2008 Villanueva & Norman 2008 With Colour Plates

Oceanography and Marine Biology: An Annual Review, 2008, 46, 105-202 R. N. Gibson, R. J. A. Atkinson, and J. D. M.
. Gordon, Editors Taylor & Francis
BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

RoGER VillANuEVA1 & MARk D. NoRMAN2 1Institut de Cincies del Mar (CSIC), Passeig Martim de la Barceloneta 3749, E-08003 Barcelona, Spain E-mail: roger@icm.csic.es 2Sciences, Museum Victoria, GPO Box 666, Melbourne, Vic 3001, Australia E-mail: mnorman@museum.vic.gov.au Abstract octopuses of the family octopodidae adopt two major life-history strategies. The first is the production of relatively few, large eggs resulting in well-developed hatchlings that resemble the adults and rapidly adopt the benthic habit of their parents. The second strategy is production of numerous small eggs that hatch into planktonic, free-swimming hatchlings with few suckers, simple chromatophores and transparent musculature. These distinctive planktonic stages are termed paralarvae and differ from conspecific adults in their morphology, physiology, ecology and behaviour. This study aims to review available knowledge on this subject. in benthic octopuses with planktonic stages, spawning characteristics and duration of planktonic life seem to play an important role in their dispersal capacities. Duration of the hatching period of a single egg mass can range from 2 days to 11 wk, while duration of the planktonic stage can range from 3 wk to half a year, depending on the species and temperature. Thus these paralarvae possess considerable potential for dispersal. in some species, individuals reach relatively large sizes while living as part of the micronekton of oceanic, epipelagic waters. such forms appear to delay settlement for an unknown period that is suspected to be longer than for paralarvae in more coastal, neritic waters. During the planktonic period, paralarval octopuses feed on crustaceans as their primary prey. in addition to the protein, critical to the protein-based metabolism of octopuses (and all cephalopods), the lipid and copper contents of the prey also appear important in maintaining normal growth. littoral and oceanic fishes are their main predators and defence behaviours may involve fast swimming speeds, use of ink decoys, dive responses and camouflage. sensory systems of planktonic stages include photo-, mechano- and chemoreceptors controlled by a highly evolved nervous system that follows the general pattern described for adult cephalopods. on settlement, a major metamorphosis occurs in morphology, physiology and behaviour. Morphological changes associated with the settlement process include positive allometric arm growth; chromatophore, iridophore and leucophore genesis; development of skin sculptural components and a horizontal pupillary response. At the same time, animals lose the klliker organs that cover the body surface, the lateral line system and the oral denticles of the beaks. strong positive phototaxis is a common response for hatchlings and some later paralarval stages but this response reduces, disappears or reverses after settlement. There are many gaps in our knowledge of the planktonic phases of benthic octopuses. Most of our understanding of octopus paralarvae comes from studies of just two species (Octopus vulgaris and Enteroctopus dofleini) and knowledge of the vast majority of benthic octopus species with planktonic stages is considered rudimentary or non-existent. Research is needed in a variety of fields, from taxonomy to ecology. studies of feeding and nutrition are critical in order to develop the nascent aquaculture of key species and ageing studies are necessary to understand planktonic population dynamics,
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RoGER VillANuEVA & MARk D. NoRMAN particularly in commercially valuable species targeted by fisheries. current and potential anthropogenic impacts on these early life stages of octopuses, such as pollution, overfishing and global warming, are also identified.
