Dispersal Foraminifera

MA04CH10-Gooday ARI 12 November 2011 11:51
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in Deep-Water Settings
Andrew J. Gooday1 and Frans J. Jorissen2
by University of Bristol on 09/13/12. For personal use only.
1
National Oceanography Centre, University of Southampton, Southampton SO14 3ZH,
United Kingdom; email: ang@noc.ac.uk
2
Laboratory of Recent and Fossil Bio-Indicators, University of Angers 2, 49045 Angers Cedex,
France; Laboratoire d’Etude des Bio-Indicateurs Marins, Ker Chalon, 85350 Ile D’Yeu, France;
email: frans.jorissen@univ-angers.fr
Annu. Rev. Mar. Sci. 2012. 4:237–62 Keywords

First published online as a Review in Advance on protist, abyssal, bathyal, biodiversity, endemic, cosmopolitan
September 19, 2011
The Annual Review of Marine Science is online at Abstract

marine.annualreviews.org
Benthic foraminifera, shell-bearing protists, are familiar from geologi-
This article’s doi: cal studies. Although many species are well known, undescribed single-
10.1146/annurev-marine-120709-142737
chambered forms are common in the deep sea. Coastal and sublittoral species
Copyright c 2012 by Annual Reviews. often have restricted distributions, but wide ranges are more frequent among
All rights reserved
deep-water species, particularly at abyssal depths. This probably reflects the
1941-1405/12/0115-0237$20.00 transport of tiny propagules by currents across ocean basins that present few
insurmountable barriers to dispersal, combined with slow rates of evolution.
Undersampling of the vast deep-sea habitat, however, makes it very difficult
to establish the ranges of less common foraminiferal species, and endemism
may be more prevalent than currently realized. On continental slopes, some
species have restricted distributions, but wide-ranging bathyal species that
exhibit considerable morphological variation are more common. This may
be linked to the greater heterogeneity of continental slopes compared with
oceans basins. Improved knowledge of deep-sea foraminiferal biogeogra-
phy requires sound morphology-based taxonomy combined with molecular
genetic studies.
237
1. INTRODUCTION
Foraminifera, heterotrophic protists classified within the protistan supergroup Rhizaria (Adl et al.
2005), are ubiquitous organisms in marine (Murray 2006) as well as freshwater (Holzmann &
Pawlowski 2002) and terrestrial (Lejzerowicz et al. 2010) environments. Although some marine
species are important constituents of the plankton, most are benthic. Foraminifera have an out-
standing fossil record, and much of the research on them has been conducted by geologists who
have described most of the known species. Estimates of the number of extant species range from
∼4,100 (Murray 2007) to 10,000–12,000 (Boltovskoy & Wright 1976). Many of the described
benthic species have robust shells (“tests”) composed of calcareous material and fossilize readily.
Others have agglutinated tests composed of mineral or biogenic particles acquired from the sur-
rounding sediment and are less likely to fossilize. In addition to these well-known taxa, recent
studies have revealed a profusion of species with flexible, single-chambered (monothalamous)
tests composed of organic or agglutinated material and having very little fossilization potential
(Gooday 2002, Habura et al. 2008). In contrast to the hard-shelled species, these soft-shelled
monothalamous foraminifera are poorly known and largely undescribed.
Because of their importance in reconstructing ancient marine environments, an enormous
literature exists on the relationship between modern foraminiferal species and environmental
parameters. However, their use as paleoenvironmental proxies is hampered by the complexity of
these distributional controls (Murray 2001, Gooday 2003, Jorissen et al. 2007). In deep water, the
organic matter flux to the seafloor is believed to exert a particularly strong influence on benthic
foraminiferal ecology. Altenbach et al. (1999) plotted the percentage abundance of some key
deep-sea species in samples from the Guinea Basin to the Arctic Ocean against flux estimates.
All species were abundant only within certain limits, but they also occurred at lower densities
across a wide range of flux values. Thus, species that are considered typical of high productivity
areas were also found in oligotrophic regions, and vice versa. As Mackensen et al. (1995) remark,
“apparently similar assemblages correspond to very different environmental conditions in different
ocean basins.” This represents a major obstacle for the development of transfer functions, aiming
to quantitatively reconstruct single environmental parameters on the basis of faunal composition.
A comprehensive treatment of the mass of conflicting information regarding ecological controls
on the distribution of modern benthic foraminiferal species is beyond the scope of this short review.
Instead, we focus on the distribution and ecology of some key species from different environmental
settings, incorporating molecular evidence when available. The study of foraminifera straddles
biology and geology. In addition to being important proxies in paleoecological studies, their
high density and diversity in various settings make foraminifera ideally suited to address broader
questions concerning the distribution of marine species (Buzas & Culver 1989). Among these is
the contentious issue of whether or not protists and small-sized animals exhibit biogeographic
patterns. One school of thought maintains that small organisms have ubiquitous distributions and
occur around the globe wherever the environmental conditions are suitable (e.g., Finlay & Fenchel
2004). Another view is that some species are cosmopolitan but others exhibit distinct biogeographic
patterns that are not dependent on the existence of suitable habitats (the moderate endemicity
model) ( Jenkins et al. 2007, Foissner 2008). Many foraminifera fall within the transition zone
(0.1 to 10 mm) between large and small organisms where distributions switch from ubiquitous to
restricted, according to Finlay & Fenchel (2004). Their patterns of distribution are therefore of
particular interest in the context of this debate (Gooday 1999).
With these considerations in mind, we address the following questions:
1. Are there “typical” patterns of geographical distribution among deep-water foraminiferal

species, and do they differ from those of foraminifera in shelf settings?
238 Gooday · Jorissen

2. What are the main factors influencing these distribution patterns, and do they differ in
different settings (continental margins, ocean basins, hypoxic habitats)?
3. What is the degree of connectivity between populations in different regions and habitats?
Morphospecies: a
4. Are widely distributed foraminiferal morphospecies genetically coherent, or do they conceal species defined on the
genetically distinct but morphologically very similar cryptic species? basis of morphological
5. To what extent does imperfect taxonomy obscure biogeographic patterns? features; almost all
foraminiferal
We return to these questions in the Summary Points at the end of this review. Although our morphospecies are
main focus is on modern deep-water foraminifera, for comparative purposes we also touch on the characterized by
distribution of those living in shelf and coastal settings. features of their shells
Cryptic species:
a morphospecies
2. PROBLEMS IN DETERMINING DISTRIBUTION PATTERNS containing populations
that are different
Many marine foraminifera are well known and widely reported, and their distributions are appar-
genetically, but very

ently well established (Murray 1991). However, the description of the same species under different similar
names is a recurrent problem (Boltovskoy 1965); Murray (2007) estimates that 10% to 25% of morphologically
modern species are synonyms. The opposite tendency, lumping different species under one name, Abyssal seafloor:
also hampers the study of geographical ranges, especially in the case of agglutinated taxa. Some deep seafloor situated
between 3,500 m and
species names established early in the history of foraminiferal taxonomy have been applied to 6,500 m water depth,
morphotypes rather than to single species. For example, published images of Reophax scorpiurus much of it constituting
de Montfort 1808, a species reported from coastal to abyssal sites around the world, show a wide the abyssal plains
range of test morphologies that must encompass a variety of different biological species. Another Deep sea: the ocean
concern is the existence of cryptic speciation among “species” in which the test morphology is floor beyond the edge
fairly consistent (Tsuchiya et al. 2003, Hayward et al. 2004, Pawlowski et al. 2008). Although of the continental shelf
most hard-shelled species have been described, a large proportion of monothalamous taxa remain (the shelf break),
generally located at a
undescribed (Habura et al. 2008), particularly in the deep sea where many species are rare and depth of 200–300 m
have been recorded at only one site. The minute proportion [McClain (2007) gives a “very high
Endemic species: a
estimate” of 0.5%] of this vast habitat that has ever been sampled makes it impossible to dis- species that is confined
tinguish genuinely endemic species distributions from restricted occurrences that are artifacts of to a particular
undersampling (Gooday et al. 2004, McClain & Mincks Hardy 2010, Tittensor et al. 2010). geographical area
Spatial and temporal patchiness create additional problems (Sen Gupta & Smith 2010). Sig-
nificant small-scale spatial variability occurs at decametric to decimetric scales (e.g., Griveaud
et al. 2010), perhaps reflecting concentrations of labile organic matter and highly localized niches
around macrofaunal burrows. Seasonal and interannual studies (Ohga & Kitazato 1997, Fontanier
et al. 2006, Langezaal et al. 2006, Gooday et al. 2010b) reveal a similar degree of faunal variability
over time, partly attributable to inputs of labile organic matter that trigger bursts of reproduc-
tion in opportunistic species. Because most distributional studies are based on single samples, this
temporal and spatial variability can strongly influence distributional pattern. Examination of dead
(hard-shelled) tests, which represent a time-integrated view of the fauna at a particular locality,
can help to alleviate this problem, as long as they have not been subject to significant postmortem
transport.
3. DISPERSAL IN FORAMINIFERA
The geographical ranges of species are related, at least in some taxa, to their dispersal ability
(Gaston 2003). Information on dispersal in marine organisms is limited and biased toward low-
dispersing metazoan species in low-latitude settings (Bradbury et al. 2008). Analyses of proxies for
dispersal (e.g., genetic differentiation and duration of planktonic larval stages) suggest that marine
www.annualreviews.org • Benthic Foraminiferal Biogeography 239

