attributes
with other tropical marginal seas, where protistan (e.g. ciliates) and gelati-
nous grazers account for a high proportion of zooplankton primary con-
sumers. Mesozooplankton such as copepods become more abundant in
areas where ‘new’ nutrients are introduced, and these are important prey
to visual predators such as fish larvae (McKinnon et al., 2014).
To our knowledge, there are no production rate measurements of zoo-
plankton in the Coral Sea other than the study of Shushkina (1971), who
measured production to biomass ratios; small copepods had P–B ratios of
22–28%, small chaetognaths 15–20%, herbivorous copepods 6–10% and car-
nivorous copepods 5–8%. The gelatinous zooplankton of the Coral Sea is
characterised by a high relative abundance of pelagic tunicates such as
larvaceans, salps, doliolids and pyrosomes, together with large concentra-
tions of narcomedusan jellyfish such as Pegantha spp., Aegina rosea and
Solmundella bitentaculata, which are known to be specialist predators of gelat-
inous prey (Dhugal Lindsay, unpublished data).
4.4. Micronekton
Trophically, micronekton (fauna 2–20 cm) links plankton to mid- and
top-order predators in the Coral Sea. There are >350 species of fish, crusta-
ceans and squid in the micronekton in the Coral Sea (Valerie Allain,
unpublished data). This micronekton is distinct from the nearby Tasman
Sea fauna (Griffiths and Wadley, 1986). Flynn (2012) identified a Coral Sea
biogeographic region based on lanternfish (Myctophidae) distribution,
coinciding with Condie and Dunn’s (2006) biogeographic boundary at
25 S, which also functions as a boundary for demersal fishes (Last et al.,
2005). Biogeochemical indicators also show evidence of a transition zone at
25–28 S (Hobday et al., 2011; Revill et al., 2009). This differs slightly from
the productivity boundary identified by Jitts (1965) at 20 S (see Section 4.2).
Micronekton species diversity differs between seamounts (Flynn and
Paxton, 2012), open waters (Young et al., 2011) and the vicinity of reefs
and islands (Allain et al., 2012). On a seamount in the western Coral Sea,
the Dana lanternfish Diaphus danae aggregate in spring, attracting top
predators (Flynn and Paxton, 2012). At the southern end of the Coral
Sea, oceanic waters have a broad mix of micronektonic fishes dominated
by the myctophids, Warming’s lanternfish Ceratoscopelus warmingii (Young
et al., 2011).
In New Caledonia, daytime biomass was greatest at 400–500 m depth,
with the dominant fish species belonging to the families Gonostomatidae,
Sternoptychidae, Myctophidae, Opisthoproctidae, Scopelarchidae and
Phosichthyidae, similar to the dominant fish families previously recorded
by Grandperrin (1975) off New Caledonia. At night, a large proportion
of this biomass migrates toward the surface. The 200–400 m layer is depau-
perate, but a peak in biomass was recorded on the eastern slope of the Ches-
terfield atoll between 200 and 300 m depth, with large schools of hatchetfish
Polyipnus (Sternoptychidae; Valerie Allain, unpublished data).
5. BENTHIC ECOSYSTEMS
High diversity and habitat complexity in Coral Sea benthic ecosystems
is conferred by the region’s large geographic extent and complex seafloor
topography across a broad range of depth (surface to >5000 m) and latitude
(8–32 S; Figure 4.1). The region has a complex biogeographic history
(Sections 3.1, 9) and is bathed by ocean currents from numerous sources,
including the biodiverse Indo-West Pacific region (Section 3.2). The pri-
mary benthic ecosystems of the Coral Sea can be broadly characterised as
coral reefs, seamounts, deep shelf and abyssal (bathyal) habitats. Most benthic
ecological studies in the Coral Sea have been conducted on shallow (<20 m)
communities. Sampling of deeper habitats has been scarce. An increased use
of enabling technology such as swath-acoustic seabed mapping and camera
platforms is rapidly expanding knowledge of mesophotic coral communities
(e.g. Bongaerts et al., 2011), but research in bathyal habitats remains
localised.
In general, photosynthetic organisms or organisms with photosynthetic
symbionts (scleractinian corals, zooxanthellate octocorals and sponges) dom-
inate to depths of 60 m, with transition to, then dominance by,
azooxanthellate filter feeders (notably octocorals) in 60–140 m (Dalzell
et al., 1996). Mesophotic, or low-light, coral-based ecosystems have only
recently been observed directly, but are thought to be potentially vast—
extending along at least the 900 km of submerged shelf-edge reefs in the
central GBR (Bridge et al., 2011). In New Caledonian waters, gorgonians,
The Coral Sea 243
brachiopods and sponges become the dominant benthic taxa below the shelf
edge (Richer de Forges, 1998), and galatheid crustaceans dominate the
motile deep-sea macrofauna (Rowden et al., 2010b). At depths >700 m,
the absence of a latitudinal pattern in assemblage structure of ophiuroids
was attributed to the continuity of Antarctic Intermediate Water in the
Coral Sea (O’Hara et al., 2011).
5.1. Coral reefs

Shallow reefs represent <1% of the total Coral Sea area (Heap and Harris,
2008; Figure 4.9), but are biodiversity hot spots, since coral reefs worldwide
host 25% of the world’s known marine biodiversity (Plaisance et al., 2011).
Figure 4.9 Distribution of the major coral reefs in the Coral Sea and surrounding areas.
GBR: Great Barrier Reef; PNG: Papua New Guinea; SOL: Solomon Islands; ACS: Australian
Coral Sea; CHB: Chesterfield and Bellona; LHI: Lord Howe Island; NC: New Caledonia; LOY:
Loyalty Islands; VAN: Vanuatu. Data from the Millennium Coral Reef Mapping Project
(Andréfouët et al., 2006).
The widespread occurrence of shallow coral reefs across the Coral Sea from
the GBR to New Caledonia suggests an important role as ‘stepping stones’
between these areas.
There have been sporadic surveys of the flora and fauna of Coral Sea reefs
in New Caledonian and Australian waters since the 1960s and, to a lesser
extent, on Vanuatu, Solomon Islands and PNG reefs. For instance, there
are at least 56 documents published about Australia’s Herald Cays, whilst
only one ecological study has investigated the Indispensable Reefs and
Rennell/Bellona Islands, an analogous reef system in the Solomon Islands
(Sulu et al., 2002). Extensive multitaxa sampling by the Santo 2006 expedi-
tion around Espiritu Santo Island identified Vanuatu as a biodiversity hotspot
(Bouchet et al., 2011), but outlying reefs and islands of Vanuatu remain
unexplored. Researchers still routinely find new species, new records and
range extensions (e.g. Borsa et al., 2013; Randall and Kulbicki, 2005;
Randall and Walsh, 2010). These discoveries include not just small or
cryptic species, but also large, iconic species such as, for example, the giant
clam Tridacna tevoroa, which was discovered in Tonga and Fiji in 1990 and
recorded for the first time on Lifou Island (New Caledonia) in 2000
(Bouchet et al., 2001) and on Lihou Reef (Australia) in 2008 (Ceccarelli
et al., 2009).
There is little knowledge of patterns or gradients of coral reef benthic
biodiversity or community structure across the Coral Sea, apart from the
general decline in species richness of many reef organisms with increasing
distance from the Coral Triangle (Messmer et al., 2012). The most recent
checklist of scleractinian corals in New Caledonia (which includes the
New Caledonian barrier reef ) lists 309 species in these waters alone
(Pichon, 2006), compared to over 500 in the whole Coral Triangle
(Veron et al., 2011). The Chesterfield Islands alone host 866 species of fish
(Kulbicki et al., 1994), compared with over 3000 reef fish species recorded
in the much larger Coral Triangle (Veron et al., 2011). Macroalgal research
has resulted in an inventory of hundreds of species from PNG, the Solomon
Islands, Espiritu Santo in Vanuatu and New Caledonia including the Ches-
terfields and Loyalty Islands (e.g. Silberfeld et al., 2013). Based on the pub-
lished data (Bittner et al., 2011; Dijoux et al., 2012) the number of species
in several macroalgal groups show that New Caledonia displays higher
species richness than surrounding areas, making this a macroalgal diversity
hotspot. Collating these individual inventories may be a useful
first step for identifying gradients in abundance and species richness (see
Section 6.1.1).
The Coral Sea 245
Reefs and cays in the Coral Sea are relatively undisturbed (Young et al.,
2012). Coral cover, the most common measure of reef condition, is typically
low in exposed habitats and on smaller reefs, and higher in sheltered habitats
and on larger or interconnected reefs with lagoons. Estimates of reef-wide
coral cover range from 7% (Coringa–Herald), through 40%
(d’Entrecasteaux Reefs), to 60% (Osprey Reef; Ceccarelli, 2011;
Garrigue et al., 2000). In many shallow habitats (slopes, reef flats and
lagoons), the dominant biotic benthos is low-profile turf algae and crustose
coralline algae. Community structure and density of motile reef-dwelling
organisms (invertebrates and fish) are heavily influenced by reef size, expo-
sure, isolation, latitudinal position and fine-scale topographic complexity
(Ceccarelli et al., 2009; Kulbicki, 2007).
Only three published studies have addressed ecological processes on
Coral Sea reefs, linking higher internal bioerosion rates to low sedimentation
on oceanic reefs (Hutchings et al., 2005), indicating that reef sponges con-
tribute little (10%) to benthic productivity (Wilkinson, 1987) and identi-
fying a high regeneration rate of corals following a bleaching mortality event
on Lihou Reef, Australia (Ceccarelli et al., 2009). Identifying reefs with a
high capacity for recovery is important in a time of large-scale coral reef deg-
radation (Polidoro and Carpenter, 2013), where more than half of the
world’s reefs are severely degraded and one-third of the world’s 845 species
of reef-building corals are considered to be at elevated risk of extinction
(Carpenter et al., 2008). Coral cover in the GBR has declined by 50% in
the past 27 years (De’ath et al., 2012). In future, relatively unimpacted reefs
such as those of the Coral Sea are likely to become rarer. The potential
for limited resilience on isolated reefs increases the risk of local extinctions
(Graham et al., 2006).
5.2. Seamounts
Seamounts are widespread in the deep Coral Sea, and form part of promi-
nent seabed features including the Tasmantid seamount chain, Lord Howe
Rise, Norfolk Ridge and Louisiade cluster (Figure 4.10). It is predicted that
there are 500 individual seamounts in the Coral Sea (Yesson et al., 2011),
based on an ecological definition that includes seamounts, knolls and hills
(Heap and Harris, 2008). Some seamounts support isolated and rich benthic
communities, elevated faunal biomass (Rowden et al., 2010a) and possibly
unique biodiversity (Castelin et al., 2010), but these properties do not char-
acterise all seamounts and are not quantitatively defined for seamounts in the
Figure 4.10 Locations of Coral Sea seamounts with the primary seamount chains labelled, and the named seamount clusters and seamounts
identified; the prominent and sampled seamounts are highlighted (red diamonds) (CenSeam Project, http://censeam.niwa.co.nz/). The predicted
distribution of large (>1000 m elevation) (○) and smaller (<1000 m elevation) (þ) seamounts follows Yesson et al. (2011). Boundary lines identify
the Coral Sea (red line) and EEZs (yellow lines) (VLIZ Maritime Boundaries Geodatabase, http://www.marineregions.org/).
The Coral Sea 247
Coral Sea. For instance, some Lord Howe Rise seamounts support diverse,
high-density fauna (Williams et al., 2010), but abundance can be sparse on
others (Anderson et al., 2011). Known between-seamount differences in the
Coral Sea include limited overlap of macrofauna between the Chesterfield
Ridge and the Norfolk Ridge (Richer de Forges, 1998) and considerable
differences in macrofauna on New Caledonian seamounts with summits
in a similar bathymetric zone (Rowden et al., 2010a). The Chesterfield
Ridge seamounts have very low biomass compared to those on the Norfolk
Ridge (Richer de Forges, 1998), whilst the Lord Howe Rise and Fairway
and Lansdowne Ridges host Halimeda algal banks and a rich macrofauna
(Richer de Forges et al., 2000). Endemism is scale-specific, and some reports
of small-scale endemism could be artefacts of undersampling (O’Hara et al.,
2011; Samadi et al., 2007).
Whilst the general environmental drivers of seamount benthic commu-
nity structure include depth and proximity to the photic zone, geomorphol-
ogy and substratum type, productivity, chemistry and hydrodynamics of the
overlying water column (Clark et al., 2010), these factors have not been sys-
tematically studied on Coral Sea seamounts. Elsewhere, many seamounts
support relatively high biomass of plankton and higher consumers compared
to the surrounding ocean, particularly in oligotrophic regions (Clark et al.,
2010), and may contribute to their use by migratory pelagic species as mat-
ing, feeding and nursery grounds (Shank, 2010). Coral Sea examples include
the Cairns Seamount (Flynn and Paxton, 2012) and the Tasmantid seamount
chain (Williams et al., 2012a). However, in situ production (via increased
vertical nutrient fluxes and material retention) may be less important than
interruption of deep scattering layers that permit advection and trapping
of zooplankton and micronekton (Clark et al., 2010).
Connectivity between seamounts could be expected to be low, especially
when separated by large expanses of open water. However, the similarity of
the sponge community on the top of the Britannia Seamount (off Brisbane)
with some Norfolk Ridge seamounts (south of New Caledonia) suggests
connectivity between them. Recent population genetic studies, in the Coral
Sea and elsewhere, have found higher than expected connectivity between
seamounts and adjacent slopes (Baco and Cairns, 2012), but not for all taxa
(e.g. molluscs, Castelin et al., 2010). This is, in part, because population struc-
ture is also significantly influenced by dispersal mechanisms and other life his-
tory strategies (Samadi et al., 2006). Genetic differentiation among depth
strata of the same seamount suggests that depth may drive genetic structure
in populations on individual seamounts (Miller et al., 2010).
5.3. Bathyal habitats