Introduction
Amongst the cephalopods, one of the most familiar groups is the bottom-dwelling or benthic octopuses of the family octopodidae. This large family contains over 200 species (Norman & hochberg 2005a), which range in size from pygmy taxa mature at <1 g (e.g., Octopus wolfi) to giant forms exceeding 100 kg (e.g., Enteroctopus dofleini) (Norman 2000). Member species occupy all marine habitats from tropical intertidal reefs to polar latitudes and into the deep sea to nearly 4000 m (Voss 1988). Benthic octopuses adopt two major life-history strategies (Boletzky 1977a, 1992). The first is production of relatively few, large eggs resulting in well-developed hatchlings that resemble the adults and rapidly adopt the benthic habit of their parents (Figure 1c,D). The second strategy is production of numerous small eggs that hatch into distinctive free-swimming, planktonic and semitransparent hatchlings occupying ecological niches distinct from those of the adults (Figure 1A,B). This latter category of hatchling typically has poorly developed limbs, few suckers, simple chromatophores and transparent musculature. This marked contrast between the morphology and ecology of the planktonic stages of cephalopods and their adult form led to the coining of the term cephalopod paralarva. young & harman (1988, p. 202) defined paralarva as a cephalopod of the first post-hatching growth stage that is pelagic in near-surface waters during the day and that has a distinctly different mode-of-life from
Figure 1 (see also colour Figure 1 in the insert following p. 250.) planktonic and benthic hatchlings in octopodidae. Adult female Wunderpus photogenicus 26 mm Ml in laboratory carrying egg strings with developing embryos within the arms (A) and hatchling (total length ~3.5 mm) from same egg mass (B). Note the well-developed dorsal mantle cavity of the paralarvae. (Reproduced with permission from Miske & kirchhauser 2006.) Female Octopus berrima at the time of hatching in the laboratory with a benthic juvenile hatchling (total length ~20 mm) in foreground (c) and within 10 min of hatching (D) showing well-developed arms and chromatic and sculptural components of the skin. (photos: David paul.) 106
BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs that of older conspecific individuals. This term alludes to the metamorphic transformations seen in arthropods and fishes from a larval juvenile form to a morphologically distinct adult form. As the transformation in cephalopod species with planktonic young is less dramatic, the term paralarva was considered appropriate. octopus paralarvae can be considered members of the meroplankton because these young octopuses live as plankton for only a part of their life cycle. According to their size (in total length), most planktonic octopuses can be considered mesoplankton (0.220 mm) (harris et al. 2000). Egg size and adult body size show significant variation within the family octopodidae (hochberg et al. 1992). pygmy species with benthic young can produce eggs smaller in size than those of giant taxa with planktonic young. As a consequence, egg size alone is not an effective indicator of which life-history strategy is adopted. Boletzky (1977a, 19781979) proposes that egg size relative to body size is a more effective predictor. he proposes that the boundary between these two strategies occurs when egg length represents 1012% of mantle length (Ml). Eggs >12% of Ml produce benthic hatchlings while eggs <10% of Ml produce planktonic hatchlings. Table 1 lists those octopus species known or likely to have planktonic paralarvae. it comprises three classes of information species for which planktonic paralarvae have been described; species that produce small-type eggs (<10% of Ml; sensu Boletzky, 1977a); and species for which only submature material is available and eggs in the submature ovary are numerous and appear to be of the small-type category. After residence in the plankton of varying duration, octopus paralarvae undergo a dramatic morphological and ecological transition from a free-swimming pelagic animal to the predominantly benthic life of the juvenile stage. The end of the paralarval period varies, dependent on the species and/or the environmental context. some species such as Octopus vulgaris have a relatively short presettlement period during which they rapidly become benthic in habit. other paralarvae have an expanded, transitional presettlement phase split between periods of swimming in the water column and benthic crawling. There is a third category of a prolonged/suspended paralarval state in which some paralarvae reach considerable sizes in epipelagic waters. At the start of this pelagic period, these relatively large, actively swimming young octopuses (<2 cm total length) can be considered planktonic (sensu omori & ikeda 1984) because their power of locomotion is insufficient to prevent them from being passively transported by currents. At the end of this phase, however, they are clearly micronektonic (sensu pearcy 1983, animals 210 cm in total length), attaining the ability to swim freely without being overly affected by currents. Most of our knowledge of octopus paralarvae comes from studies of just two species, O. vulgaris and Enteroctopus dofleini, potentially due to both their fisheries value and their proximity to major centres of scientific research in the Northern hemisphere. At this stage, knowledge of the vast majority of benthic octopus species with planktonic stages is considered rudimentary or nonexistent. This is despite references to octopus paralarvae dating back more than 2300 yr. probably referring to Octopus vulgaris paralarvae of the Mediterranean sea, Aristotle noted that the creature is extraordinarily prolific, for the number of individuals that come from the spawn is something incalculable and they are so small and helpless that the greater number perish. hochberg et al. (1992) drew together published and unpublished data on identification of octopus paralarvae and proposed both a suite of taxonomic characters and a standardized format for morphological description. This work remains the seminal study on identification of octopus paralarva over a wide range of taxa. Boletzky (2003) reviewed recent literature on the early stages of cephalopods, particularly issues of yolk absorption and biological adaptations throughout these early growth stages. A note of caution must be made on species identifications for octopus paralarvae treated in the literature. considerable historical confusion surrounds the taxonomy of adult benthic octopuses (see Norman & hochberg 2005a). similarly, the absence of detailed morphological descriptions for all paralarval species and the lack of appropriate taxonomic tools mean that taxonomic identifications for many studies (particularly those based on wild-caught paralarvae) must be taken as tentative.