metazoans exhibit a wide range of dispersive capabilities (Bradbury et al. 2008), although these
are not necessarily linked to species ranges (e.g., Emlet 1995).
Dispersal mechanisms in benthic foraminifera are reviewed by Alve (1999) and Murray (2006).
The active movement of free-living species across the seafloor is too slow to account for wide-scale
dispersal. Likewise, planktonic life stages, although a potentially efficient means of transport, are
reported in only a few species. Most species, therefore, are probably passively entrained into the
water column and transported by currents, either as adults or juveniles or as tiny propagules. Small
adult and juvenile benthic foraminiferal tests have been caught in plankton-net and sediment-trap
samples obtained well above the seafloor (Alve 1999, Brunner & Biscaye 2003, Murray 2006). In a
series of elegant experiments, Alve & Goldstein (2010; also see their earlier papers) convincingly
demonstrated the transport of propagules small enough to pass through a 32-μm mesh sieve. Large
numbers of foraminifera belonging to coastal benthic species appeared and grew when the 32-μm
fractions of sediments collected at 320-m water depth were exposed to simulated shallow-water
conditions in sealed containers on a window ledge. Similar results were obtained using sediment
that had been kept in a dark cold-room for two years, suggesting that propagules can remain viable
for at least this period. If foraminiferal propagules have characteristics similar to those of metazoan
larvae (Bradbury et al. 2008), they are likely to survive longer at low temperatures, enhancing their
potential for wide dispersal in the deep sea.

On geological timescales, benthic foraminifera seem to disperse instantaneously (Buzas &
Culver 1991). Mediterranean sapropels provide good evidence of their rapid dispersal. These
recurrent anoxic events have repeatedly wiped out benthic faunas across the entire eastern
Mediterranean, at least below water depths of 500 to 1,000 m ( Jorissen 1999). Each lasted
for several thousands of years, after which the seafloor was rapidly repopulated by benthic
foraminifera. These species must have either persisted in shallow-water refugia in the eastern
Mediterranean or migrated from the western Mediterranean after reoxygenation of the water
column. Although recolonization was apparently very rapid (several decades to a few centuries
at most), it seems to have taken several millennia to fully restore biodiversity, suggesting that
recolonization may be considerably slower for some taxa (Schmiedl et al. 2003).
In addition to natural mechanisms, species can be transported long distances in the ballast
tanks of ships (Radziejewska et al. 2006). This mechanism may explain the disjunct distribution
of one phylotype of the coastal genus Ammonia (Pawlowski & Holzmann 2008), the Japanese
species Trochammina hadai in San Francisco Bay (McGann & Sloan, 1996), and the European
and North American species Haynesina germanica in an Argentinean estuary (Calvo-Marcilese &
Langer 2010).
4. ENVIRONMENTAL PARAMETERS INFLUENCING

FORAMINIFERAL ASSEMBLAGES
Murray (2006) identified salinity, temperature, oxygen, tides and currents, substrate and food sup-
ply, as well as competition and predation, as important factors influencing foraminiferal assem-
blages (also see sidebar, Benthic Foraminifera as Paleoceanographic and Paleoecological Indica-
tors). Additional factors on the shelf include coverage of the seafloor by seagrasses and macroalgae
(e.g., Mateu-Vicens et al. 2010) and light penetration, the latter being crucial for symbiont-bearing
species. Salinity plays a role mainly in marginal marine areas subject to freshwater discharges (e.g.,
Baltic Sea, Black Sea) or to strong evaporation (e.g., Dead Sea, Red Sea). Although temperature is
an important factor in coastal environments (Culver & Buzas 1999), it is relatively uniform in most
parts of the deep sea and therefore probably not a major parameter for foraminifera, at least in
modern oceans. Currents and particularly tides also mainly operate in shallow water, but elevated

BENTHIC FORAMINIFERA AS PALEOCEANOGRAPHIC

AND PALEOECOLOGICAL INDICATORS
Foraminifera are by far the most abundant and widely distributed benthic organisms preserved in the fossil record
and are used widely to reconstruct conditions on ancient ocean floors (paleoceanography) as well as in near-shore
settings (paleoecology). Faunal characteristics (abundance, diversity, taxonomic composition) have been used to
infer, e.g., the food flux to the seafloor (and hence surface primary productivity), bottom-water oxygenation, current
activity, and the depth of the carbonate compensation depth. This approach depends on an accurate knowledge of
the distribution of species in relation to environmental parameters in modern oceans. Another approach depends
on the chemical composition (stable isotope and elemental ratios) of foraminiferal carbonate shells. For instance,
the Mg/Ca ratio is used to reconstruct temperature, and stable carbon isotope ratios reflect the organic-matter
flux to the seafloor and ocean circulation. Once temperature is known, oxygen isotopes can be used to estimate
paleosalinity. In coastal settings, foraminifera have been used to reconstruct past sea levels. Efforts have been made
to develop quantitative proxies (transfer functions) for environmental variables on the basis of benthic foraminifera,
but these are often fraught with difficulties. In recent years, benthic foraminifera have been used increasingly to
monitor the impact of anthropogenic activities in marine ecosystems.
flows are encountered in some deep-sea areas, where they are associated with distinctive epifau-
nal assemblages (e.g., Schönfeld 1997). Sessile foraminiferal species depend on the availability of
firm attachment surfaces. In the predominantly sediment-covered deep ocean, suitable substrates
include rocky outcrops, glacial drop stones, manganese nodules, biogenic structures, and larger
sessile or even mobile animals. Carbonate dissolution is a major limiting factor for deep-sea calcare-
ous foraminifera. Below the carbonate compensation depth, calcareous species disappear almost
entirely and foraminiferal assemblages are composed of agglutinated and organic-walled forms
(Saidova 1965). In areas such as oxygen minimum zones (OMZs), low bottom-water dissolved
oxygen (DO) concentrations eliminate hypoxia-sensitive species, leading to the formation of low-
diversity, high-dominance faunas. However, DO is limiting only when concentrations decline to
low levels (∼0.5 ml per liter or less), at least where hypoxia is permanent, as in OMZs (Levin 2003).
In addition to these physical and chemical parameters, recent literature has placed considerable
emphasis on food inputs derived from surface primary production as a major influence on the
structure and functioning of deep-sea communities in general (Smith et al. 2008), as well as on
foraminiferal assemblage composition (e.g., Altenbach et al. 1999, Gooday 2003, Jorissen et al.
2007), diversity (Wollenburg & Mackensen 1998), and faunal patterns with water depth (De
Rijk et al. 2000). Distinctive assemblages are also associated with regions that have a pronounced
seasonality in the organic-matter flux to the seafloor (Loubere & Fariduddin 1999, Sun et al. 2006).
5. GEOGRAPHICAL DISTRIBUTIONS OF (MORPHO)SPECIES