The most extensive research programmes targeting deep-sea species in the
Coral Sea, the MUSORSTOM Tropical Deep-Sea Benthos Program and
CIDARIS expeditions, described >2000 new species (Richer de Forges,
1998). At shallower depths (1000 m), off-slope GBR debris flows
(Gloria Knolls) were mapped and sampled in 2007/2008, revealing rich
cold-water coral communities with similarities to those found at equivalent
depths elsewhere in the western Pacific (Beaman and Webster, 2008). The
New Caledonian bathyal environment, including the Loyalty Basin and its
slopes, the Norfolk Ridge and the Lord Howe Rise, is one of the best
known in the Pacific (Richer de Forges et al., 2005; Roux, 1994).
Deep-sea benthic communities in the Coral Sea, including microbial
assemblages in deep-sea soft sediments (Alongi, 1992), are primarily structured
along depth gradients (Richer de Forges, 1998) and with some classes of geo-
morphological structures (Anderson et al., 2011; Beaman and Harris, 2007).
Generally, species richness declines with depth, especially below 800 m
(Castelin et al., 2011). The density of organisms, however, does not necessarily
follow the same pattern. In the deep Loyalty Basin, few species (primarily
ophiuroids and asteroids) were found in high abundance, whilst abundance
was lower but species richness higher on the Loyalty Rise lower slope
(Richer de Forges, 1990). Slopes of the Loyalty Basin and the Norfolk Ridge
revealed ‘living fossils’, including stalked crinoids, sponges and pterobranchs
previously thought to have been extinct since the Jurassic (Roux, 1994).
Quantitative surveys of micro- and meiobenthos in sediment habitats in
300–1600 m depths in the western Coral Sea identified conspicuous
depth-related changes in community composition, together with relatively
high levels of phytodetritus and low concentrations of organic carbon and
nitrogen compared to sediments in other deep areas (Alongi, 1987). These
patterns—including abundant protozoan populations at depth—suggest
potentially rapid microbial activity and detrital utilisation in deep surface sed-
iments on the floor of the western Coral Sea. Densities of protozoans,
meiofauna, and macroinfauna, and bacterial densities and productivity, are
related to (cool) temperatures and materials transported from shallow waters.
6. FISH COMMUNITIES AND FISHERIES

The Coral Sea hosts demersal and pelagic fish communities, both of
which are targeted by fisheries. Demersal fish communities are stratified by
depth, with a distinct fish fauna associated with coral reefs; demersal fisheries
The Coral Sea 249
tend to target deepwater fishes. The largest ecosystem in the Coral Sea is pelagic,
and correspondingly pelagic fishes such as tunas and billfishes have been the
focus of much attention in relation to fisheries research. We summarise infor-
mation on fish communities, including a hierarchical cluster analysis on existing
coral reef fish checklists, and present catch data from demersal and pelagic fish-
eries in the Coral Sea. Even though the greatest direct human impact on the
Coral Sea comes from fisheries, the extraction level within the Coral Sea, com-
pared with other areas of the western Pacific, is relatively small.
6.1. Demersal fish

The Coral Sea remains Australia’s largest knowledge gap for demersal fishes due
to the paucity of biological surveys, with the inference that this is also true for
other biota (Last et al., 2005). The best information on the Coral Sea’s demersal
fishes comes from shallow reefs (Allen, 2008; Kulbicki, 2007). For depth-
constrained demersal fishes (and other biota), large-scale biogeographic patterns
often mirror those of terrestrial and freshwater species, having shared similar
histories of rifting, rafting and dispersal. Deep ocean trenches and basins can
act as barriers to dispersal, and a recent investigation of the biogeography of
Australian fishes (Last et al., 2011) suggests the region is even more bio-
geographically complex than previously thought. Of the teleost specimens
examined in detail from the western Coral Sea, many are new to science or
endemic to the Coral Sea, and sister species indicate separation of the Queens-
land and Marion Plateaux (P. Last, pers. comm.).
6.1.1 Coral reef fishes

The Coral Sea is one of the world’s richest regions for reef fishes. Checklists for the
whole region (including the GBR and New Caledonian barrier reefs) include
2480 species, representing 62% of Pacific reef fishes and 38% of global reef fishes
(Parravicini et al., 2013). However, reef fishes have been surveyed on few reefs,
using disparate methods, complicating Coral Sea-wide assessments of patterns of
biodiversity, endemism and taxonomic and trophic structure. To address these
problems, we gathered available datasets and performed a hierarchical cluster
analysis to compare checklists from individual reefs in the region (Appendix 2;
see supplementary material in the web version of this chapter). Coral Sea reefs
form a related group, characterised by high diversity and low endemism com-
pared to reefs further south (northern New Zealand, New South Wales and
the Kermadec reefs). A southern Coral Sea group, represented by Elizabeth
and Middleton Reefs and related to the reef fish fauna of the Capricorn–Bunker
reefs (GBR), Lord Howe Island and Norfolk Island, links the tropical Coral Sea
fauna to cooler-water assemblages of southern reefs (Figure 4.11).
Figure 4.11 Taxonomic composition of shallow reef fishes across the Coral Sea. Num-
bers represent the cophenetic variation based on 1000 bootstraps. Methods and refer-
ences used to compile the checklists for this analysis are provided in Appendix 2.
The Coral Sea 251
There are north (equatorial) to south (poleward) gradients in species

richness, size and trophic role of reef fishes in the Coral Sea. Species richness
declines with distance from the equator, with 200 species per 3000 m2 on
the Lihou and d’Entrecasteaux reefs and 43–60 species per 3000 m2 on Eliz-
abeth and Middleton Reefs (Appendix 2, Tables S4 and S5; see supplemen-
tary material in the web version of this chapter). Gradients in life history
characteristics include an equatorward increase in the proportion of small
(<15 cm) and planktivorous taxa and a poleward increase in larger species
that are predominantly piscivores, macroalgal browsers and mobile inverte-
brate feeders (Appendix 2, Table S3; see supplementary material in the web
version of this chapter). Recent data collected with Reef Life Survey
methods (Edgar et al., 2010) on 13 reefs in the Australian Coral Sea, from
the Herald Cays in the north to Elizabeth and Middleton Reefs in the south,
also detected a species richness gradient—albeit not as dramatic—ranging
from 529 species per 3000 m2 in the Herald Cays to 287 species per
3000 m2 on Middleton Reef.
Biomass estimates on New Caledonian reefs ranged from 80 g m2 in the
Chesterfield Islands to 463 g m2 at Astrolabe Reef (excluding sharks). These
values were higher than on the New Caledonian barrier reef (Appendix 2;
Tables S4 and S5; see supplementary material in the web version of this chap-
ter) and within the range reported for some of the most pristine coral reefs in
the world (Graham and McClanahan, 2013). High biomass was linked to a
high abundance of top predators (e.g. sharks, large groupers and carangids),
large piscivores and invertebrate feeders (emperors, snappers, Napoleon wrasse
Cheilinus undulatus and eagle rays) and herbivorous surgeonfishes, which could
represent over half of the total biomass at Astrolabe and d’Entrecasteaux reefs.
Diversity and abundance tended to decrease with increasing isolation and lat-
itude and decreasing habitat size (Appendix 2, Figures S2 and S3; see supple-
mentary material in the web version of this chapter). Species richness was
dominated by invertebrate feeders (39%), followed by piscivores, herbivores
and omnivores, whilst abundance was dominated by plankton feeders
(46%), followed by herbivores and invertebrate feeders. The contribution
of regional endemics to diversity and relative abundance increased from
<1% on the northernmost reefs to >30% on the southern reefs (Lord Howe,
Elizabeth and Middleton Reefs; see also Edgar et al., 2010).
6.1.2 Deepwater fishes

Deepwater fishes in the Coral Sea are known from individual expeditions
targeting specific areas and often linked to fisheries; species identification is
often problematic. The most extensive and best-documented exploratory fish-
ing expeditions and scientific sampling have been conducted in New
Caledonian and Australian waters (e.g. Williams et al., 2006). HALIPRO 2

sampled deep ichthyofauna between 230 and 1860 m in the southeastern
Coral Sea, and 40% of collected species were new to science (Grandperrin
et al., 1997). Exploratory deepwater fishing in the Solomon Islands, Vanuatu
and New Caledonia discovered >200 species of deepwater demersal fishes
belonging to 93 genera (Dalzell and Preston, 1992), although many more were
not identified. Last et al. (2005) found that of 1500 fish species from Austra-
lian continental slopes, 21% did not have current names, and many were likely
to be new to science. Given the paucity of sampling, we could expect similar
levels of complexity and novelty among demersal fishes of the Coral Sea.
Eteline snappers, which are targeted by small-scale fisheries in most South
Pacific nations, are an important part of the deepwater fish fauna (Table 4.4).
6.2. Deepwater fisheries