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RoGER VillANuEVA & MARk D. NoRMAN Table 1 species of octopodidae known (or likely) to possess planktonic paralarvae: maximum values of egg length (Elmax, in mm) and egg length index (Elimax, egg length as percentage of mantle length)
species Abdopus abaculus Abdopus aculeatus Abdopus tonganus Amphioctopus aegina Amphioctopus arenicola Amphioctopus burryi Amphioctopus exannulatus Amphioctopus kagoshimensis Amphioctopus cf kagoshimensis Amphioctopus marginatus Amphioctopus mototi Amphioctopus neglectus Amphioctopus ovulum Amphioctopus rex Amphioctopus robsoni Amphioctopus siamensis Amphioctopus varunae Aphrodoctopus schultzei Callistoctopus aspilosomatis Callistoctopus lechenaultii Callistoctopus luteus Callistoctopus macropus Callistoctopus nocturnus Callistoctopus ornatus Cistopus indicus Eledone cirrhosa Enteroctopus dofleini Elmax 2.4 3 2.8 2.4 2.7 2.5 3.9 1.8 3.8 3 6 Elimax 7.9 7.2 4 ~4 Reference Norman & Finn 2001 Norman & Finn 2001 Norman & Finn 2001 Norman unpubl. data huffard & hochberg 2005 hochberg et al. 1992 Norman 1992a Norman unpubl. data Norman & kubodera 2006 Norman 1992b Norman 1992a Nateewathana & Norman 1999 sasaki 1929 Nateewathana & Norman 1999 Norman 1992a Nateewathana & Norman 1999 Norman 1992a smith 1999 Norman 1992c Norman unpubl. data Norman & sweeney 1997 Mangold 1998 Norman & sweeney 1997 Norman 1993 Norman & sweeney 1997 Boyle 1983 hochberg 1998 paralarvae hatched in laboratory
Eibl-Eibesfeldt & scheer 1962, ignatius & srinivasan 2006
Forsythe & hanlon 1985
7.3 8.3 4.3 7.8 7
3 3 5.2 1.7 2 7.5
6.5 8.8
1 2.5
3.3 7 small type small type 0.8
Boletzky et al. 2001
small type 3.5 4.5 7.5 8 2.7 3.8 small type small type
Mangold et al. 1971 Gabe 1975, okubo 1979, 1980, Marliave 1981, snyder 1986a,b, and others ortiz et al. 2006 overath & Boletzky 1974 Batham 1957 hanlon et al. 1985
Enteroctopus magnificus Enteroctopus megalocyathus Euaxoctopus panamensis Hapalochlaena lunulata Macroctopus maorum Macrotritopus defilippi Octopus alecto Octopus berenice
7 12 1.4 3.5 7 2.1 2.5 1.5
1.9 0.2
2.7
Villanueva et al. 1991 ortiz et al. 2006 Voss 1971 hochberg et al. 1992 stranks 1996 Mangold 1998 hochberg et al. 1992 hochberg et al. 1992
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs Table 1 (continued) species of octopodidae known (or likely) to possess planktonic paralarvae: maximum values of egg length (Elmax, in mm) and egg length index (Elimax, egg length as percentage of mantle length)
species Octopus bimaculatus Octopus bocki Octopus campbelli Octopus cyanea Octopus favonius Octopus filosus Octopus hawiiensis Octopus hummelincki Octopus huttoni Octopus joubini Octopus laqueus Octopus mimus Octopus parvus Octopus rubescens Octopus salutii Octopus selene Octopus tetricus Octopus tetricus West Australia Octopus veligero Octopus vitiensis Octopus vulgaris Octopus warringa Octopus wolfi Pteroctopus tetracirrhus Robsonella fontanianus Scaeurgus jumeau Scaeurgus nesisi Scaeurgus patiagatus Scaeurgus tuber Scaeurgus unicirrhus Thaumoctopus mimicus Wunderpus photogenicus Elmax 4 2 1.7 2.5 1.8 3 3 3.1 4.8 2.8 3 1.8 4 6 1.6 2.5 2.4 small type small type small type small type 5 3.2 Elimax 9.5 small type 1.7 small type Reference hochberg et al. 1992 Norman & sweeney 1997 oshea 1999 Norman 1991 Norman unpubl. data Voss & Toll 1998 hochberg et al. 1992 hochberg et al. 1992 oshea 1999 Voss & Toll 1998 kaneko et al. 2006 cortez et al. 1995a sasaki 1929 hochberg et al. 1992 hochberg et al. 1992 Voss 1971 hochberg et al. 1992 Norman unpubl. data hochberg unpubl. data Norman unpubl. data hochberg et al. 1992 Norman 2000 Norman unpubl. data Boletzky 1981 hochberg et al. 1992 Norman et al. 2005 Norman et al. 2005 hochberg et al. 1992 Norman et al. 2005 hochberg et al. 1992 Norman & hochberg 2005b hochberg et al. 2006 paralarvae hatched in laboratory Ambrose 1981
Van heukelem 1973
Brough 1965 (as Robsonella australis) Forsythe & Toll 1991 kaneko et al. 2006 Ziga et al. 1997, Warnke 1999, Baltazar et al. 2000, Montoya 2002
Mangold-Wirz et al. 1976
Joll 1976, 1978
small type 2 2.7 3 8.3 5 2.6 1.7 2.5 2.7 2.5 small type small type 9 small type 11 3.6 6.2 small type 3.6 10.1
Naef 1928, Vevers 1961, itami et al. 1963 and others Norman 2000
Gonzlez et al. 2006
Boletzky 1984
Miske & kirchhauser 2006
Note: The list includes (1) species that produce small-type eggs (Eli < 10, sensu Boletzky 1977a), (2) species for which only submature material is available and eggs in the submature ovary are numerous and appear to be of the small-type category and (3) species for which planktonic paralarvae have been described from laboratory hatched individuals.