IN DIFFERENT HABITATS
5.1. Continental Shelf and Slope

Analyses of large data sets suggest that many foraminiferal species have restricted ranges on
continental margins. Distributions around the North American continent (intertidal to abyssal
depths) have been examined in detail by Stephen Culver and Martin Buzas in a series of publications
(e.g., Buzas & Culver 1991, Culver & Buzas 1998) based on literature sources combined with an
extensive reexamination of museum material. Within this region, the majority (57%) of the 2,329

species recognized were endemic, in the sense of being confined to one of five regions (Caribbean,
Gulf of Mexico, Atlantic, Arctic, and Pacific); only 5% occurred in all regions. However, the
majority of endemic species were rare. Similarly, Murray (2007) concluded that a high proportion
(83%–90%) of species from marshes, lagoons/estuaries, and shelf seas were restricted to one or
two of the six areas spanning either the three major oceans (marshes, lagoons/estuaries) or the
eastern and western margins of the Atlantic Ocean (shelf seas). Mikhalevich (2004) estimates that
as many as 80% of shallow-shelf (2–50 m) foraminiferal species around the Antarctic continent
are endemic.
A different view emerges from a comprehensive survey of foraminifera in the Gulf of Mexico
(Sen Gupta & Smith 2010). This may reflect differences in the scale at which endemism and
ubiquity were evaluated, either around the North American continent (Buzas & Culver 1991,
Culver & Buzas 1998) or globally (Sen Gupta & Smith 2010). Only 4% of the 987 species reported
from the Gulf of Mexico (0–3,850 m) are endemic to this region. Of the 557 species confined to
depths <1,000 m, 29% are cosmopolitan (occurring in the three major oceans or in both polar
oceans and two of the three major oceans), compared with 35% of the 48 species from depths
>1,000 m and 47% of the 360 species that straddle this boundary. Evidence for wide species
distributions in the Gulf of Mexico also comes from a study of benthic foraminifera associated
with hydrocarbon seeps, an important source of heterogeneity on this margin. Lobegeier & Sen
Gupta (2008) recognized 183 species in 23 seep samples and 5 nonseep control samples (depth
range 245–2,918 m). Although no species was endemic to the seep habitats, some (e.g., Bolivina
spp.) were concentrated in seep samples, whereas others (Saccorhiza ramosa, Eponides turgidus,
Nuttallides decorata) were more or less confined to nonseep samples. Other seep sites, notably
in Monterey Bay, California, are also reported to lack endemic species (Bernhard et al. 2001,
Rathburn et al. 2003). Data from around New Zealand (0–5,000 m), compiled by Hayward et al.
(2011), suggest that cosmopolitan distributions are more prevalent (69%) at depths >100 m than
at shallower sites (55%).
5.1.1. Species with wide distributions. Uvigerina peregrina, a species reported from all ocean
basins (Table 1), encompasses a plexus of morphotypes, mainly differing in their length-width
ratio and test ornamentation, which varies from entirely costate to entirely spinose. Two different
taxonomic concepts have been applied to this plexus. Some authors proposed new species names
for different morphotypes, whereas the existence of many intermediate specimens has led others
to apply the name U. peregrina to the entire plexus; in the latter case the various morphotypes are
distinguished at a subspecies, variety, or informal level. Lutze (1986) distinguished six morphotypes
within this complex on the basis of hundreds of samples from the eastern Atlantic continental slope
(10◦ –50◦ N). Typical U. peregrina, characterized by very sharp costae and no intervening spines,
was found between 900-m and 2,000-m depth. In deeper water, U. peregrina was progressively
replaced by a morphotype with spines between the costae, and often an entirely spinose last
chamber (Uvigerina hollicki ). Below 3,000 m, completely spinose morphotypes, mostly identified
(e.g., Van Leeuwen, 1986) as Uvigerina hispida, became increasingly dominant. Toward shallower
water, the serrate costae of U. peregrina started to break up into irregular rows of spines. Uvigerina
parva, which is smaller than typical U. peregrina, occurred between 300-m and 1,100-m depths.
Lutze (1986) found two other morphotypes on the upper slope off northeast Africa. Uvigerina
bifurcata (300–450 m depth) has an elongated test with regular costae, whereas Uvigerina sp. 221
( = Uvigerina celtica; Schönfeld 2006) resembles U. bifurcata but has numerous small spines between
the costae. Lutze (1986) found it between 100-m and 300-m depths.
Lutze (1986) described a complete bathymetric succession of these Uvigerina morphotypes
between 10◦ N and 20◦ N in the eastern North Atlantic (Figure 1). Further north, U. hollicki and

1,000
"celtica"
"parva"
"bifurcata”
Water depth (m)
2,000
Sample location map
25° N
"peregrina”
Atlantic Ocean
3,000
20° N Africa
"hollicki”
15° N Dakar
4,000 Collection
10° N area
"hispida"
5° N
30° W 20° W 10° W
Figure 1
Bathymetric distribution (red lines) of Uvigerina morphotypes on the east Atlantic margin, 10◦ –20◦ N. The
species names applied by some authors to these forms are given within quotation marks because there is no
evidence that they represent distinct species. The map shows the area off northwest Africa within which
these morphotypes form a bathymetric succession.
U. bifurcata disappear, whereas others persist (Schönfeld, 2006). Unfortunately, only one genetic
study partially elucidates the biological status of these various forms. Schweizer et al. (2005)
studied small-subunit ribosomal DNA (SSU rDNA) sequences of U. peregrina from the Skagerrak.
The divergence between the four recognized morphotypes, which belonged to U. hollicki and/or
U. celtica, was rather minimal, leading to the conclusion that, despite substantial morphological
variability, the Uvigerina assemblages from the Skagerrak were genetically homogenous. Further
genetic studies are needed to understand the relationships between the various morphotypes within
the U. peregrina plexus.
The huge morphological variability encompassed by U. peregrina appears to be exceptional,
although this may reflect the popularity of this very common species. Some other cosmopolitan
taxa, such as the Gyroidina orbicularis/neosoldanii, Melonis barleeanum/zaandami, and Globobulimina
affinis/pyrula groups as well as the biconvex Cibicoides (including C. pseudungerianus) (Table 1), also
show substantial morphological variability, which has yet to be examined genetically. In contrast,
bathyal species with a wide geographical distribution and a consistent morphology appear to
Bathyal seafloor:
be uncommon. Hoeglundina elegans is probably the best example (Table 1), although other less deep seafloor situated
frequent but widely distributed taxa also have stable morphologies. Amphicoryna scalaris and several between 300-m and
miliolids (Pyrgo subsphaerica, Pyrgo depressa, Sigmoilopsis schlumbergeri ) are good examples. 3,500-m water depths;
In summary, it appears that most common bathyal species with wide geographical ranges are typically coinciding
with the continental
characterized by substantial morphological variability. The number of genetic studies investigating
slope and continental
these morphological complexes is still very limited, and at present, there is no positive evidence rise
that the various morphotypes represent different biological species.

MA04CH10-Gooday
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244
Table 1 Distribution of selected benthic foraminifera in different oceans∗
Atlantic Ocean Indian Ocean Pacific Ocean Mediterranean
Gooday
Gulf of Red Southern Arctic
·
North South Mexico North South Sea North South Ocean Ocean West Easta
12 November 2011
Agglutinated species
Jorissen
Cribrostomoides subglobosa 19, 26, 29, 34 22, 33 23 19 19 12, 13, 15 19, 41 14, 3, 11, 12
39 36
11:51
Cyclammina cancellata 8, 25 8 8, 29, 34 33 7 2, 17 6, 13,15 36 3

Eggerella bradyi 32, 39 31 29 22, 33 4, 27 7, 9, 16, 12, 17 6, 15 10
32
Hormosina globulifera 2, 8 2 29 22 7, 9, 16 2, 12 12, 13, 15 36
Hyperammina subnodosa 2, 8 2 2 2, 12 17 8 8, 40 36 3
Rhabdammina abyssorum 2, 8 2 8 2 7, 9, 16 2, 12 2, 12, 15 2, 12 36
Reophax dentaliniformis 25 34 33 16 17 15 14
Spiroplectammina biformis 8 16 2, 17 10, 13 12, 40,
41
Calcareous species
Cassidulina 2, 25, 26 2, 31 28 22, 33 27 2, 30 2, 38 2, 17 2, 13 2, 12 35 3, 20
laevigata/carinatab
Chilostomella oolina 2, 5, 25 31 29 22, 33 2, 38 2, 17 14
Cibicidoides pseudungerianus 39 31 29 17 15 3, 36 3, 20
Cibicidoides wuellerstorfi 26 24, 31 29 33 4, 27 30 7, 9, 16 12 12, 15 12, 18, 21
40, 41
Epistominella exigua 12, 25, 31 12 22, 33 4, 27 12 12, 17 6, 13 40, 41 11
26
Globobulimina affinis 5 29 22 17 1c
Globocassidulina subglobosa 2, 39 24, 31 34 33 4, 27 30 2 2, 6, 13, 36 3, 20
15
Gyroidina 2 29 22, 33 4, 27 2, 30 2 2, 15 14 3, 20
orbicularis/neosoldaniib
MA04CH10-Gooday
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Hoeglundina elegans 12, 25, 24, 31 12 22 4, 27 7, 9, 38 2, 12, 15 14, 3, 12, 20