6.2.1 Catch
Small-scale commercial fisheries became established in PNG, the Solomon
Islands, Vanuatu and New Caledonia after the exploratory fishing expedi-
tions in the 1970s and 1980s indicated potential for commercial develop-
ment of deepwater resources (Dalzell and Preston, 1992). Reported
landings from these fisheries have been inconsistent at best, precluding reli-
able estimates of total catch from any country. In Australia, a small number of
commercial vessels have participated in deepwater fisheries in the Coral Sea
since the late 1960s. Catches from these fisheries have varied considerably
over time, but in 2010–2011, total catch was over 70 t in the Common-
wealth Coral Sea Fishery (Woodhams et al., 2012) and around 7 t in the
Queensland Deep Water Fin Fish Fishery (Holmes, 2012).
Artisanal deepwater fisheries in the Coral Sea predominantly use manually
operated vertical drop lines with multiple hooks. Deepwater snappers (genera
Etelis and Pristipomoides) are the primary species targeted by these fisheries,
although a wide range of other species are harvested, including other snappers
(in the genera Paracaesio, Aphareus, Aprion and Lipocheilus), groupers
(Hyporthodus, Epinephelus and Saloptia), carangids (Seriola and Caranx),
emperors (Wattsia), pomfrets (Brama and Taractichthys), snake mackerel
Gempylus serpens, dogtooth tuna Gymnosarda unicolor, oilfish Ruvettus pretiosus
and sharks (Dalzell and Preston, 1992). In Australia, deepwater fisheries in
the Coral Sea use motorised vertical drop lines, trotlines (bottom set long-
lines) and traps to target the same suite of species, in addition to temperate
deepwater species such as hapuku Polyprion oxygeneios, bar cod Epinephelus
ergastularius and blue-eye trevalla Hyperoglyphe antarctica (Woodhams et al.,
The Coral Sea 253
Table 4.4 Species composition of demersal fish caught by drop-line and longline
sampling over the outer barrier reef slope, off western New Caledonia, in water depths
65–350 m (Adrian Flynn, unpublished data)
Scientific name English name French name
Serranidae (groupers)
Epinephelus Blunt-headed rock cod Loche rouge à 6 bandes
amblycephalus claires
Epinephelus magniscuttis Speckled grouper Loche à grosses écailles
Hyporthodus Seven-lined rock cod Loche bagnard
septemfasciatus
Epinephelus cyanopodus Blue maori Loche bleue
Epinephelus chlorostigma Brown-spotted grouper Loche pintade
Mycteroperca morrhua Comet grouper Loche morue
Lutjanidae (snappers)
Etelis carbunculus Ruby snapper Vivaneau chien rouge
Etelis coruscans Flame snapper Vivaneau flamme
Pristipomoides Rosy jobfish Vivaneau rose
filamentosus
Pristipomoides multidens Goldband snapper Vivaneau poulet
Pristipomoides flavipinnis Goldeneye jobfish Vivaneau jaune
Aphareus rutilans Rusty jobfish Lantanier rouge
Lutjanus malabaricus Saddle-tailed perch Perche écarlate
Lutjanus bohar Red bass Anglais
Lethrinidae (emperors)
Lethrinus olivaceus Long-nosed emperor Bec de cane malabar
Lethrinus miniatus Sweetlip emperor Gueule rouge
Wattsia mossambica Mozambique large-eye Brême olive
bream
Carangidae (trevallies)
Seriola rivoliana Almaco jack Carangue amoureuse
Holocentridae (squirrelfishes)
Sargocentron spiniferum Sabre squirrelfish Poisson-écureuil
Continued
Table 4.4 Species composition of demersal fish caught by drop-line and longline
sampling over the outer barrier reef slope, off western New Caledonia, in water depths
65–350 m (Adrian Flynn, unpublished data)—cont'd
Scientific name English name French name
Sharks
Heptranchias perlo Sharpnose sevengill shark Requin perlon
Centrophorus moluccensis Endeavour dogfish Saumonette
Hydrolagus sp. Chimera Chimère
2012). In the southwest Coral Sea, other important genera targeted by mid-
water trawling include alfonsino Beryx spp., blue-eye trevalla and boarfish
(family Pentacerotidae).
6.2.2 Impacts
Formal stock assessments for deepwater fisheries in the Coral Sea have been
hampered by the lack of reliable fisheries data and poor understanding of the
biology of most species. Exceptions include assessments of the trawl fishery in
the southwest Coral Sea that indicate that alfonsino are not overfished
(Woodhams et al., 2012) and the simple depletion models that used explor-
atory fishing data from PNG, the Solomon Islands, Vanuatu and New Cale-
donia to estimate maximum sustainable yields (MSY) for the deepwater fish
complex in each country, based on the length of the 200 m isobath (Dalzell
and Preston, 1992). These estimates of MSY are considered highly uncertain
(Williams et al., 2012b), and recent research has revealed that life histories of
deepwater fishes in the Coral Sea are characterised by extended longevity,
slow growth rates, late maturity and low rates of natural mortality (Fry
et al., 2006; Williams et al., 2013). For example, longevity has been estimated
at 47 years for eightbar grouper Hyporthodus octofasciatus, 40 years for crimson
jobfish Pristipomoides filamentosus, 35 years for ruby snapper Etelis carbunculus,
18 years for flame snapper Etelis coruscans and 19 years for saddle-back snapper
Paracaesio kusakarii (Andrews et al., 2011, 2012; Fry et al., 2006; Wakefield
et al., 2013; Williams et al., 2013). As such, many exploited deepwater species
in the Coral Sea are assumed to have exceptionally low production potential
and are likely to be vulnerable to overexploitation (Williams et al., 2012b).
6.3. Pelagic fish

Knowledge of large pelagic fishes in the Coral Sea has benefited from a sig-
nificant amount of fisheries research, but virtually no fishery-independent
The Coral Sea 255
research exists. Many of these species use the Coral Sea during critical
periods of their life cycles. Genetic data suggest that there is no partitioning
of yellowfin Thunnus albacares and bigeye tuna Thunnus obesus stocks in the
western and central Pacific Ocean (Grewe and Hampton, 1998; Ward et al.,
1994), though tagging data indicates weak connectivity between equatorial
regions and the western Coral Sea (Campbell, 2011b). Larvae of these spe-
cies are found extensively across the subtropical ocean all year round,
suggesting widespread and continuous spawning, although in the north-
western Coral Sea, these species aggregate and spawn over periods of the full
moon during October–January (McPherson, 1991a). Albacore tuna
Thunnus alalunga is considered a single stock across the South Pacific
(Hoyle et al., 2012), although recent analyses suggest genetic heterogeneity
(Montes et al., 2012). Striped marlin Kajikia audax and broadbill swordfish
Xiphias gladius are believed to constitute separate stocks within the southwest
Pacific (Alvarado-Bremer et al., 2005; McDowell and Graves, 2008), with
seasonal spawning well into the southern Coral Sea (Young et al., 2003).
Black and blue marlins Makaira indica and Makaira mazara are believed to
comprise single stocks across the entire Pacific.
Black marlins congregate in the northwest Coral Sea to spawn from
September to December and subsequently disperse to unknown regions.
This is the only known spawning aggregation of black marlin in the world
(Domeier and Speare, 2012). There is evidence of southward movement
of juvenile black marlin in eastern Australia from game fish tagging data
(Pepperell, 1990), representing strong connectivity between coastal
resources (as juveniles feed and migrate on the GBR shelf ) and the wider
Coral Sea. Tagging studies off eastern Australia show that smaller fish can
disperse large distances (>8000 km), but ‘homing’ behaviour has also been
shown (Domeier and Speare, 2012). Detailed information on the sex struc-
ture of black marlin caught around the Coral Sea rim, particularly in areas
influenced by the New Guinea Coastal Undercurrent, could greatly help
resolve the possibility of sex-dependent migration patterns.
6.4. Pelagic fisheries

6.4.1 Catch
Pelagic fisheries in the Coral Sea form part of the world’s largest tuna fishery
in the Western and Central Pacific Ocean, which in 2011 caught in excess of
2.2 million tonnes or 55% of the global tuna catch (Williams and Terawasi,
2012). However, for most species, the catch in the Coral Sea itself is small
compared with catches further north (Figure 4.12). Tunas and billfishes
Figure 4.12 Catch data from the WCPO pelagic fisheries. (A) Total catch (longline, purse
seine and pole line) by 5 5 degree cells for the decade 1950–1959, (B) and for the
decade 2000–2009, (C) longline-only catch by 5 5 degree cells for the decade
1950–1959, (D) and for the decade 2000–2009, (E) longline nominal CPUE by 5 5
degree for the decade 1950–1959, (F) and for the decade 2000–2009. Note: Data used
for these figures are public-domain data published by the Western Central Pacific Fish-
eries Commission. Pie charts show skipjack tuna (dark green), albacore tuna (light
green), bigeye tuna (blue), yellowfin tuna (yellow), billfish (pink) and others (red).
The Coral Sea 257
account for by far the greatest proportion of the total regional fisheries catch,
although xiphiids (swordfish), coryphaenids (mahi-mahi, or dolphinfish)
and sharks are also targeted. In the Coral Sea, the primary fishery method
is longlining, targeting adult albacore, yellowfin and bigeye tunas and
swordfish. Catch and effort statistics for the Coral Sea region (defined as
10–30 S, 140–170 E) were collated from both aggregate annual and quar-
terly 5 5 data covering the western and central Pacific Ocean
(Figure 4.12). Since longline fishing began in the Coral Sea in 1952,
yellowfin tuna (36%) and albacore tuna (30%), followed by skipjack tuna
Katsuwonus pelamis (18%), have been the dominant species taken by all
methods combined. Catch methods are dominated by longlining (78%),
followed by purse seine (18%). Apart from pole and line, effort has increased
substantially since the late 1990s. Annual catches also show concomitant
increases over the past decade, with the mean annual catch of the eight main
tuna and billfish species shown since 2000 (36,901 mt) being double that
taken during the 1990s (18,524 mt; Figure 4.12).
Over the past decade, the annual catch of albacore, yellowfin, bigeye and
skipjack tuna caught in the Coral Sea (39,100 mt) was only a small propor-
tion (1.7%) of the total catch of these species in the western and central
Pacific Ocean, amounting to 11.1%, 2.5%, 1.5% and 0.7%, respectively, for
the individual species. For other species, however, the proportion of the catch
taken from the single stock within the South Pacific Ocean is much higher:
19.2% for albacore, 23.6% for striped marlin and 16.4% for swordfish.
Recreational anglers and spearfishers have caught tunas and billfishes and
other large pelagics off eastern Australia since the early 1900s (Anon, 2000),
whilst artisanal fishers in Vanuatu and the Solomon Islands may have been
targeting these species much earlier. The recreational fishery that targets
pre-spawning aggregations of black marlin in the Cairns/Lizard Island region
off northeastern Australia is internationally renowned, regularly yielding world
record fish. Boutique charter operations in the Coral Sea for spearfishing of
pelagic predators have also emerged in recent years. Due to a lack of logbook
data from these fisheries, the level of take in the recreational sector is unknown.
6.4.2 Impacts
For yellowfin tuna, the most recent assessment (Langley et al., 2011) indi-
cates that the stock in the Western and Central Pacific Ocean is only mod-
erately depleted, whilst bigeye tuna (Davies et al., 2011) is more heavily
depleted and currently at 40% of its unfished biomass. The assessment for
skipjack, South Pacific albacore, southwest Pacific striped marlin and
broadbill swordfish is not spatially disaggregated, making it difficult to infer

the fishery impacts on these species within the Coral Sea alone. Assessments
for blue and black marlin have not yet been completed. However, a total
abundance index based on Japanese longline catch and effort shows large
declines for each of the three marlin species over the past 50 years in the
Coral Sea (Figure 4.12).
Alongside the target species, 100 non-target or bycatch species are cau-
ght by longline fishing in the Coral Sea, some of which are kept (especially
mahi-mahi, wahoo and opah), whilst others are discarded and usually die at
sea (e.g. lancet fish and oilfish). There are some interactions with seabirds
and turtles in the New Caledonia EEZ, but more frequent interactions with
sharks. Shark finning was a common practise until the beginning of the
2000s, but has decreased and was declared illegal since the New Caledonia
EEZ was declared a shark sanctuary in 2013; shark finning was banned in
Australian waters in 2000 (Clarke, 2011).
7. ICONIC AND PROTECTED SPECIES

The Coral Sea has a rich diversity of iconic and protected species
(Appendix 3; see supplementary material in the web version of this chapter),
and the southwestern edge of the Coral Sea is a global hotspot of predator
biodiversity (Worm et al., 2003). A number of species listed under national
or international agreements or legislative documents for special protection
because of their rarity, migratory habits, restricted habitats or other charac-
teristics exist in the Coral Sea, but their exact distribution and abundance are
poorly known. Even seabirds and turtles, whose populations have been rel-
atively well monitored, have not been documented except at a few individ-
ual Coral Sea cays (Figure 4.13).
7.1. Marine mammals