For such samples that are not directly linked to spawning adult females, there is potential for misidentification or oversimplification of the diversity of taxa represented in a region. As hochberg et al. (1992, p. 245) state, their work: is a preliminary study whose sole purpose is to summarize
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RoGER VillANuEVA & MARk D. NoRMAN the current status of our knowledge. it should not be used as an identification manual without considerable reservation and without further critical study. A number of other octopod families have a completely pelagic life cycle that includes planktonic hatchlings. These include the families Amphitretidae, Vitreledonellidae, Bolitaenidae and the superfamily Argonautoida (Alloposidae, Tremoctopodidae, ocythoidae and Argonautidae). These octopods are represented by approximately 21 species (sweeney & Roper 1998) and have not been included in the present review. Their origins and links to paralarval strategies are discussed in the section permanent paralarvae: neoteny and holopelagic octopuses, p. 182. The aim of the current work is to review available knowledge on all aspects of octopus paralarvae of the benthic octopuses (family octopodidae) and encompasses their diversity, spawning characteristics, morphology, sensory systems, diet, biochemical composition, growth, behaviour, predators, distribution, settlement, biogeography and evolution. This review is also presented as a vehicle for identifying gaps in our knowledge and candidates for future research.
Spawning and hatching characteristics of benthic octopuses with planktonic paralarvae and implications for dispersal
Egg care and duration of embryonic development
in all species of incirrate octopuses (including the benthic octopuses, family octopodidae), the eggs are highly vulnerable to predation (see predators on egg masses and paralarvae, p. 170). The eggs of these octopus groups only have the chorionic membrane protecting the ovum. They lack the additional protective membranes, capsules or jelly masses found in other cephalopod groups (Budelmann et al. 1997, Boletzky 1998). These additional outer layers appear to convey physical and/or chemical protections that enable nautilus, cuttlefish, squid and cirrate octopuses to deposit eggs that require no parental care. All female incirrate octopuses must guard their eggs throughout the developmental period, after which the females die. The female must continuously clean the egg surfaces with her suckers, ventilate the eggs with water flushes from the funnel and protect the eggs from potential predators. The eggs of these octopuses possess a stalk of varying length (the chorion stalk) that is used to attach the egg directly to a hard substratum or can be joined together to form egg strings or festoons (i.e., cosgrove 1993, huffard & hochberg 2005). The eggs are typically attached to hard surfaces in protected shelters such as caves, crevices or mollusc shells but in some groups can be carried directly within the webs of the female (i.e., as in some pygmy species, Forsythe & hanlon 1985; genus Wunderpus, Miske & kirchhauser 2006; genus Hapalochlaena, Norman 2000; and genus Amphioctopus, huffard & hochberg 2005). Females of wholly pelagic octopus families also carry the eggs in a variety of manners: within the arm crown (families Bolitaenidae, Vitreledonellidae, Amphitretidae, Alloposidae), within greatly elongated distal oviducts (family ocythoidae), attached to small mineralized rods (family Tremoctopodidae) or within an encased shell-like capsule (family Argonautidae) (young 1972, Nesis 1987). Eggs laid by octopuses with planktonic hatchlings typically number in the thousands but can reach as high as 500,000 in Octopus vulgaris (Mangold 1983) and 700,000 eggs in O. cyanea (Van heukelem 1983). however, lower numbers of eggs can also be produced by certain species with planktonic hatchlings (i.e., 450 for Wunderpus photogenicus; Miske & kirchhauser 2006). Body size constraints for pygmy octopus species that produce planktonic young also make it likely that egg production for such species would be in the hundreds not thousands of eggs. Within each species-specific range, temperature is the main factor regulating the development of the octopod embryos, which is faster at higher temperatures. For small-egg species of the family octopodidae, the fastest embryo development is found in tropical species. Examples of rapid development are 1820 days for Amphioctopus aegina incubated at 2830c (ignatius & srinivasan 2006), 21 days