39 36
12 November 2011
Laticarinata pauperata 25 29 27 7, 9, 16 17 12, 15

Melonis 5, 25, 31 29 22, 33 4, 27 18 12 18, 40, 14, 3, 11, 12
barleeanum/zaandamaeb 26, 39 41 36
11:51
Nuttallides umbonifera 5, 12 24, 31 4, 27 16 12 13 12

Oridorsalis umbonatus 25, 26 24, 31 12 33 27 7, 9, 16, 12 12 18 36 20
38
Oridorsalis tenera 5 24 29 4 17 12, 13 12, 18,
40, 41
Pyrgo murrhina 2, 5 31 29 22 4 9 2, 17 12, 13, 15 36 12, 20
Uvigerina peregrina 25, 26, 24, 31 29 22, 33 27 30 38 17 37d 41 14 20
39
∗
The literature records are selective and have not been verified. Numbers in columns indicate references, which correspond to the following citations: 1. Avşar (2010), 2. Brady (1884),
3. Cimerman & Langer (1991), 4. Corliss (1979), 5. Corliss (1991), 6. Cornelius & Gooday (2004), 7. Cushman (1910), 8. Cushman (1918), 9. Cushman (1921), 10. Cushman (1922), 11. De
Stigter (1996), 12. Douglas & Woodruff (1981), 13. Echols (1971), 14. Fontanier et al. (2008), 15. Herb (1971), 16. Hess & Kuhnt (1996), 17. Ingle et al. (1980), 18. Ishman & Foley (1996),
19. Jones et al. (1993), 20. Jorissen (1987), 21. Jorissen et al. (1993), 22. Kurbjeweit et al. (2000), 23. Lindenberg & Auras (1984), 24. Lohmann (1978), 25. Lutze (1980), 26. Mackensen et al.
(1985), 27. Peterson (1984), 28. Phleger (1951), 29. Pflumm & Frerichs 1976, 30. Said (1950), 31. Schmiedl et al. (1997), 32. Schröder et al. (1988), 33. Schumacher et al. (2007), 34. Sen Gupta
& Smith (2010), 35. Sgarrella et al. (1983), 36. Sgarrella & Montcharmont Zei (1993), 37. Theyer (1971), 38. Walton (1955), 39. Weston (1985), 40. Wollenburg & Mackensen (1998),
41. Wollenburg & Mackensen (2009).
a
Including the Adriatic Sea.
b
Species considered to be synonyms.
c
Sea of Marmara.
d
Uvigerina peregrina dirupta.
www.annualreviews.org • Benthic Foraminiferal Biogeography

245
5.1.2. Species with restricted distributions. As indicated above, there is conflicting evidence
regarding the distribution of foraminiferal species on continental margins (Buzas & Culver 1991,
Culver & Buzas 1998, Sen Gupta & Smith 2010). However, there do appear to be relatively
few common species with restricted distributions living on bathyal continental slopes not subject
to oxygen minima. One example is Uvigerina mediterranea, which strongly dominates Mediter-
ranean faunas (>125-μm size fraction) and occurs in the eastern Atlantic between 15◦ N and 50◦
N (Lutze 1986), but apparently not in the western Atlantic or in other ocean basins. Planulina
ariminensis appears to have a very similar distribution, whereas Uvigerina elongatastriata is found
exclusively in the eastern Atlantic. The deep-water miliolid Articulina tubulosa is known only from
the eastern Mediterranean, where it has adapted to the extremely oligotrophic conditions of the
deep Levantine Basin. These endemic species, restricted to the Mediterranean and east Atlantic,
support the concept of the Mediterranean as a hot spot for benthic foraminiferal evolution due
to repeated anoxic episodes, at least since the beginning of the Pliocene (Verhallen 1991). Ac-
cording to Mikhalevich (2004), endemism among bathyal foraminiferal faunas in the Southern
Ocean is “significant,” as it is for many metazoan taxa (Brandt et al. 2007). Species with apparently
restricted geographical distributions also occur at depths between 200 and 2,000 m around New
Zealand. Hayward et al. (2011) record 41 such species within this depth range. These include 3
species of Notorotalia, a genus restricted to the Southern Hemisphere that probably originated and
radiated in the New Zealand region. Of the 41 bathyal (200–2,000 m) endemic species recognized
by Hayward et al. (2011), 10 extend below 2,000 m.
5.2. Abyssal Seafloor

Much of the ocean floor is situated at abyssal depths (Smith et al. 2008). In their recent review,
McClain & Mincks Hardy (2010) concluded that “many taxa appear broadly distributed across the
deep-sea floor.” By contrast, Vinogradova (1997) argued for a high degree of endemism among
macro- and mega-faunal animals confined to abyssal depths. In the case of foraminifera, the general
perception (e.g., Douglas & Woodruff 1981, Murray 2006) is that many morphospecies occupying
this vast habitat are cosmopolitan, a view supported by literature records from different oceans
(Table 1). As noted above, however, inconsistencies in the identification of species mean that
such records should not be accepted without reference to published photographs, or preferably to
original material. Nevertheless, specimens of organic-walled, agglutinated, and calcareous species
from widely separated oceanic areas are often remarkably similar in terms of the general appearance
and structure of their tests (Figure 2). The existence of cosmopolitan deep-sea foraminiferal
species is also indicated by ultradeep sequencing of short, highly variable regions of the SSU
rDNA gene in sediment samples from deep-sea sites in the Arctic, North Atlantic, Southern,
and Pacific Oceans and the Caribbean Sea (Lecroq et al. 2011). However, most of the operational
taxonomic units recognized were confined to one or two sites, and replicates from the same station
yielded similar species compositions, suggesting that some species may have restricted distributions
( J. Pawlowski, written communication).
5.2.1. Species with wide distributions. We focus on four well-known, predominantly abyssal
species, all belonging to the order Rotaliida, for which molecular data are available.
Epistominella exigua is reported from all oceans (Table 1) and from depths between 500 m and
7,500 m (Murray 1991). However, it is a predominately abyssal species, and the shallower records
are questionable. This epifaunal/shallow infaunal species occurs across a wide range of organic-
matter flux rates (Altenbach et al. 1999). It appears to feed on algal cells embedded within lumps
of phytodetritus derived from surface production. In the northeast Atlantic, E. exigua exhibits an

a b
c d
e f
g h
i j
Figure 2
Similar foraminiferal morphospecies from different oceans. Purple outline indicates specimens from the
North Atlantic: Porcupine Abyssal Plain, 48◦ 59.4 N, 16◦ 30 W, 4,840-m water depth (a,c,e,g) and 57◦ 5.3 N,
12◦ 24.3 W, 1,980-m water depth (i ). Blue outline indicates a specimen from the North Pacific: 48◦ 59.4 N,
176◦ 55.06 W, 5,289-m water depth. Red outline indicates specimens from the central Pacific: 9◦ 14 N,
146◦ 15 W, 5,300-m water depth (d ) and ∼151◦ N, ∼119◦ W, ∼4,100-m water depth ( f,h). Green outline
indicates specimens from the Weddell Sea: 65◦ 20.09 S, 54◦ 14.72 W, 1,108-m water depth. Species
identifications are as follows: (a,b) Conicotheca sp.; (c,d ) Nodellum-like form 2; (e,f ) Lagenammina sp.;
( g,h) Adercotryma glomerata; (i,j) Epistominella arctica.

opportunistic, population-level response to pulsed inputs of phytodetritus (Gooday 1988).