At least 27 species of dolphins and whales frequent the Coral Sea (Borsa,
2006; Garrigue, 2007; Garrigue and Poupon, 2013). There are indications
that the Coral Sea hosts dwarf minke whales Balaenoptera acutorostrata, hump-
back whales Megaptera novaeangliae and sperm whales Physeter macrocephalus
(Arnold et al., 2005; Borsa, 2006), but patterns of colonisation and popula-
tion exchanges between the Coral Sea and other regions remain poorly
understood (Oremus and Garrigue, 2013). The Coral Sea is an important
migration corridor and breeding habitat for humpback whales
(Constantine et al., 2012). Whaling logbook records from the nineteenth
Figure 4.13 Iconic and protected species and their key habitats in the Coral Sea. Individual images: grey reef shark, masked booby, green turtle:
Daniela Ceccarelli oceanic whitetip shark: ©Secretariat of the Pacific Community copyright; Nautilus, minke whale: John Rumney, Eye to Eye Marine
Encounters; endemic sea krait Laticauda saintgironsi: Philippe Borsa humpback whale: Claire Garrigue; black marlin: © John Ashley/OceanwideImages.
com.
century indicate that the Chesterfield archipelago was one of the main whal-
ing grounds for humpback whales in the South Pacific (Townsend, 1935;
Bourne et al., 2005). In the late 1950s and early 1960s, whaling reduced
the 10,000 population to an estimated 500 individuals, and recovery since
the 1963 humpback whaling ban has been slow (Vang, 2002).
A long-term study has followed the dynamics of a population of dwarf
minke whales on the northern GBR, which most probably extends into the
western Coral Sea (Arnold et al., 2005). There are seasonal trends in the
occurrence of sperm whales and, possibly, year-round occurrence of pygmy
sperm whales Kogia breviceps (Borsa, 2006). Studies on depredation of long-
line catches by toothed whales suggest there may be long-term fluctuations
in populations of false killer whales Pseudorca crassidens and short-finned pilot
whales Globicephala macrorhynchus in the Coral Sea (McPherson et al., 2003).
Despite limited information, it appears that toothed whales congregate
around the black marlin spawning aggregation in the northwestern Coral
Sea between October and December (McPherson et al., 2003).
7.2. Seabirds
The Coral Sea cays host at least 18 species of nesting seabirds (Borsa et al.,
2010; Bourne et al., 2005; Robinet et al., 1997). The Australian cays host a
significant proportion of Australia’s breeding population of several species,
including the red-footed booby Sula sula, lesser frigate bird Fregata ariel, great
frigate bird Fregata minor and red-tailed tropicbird Phaethon rubricauda. The
d’Entrecasteaux, Chesterfield–Bampton and Bellona cays host large nesting
colonies of red-footed and brown boobies Sula leucogaster, lesser frigate birds
and great frigate birds Fregata minor, wedge-tailed shearwater Puffinus
pacificus, sooty tern Onychoprion fuscata and black Anous minutus and brown
Anous stolidus noddies (Borsa et al., 2010; Bourne et al., 2005; Robinet et al.,
1997). They also host a few dozen breeding pairs of the New Caledonian
fairy tern (Sternula nereis exsul; Barré et al., 2012; Rancurel, 1976), which
is a significant proportion for this rare species.
Seabird populations have remained mostly stable, except for dramatic
declines in populations of frigate birds and black noddies on the Herald Cays
(Wilcox et al., 2007) and an increase in brown boobies in the Chesterfield
Islands (Borsa et al., 2010). Causes for the changes have been attributed to a
complex set of changes in food sources, suitable nesting habitat, SST and
other climatic conditions since the 1997/1998 El Niño event (Devney
et al., 2009; Wilcox et al., 2007). Seabirds provide the key link between
The Coral Sea 261
terrestrial and marine habitats on oceanic cays, preying on fish in surface

waters and nesting and roosting on cay vegetation, transporting seeds in their
plumage, causing vegetation disturbance, but also contributing to soil devel-
opment and fertilisation through their guano and carcasses (Batianoff et al.,
2010). These links are even more important for unvegetated cays, where
ephemeral fauna and microbial communities are sustained largely by seabird
carrion (Heatwole, 1971).
7.3. Turtles
Six of the world’s seven species of sea turtles are found in the Coral Sea:
green Chelonia mydas, hawksbill Eretmochelys imbricata, loggerhead Caretta car-
etta, leatherback Dermochelys coriacea, flatback Natator depressus and olive rid-
ley Lepidochelys olivacea turtles. The annual monitoring of nesting green
turtles on the Coringa–Herald Cays between the early 1990s and 2005 found
high regional fidelity, with 75% of tagged nesting females returning within a
4–6-year period (Harvey et al., 2005). Green turtles that nest in the Coral
Sea form a distinct genetic group, targeted by fisheries in their foraging gro-
unds in PNG and the Torres Strait (Moritz et al., 2002). Individuals from
other populations cross the Coral Sea during their breeding migration,
and loggerhead turtles travel from islands surrounding the Coral Sea to nest
on the Queensland coastline and in New Caledonia (Limpus et al., 1992).
Leatherback and olive ridley turtles travel through the Coral Sea to forage in
Australian waters. Major ocean currents play an important role in the migra-
tion of hatchlings (Boyle et al., 2009).
7.4. Sea snakes

In the Coral Sea, Guinea (2002) reported 31 sea snake species in Australian
waters, 21 in southern PNG and 14 in New Caledonia. Sea snakes play a
significant role as predators of fishes on coral reefs (Brischoux et al., 2011;
Ineich and Laboute, 2002). Laticauda saintgironsi and Hydrophis laboutei are
Coral Sea endemics, with the former found only in New Caledonia and
the latter found only in the Chesterfield lagoon (Ineich and Laboute,
2002), and the understanding of patterns of endemicity may evolve with fur-
ther sampling and ongoing genetic analysis (Sanders et al., 2013). Available
information suggests a decline in sea snake abundance on some Coral Sea
reefs over the past 20 years, but causes are poorly understood, although some
cases of commercial catches for skins are reported (Lukoschek et al., 2010).
Recent surveys indicate that the southwestern Coral Sea has unusually
high sea snake abundance, with numbers averaging 1 animal per 500 m2
on the Saumarez, Marion, Kenn, Frederick, Cato and Wreck reef systems,
but with no snakes observed on more northern Coral Sea reefs or on the
southern Elizabeth and Middleton Reefs (Appendix 4; see supplementary
material in the web version of this chapter). Surveys using Reef Life Survey
transect methodology (Edgar and Stuart-Smith, 2009) on the GBR indicated
numbers over an order of magnitude lower (0.03 per 500 m2).
7.5. Elasmobranchs
Estimates of species composition, distribution and abundance of elasmo-
branchs (sharks and rays) in the Coral Sea can be obtained from fisheries data
(mainly longline and trawl catches), coral reef surveys and dedicated sam-
pling by trawls or video-based surveys. Based on commercial fishing catch
and bycatch records, the most abundant pelagic sharks in the Coral Sea are
blue sharks Prionace glauca and shortfin mako sharks Isurus oxyrhynchus.
Recently, trophic studies have contributed important new information
on the role of sharks in pelagic ecosystems of the Coral Sea (Revill et al.,
2009). While most pelagic predators have dietary overlap, the shortfin mako
shark has the most specialised diet (with a high proportion of large teleost
prey) and therefore a unique role in the pelagic system of the Coral Sea
(Young et al., 2010).
Other sharks are more sporadically associated with the pelagic ecosystems
of the Coral Sea, undertaking regular movements between coastal and oce-
anic habitats. Tiger sharks Galeocerdo cuvier travel between oceanic islands
and coastal waters (Fitzpatrick et al., 2012), and juveniles have been sighted
at depths of up to 360 m in the Coral Sea around aggregations of Eteline
snappers (Lindsay et al., 2012). The great white shark Carcharodon carcharias
is a winter visitor to the Coral Sea (Bonfil et al., 2010; Tirard et al., 2010),
with peak abundance around New Caledonia coinciding with that of hump-
back and sperm whales (Tirard et al., 2010). Sightings of whale sharks
Rhincodon typus have been reported offshore of the GBR, associated with
lantern fish, tuna and black marlin aggregations in October and November
(Colman, 1997).
Reef sharks in the Coral Sea include resident species and sporadic visitors
(Smith et al., 2008). Coral reefs of the Queensland Plateau also host at least
three species of shallow-water rays (Ceccarelli et al., 2009). Despite their
largely sedentary nature and fidelity to one reef, reef sharks can undertake
The Coral Sea 263
long-range movements, with one grey reef shark Carcharhinus amblyrhynchos

tracked as it travelled between Osprey Reef and the GBR, a distance of
134 km (Heupel et al., 2010). Because reef shark numbers increase with pro-
tection from fishing (Ayling and Choat, 2008), densities of reef sharks are
often used as an indicator of the general health of reef populations
(Sandin et al., 2008). Habitat structure and prey availability are most prob-
ably equally important for supporting healthy shark populations, with higher
abundances of sharks on large and networked coral reefs (e.g. Lihou Reef,
Ceccarelli et al., 2009) than on small, isolated reefs (e.g. Coringa–Herald,
Ceccarelli et al., 2008). Deepwater sharks dwell on the plateaux, slopes
and rises of the Coral Sea (Compagno and Stevens, 1993). A number of
deepwater skates, rays and stingarees have been recorded from the deep
slopes and plateaux, some of which are known only from there (e.g. Iglesias
and Levy-Hartmann, 2012; Seret and Last, 2003). Last and White (2011) also
note the relatively high number of microendemic sharks and rays despite the
paucity of surveys. Some 57% of shark and ray species from slope waters off
central Queensland appear to be endemic to this region.
7.6. Nautilus
Several species of chambered Nautilus are found around coral reefs of the
Indo-Pacific and have been relatively well-studied on Osprey Reef, in
the northwestern Coral Sea (Dunstan et al., 2011a,b). The Coral Sea pop-
ulation of Nautilus pompilius, a member of the cephalopod class between 1
and 5 million years old and capable of extremely deep dives (400 m), is
genetically distinct from the GBR population. This suggests that despite
their ability to undertake deep dives, their horizontal movements may be
more restricted (Sinclair et al., 2007). Furthermore, the species found in
New Caledonian and Vanuatu waters, Nautilus macromphalus, is endemic
to this eastern portion of the Coral Sea. The Loyalty Islands and Vanuatu
stand out as places where Nautilus spp. can be found in relatively shallow
waters at night (Dunstan et al., 2011b).
8. ECOSYSTEM LINKAGES AND HOTSPOTS

IN THE CORAL SEA
Interactions between topographic complexity, oceanographic pat-
terns and animal movements determine the broadscale ecological processes,
trophic structure and the direction, strength and timescale of connectivity
between different ecosystems in the Coral Sea. A useful classification of
Figure 4.14 Schematic diagram of key features and defining characteristics of the
northern, central and southern Coral Sea. Cross-section profiles were adapted from
bathymetry data provided by Robin Beaman
the Coral Sea is based on the major structural features, which vary among the
northern, central and southern sectors (Figure 4.14). The northern Coral Sea
is predominantly an open-water habitat (>4000 m), with the Hiri Gyre hav-
ing a strong influence on pelagic ecology. The central Coral Sea hosts the
highest density of coral reefs and islands, creating a network of stepping sto-
nes between the Australian coast and GBR in the west and the islands of
New Caledonia and Vanuatu in the east. The southern Coral Sea is
The Coral Sea 265
characterised by three prominent rises with abundant seamounts, separated

by deep basins and trenches (>3500 m) and influenced by the proximity of
the oceanographic boundary of the Tasman Front. The following sections
highlight the ecological features and linkages typical of the three Coral Sea
sectors.
8.1. Northern Coral Sea