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs in Octopus cyanea at mean temperature of 27.1c (Van heukelem 1973), 2225 days in O. vulgaris at 25c (Mangold 1983), 2230 days in O. laqueus at 26c (kaneko et al. 2006) and 23 days at 26c in Wunderpus photogenicus (Miske & kirchhauser 2006). in contrast, cold-adapted species have much longer embryo development, as found in the giant octopus Enteroctopus dofleini from the north pacific, which shows the longest known egg incubation period for an octopus species with planktonic hatchlings, lasting 161 days at 9.213.9c when the female tends the eggs (Gabe 1975) and up to 56 months at 9.413c when the eggs are incubated experimentally without the female in breeder nets (snyder 1986a, s. snyder unpublished manuscript). For Eledone cirrhosa, 34 months at 1418c are necessary for hatching (Mangold et al. 1971).
The hatching process and dispersal

Stimulus for hatching When an octopus embryo is fully developed inside the egg and apparently ready to hatch, the physiological mechanism(s) that promote the hatching process are unknown. A natural tranquillizer described in the perivitelline fluid of loliginid squid prevents premature hatching (Marthy et al. 1976); however, its presence in octopus eggs has not been assessed. Mechanical stimulation provided by the brooding female may aid or regulate the timing of hatching but no quantitative studies have been done on this subject. During hatching, brooding females sometimes forcibly expel water through the funnel over the eggs (sarvesan 1969, kaneko et al. 2006). This turbulence may act as a stimulus to instigate hatching. During laboratory incubation of eggs without female care, hatching predominantly occurred after agitation as has been observed for Octopus cf tetricus (Joll 1978 as O. tetricus) and Enteroctopus dofleini (snyder 1986a). Mechanics of hatching laboratory observations on Octopus bimaculatus showed prehatching individuals pumping energetically in their egg cases prior to hatching (Ambrose 1981). To escape the chorion membrane, rapid mantle contractions by the embryo may mechanically put pressure on the chorion membrane or it may ensure that the hatching gland is pressed firmly against the inner wall of the chorion to ensure direct application of the enzymatic solution released from this gland (see description p. 118). Active use of the arms and suckers has also been observed in some species such as Scaeurgus unicirrhus (Boletzky 1984). After the enzymatic secretions of the hatching gland dissolve and hence perforate the chorion membrane, the klliker organs also probably help to prevent the retraction of the emerging octopus back into the egg capsule during hatching (Naef 1923, Boletzky 1966) (see surface epithelia and integumentary structures, p. 116). The hatching period can take up to 44 min to complete under laboratory conditions in Octopus tetricus (le souef & Allan 1937 as O. cyanea). A schematic drawing of the hatching process is given in Figure 2. Timing of hatching In situ observations found that hatching occurred at night or in darkened conditions in egg masses of Enteroctopus dofleini at 1724 m depth (cosgrove 1993), whereas daytime hatching was observed for paralarvae of Octopus bimaculatus, swimming upwards and reaching depths of 15 m below the surface (Ambrose 1981). under laboratory conditions, paralarvae of O. cyanea hatch only at night (Van heukelem 1973) and both day and night hatching has been observed in O. cf tetricus (Joll 1978). in addition to embryonic rhythms, species-specific differences in the timing of hatching may be influenced by adult rhythms. Mechanical stimulation provided by the brooding female on the egg mass may differ between nocturnal and diurnal species, making maternal activity an unquantified factor in the hatching process. under laboratory conditions, non-brooding adult O. vulgaris prefer
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RoGER VillANuEVA & MARk D. NoRMAN
Figure 2 line drawing showing the hatching process in Octopus vulgaris. The hatching gland (or hoyles organ) is present on the distal tip of the mantle and the glandular cells are limited to a narrow transverse band. The hatching gland and the klliker organs covering the body surface have been emphasized to show position and orientation. see text for details. (original drawing from Jordi corbera with permission.)