Cibicidoides wuellerstorfi is also reported from all the main oceans. It is often attached to substrates
such as stones, sponges, and other biogenic structures and is considered to be a suspension feeder
that intercepts fresh phytodetrital aggregates just above the seafloor (Lutze & Thiel 1989).
Oridorsalis umbonatus is another widely distributed species. Epistominella arctica is a tiny species
described from the deep Arctic Ocean and subsequently reported from the North Atlantic and
Southern Oceans (Figure 2).
Pawlowski et al. (2007b) explored genetic differentiation between Arctic and Antarctic popula-
tions of E. exigua, C. wuellerstorfi, and O. umbonatus separated by a distance of 17,000 miles. Analyses
of a fragment of the SSU rDNA gene from specimens collected west and north of Svalbard (Arctic
Ocean) and in the Weddell Sea (Southern Ocean) revealed no differences between populations of
C. wuellerstorfi and only minor differences in the case of E. exigua. The degree of differentiation
was higher in O. umbonatus, which exhibited a maximum sequence divergence of 2.9% as well as
a substantial degree of genetic polymorphism within an individual. Lecroq et al. (2009) reported
a similar lack of differentiation between Arctic and Antarctic populations of E. arctica. Analyses of
the highly variable internal transcribed spacer (ITS) region of the rDNA gene from the northern
and southern polar sites likewise yielded very similar sequences in all three species, with mean
divergencies of <1% (Pawlowski et al. 2007b). Some differences were observed between Antarctic
and Arctic populations of O. umbonatus when ITS sequences were analyzed, but there was no
evidence for differentiation in the other two species. However, a population-genetics approach
involving an analysis of molecular variance indicated that a deep abyssal (4,650–4,975 m) Antarctic
population of E. exigua was genetically distinct from shallower abyssal Antarctic (2,600–4,600 m)
and bathyal northern (1,352–2,784 m) populations of this species. Arctic and Antarctic populations
of O. umbonatus were also significantly differentiated, whereas those of C. wuellerstorfi were not.
Subsequent analyses by Lecroq et al. (2009) of SSU rDNA sequences of E. exigua from deep
water off the coast of Japan revealed a striking degree of genetic similarity between these western
Pacific populations and those from the Antarctic, Atlantic, and Arctic studied by Pawlowski et al.
(2007b). A population-genetics analysis based on ITS rDNA sequences also failed to demonstrate
any evidence for cryptic speciation within this species. Instead, much of the genetic variation was
attributable to differences between specimens within, rather than between, populations (Lecroq
et al. 2009). These results echo those for other protistan taxa, such as heterotrophic flagellates,
which include marine species with cosmopolitan distributions (e.g., Scheckenbach et al. 2005).
5.2.2. Species with restricted distributions. The dual problems of rarity and undersampling are
particularly acute in deep-ocean basins, making it difficult to establish the existence of endemism.
In the abyssal equatorial Pacific, there are some obvious faunal differences between the Kaplan
East (Nozawa et al. 2006) and Kaplan Central (N. Ohkawara & A.J. Gooday, unpublished results)
sites. In particular, Saccammina minimus, the overwhelmingly dominant species at the Central
site (5,042-m water depth) (Ohkawara et al. 2009), is absent at the shallower (4,100 m) East site.
However, because this minute species has an extremely patchy distribution at small spatial scales
and is easily overlooked, no conclusions can be drawn about its wider distribution.
At regional and global scales, some deep-sea foraminifera appear to be restricted to particular
basins or oceans. Despite close faunal links between the Southern Ocean and North Atlantic
abyssal faunas (Cornelius & Gooday 2004), certain species may be confined to deep Antarctic
waters. These include a distinctive form of the cosmopolitan deep-sea genus Vanhoeffenella,
characterized by a broad agglutinated rim and a three-dimensional morphology. Another possible
example is Haplophragmoides umbilicatum, a species known only from the abyssal Southern Ocean
(N. Cornelius, personal communication). There are also faunal differences between the Pacific

and Atlantic Oceans. Among large and distinctive foraminifera that are unlikely to be overlooked,
stannomid xenophyophores and the tubular species Jugimurammina stellaperuta are largely or
entirely confined to the Pacific (Gooday et al. 2004). Conversely, the discoidal miliolid Discospirina
tenuissima is currently reported only from the Atlantic and Indian Oceans. Similar examples prob-
ably exist among the smaller foraminifera. Given the different geological ages and environmental
characteristics (bottom-water oxygenation and corrosivity, sediment types, sedimentary processes,
timing and magnitude of primary production) of the Pacific and Atlantic Oceans (Levin & Gooday
2003), it seems highly unlikely that all deep-water foraminiferal species occur in both oceans.
5.3. Hypoxic Environments

Deep-water hypoxia (O2 <0.5 ml per liter) has persisted over millennial-scale time periods at
bathyal depths in stratified basins and OMZs, where it is associated with upwelling combined with
reduced circulation, water column stratification, and oxygen-depleted source waters (Levin 2003).
OMZs are developed intensely in the eastern Pacific and in the northern Indian Ocean (Arabian
Sea and Bay of Bengal), and somewhat less so in the eastern Atlantic (Diaz & Rosenberg 1995,
Levin 2003, Helly & Levin 2004). Where they impinge on the seafloor, OMZs create strong
bottom-water oxygen gradients. In addition to oxygen depletion, these regions are characterized
by high sediment organic carbon content, lowered pH, and soft, unconsolidated sediments with a
high water content (Gooday et al. 2010a).
Bathyal hypoxic environments are usually inhabited by low-diversity, high-dominance assem-
blages of foraminiferal species. Despite the depressed pH, calcareous taxa typically dominate these
faunas. Many species exhibit at least some morphological, physiological, or ultrastructural adap-
tations to hypoxia (Bernhard & Sen Gupta 1999). These include an ability to accumulate and
respire nitrate, as demonstrated initially in Globobulimina (Risgaard-Petersen et al. 2006) and sub-
sequently in numerous other taxa (Piña-Ochoa et al. 2010). Deep-infaunal species, which occupy
habitats deeper in the sediment in well-oxygenated benthic environments, replace species that are
less resistant to hypoxia in low-oxygen settings. Specialized shallow-infaunal taxa may also appear.
Whereas the deep-infaunal taxa are mostly cosmopolitan, the hypoxia-resistant surface dwellers
often show more regional distributions. OMZs undoubtedly limit species ranges by excluding
hypoxia-sensitive species (Gooday 2003). They may also act as a strong barrier to the spread of
species between upper and lower slope environments (Rogers 2000).
There is mounting evidence that the extent and thickness of OMZs in tropical and subtropical
regions of the oceans have increased since the 1960s (Stramma et al. 2008, 2010). Continued
expansion of OMZs (Hofmann & Schellnhuber 2009) is likely to have profound consequences for
marine life (Stramma et al. 2010, Gruber 2011). These effects will probably include an increased
dominance of carbon processing by hypoxia-tolerant foraminiferal species (Woulds et al. 2007)
and an expansion of their geographical ranges.
5.3.1. Species with wide distributions. The best example is Virgulinella fragilis, reported at
depths between 16 m and >100 m from off west Africa, the eastern Arabian Sea, the Japanese
islands, the Australian and New Zealand margins, the Peru margin, the Gulf of Mexico, and the
Venezuelan shelf (Tsuchiya et al. 2008, Leiter & Altenbach 2010). This species appears to be a
habitat endemic (Anderson 1994) that is confined to sulfidic/hypoxic environments; it occupies
a deep-infaunal microhabitat where the bottom-water oxygen content is <0.3 ml per liter (Leiter
& Altenbach 2010). Molecular analyses of individuals from three widely separated and isolated
populations off Japan, New Zealand, and Namibia demonstrated a remarkable degree of genetic
homogeneity with no hint of cryptic speciation (Tsuchiya et al. 2008). Because gene flow between