The Hiri Gyre, which flows from the northern arm of the bifurcation of the
SEC at the Australian continental margin, plays a major role in the northern
Coral Sea’s oceanography and in the life cycle of species such as the rock lob-
ster (Panulirus ornatus; Figure 4.14). Rock lobster breeding areas in the eastern
Gulf of Papua, on the shelf edge of the far northern GBR and along the east
coast of Queensland, produce larvae that are entrained into the Hiri Gyre,
where they develop, and settle in the Torres Strait and the northern GBR
(Dennis et al., 2001). Also, a high density and diversity of eel leptocephalus
larvae have been collected from the northwestern Coral Sea, with larvae of
at least 40 species (Miller, 2009). This area may represent a spawning ground
for eels that migrate from freshwater systems >1000 km away. Eel leptoceph-
ali and the larvae of tunas feed on pelagic tunicates and jellyfishes, which are an
important part of the ‘jelly food web’ typical of this region (see Section 4.3).
The question of whether the Hiri Gyre enhances connectivity through the
area, or acts as a barrier to dispersal, remains unanswered, and it may play dif-
ferent roles for different species. The Coral Sea basin appears to be the Coral
Sea’s most prominent topographic barrier to larval dispersal between shallow-
water habitats at its margins (Mora et al., 2012).
Another prominent element of the northern Coral Sea is the ‘Cairns hot
spot’, featuring myctophid spawning grounds (Flynn and Paxton, 2012),
possible spawning and mating grounds for yellowfin and bigeye tuna
(McPherson, 1991b), and the world’s only known black marlin spawning
aggregation (Domeier and Speare, 2012). A lunar periodicity in aggregations
of tuna and billfishes noted in Japanese catches is thought to be related to
changes in current strengths, which may create a deep turbulence that gen-
erates an upwelling or doming effect. Church and Boland (1983) suggested
that plankton swept southward by the surface EAC may be carried north-
ward at a later stage by an undercurrent, influenced by the bathymetry of
the area. Myctophid populations in the Queensland Trough may be carried
southward during the night and returned northward by the deeper under-
current during the day.
Further east, the Louisiade Plateau, Rennell and Bellona Islands, the
New Hebrides Trench and the islands of northern Vanuatu are perhaps
the least known of the Coral Sea’s ecosystems. Fisheries catches of yellowfin
and skipjack tuna tend to be higher in this region than in the rest of the Coral
Sea (Figure 4.12), suggesting high productivity.
8.2. Central Coral Sea

The central region hosts potentially the highest biodiversity of the Coral Sea,
given its abundance of coral reefs, and a high proportion of research on the
Coral Sea’s shallow-water habitats comes from this central region. Small
islands and cays are a negligible proportion of the Coral Sea’s surface area,
but these are concentrated in the central Coral Sea, providing resting, feed-
ing and nesting habitat for migratory species such as seabirds and turtles. This
region is also likely to have the highest benthic productivity and is the region
of major transport from east to west by the prevailing jets of the SEC
(Figure 4.14).
Population and genetic connectivity of coral reefs in the Coral Sea is a
key issue, since oceanic coral reefs are generally vulnerable to overex-
ploitation and climate change impacts and may rely on self-seeding or spo-
radic external sources for recruitment. Isolation and high exposure to
cyclones make Coral Sea reefs more vulnerable to natural catastrophic
impacts than the continuous reef systems of New Caledonia or the
GBR (Graham et al., 2006). Models of dispersal-driven connectivity sug-
gest that links across the Coral Sea are weak, depend on a long larval dura-
tion, and are stronger during El Niño years (Treml et al., 2008), whilst
other research highlights the stepping stone role of Coral Sea reefs in
the dispersal of shallow-water taxa (e.g. van Herwerden et al., 2009). How-
ever, the role of oceanographic patterns is still unclear; gyres can form over
individual plateaux (e.g. the Marion Plateau), potentially entraining species
and their larvae and enhancing the probability of endemism (Middleton
et al., 1994).
Most research on mesophotic reefs and deepwater corals (e.g. the Gloria
Knolls) has been in this central section of the Coral Sea, generating hypoth-
eses about the role of deeper-water communities as refugia for the recovery
of shallow habitats that are at greater risk of disturbance from storms and
coral bleaching (Bongaerts et al., 2011). Coral Sea reefs may also have
had a role as refugia during periods of lower sea levels; they may act as refugia
again as reefs closer to human populations become increasingly degraded.
The Coral Sea 267
8.3. Southern Coral Sea

A cross-section of the southern Coral Sea reveals a series of three rises and
ridges, punctuated by seamounts and separated by deep basins (Fig. 14.3).
Some of the seamounts (especially the northernmost ones) are crowned
by emergent reefs and islands, but most are submerged and serve as isolated
habitat patches for deep-sea biota. Communities are influenced by localised
upwelling, eddies driven by the flow of the EAC, and the proximity of the
Tasman Front. Benthic communities in this region have received little
attention, and new species of both vertebrates and invertebrates have been
collected in the past decade (Bruce, 2009; Imamura and Knapp, 2009; Last
and Yearsley, 2002; Poutiers, 2006).
Links between the central and eastern parts of this region to New
Zealand (e.g. through genetics of sessile and demersal taxa) and the Southern
Ocean (e.g. through migrating whales) are strong. For fish, strong faunal
relationships exist between the northern ends of the seamount chains and
more northern regions of the Coral Sea and the Queensland continental
shelf, whilst fishes in the southern half of the seamounts relate more closely
to New Zealand (Zintzen et al., 2011). Invertebrate affinities are more com-
plex and may occur at a finer scale (Williams et al., 2006); ophiuroids from
waters >150 m are more closely related to New Zealand and New Caledo-
nia deep-sea faunas than to Australian fauna. Migrating humpback whales
traverse the area annually (Garrigue et al., 2011), as do freshwater eels
migrating from spawning grounds in northern Coral Sea to New Zealand
and southeastern Australia (McDowall et al., 1998).
9. BIOGEOGRAPHY AND CONNECTIVITY WITHIN

AND BEYOND THE CORAL SEA
The Coral Sea is at the interface of a number of large biogeographic
regions, including the Coral Triangle and the GBR, which contain the
highest marine biodiversity in the world. For invertebrates and fishes, con-
nectivity between habitats and regions depends on the interaction of ocean
currents with larval behaviour, swimming ability, survival and successful set-
tlement on suitable habitats (Cowen and Sponaugle, 2009). For larger, more
mobile fauna, behaviour and seasonal migrations determine patterns of
connectivity.
The complex geological history of the Coral Sea and the varied topog-
raphy of today’s seabed have contributed to its current biogeographic
complexity. The evolution of species in the Coral Sea may have been driven
by the separation of plateaux, ridges and island chains from the Gondwanan
continent, by the appearance and disappearance of islands and by large sea-
level fluctuations (Pelletier, 2006). For instance, as recently as 20,000 years
ago, during the Last Glacial Maximum, sea level was >120 m below that of
today. Conversely, during warmer periods, sea levels rose by 100 m in
more recent times, drowning reefs and shoals and forcing shallow-water spe-
cies to re-colonise elsewhere. Effects of plate tectonics and fluctuating sea
levels resulted in greater numbers of, and more closely spaced, emergent
reefs, island chains and shallow ridges, providing stepping stones for the
potential dispersal of species. Many marine, terrestrial and freshwater species
common to New Caledonia, Australia, PNG and surrounding islands are
likely a result of these historic connections (Pelletier, 2006).
The level of functional connectivity between the main coral reef areas
of the Coral Sea remains poorly characterised. However, several gene
flow studies have used Coral Sea samples in a larger Indo-Pacific context
(e.g. sea snake Aipysurus laevis; fishes Scomberomorus commerson, Cephalopholis
argus and Triaenodon obesus; echinoderms Linckia laevigata and Acanthaster
planci; and a variety of algae), but few have focused on the Coral Sea itself.
Patterns and processes vary widely and may be subjected to frequent mod-
ifications with larger sampling efforts (e.g. Lester and Ruttenberg, 2005).
The Chesterfields, for example, are isolated from the GBR to the west
and New Caledonia to the east by basins 3500 m deep, restricting
dispersal of many demersal species, which are often limited to narrow
bathymetric ‘bands’. However, high connectivity in coral reef fishes may
be assisted by their lengthy larval duration (typically 28–35 days), although
historical changes in connectivity with fluctuating sea levels make the
relationship between larval duration and genetic relatedness inconsistent.
Dispersal capability of demersal species may also be facilitated along ridges
such as the Norfolk Ridge or across areas of shallow habitats. For instance,
several western Australian echinoderm populations were more closely
related to Pacific populations than those in the Indian Ocean (Benzie,
1998), suggesting possible pathways between the Coral Sea and the Arafura
and Timor Seas through the Torres Strait (Mirams et al., 2011). Alterna-
tively, the link between these populations could pre-date the collision of
the Australian plate with Southeast Asia (50 Mya) (Andreakis et al., 2012).
Dispersal pathways from eastern PNG southeast along the Solomon
Islands, Vanuatu and New Caledonia island chains and from PNG south-
ward to the GBR across the Torres Strait are likely for some species, given
The Coral Sea 269
the proximity of available habitats (Benzie, 1998). On the other hand, iso-
lated reefs such as those throughout the central Coral Sea appear to be largely
reliant on self-seeding (Ayre and Hughes, 2004), and species with limited
larval dispersal capabilities have developed genetically distinct populations
at short spatial scales (Planes et al., 2001).
Larval transport of shallow benthic invertebrates (e.g. sponges and clams)
may have occurred westward from the Pacific, with reefs forming stepping
stones across the Coral Sea (Benzie, 1998; Treml et al., 2008). Jets of the SEC
may therefore provide both the connectivity pathways between eastern and
western reefs and a dispersal barrier between north and south. Conversely,
the EAC enhances connectivity between the central Coral Sea and temperate
waters to the south, and the North Queensland Current provides a northern
pathway from the Coral Sea into the Solomon Sea. At a finer scale, separation
is indicated in the marine flora of the Chesterfield and Bellona Plateau, the
Loyalty Islands and the New Caledonian coastal reefs and lagoons, with less
than 25% of species in common (Claude Payri, unpublished data).
Fisheries tagging research or large-scale biodiversity sampling (Census of
Marine Life, Lifou 2000, Santo 2006, Niugini 2012, etc.) can highlight crit-
ical locations and habitats across multinational boundaries. Pelagic apex
predators exploit their environment in predictable ways, returning regularly
to key feeding and breeding grounds (Block et al., 2011) and displaying some
degree of regional fidelity (Evans et al., 2011). Great white sharks move from
New Zealand waters to more equatorial latitudes of the southwestern Pacific
(including the Coral Sea), presumably following the migration pathways of
humpback whales (Tirard et al., 2010). Leatherback turtles travel from
southeastern Australia to the Solomon Sea and then across the Pacific to
the California Current Large Marine Ecosystem (Block et al., 2011). Tagged
tunas and billfishes regularly travel from the Coral Sea to the equatorial,
northern and eastern Pacific (Campbell, 2011a).
Movements of large animals link not just geographic areas but also dif-
ferent ecosystems (McCauley et al., 2012). In the Coral Sea, seasonal move-
ments of tunas, marlin, swordfish and pelagic sharks form a key link between
temperate regions (the Tasman Sea) and tropical areas (the Coral Sea;
Hobday et al., 2011; Stevens et al., 2010). Much less is known about dis-
persal and connectivity in deep-sea habitats, and depth stratification appears
more significant than geographic distance for some species, even across loca-
tions as widely separated as Australia, New Zealand and Chile (Miller et al.,
2011). Such comparisons have yet to be carried out between deep-sea ben-
thos of the Coral Sea and other locations connected by deeper water masses.
10. RESEARCH AND MANAGEMENT PRIORITIES

Despite at least seven decades of research in the Coral Sea, there
remain large knowledge gaps that hinder the understanding of ecosystem
processes (Table 4.1). Here, we highlight the most significant areas that
could help prioritise future research and argue that there is a need for a more
integrated management approach.
10.1. Species inventories

At the most basic level, species inventories are still needed for most habitats;
even coral reef communities, which have perhaps been the best studied, still
lack the geographic scope to aid the definition of patterns of biodiversity,
endemism, community structure and species composition. Species-level
inventories have an important role in establishing the foundations of ecosys-
tem functioning (Vermeulen, 2013) and ultimately informing management
decisions that focus on biodiversity conservation (Dunstan et al., 2012). Sev-
eral taxa are well studied (e.g. coral reef fish and algae), but gaps remain. The
discovery of new species in the last decade, even in shallow waters, suggests
that visual census and sampling by collection are likely to be of great value,
especially in areas that remain undersampled (e.g. the northeastern Coral
Sea). Existing knowledge suggests a number of biogeographic provinces
within the Coral Sea, but without the characterisation of species composi-
tion throughout the area, these are not yet defined. Similarly, fine-scale
endemism cannot be resolved without more intensive sampling. It is also
important that taxonomic descriptions keep pace with ecological research;
integrative taxonomy (using morphological and molecular data) will help
uncover cryptic species and address broader questions of phylogeography
and evolutionary ecology.
In areas difficult to access due to remoteness or depth, the use of habitat
proxies or surrogates has shown promising results for inferring biodiversity
patterns. In deep-sea environments, physical seabed characteristics can be
good predictors of taxonomic composition and the proportional cover of
benthic taxa (Anderson et al., 2011; Dunstan et al., 2012). Trails, burrows
and other traces of life (lebensspuren) are a useful indicator of assemblage
structure in the Coral Sea (Dundas and Przeslawski, 2009). Biophysical sur-
rogates and lebensspuren can both be sampled remotely, and the develop-
ment of remote sampling devices for the collection of images or actual
samples has advanced rapidly in recent years (e.g. Lindsay et al., 2012).
The Coral Sea 271
10.2. Movement, migration and connectivity

Ecological connectivity at all scales remains poorly known. Patterns of
connectivity have crucial conservation and sustainability implications,
especially given the position of the Coral Sea in relation to biodiversity
hotspots in the Coral Triangle and on the GBR. Connectivity is vital to
communities for larval replenishment and the exchange of genetic mate-
rial to maintain resilience and diversity, especially after periods of stress or
disturbance (Bernhardt and Leslie, 2013; Thrush et al., 2013). Molecular
markers (Baco and Cairns, 2012), numerical simulation (Treml and
Halpin, 2012) and trace elemental fingerprinting (Thorrold et al.,
2007) have been the primary methods emerging during the past decade,
but usually, these studies have focused on one or two species, rather than
assemblage-level investigations (Lopez-Duarte et al., 2012). Understand-
ing connectivity at the level of multispecies assemblages would give
insight into the recovery potential of communities in a time of increasing
disturbance (Thrush et al., 2013). Management decisions increasingly rely
on establishing source and sink populations and connectivity pathways,
and the ongoing development of genetic tools is improving the ability
to locate these pathways.
There is little knowledge of migration routes and residency of threatened
and endangered species, as most studies on the movement of large oceanic
species have focused on fishes and sharks of commercial importance. It is
increasingly understood that large, mobile marine animals link different
regions and ecosystems through their movements (McCauley et al.,
2012). Genetic analyses, satellite tags and acoustic arrays have provided
insights into movement of individual animals and could be coupled with
visual surveys and mapping techniques to identify multispecies pathways.
10.3. Temporal dynamics and ocean observation

We know relatively little about the natural variability of Coral Sea ecosystem
structure and processes. Long-term studies are critical for understanding
ecological responses to physical changes in the environment, detecting eco-
system processes over long (e.g. decadal) timeframes and providing data to
support population models, multidisciplinary research and management
decisions (Lindenmayer et al., 2012). Only fishes of commercial importance
and species that make some use of terrestrial environments (seabirds and tur-
tles) have been the subject of dedicated monitoring in the Coral Sea (Baker
et al., 2005; Harvey et al., 2005).
In a time of rapidly changing environmental conditions, describing

‘baseline’ conditions against which to measure change is increasingly diffi-
cult. With relatively low anthropogenic impact, the Coral Sea represents a
tropical sea close to its environmental baseline. Long-term datasets are
increasingly available through remote sources (e.g. satellite imagery), but
the links between remotely sensed parameters and biological responses are
theoretical at best and unknown for most species. There needs to be a con-
certed effort in the Coral Sea to collect baseline biological data.
10.4. Ecosystem modelling for a whole-of-system

understanding
Ecosystem models are increasingly used for strategic assessment of broad
management strategies and for exploring marine ecosystem function and
structure (Plagányi, 2007; Travers et al., 2007). ‘Whole-of-system’ models
have been used to: (1) integrate extensive amounts of system information
and highlight major gaps in knowledge; (2) increase understanding of sys-
tem dynamics and identify major processes, drivers and responses; and (3)
simulate alternative options for management (including monitoring
schemes and the potential cumulative effects of anthropogenic impacts;
Fulton et al., 2011). For example, ecosystem models such as Ecopath with
Ecosim have been formulated to evaluate the role of squid and micronekton
fish under various climate impact scenarios in the region (Griffiths
et al., 2010).
A whole-of-system model for the Coral Sea currently in development
(CSIRO, Australia) using the Atlantis framework (Fulton et al., 2011) faces
major challenges associated with data availability. Once complete, this
model should provide improved understanding of the ecosystem dynamics
and major processes and allow evaluation of the consequences of different
management approaches.
Qualitative models can be used as an initial step to describe the system
using available expert knowledge and identify key inconsistencies and gaps,
before the full implementation of any quantitative modelling exercise
(Dambacher et al., 2009). A key output for informing management in this
case would be an outline of key uncertainties and a ‘value of information
analysis’ of what data and information are critical for management of the
Coral Sea. Given the lack of understanding of system dynamics, any
large-scale ecosystem modelling would be more of a ‘proof of concept’
and as an initiative would at best evaluate broad questions, which could,
The Coral Sea 273
for example, consider large-scale climate-related impacts or strategic ques-

tions such as the potential effects of MPAs on the system as a whole. The
development of models that could evaluate the value of management actions
is still some way off, given the uncertainties in data, system processes and
ecosystem function, although initiatives are under way to use models of
intermediate complexity (Plagányi et al., 2012).
10.5. Human use and impacts

Despite relatively low human impact in the Coral Sea, the area has a history
of fishing, shipping and other low-impact human uses (e.g. tourism and
research). Fisheries activities beyond the continental shelf span at least
70 years, and some have been well documented (e.g. longline tuna fisheries).
However, even for these fisheries, unanswered questions remain regarding,
amongst others, population connectivity and migration pathways between
the Coral Sea and adjacent regions, the relationship between fish movement
and climate and oceanography, biological parameters of bycatch species, and
spawning and residency times. Artisanal and boutique charter fisheries that
may range beyond the continental shelves, and recreational fisheries (espe-
cially in Australian waters), are poorly documented. For instance, the num-
bers of boutique game fishing and spearfishing charters to Coral Sea reefs
from the Australian coastline have increased in the past decade, but there
is no information on species composition or magnitude of the catch. Given
the isolated nature of Coral Sea reefs, serial depletion of stocks of target spe-
cies on individual reefs is a real possibility.
A major shipping lane crosses the Coral Sea between southeastern
Australia and Southeast Asian ports, but the risks to the environment of
commercial shipping have not been assessed. Further high-impact human
uses, such as mining, have yet to occur in the Coral Sea, although there
has been some petroleum exploration within the New Caledonia EEZ
(Brodien et al., 2003). Plastic pollution is a pervasive problem throughout
the world’s oceans and has yet to be quantified for the Coral Sea. There
is a need to understand how a changing climate and increased seafood
demand, vessel traffic and marine debris may affect the Coral Sea.
10.6. International collaboration on research and management

EEZs of five nations lie in the Coral Sea, but the only joint research
programmes have been French–Australian–New Zealand collaborations
and cruises in the southern regions of the Coral Sea. International workshops
have considered aspects of the Coral Sea, but until a recent meeting
(Brisbane, March 2013), there have been no specific workshops focused
on the region as a whole. There is a desire from scientists and managers
to better coordinate the management of the Coral Sea, particularly between
Australia and New Caledonia in the context of the potential co-management
of a future large marine protected area.
Investment in research and management should reflect the scale of the
Coral Sea, including collaboration and capacity building, as necessary, for
the bordering countries. Key transboundary issues include ecologically
significant and migratory species, seamounts, coral reefs and human pres-
sures on those environments (including fisheries); these will need to be
managed at regional (or even global) scales to be effective. Useful focal
points for collaboration on science and management include the sharing,
collation and synthesis of existing datasets; the standardisation of data col-
lection and storage methods; the development of a bioregional profile
that includes all five EEZs; and the sharing of technical expertise and
equipment. A series of shared, multidisciplinary and multinational voy-
ages tackling some of the issues raised in this chapter would substantially
improve our knowledge of the Coral Sea and provide the foundation for
improved management. A regional conference on current research in the
Coral Sea could help stimulate collaboration.
11. CONCLUSIONS
The Coral Sea is an important component of the southwestern Pacific,
with particular significance because of its relatively unimpacted state. It con-
nects the tropical centre of marine biodiversity with subtropical and temper-
ate seas, and its oceanography influences Pacific-wide climate dynamics. It
contains critical spawning and breeding habitats for wide-ranging pelagic
species whose movements link it to Antarctic waters and to the eastern
and northern Pacific. The Coral Sea’s character changes latitudinally in
response to oceanographic–topographic interactions. The reefs and islands
have unique assemblages that show varying degrees of connectivity within
the Coral Sea, links to the western Pacific, individual sectors of the GBR and
the wider Indo-Pacific beyond.
This synthesis of current knowledge has allowed the identification of a
number of key areas of global and regional significance, most of which
require further investigation. The Coral Sea offers a rare opportunity to
The Coral Sea 275
explore a tropical sea as close to its ‘baseline’ condition as any marine area in
the world. As the exploitation of living and nonliving marine resources
expands, this opportunity may be lost. Collaboration across EEZ boundaries
has already led to the streamlining of research interests and the foundation for
complementary management. This chapter provides the platform from
which key knowledge gaps can be addressed across the entire Coral Sea,
enhancing the ability to manage and assess the impacts of future human
activities.
ACKNOWLEDGEMENTS
Funds for the two workshops that led to the writing of this chapter were provided by AIMS,
CSIRO and the Agence des Aires Marines Protégées. PKD, NB and DCG were supported by
the Australian Government’s National Environmental Research Program (NERP) and
CSIRO’s Wealth from Oceans Research Flagship through the Marine Biodiversity Hub.
AJR was supported by an Australian Research Council Future Fellowship FT0991722.
We thank Peter Last, Xavier Bonnet and François Brischoux for assistance with the text;
Dr Hajime Obata (University of Tokyo) for sharing his data on micronutrients in Coral
Sea waters; and Louise Bell, Wayne Rochester and Franziska Althaus (CSIRO) for
assistance with figures.
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SUBJECT INDEX
Note: Page numbers followed by “f ” indicate figures, and “t ” indicate tables.
A benthic ecosystems, 242–248

Adult acclimation, sea urchin biogeography and connectivity, 267–269
detrimental effect, 199 biological oceanography, 235–242
energy storage tissue, sea urchins, 201 climate, 231–234
eperistomal membrane, 199 ecological and biological studies, 227
euryhalinity, 198 ecosystem linkages, 263–267
experimental designs, 199–200 and EEZ boundaries, 216, 217f
gonad index, 202, 202f fish communities and fisheries, 248–258
growth rates, sea urchins, 200 and GBR, 216
natural variation, 200 global marine research, 218–226, 226f
peristomal membrane, 199 human use and impacts, 273
PIT tag identification, 200–201 iconic and protected species, 258–263
salinity records, 198 international collaboration, research and
sea urchins, growth increment, 201f, 202 management, 273–274
space constraints, 198–199 marine resources, 215–216
test diameters, 200f, 201 modelling, ecosystem, 272–273
movement, migration and connectivity,
B 271
Benthic ecosystems and MPAs, 216
bathyal habitats, 248 nongovernment organisations, 218–226
coral reefs, 243–245 physical oceanography, 229–230
seamounts, 245–247 PNG, 216
Biological oceanography spatial distribution, 227–228, 227f
meso- and macrozooplankton, 240–241 species inventories, 270
micronekton, 241–242 tectonics and topography, 228–229
nutrients and supply, 236–238 temporal dynamics and ocean
phytoplankton and primary production, observation, 271–272
238–240
D
C Deepwater fisheries
Central Coral Sea, 266 barrier reef slope, 251–252, 253t
Climate, Coral Sea catch, 252–254
coral reefs, 232 HALIPRO 2, 251–252
GPCP data, 232, 233f impacts, 254
PCMDI5, 234 Demersal fish
pelagic systems, 232–234, 234t coral reef, 249–251, 250f
seasonal variability, 232 deepwater, 251–252, 253t
sea surface temperatures, 234, 235f Diet and feeding ecology, Irukandji
SEC transport, 232–234 crustaceans vs. larval fish, 35
SST, 231–232 energy expenditure, 35–36
Coral Sea ontogenetic shift, 35
areas and gaps, 218, 219t peculiar banding, 35–36
291
292 Subject Index
E Irukandji stings, 41–42, 42f