the populations and recent dispersal are very unlikely, Tsuchiya et al. (2008) suggested that
V. fragilis exhibits evolutionary stasis (both genetic and morphological), perhaps enhanced by
persistent asexual reproduction.
Cosmopolitan
species: a widely Some other deep-infaunal, hypoxia-tolerant species have wide distributions. Chilostomella
distributed species that ovoidea/oolina (the names are probably synonyms) is a particularly interesting example (Table 1).
is found in many parts An analysis of partial SSU rDNA sequences of specimens from disjunct, bathyal (611–1,449 m),
of the world moderately hypoxic sites in the Pacific and Atlantic Oceans and Mediterranean Sea yielded three
distinct genetic types that could not be distinguished morphologically. These types, which were
supported by ITS data, occurred in (a) the Bay of Biscay and Mediterranean (AtlMed), (b) Sagami
Bay ( Japan) and the Oregon slope (NPac), and (c) Sagami Bay and the Costa Rica slope (CPac)
(Grimm et al. 2007). The NPac and CPac types occurred on both sides of the Pacific Ocean,
probably reflecting recent or ongoing genetic exchange across the Pacific mediated by the passive
dispersal of propagules (Grimm et al. 2007). Globobulimina is another important deep-infaunal
genus that is widely distributed in hypoxic settings. It includes a number of species with only
minor and rather subtle morphological differences, in some cases supported by molecular data
(Ertan et al. 2004). One such species, Globobulimina affinis, is reported from the Atlantic, Indian,
and Pacific Oceans as well as the Sea of Marmara (Table 1).
5.3.2. Species with restricted distributions. Different species are found at different localities
within the same general area, such as the California borderland (e.g., Bernhard & Sen Gupta 1999).
Different oxygen concentrations probably explain much of this variation (Bernhard et al. 1997), but
it could also reflect restricted distributions. In the Arabian Sea, Uvigerina ex gr. U. semiornata and
Bolivina aff. B. dilatata dominate the core region of the Pakistan margin OMZ, where bottom-water
oxygen levels drop to ∼0.1 ml per liter (Schumacher et al. 2007, Larkin & Gooday 2009). Similar
forms occur on the Oman margin (Gooday et al. 2000). Following an exhaustive effort to identify
them, Schumacher et al. (2007) concluded that both were undescribed species confined to the
Arabian Sea. They contrasted the endemic character of foraminiferal species inhabiting the OMZ
core with assemblages of more cosmopolitan species (e.g., Globobulimina spp. and Chilostomella
spp.) found in the lower part of the zone.
6. CRYPTIC SPECIATION
There is good evidence among planktonic foraminiferal species for cryptic speciation, associ-
ated with slight morphological as well as biological, ecological, and physiological differences (e.g.,
Huber et al. 1997, de Vargas et al. 2002, Darling et al. 2004). However, cryptic speciation is less ev-
ident among benthic foraminifera, which evolve at a slower rate than their planktonic counterparts
(Pawlowski et al. 1997). The best evidence comes from shallow-water taxa. Analyses of ITS rDNA
sequences in Planoglabratella opercularis (Tsuchiya et al. 2003) from intertidal locations around
Japan demonstrates the existence of two cryptic species, Type A and Type B, the sequences of
which diverge by 7.0% to 8.5%. Type B is genetically closer (3.9% to 4.8% divergence) to another
species, P. nakamurai, than it is to Type A. Careful examination revealed subtle morphological dif-
ferences between the two phylotypes of P. opercularis, with Type B exhibiting some test features in
common with P. nakamurai. Cryptic speciation has also been described within Ammonia, a highly
variable coastal genus often regarded as comprising a few species with many different ecopheno-
types (Hayward et al. 2004, Pawlowski & Holzmann 2008). Partial, large-subunit rDNA sequences
revealed 13 phylotypes (T1 to T13), each sufficiently distinct to be regarded as a species and ex-
hibiting a variety of biogeographic patterns. Phylotype T1 is distributed around the world in both
hemispheres, T2 and T5 occur on either side of the North Atlantic and South Pacific, respectively,

whereas T3 is widely distributed around European coastlines. T6 has been found in Japanese and
European waters and may be an invasive species dispersed by shipping. The other 8 phylotypes
have restricted distributions. Some shallow-water morphospecies with bipolar distributions also
encompass cryptic species (Mikhalevich 2004, Brandt et al. 2007, Pawlowski et al. 2008).
Although genetic studies have revealed complexes of cryptic species among some animal groups
in the deep sea (e.g., isopods; Raupach et al. 2007), there is currently little unequivocal evidence
for cryptic speciation among bathyal or abyssal benthic foraminifera. The only real example is
Conqueria laevis, a monothalamous species of which Arctic and Antarctic individuals were genet-
ically distinct (Brandt et al. 2007). The three genetic types of Chilostomella mentioned above are
less differentiated than the five planktonic forms of Neogloboquadrina pachyderma recognized by
Darling et al. (2004) and apparently lack any clear morphological expression, leaving their tax-
onomic status uncertain (Grimm et al. 2007). Likewise, the genetic differences observed among
Arctic and Antarctic populations of O. umbonatus, and to a lesser extent in E. exigua, do not amount
to cryptic speciation (Pawlowski et al. 2007b). Some species (e.g., Adercotryma glomerata) are re-
ported from shelf to abyssal depths (Murray 1991); inaccurate taxonomy is possibly responsible
for these vast bathymetric ranges, but cryptic species occupying progressively deeper depth zones
could also be involved. Although this latter suggestion is purely speculative, it would be consis-
tent with the considerable degree of depth-related genetic differentiation observed among some
animal morphospecies (e.g., Zardus et al. 2006). By contrast, there is good molecular evidence
that the monothalamous species Bathyallogromia weddellensis is genetically coherent across a depth
range of 1,100–6,300 m in the Southern Ocean (Gooday et al. 2004). Populations of the calcareous
species Epistominella vitrea from 15 to 30 m in McMurdo Sound and bathyal depths (>1,000 m) in
the Weddell Sea on the opposite side of the Antarctic continent are genetically almost identical
(Pawlowski et al. 2007a). These wide bathymetric ranges are possibly related to the essentially
isothermal water column around Antarctica.
7. CONTROLS ON DISTRIBUTION PATTERNS

7.1. Evolutionary Factors
Coastal and shelf environments have been subject to repeated modification, for example, as a
result of sea-level changes, leading to the continual destruction and reformation of shallow-water
marine habitats. Geological and oceanographic fluctuations have also impacted bathyal continental
margins, particularly at upper-slope depths. Environmental instability of this sort is likely to
enhance genetic differentiation (Katz et al. 2005) as well as create barriers to gene flow, resulting
in a greater degree of endemism compared with deeper-water settings, which have been generally
more stable over geological timescales (Buzas & Culver 1984, 1989; Rogers 2000).
Caron (2009) suggested that different modes of reproduction (sexual versus asexual) may
influence distribution patterns in protists. Foraminifera can reproduce sexually or asexually. Most
of the species that have been studied undergo an alternation of generations. However, because
population densities are generally lower in the deep sea, asexual reproduction is more likely
to occur here than in shelf settings (Murray 1991, p. 301). If this is true, then rates of genetic
differentiation and speciation are also likely to be slower, promoting the development of larger
geographical ranges, particularly at abyssal depths (Pawlowski et al. 2007b). A slower rate of
evolution would be consistent with the greater geological longevity that seems to be typical of
deep-water species (Buzas & Culver 1984). As mentioned above, evolutionary stasis, rather than
gene flow, is one possible explanation for the remarkable genetic homogeneity between widely
separated and isolated populations of the hypoxia-tolerant species Virgulinella fragilis.