Echinoderms shallow stings, 43
aquaculture production, 204 surface-swimming tendency, 41–42
biologically important ions, 193 vertical migration, 43–44
distribution and diversity, 172–173 wind effects, 53–54
HSP production, echinoids, 203–204 Ecosystem function
marine invertebrates, 203 species-level inventories, 270
physiological basis, 203 tropical marginal seas, 218
physiological mechanism, 204 El Niño–Southern Oscillation (ENSO),
relevance and brief history of salinity 49–51, 50t
measures, 173–175 ENSO. See El Niño–Southern Oscillation
salinity tolerance and response, 175–193 (ENSO)
S. droebachiensis and hyposalinity, 194–203 Envenomation, 5
Ecology, Irukandji Eyes and vision, Irukandji
aquatic activities, 56 Cubozoan eyes, 30, 32f
bimodal seasonal distribution, 47–48 lateral pit and slit eyes, 32
cross-shelf distribution, 38–41 physical capacity, 30
diet and feeding, 35–36 structural features and different functions,
distribution, Australia, 37, 38f 30–31
effect, multiple ecological factors, 57–58 types, 30–31
environmental factors, 55 upper lensed eye, 31–32
infestation events, 55 visual capabilities, cubozoans, 30, 31t
oligotrophic shelf habitats, 41 visual ecology, 33
periodic influxes, 54–55 visual evolution, 33–34
rainfall effect, 58
safety management, 56 F
seasonality Fish communities and fisheries
climate change influence, 51–52 deepwater, 252–254
coastal stings, 44 demersal fish, 249–252
daily beach monitoring, 45–46 pelagic fish, 254–255
diurnal patterns, 48–49 Food web
ENSO, 49–51 jelly, 265
logical concern, 44 phytoplankton assemblages, 235–236
lunar periodicity, 48
marked seasonal prevalence, 47 G
reef locations, 46–47 GBR. See Great Barrier Reef (GBR)
sampling intensity, 45 Generalized linear model (GLM), 137
taxonomy, 47 GLM. See Generalized linear model (GLM)
spawning aggregations, 55 Great Barrier Reef (GBR)
species-syndrome linkages, 40 Capricorn–Bunker, 249
sting distribution, 36, 37f debris flows, 248
sunlight effect, 58 dwarf minke whales, 260
swimming behaviour, 56 New Caledonia, 266
syndrome variation, 36 Green sea urchin
systemic syndromes, 37–38 acclimation/recovery, repeated
temperature effect, 56–57 exposures, 194
tide effect, 57–58 adult acclimation, 198–203
vertical distribution Juvenile acclimation, 195–198
Subject Index 293
metabolic responses, 194 propagule pressure, 93–94

physiological acclimation, 194 snail–parasite system, 93–94
repeated exposures, hyposalinity, 194 Irukandji syndrome
stenohaline environment, 194 ecology, 35–58
tidal and seasonal salinity variation, 194 evolution
fossil evidence, 23–24
H unrooted phylogeny, Cubozoa,
Heat shock proteins (HSP), 200–201 22–23, 23f
Host–parasite system eyes and vision, 30–34
data extraction, 109–112 global distribution, knowledge, 11, 12f
geography human health, 5
AQC, DBF and OYS, 145–146 hypertension, 2–4
biogeographic relationships, 93 ISI Web of Science search, 6–11, 10f
geographic range and location, 92–93 marine tourism threats, 5
latitudinal and longitudinal medical effects, 4–5
explorations, 126, 127f mimic decompression illness, 4
marine biodiversity, 144 minor sting, 2
ports and transport time, 92–93 phototaxis, 34
source and recipient regions, 144 reproduction and life cycle, 24–30
stress-induced mortality, 145 research and management, 5
taxa stinger management, 65–69
first and second-intermediate host, 96 symptoms, 3
host population, 95–96 taxonomy, 11–22
host’s invasive range, 95–96 techniques, 69–70, 70t
life cycles, 95–96 timeline, Irukandji syndrome research,
molluscs and crustaceans, 95 6, 6t
trematodes, 96 tourism industry, 4
HSP. See Heat shock proteins (HSP) toxins (see Irukandji syndrome-producing
toxin (ISPT))
I ‘type A stinging’, 6
Iconic and protected species Irukandji syndrome-producing toxin (ISPT)
elasmobranchs, 262–263 adhesive/fibrous properties, 62
marine mammals, 258–260 adrenal medullary/catecholamine
nautilus, 263 excess, 59
oceanic whitetip shark, 258, 259f anthozoan metaproteome, 63
seabirds, 260–261 bell-shaped sting mark, 64
sea snakes, 261–262 bioactive components, 58–59
turtles, 261 bioassay-guided protein purification, 63
Introduction vector biochemistry, 62
AQC, 131–132, 133f crustacean-targeting immature
BWF and OYS, 130–131 forms, 62
marine, 111t EST resource, 63–64
R2 values, 130–131 evolution, 65
trematodes, 131–132 Irukandji jellyfish venom, toxins, and
Invasion vectors genomics, 59–61, 60t
anthropogenic categories, 93 ISPT, 64
molluscan invasions, Crassostrea virginica, Jellyfish tentacular nematocysts, 64
93–94 lethal paralysis, 63–64
294 Subject Index
Irukandji syndrome-producing toxin (ISPT) species richness, abundance and escape,

(Continued ) 114–118, 119f
medusozoan nematocyst proteomes, 62 stepwise multiple regression, 137
minimal parasympathetic effects, 61 study limitations, 158–160
neuropeptide Y, 61–62 time, introduction, 146–147
pharmacological studies, 62 vector and vector strength, 147–150
preliminary biochemical data, 59
prey capture and digestion, 58 N
types, tentacular nematocysts, 64 Northern Coral Sea, 264f, 265–266
J P
Juvenile acclimation, sea urchin Parasite escape and release
cage design, 195 Carcinus maenas, 151–152
change, weight, 196 collection methodologies and analyses,
food, cages, 196 108
growth rates, sea urchins, 197, 197f community-wide influences, 138
osmolarity, 196 data analysis, 112–113
posthyposalinity treatment wet weights, data sources, 108–109
196 extraction, data, 109–112
reaction, urchins, 197–198 global marine host–parasite systems,
sea water system, 196 152–153
stenohaline, 195 host–parasite geography, 92–93
and host taxa, 95–96
M hypothesis, 90–91
Marine and parasite invasions mechanistic factors
anthropogenic treatment, 157–158 accidental vs. intentional introduction
biological hypothesis, 152–153 vectors, 135–137
biomass, invasive species, 89 data analyses, R2 and p values,
Carcinus maenas, 154–155 118–126, 120t
Charybdis longicollis, 156–157 host–parasite geography, 126
coevolution-structured community, 89 host taxa, 128–129
community dynamics, 88 introduction vectors (see Introduction
Crassostrea gigas, 155 vector)
ecosystem function, 157–158 time, introduction, 126–128
enemy release hypothesis, 90–91 vector strength, 132–135
geography, host–parasite, 144–146 non-native organisms, 152–153
GLM, 137 species richness information, 96–108, 97t
host–parasites proportion, 113–114, 117f time, 94–95
host taxa, 113–114, 114f, 150–151 vector and vector strength, 93–94
hypothesis, 89 Parasite taxa
L. littorea, 156 ‘all parasites’ vs. ‘trematodes only’,
non-native species, 88 143–144
parasite escape and release (see Parasite direct-transmission parasites, 141–142
escape) ecosystem-level, 142–143
parasite taxa (see Parasite taxa) ectoparasites, 141
physical/biological factors, 90 host–parasite systems, 140–141
proportion, parasite taxa, 113–114, 117f parasite diversity, 141
source and recipient community, 89–90 trematodes, 141–142
Subject Index 295
Passive integrated transponder (PIT) hydrometers and refractometers,

detrimental effect, 199 174–175
peristomal membrane, 199 hyposaline and hypersaline environments,
tag identification, 200–201 175–181, 176t
Pelagic fish major ions, sea water, 6t, 173
fisheries, 255–258 ophiuroids, 182
genetic heterogeneity, 254–255 physiological and ecological components,
Makaira indica, 255 193
Thunnus albacares and Thunnus obesus, postmetamorphic and premetamorphic,
254–255 183, 184t
Pelagic fisheries rainfall patterns and tidal fluctuation,
catch, 255–257, 256f 181–182
impacts, 257–258 shallow-water habitats, 181
taxonomic changes, 181
temperature-calibrated conductivity,
R 174–175
Reproduction and life cycle, Irukandji
TEOS-10, 175
breeding grounds, 25–28
Sea surface temperature (SST)
granite islands, 25–28
GPCP data, 230, 233f
hypothesised Carukiidae life cycle,
Gulf of Papua, 232
24, 25f
HadISST 1.1, 234
lifespan and natural mortality, 29–30
SEC. See South Equatorial
metamorphosis induction, 28
Current (SEC)
ontogenetic changes, toxicity, 28–29
South Equatorial Current (SEC)
polyp and young medusa characters,
bifurcation, 229
24, 26t
eastern and western reefs, 269
primary benthic sedentary polyp, 24
Tasman Abyssal basin, 230
sampling, Cairns Region, 24–25
Southern Coral Sea, 267
SST. See Sea surface temperature (SST)
S Stinger management
Salinity tolerance and response, bioindicators, 67–68
echinoderms prediction, 66–67
abundance and distribution, 193 prevention, 68
accurate and precise estimates, 173 treatment, 68–69
aquaculture production, 193
asteroid species, 183–192 T
biogeographic patterns, 182–183 Taxonomy, Irukandji
climate change-induced salinity anatomy, carybdeid, 12, 18f
alterations, 173 ecology and syndrome characteristics,
ecological and physiological 11, 13t
investigations, 174–175 genera, cubozoans, 12, 19t
evolution, techniques and metrics, 173 nematocysts (stinging cells),
experimental studies, tolerance and 17–21, 21f
response, 183–193 species, Australian jellyfish, 11, 17f
‘first law of chemical oceanography’, statoliths, 21–22
174 types, tentacles, 11–12, 18f
homeostatic responses, 173 Thermodynamic Equation Of
hydrographic conditions, 181–182 Seawater—2010 (TEOS-10), 175
296 Subject Index
Trematode Tropical sea