7.2. Barriers to Dispersal

Grassle & Morse-Porteous (1987) noted the “lack of barriers to dispersal over very large areas” as
one of the main influences on deep-sea benthic community structure. Certainly, the generally open
nature of abyssal plains is consistent with the widespread distribution of many abyssal foraminiferal
species. Nevertheless, barriers to dispersal do exist in the deep sea. Hydrographic features, such
as strong current systems, create barriers that potentially limit the ranges of deep-sea animals
(e.g., Won et al. 2003). However, the most obvious are topographic features such as major ridges
(Vinogradova 1997). Preliminary analysis of foraminiferal assemblages on either side of the Mid-
Atlantic Ridge (49◦ –54◦ N, 2,500-m depth) did not reveal any clear faunal differences (N. Rothe
& A.J. Gooday, unpublished data). Similar abyssal foraminiferal assemblages occupy areas to the
north and south of the Walvis Ridge, a feature that rises 4,000 m above the adjacent basins
(Schmiedl et al. 1997). The bathymetric distributions of many deep-sea foraminiferal species, and
presumably of their propagules, are sufficiently broad to span these kinds of topographic obstacles
(Pawlowski et al. 2007b). Given the ability for propagules to survive inhospitable conditions for
periods of years (Alve & Goldstein 2010), the potential for the wide dispersal of foraminifera by
currents at abyssal depths is considerable. Passive transport by bottom currents across topographic
barriers has been invoked to explain the cosmopolitan distributions of abyssal harpacticoid copepod
species in the genus Mesocletodes (Menzel et al. 2011).
Additional topographic barriers exist on continental margins, which are generally much more
heterogeneous than the abyssal plains (Levin & Dayton 2009). This heterogeneity has been im-
plicated in the greater degree of morphological (Etter & Rex 1990) and genetic (Etter et al. 2005)
variability on bathyal continental slopes compared with abyssal plains. Submarine canyons, fea-
tures that often extend from near the coastline to abyssal depths, constitute one obvious source
of heterogeneity. Distinctive foraminiferal species are sometimes common within canyons but
are not present on adjacent slopes (Hess & Jorissen 2009). However, these species appear to be
adapted to special conditions inside the canyons, such as sediment instability and/or organic mat-
ter focusing. There is no evidence that canyons, or other physical obstacles, limit the geographical
distribution of any species at bathyal depths on continental margins.
Shallow sills create major barriers to the influx of species into partially land-locked basins. The
most obvious example is the Mediterranean, where the Straits of Gibraltar has limited the exchange
of species with the North Atlantic since the basin refilled following the Late Miocene Messinian
salinity crisis. As a result, the deep fauna is impoverished compared with that in the Atlantic (Murray
1991). However, the low diversity of these faunas, especially in the eastern Mediterranean, may
also reflect the extreme oligotrophy of the deep Levantine basin (De Rijk et al. 2000). As explained
above, several species (e.g., Articulina tubulosa, Rotamorphina involuta) appear to be limited to the
Mediterranean, whereas others (e.g., U. mediterranea, Planulina ariminensis, Paranomalina coronata)
may have evolved in the Mediterranean and then invaded the eastern Atlantic.
7.3. Environmental Parameters

Irrespective of the overall geographical range of a particular species, environmental factors will
determine where that species actually occurs (Finlay & Fenchel 2004, Tsuchiya et al. 2008). As
indicated above, the abundance, diversity, and composition of foraminiferal assemblages in coastal
and sublittoral environments are controlled largely by a combination of physical and chemical
parameters (temperature, salinity, currents, substrate, vegetation cover), food resources, and biotic
interactions (Culver & Buzas 1999, Murray 2006). In deep water, early studies related the oc-
currence of foraminiferal species to the physical and chemical properties of bottom-water masses
(Schnitker 1980). These ideas are no longer considered tenable ( Jorissen et al. 2007), although

some water-mass properties, notably current flow (Schönfeld 1997) and bottom-water corrosive-
ness (Schmiedl et al. 1997), may be important. Levin et al. (2001) concluded that food inputs,
bottom flow, bottom-water oxygenation, sediment heterogeneity, and ecological disturbance are
the five main influences on deep-sea diversity patterns. Mackensen et al. (1995) identified a similar
set of parameters that they considered to underlie the distribution of foraminiferal assemblages
in the South Atlantic Ocean. Jorissen et al. (2007) reformulated these as follows: (a) organic
matter exported to the seafloor and organic carbon content of the sediment, (b) bottom-water
hydrodynamics and related sediment grain-size properties, (c) bottom-water oxygenation, and
(d ) bottom-water carbonate saturation. Hayward et al. (2011) reached similar conclusions based
on their analysis of foraminiferal assemblages around New Zealand. Organic-matter flux and
carbonate dissolution are probably the dominant ecological parameters across the vast abyssal
areas, particularly in the Pacific Ocean (Saidova 2000), whereas hydrodynamics, oxygen, and
sediment grain size are more influential at bathyal depths. Carbonate dissolution, together with
sediment characteristics, is believed to exert an important influence on foraminiferal distributions

down to abyssal depths around the Antarctic continent (e.g., Echols 1971, Anderson 1975).
Particularly in oligotrophic abyssal settings, the supply of organic matter to the seafloor, which
is related to phytoplankton primary production, profoundly influences the structure, composi-
tion, and functioning of deep-sea benthic communities (Smith et al. 2008). The scale of the flux
(Altenbach et al. 1999) and its seasonality (Gooday 1988, Loubere & Fariduddin 1999, Sun et al.
2006) are both important for foraminifera. In the North Atlantic (2,178–4,673-m water depth),
an assemblage dominated by two phytodetritus species (Alabaminella weddellensis and Epistominella
exigua) is associated with a highly seasonal organic carbon flux, whereas a Globocassidulina subglobosa–
Nuttallides umbonifera assemblage is negatively correlated with a seasonal flux (Sun et al. 2006). The
surface-ocean biogeochemical provinces recognized by Longhurst (1998) provide a comprehensive
overview of the contrasting productivity regimes that undoubtedly underlie global macroecologi-
cal patterns among benthic foraminifera. However, the main impact of food availability is likely to
be on the ability of some species to outcompete others, as indicated by increases in their absolute
and relative abundance (e.g., Koho et al. 2009). Whether fluxes of labile organic matter to the
seafloor also limit species ranges is debatable. In contrast, physical and chemical parameters such
as temperature, salinity, and oxygen concentrations act as limiting factors where they approach the
tolerance level of the species under consideration (Murray 2001, 2006). At lower levels, variations
in the magnitude of these parameters probably have no effect on species distribution patterns.
Thus, given sufficient ability to disperse, species will probably occur everywhere, at higher or
lower densities according to available food resources, except in areas where physical and chemical
parameters (e.g., temperature, salinity, DO concentrations) place them under intolerable stress.
8. CONCLUSIONS
Like those of other organisms, biogeographic studies of deep-sea benthic foraminifera are ham-
pered by imperfect taxonomy, the relative rarity of many species, and undersampling of the vast
ocean-floor environment. Nevertheless, there is more information about foraminifera than many
other deep-sea taxa. In contrast to the apparent prevalence of endemic distributions among coastal
and sublittoral species, many common, well-characterized hard-shelled species appear to be dis-
tributed widely at bathyal and abyssal depths. This is consistent with the pattern of moderate
cosmopolitanism and low endemism among species in the Gulf of Mexico (Sen Gupta & Smith
2010). However, this generalization must be tempered with some important caveats. Broad ranges
are supported by genetic data in only a few cases, and widespread bathyal species often exhibit
considerable morphological variation. It is possible that endemism is more prevalent among rare

species than currently realized, although conclusive evidence for restricted distributions will be
difficult to obtain.
SUMMARY POINTS
Here, we return to the questions posed in the Introduction (see section above).
1. Do deep-water foraminiferal species have typical distribution patterns? Many common
bathyal and abyssal morphospecies appear to have broad ranges (in few cases, supported
by genetic analyses), while relatively few have restricted distributions. This contrasts with
the frequency of apparent endemic distributions among shallow-water species. However,
many deep-sea foraminiferal species are rare, often undescribed in the case of monothal-
amous taxa, and known only from one or a few samples. This makes it impossible to draw
sensible conclusions about their geographical ranges.
2. What are the main factors influencing distribution patterns? Foraminiferal species dis-
tributions are influenced by their evolutionary history and environmental controls. In
shallow-water settings, species ranges are limited by temperature and salinity close to
the shore as well as by sediment characteristics, vegetation cover, and light penetration
on the shelf. On the continental slope, distributions are influenced by food quantity
and quality, sediment characteristics, topographic features (e.g., canyons), and, in places,
bottom-water DO concentrations and current flow. On the environmentally more uni-
form abyssal plains, the main factors are the quantity and quality of organic matter
reaching the seafloor, its seasonality, and the carbonate corrosion of the bottom water.
3. What is the degree of connectivity between populations? Most foraminifera appear to
have excellent dispersive capabilities, mediated mainly by microbe-sized propagules,
which can remain viable for several years. Transport of propagules by thermohaline
and other currents has the potential to link distant populations genetically, either di-
rectly or via intermediate populations. However, slow evolution may also account for a
lack of genetic differentiation, as is likely in the case of isolated populations of Virgulinella
fragilis, a species confined to hypoxic/sulfidic habitats.
4. Are widely distributed benthic foraminiferal morphospecies genetically coherent or do
they conceal cryptic species? There is good evidence for cryptic speciation (combined
with slight morphological differences) in a few coastal benthic foraminifera as well as
in planktonic species. Distant populations of certain bathyal and abyssal species have
diverged genetically but probably not enough to regard them as cryptic species. Some
morphologically simple monothalamous species, which possess few taxonomically useful
characters, may encompass cryptic species. It is also possible that morphospecies with
wide bathymetric ranges are genetically differentiated, although evidence is lacking.
5. To what extent does imperfect taxonomy obscure biogeographic patterns? Establishing
species ranges depends crucially on the consistent use of species names. Synonyms appear
to be quite prevalent among shelf-dwelling species and may lead to the inappropriate
splitting of widely distributed species (pseudoendemism). The opposite problem, that of
including disparate forms within one species name, seems to be quite common in some
monothalamous and agglutinated taxa. This can artificially inflate species ranges.

FUTURE ISSUES
1. Taxonomy: Determining biogeographic patterns among foraminifera requires accurate
taxonomy. A major effort is needed to revise difficult species groups (e.g., Uvigerina and
Globobulimina spp.) and to describe novel species, particularly those belonging to the
monothalamous taxa that abound in deep-sea sediments.
2. Endemism: How can endemic distributions be recognized, given the difficulty in estab-
lishing the presence of rare species in a particular area? The problem of undersampling is
particularly acute in the deep sea, where only a tiny proportion of the vast benthic habitat
has ever been sampled and the proportion of rare species, many of them undescribed, is
particularly high.
3. Cosmopolitanism: Conversely, claims for ubiquitous species distributions based on lit-
erature sources from different regions depend crucially on the assumption that the species
are accurately identified. Imperfect taxonomy means that, unless species are clearly il-
lustrated, or the original material reexamined, reliance on faunal lists for distributional
records is risky.
4. Molecular genetics: Only a handful of deep-sea species has been studied genetically.
More analyses based on the SSU and ITS regions of the rDNA gene would reveal the
degree of genetic differentiation between geographically and bathymetrically dispersed
populations of the same morphospecies, as well as the possible existence of cryptic species.
New generation sequencing will provide a rapid way to identify species in sediment
samples as well as reveal species that cannot easily be detected visually.
5. Climate change: The consequences of ocean warming will create multiple challenges
for benthic foraminifera. Many species feed at the base of the food chain on detrital
material and will be impacted by warming-related changes in the quantity and quality
of surface-derived organic matter reaching the seafloor. This is likely to lead to shifts
in the diversity and dominance of foraminiferal assemblages, as well as species ranges,
particularly at abyssal depths. In bathyal settings, hypoxia-tolerant species will become
more widely distributed as OMZs expand and intensify.
6. Reproduction: Foraminifera can reproduce both sexually and asexually. Species that
reproduce asexually may evolve more slowly and hence establish wider geographical
ranges. Very little is known about which mode is typical for deep-sea foraminifera, al-
though asexual reproduction seems more likely in the case of rare species, particularly
at abyssal depths. This question could be investigated by studying the prevalence of
microspheric and megalospheric forms in deep-sea samples.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We thank Jan Pawlowski for his comments on an earlier draft of this paper. This paper is a contri-
bution to the Oceans 2025 Project funded by the Natural Environment Research Council, United

Kingdom, and the Collaborative Project HERMIONE funded under the European Commission’s
Framework 7 program.
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A Conversation with Karl K. Turekian

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Climate Change Impacts on Marine Ecosystems

Scott C. Doney, Mary Ruckelshaus, J. Emmett Duffy, James P. Barry, Francis Chan,
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Nancy Knowlton, Jeffrey Polovina, Nancy N. Rabalais, William J. Sydeman,
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Shifting Patterns of Life in the Pacific Arctic and Sub-Arctic Seas
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Understanding Continental Margin Biodiversity: A New Imperative
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Nutrient Ratios as a Tracer and Driver of Ocean Biogeochemistry
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Progress in Understanding Harmful Algal Blooms: Paradigm Shifts
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Thin Phytoplankton Layers: Characteristics, Mechanisms,
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Jellyfish and Ctenophore Blooms Coincide with Human Proliferations
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Benthic Foraminiferal Biogeography: Controls on Global Distribution
Patterns in Deep-Water Settings
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vi
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Plankton and Particle Size and Packaging: From Determining Optical

Properties to Driving the Biological Pump
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Overturning in the North Atlantic
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The Wind- and Wave-Driven Inner-Shelf Circulation
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Serpentinite Mud Volcanism: Observations, Processes,
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Marine Microgels
Pedro Verdugo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 375

The Fate of Terrestrial Organic Carbon in the Marine Environment
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Marine Viruses: Truth or Dare
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The Rare Bacterial Biosphere
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Marine Protistan Diversity
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Errata
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• Our comprehensive search

Annu. Rev. Mar. Sci. 2012. 4:237–62 Keywords

The Annual Review of Marine Science is online at Abstract

1. Are there “typical” patterns of geographical distribution among deep-water foraminiferal

238 Gooday · Jorissen

genetically, but very

www.annualreviews.org • Benthic Foraminiferal Biogeography 239

potential for wide dispersal in the deep sea.

4. ENVIRONMENTAL PARAMETERS INFLUENCING

240 Gooday · Jorissen

BENTHIC FORAMINIFERA AS PALEOCEANOGRAPHIC

5. GEOGRAPHICAL DISTRIBUTIONS OF (MORPHO)SPECIES

5.1. Continental Shelf and Slope

www.annualreviews.org • Benthic Foraminiferal Biogeography 241

242 Gooday · Jorissen

www.annualreviews.org • Benthic Foraminiferal Biogeography 243

Cyclammina cancellata 8, 25 8 8, 29, 34 33 7 2, 17 6, 13,15 36 3

Hoeglundina elegans 12, 25, 24, 31 12 22 4, 27 7, 9, 38 2, 12, 15 14, 3, 12, 20

Laticarinata pauperata 25 29 27 7, 9, 16 17 12, 15

Nuttallides umbonifera 5, 12 24, 31 4, 27 16 12 13 12

www.annualreviews.org • Benthic Foraminiferal Biogeography

5.2. Abyssal Seafloor

246 Gooday · Jorissen

www.annualreviews.org • Benthic Foraminiferal Biogeography 247

opportunistic, population-level response to pulsed inputs of phytodetritus (Gooday 1988).

248 Gooday · Jorissen

5.3. Hypoxic Environments

www.annualreviews.org • Benthic Foraminiferal Biogeography 249

250 Gooday · Jorissen

7. CONTROLS ON DISTRIBUTION PATTERNS

www.annualreviews.org • Benthic Foraminiferal Biogeography 251

7.2. Barriers to Dispersal

7.3. Environmental Parameters

252 Gooday · Jorissen

sediment characteristics, is believed to exert an important inﬂuence on foraminiferal distributions

www.annualreviews.org • Benthic Foraminiferal Biogeography 253

254 Gooday · Jorissen

www.annualreviews.org • Benthic Foraminiferal Biogeography 255

propagules can disperse 21:69–96

256 Gooday · Jorissen

www.annualreviews.org • Benthic Foraminiferal Biogeography 257

assemblages at the Porcupine Abyssal Plain, NE Atlantic. Deep-Sea Res. II 57:1362–82

258 Gooday · Jorissen

www.annualreviews.org • Benthic Foraminiferal Biogeography 259

260 Gooday · Jorissen

www.annualreviews.org • Benthic Foraminiferal Biogeography 261

adapted to hypoxic and South Atlantic. Utrecht Micropaleontol. Bull. 35:47–65

262 Gooday · Jorissen

Volume 4, 2012 Contents

A Conversation with Karl K. Turekian

Climate Change Impacts on Marine Ecosystems

Chad A. English, Heather M. Galindo, Jacqueline M. Grebmeier, Anne B. Hollowed,

Plankton and Particle Size and Packaging: From Determining Optical

Pedro Verdugo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 375

Neal E. Blair and Robert C. Aller p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 401

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