description, 96 coastlines, 215–216
host taxa, 112–113, species diversity, 215–216
114f zooplankton, 240–241
life cycle complexity, 96
parasite escape regression, W
126 Wind effects, 53–54
TAXONOMIC INDEX
Note: Page numbers followed by “f ” indicate figures and “t ” indicate tables.
A A. lincki, 176t
Acanthaster planci, 184t, 268 A. rubens, 176t, 183, 184t, 192
Acromitoides purpurus, 13t A. vulgaris, 176t, 184t, 192
Aegina rosea, 241 Asterina
Aiptasia pulchella, 61–62 A. burtoni, 176t
Aipysurus laevis, 268 A. exigua, 184t
Alatina spp., 13t, 18f, 22–23, 23f, 24, 26t, 28, A. gibbosa, 184t
29, 30, 32f, 33, 36, 37, 40, 41, 42–43, A. phylactica, 184t
46–47, 48–49, 55, 56, 57–58, 68 Astropecten
A. mordens, 6t, 13t, 22–23, 23f, 29, 34, 40, A. articulatus, 176t
42, 48, 52, 59–61, 60t, 75–76 A. hemprichi, 176t
A. moseri, 13t, 22–23, 25–28, 29, 41, 48, A. irregularis, 184t
52, 55, 63, 75–76 A. monacanthus, 176t
A. rainensis, 23f A. polyacanthus phragmorus, 176t, 182
Alosa sapidissima, 97t Aurelia, 43–44
Amphioplus abditus, 184t Austrobilharzia variglandis, 141–142
Amphipholis squamata, 176t, 182, 184t
Amphiura
A. chiajei, 176t, 184t
B
Balaenoptera acutorostrata, 258–260
A. fasciata, 176t, 182
Batillaria, 90–91
A. filiformis, 176t
B. attramentaria, 90–91, 97t, 161
A. florifera, 176t
B. australis, 97t
Anaspis, 65
Beryx, 252–254
Anous
Bipedalia cerinensis, 24
A. minutus, 260
Brama, 252–254
A. stolidus, 260
Anthocidaris crassispina, 184t
Anthracomedusa, 24 C
A. turnbulli, 23–24 Caranx, 252–254
Aphareus, 252–254 Carcharhinus amblyrhynchos, 262–263
A. rutilans, 253t Carcharodon carcharias, 262
Apollonia melanostoma, 97t, 150 Carcinus
Apostichopus C. aestuarii, 97t, 154–155
A. japonicas, 203–204 C. maenas, 91–92, 94–95, 97t, 108–109,
A. japonicus, 184t, 193 146–147, 151–152, 153–155
Aprion, 252–254 Caretta caretta, 261
Aquilonastra burtoni, 176t, 182 Carukia spp., 18f, 22, 35–36, 41–42, 52, 55,
Arbacia 56, 64, 68, 75
A. lixula, 184t, 193 C. barnesi, 5, 6, 6t, 11–12, 13t, 21, 23f, 24,
A. punctulata, 184t 25f, 26t, 28, 29, 35, 36, 38–39, 41–42,
Asterias 45, 52, 57–58, 59–61, 60t, 62, 63–64,
A. amurensis, 97t, 184t 68, 72, 73, 74
A. forbesi, 176t, 184t, 192 C. shinju, 6t, 13t, 21f, 34, 40
297
298 Taxonomic Index
Carybdea, 11, 18f, 22, 29, 48–49, 56, 64, Cyanea capillata, 61–62
73–74 Cyclope neritea, 97t
C. alata, 36, 42–43, 55
C. branchi, 23f D
C. marsupialis, 26t, 28 Dendraster excentricus, 184t
C. mora, 26t, 48–49 Dermochelys coriacea, 261
C. morandinii, 26t, 28 Diaphus danae, 241–242
C. rastonii, 23f, 26t, 29, 48–49
C. sivickisi, 26t
C. xaymacana, 13t, 22, 23f, 26t, 28, E
48–49 Echinarachnius
Catostylus, 13t E. parma, 184t
Centrophorus moluccensis, 253t Echinaster sp., 184t
Cephalopholis argus, 97t, 268 E. sentus, 176t
Ceratoscopelus warmingii, 241–242 Echinocardium
Cereithidea californica, 161 E. cordatum, 176t, 184t
Cerithidea, 90–91 Echinocyamus pusillus, 176t
C. californica, 90–91 Echinodermata, 172
Charybdis longicollis, 97t, 153–154, 156–157, Echinodiscus auritus, 176t
159 Echinoidea, 172
Chelonia mydas, 261 Echinometra
Chirodectes maculatus, 23f E. lucunter, 176t, 184t
Chironex, 35–36, 48–49, 64 E. lucuntur, 193
C. fleckeri, 6t, 23f, 26t, 28, 35, 43, 56, E. mathaei, 176t
59–62, 63 Ensis americanus, 97t
Chiropsalmus sp., 35 Epinephelus, 252–254
C. quadrumanus, 23f E. amblycephalus, 253t
Chiropsella E. chlorostigma, 253t
C. bart, 23f E. cyanopodus, 253t
C. bronzie, 23f, 35 E. ergastularius, 252–254
Chrysaora quinquecirrha, 37–38 E. magniscuttis, 253t
Clypeaster humilis, 176t E. morrhua, 253t
Copula, 49 E. septemfasciatus, 253t
C. sivickisi, 23f, 26t, 49 Eretmochelys imbricata, 261
Crassostrea Etelis, 252–254
C. gigas, 97t, 108–109, 143–144, 151, E. carbunculus, 253t, 254
153–154, 155 E. coruscans, 253t, 254
C. virginica, 93–94 Eupentacta
Crepidula fornicata, 97t E. fraudatrix, 184t
Crinoidea, 172 E. quinquesemita, 176t, 184t
Crocosphaera watsonii, 239 Evasterias troscheli, 176t
Crossaster papposus, 176t, 184t Evechinus chloroticus, 184t
Cryptasterina sp., 184t
Cucumaria F
C. frondosa, 184t Fistularia commersonii, 97t
C. kirschbergii, 176t Fregata
C. miniata, 176t, 184t F. ariel, 260
C. vega, 176t F. minor, 260
Taxonomic Index 299
G Lethrinus
Galeocerdo cuvier, 262 L. miniatus, 253t
Gempylidae, 252–254 L. olivaceus, 253t
Gerongia, 18f, 22, 52, 56 Libitum, 195
G. rifkinae, 6t, 13t, 23f Linckia
Globicephala macrorhynchus, 260 L. laevigata, 268
Gonionemus L. multifora, 176t
G. oshoro, 13t, 29, 37–38 Lipocheilus, 252–254
G. vertens, 13t, 37–38 Liriope, 67
Gymnosarda, 252–254 Littorina
L. littorea, 97t, 108–109, 153–154, 156
H L. obtusata, 156
Halimeda, 245–247 L. saxatilis, 97t, 156
Haminoea japonica, 97t Lobonema smithii, 13t, 37–38
Haplosporidium nelsoni, 155 Luidia
Heliocidaris crassispina, 184t, 193 L. clathrata, 176t
Hemigrapsus sanguineus, 94–95, 97t L. maculata, 176t
Henricia sanguinolenta, 184t Luidia clathrata, 184t
Heptranchias perlo, 253t Lutjanus spp., 150
Holothuria L. bohar, 253t
H. leucospilota, 176t L. fulvus, 97t
H. spinifera, 184t, 193 L. kasmira, 97t
Holothuroidea, 172 L. malabaricus, 253t
Hydra magnipapillata, 62 Lytechinus variegatus, 176t, 184t,
Hydrolagus sp., 253t 193, 204
Hydrophis laboutei, 261
Hyperoglyphe antarctica, 252–254 M
Hyporthodus, 252–254 Makaira
H. octofasciatus, 254 M. indica, 255
M. mazara, 254–255
I Malo sp., 13t, 18f, 22, 33, 37–38, 39, 40–41,
Ilyanassa obsoleta, 93–94, 97t, 141–142 46–47, 52, 55, 56, 61–62, 68
Isostichopus badionotus, 184t, 193 M. kingi, 6t, 11–12, 13t, 21f, 23f, 34, 36,
Isurus oxyrhynchus, 262 60t, 63–64
M. maxima, 6t, 13t, 21f, 23f, 34, 40, 57,
K 59–61, 60t, 68
Kajikia audax, 254–255 M. philippina, 13t
Kogia breviceps, 260 Marthasterias glacialis, 176t
Megaptera novaeangliae, 258–260
L Mellita
Laticauda saintgironsi, 261 M. isometra, 184t
Lepidochelys olivacea, 261 M. quinquiesperforata, 176t
Leptasterias Metacarcinus novaezelandiae, 97t
L. hexactis, 176t, 184t, 194 Mnemiopsis leidyi, 97t
L. polaris, 176t Morbakka sp., 4, 13t, 18f, 22, 37–38, 39,
Leptosynapta 40–41, 46–47, 52, 56, 68
L. chela, 176t, 182 M. fenneri, 6t, 13t, 23f
L. inhaerens, 176t M. virulenta, 13t, 40–41
300 Taxonomic Index
Musculista senhousia, 97t P. pseudoexigua, 184t

Mya arenaria, 97t P. regularis, 176t, 181–182, 184t
Pegantha spp., 241
N Phaethon rubricauda, 260
Natator depressus, 261 Physalia spp., 13t, 64
Nautilus spp., 263 P. physalis, 61–62
N. pompilius, 263 Physeter macrocephalus, 258–260
Nematostella vectensis, 63 Pisaster ochraceus, 184t
Nemopilema nomurai, 13t, 37–38 Poecilia latipinna, 97t
Neogobius melanostomus, 97t Polyipnus, 242
Nudechinus scotiopremnus, 176t Polyprion oxygeneios, 252–254
Prionace glauca, 262
O Pristipomoides, 252–254
Odontaster validus, 184t P. filamentosus, 253t, 254
Oestergrenia digitata, 176t P. flavipinnis, 253t
Olindias sambaquiensis, 62, 63 P. multidens, 253t
Onychoprion fuscata, 260 Prochlorococcus spp., 239
Ophiocomina nigra, 184t, 193 Psammechinus miliaris, 176t, 184t
Ophiocten sp., 176t Pseudorca crassidens, 260
O. sericeum, 176t Puffinus pacificus, 260
Ophioderma
O. brevispina, 176t, 184t R
O. brevispinum, 184t Rhincodon typus, 262
Ophiolepis elegans, 176t Ruditapes philippinarum, 97t
Ophiopholis aculeata, 176t Ruvettus, 252–254
Ophiophragmus filograneus, 176t, 184t
Ophiothrix S
O. angulata, 176t, 184t Sacculina spp., 151–152
O. fragilis, 176t Saloptia, 252–254
O. savignyi, 176t Sargocentron spiniferum, 253t
Ophiura Scaphechinus mirabilis, 184t
O. albida, 176t, 184t Sclerodactyla briareus, 176t, 184t, 192
O. ophiura, 176t Scomberomorus commerson, 268
O. robusta, 176t Seriola, 252–254
O. texturata, 176t S. rivoliana, 253t
Ophiuroidea, 172 Siganus rivulatus, 97t
Ostracoblabe implexa, 155 Silene latifolia, 90–91
Solaster papposus, 176t, 184t
P Solmundella bitentaculata, 241
Panulirus ornatus, 265 Stegophiura nodosa, 176t
Paracaesio, 252–254 Sterechinus neumayeri, 184t
P. kusakarii, 254 Stereoderma kirchsbergii, 176t
Paracarybdea lithographica, 24 Sternula nereis exsul, 260
Paralithodes camtschaticus, 97t Strongylocentrotus
Parechinus angulosus, 184t S. droebachiensis, 176t, 184t, 193,
Patiria pectinifera, 184t 194, 204
Patiriella S. intermedius, 184t
P. exigua, 184t S. pallidus, 184t
P. mortenseni, 184t S. purpuratus, 184t, 203, 204
Taxonomic Index 301
Sula Tridacna tevoroa, 244

S. leucogaster, 260 Tripedalia, 31–32, 49
S. sula, 260 T. cystophora, 23f, 26t, 49
Synapta hispida, 176t Tropiometra carinata, 184t, 192
Synaptula reciprocans, 176t
Synechococcus spp., 239 U
Urasterias lincki, 176t, 182–183
T
Tamoya, 11–12
Taractichthys, 252–254
V
Vibrio spp., 155
Temnopleurus toreumaticus, 176t
Thunnus
T. alalunga, 254–255 W
T. albacares, 254–255 Wattsia, 252–254
T. obesus, 254–255 W. mossambica, 253t
Thyone briareus, 184t, 192
Triaenodon obesus, 268 X
Trichodesmium, 236–238, 239 Xiphias gladius, 254–255

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Biology and Ecology of Irukandji

Advances in Marine Biology, Volume 66 # 2013 Elsevier Ltd 1

Keywords: Irukandji syndrome, Marine stingers, Envenomation, Jellyfish

World Health Organization failed to recognise the hazard in their 2003

1.1. History of study

Table 1.1 Timeline of the history of Irukandji research—cont'd

Table 1.1 Timeline of the history of Irukandji research—cont'd

Table 1.1 Timeline of the history of Irukandji research—cont'd

Cumulative number of marine papers

appears to be unique to the Carukiidae, though not all species have it

2.2.2 Fossil evidence

2.3. Reproduction and life cycle

2.3.1 Where do they breed?

collection data appear to falsify this hypothesis, at least in part. Sampling in

2.3.2 Metamorphosis induction

2.3.3 Ontogenetic changes in toxicity

In one recent study, gel electrophoresis of specimens pooled into imma-

2.3.4 Lifespan and natural mortality

Statolith studies on other species demonstrate the presence of daily

2.4. Eyes and vision