nocturnal activity patterns (Brown et al. 2006) and for this species most hatching events occur at night (R. Villanueva personal observation). paralarval hatching in cephalopod species without maternal care, as in the squid Loligo vulgaris, is influenced by the transition from light to dark, which seems to function as a zeitgeber or synchronizer, stimulating hatching (paulij et al. 1990). The attraction of visual fish predators to the brooding octopus site may prevent major hatching during daytime, selecting for night hatching to avoid predation (Van heukelem 1973), as has been observed in other invertebrate larvae such as the hatching of decapod crustacean zoeae (Forward 1987, Ziegler & Forward 2005, 2006). The tendency for sunset and nocturnal hatching in octopus paralarvae needs to be confirmed and quantified, with the influence of tidal and lunar rhythms taken into account. similarly, the roles of external synchronizers and circadian rhythms in adult octopuses are poorly known (houck 1982, Wells et al. 1983a, cobb et al. 1995a,b, Brown et al. 2006, Meisel et al. 2006) but future research on this field may shed light on the potential links between female brooding behaviour and the timing of hatching. Hatching duration within an egg mass The hatching period from a single egg mass can be rapid (i.e., hours), continue over a few days or for weeks, influenced by factors such as the duration over which the eggs were laid, the incubation
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs temperature and the species. Egg laying under aquarium conditions in temperate and tropical species takes 10 days at 18.220c in Octopus luteus (Arakawa 1962), 47 days at 2127c (caverivire et al. 1999) and 9 days at 1719c in O. vulgaris (iglesias et al. 2004). in cold water species, it takes 14 days at 9.210.3c (Gabe 1975) and 20 days at 15.2c (yamashita 1974) for Enteroctopus dofleini, and for Eledone cirrhosa, it can take from 8 days (Joubin 1888), to 1015 days at 14c (Mangold et al. 1971) or nearly 1 month (Gravely 1908). As a consequence of these diverse egglaying periods a single octopus egg mass can contain eggs in different developmental stages. The duration of the hatching period of a single egg mass observed under laboratory conditions ranges from 2 days at 26c in Octopus laqueus (kaneko et al. 2006) to 78 days at 1012.8c for Enteroctopus dofleini (Gabe 1975). Examples of duration of hatching period from a single egg mass in octopodidae species with planktonic hatchlings are listed in Table 2. The times listed are likely to be underestimates for all species as there have been no laboratory or field studies undertaken that collected and quantified the daily hatching rate for these species. They probably underestimate minor hatchings at the beginning and end of the hatching period. Advantages and disadvantages of a single major hatching event in comparison with minor events spread over days to weeks have not been quantified for cephalopods and, again, further research is required. Experimental designs under laboratory conditions to quantify hatching should minimize observer influence as much as possible. Variations in light regimes, degree of exposure of study animals (i.e., removal of protective cover to allow observation can unnaturally expose the brooding octopus), observer behaviour, use of flash photography, mechanical vibrations and temperature fluctuations may all act as hatching stimuli for the embryos, causing or altering hatching processes. Wild brooding females disturbed by human observers may also cause premature hatching through increased light levels, increased water turbulence around the egg mass and behavioural responses by the female. use of remote low-lightlevel videography may be a promising avenue for investigating natural hatching processes.
Morphological characteristics of planktonic octopus paralarvae

At hatching, the external attributes of octopus paralarvae are distinctive and often markedly different from that of post-settlement juveniles and the first growth stages of species with benthic hatchlings. All inner organs of planktonic octopus paralarvae are well differentiated at hatching except for the reproductive system. however, there are few data on the development of the digestive, circulatory, respiratory, excretory and muscular systems after hatching and prior to settlement. Most information comes from embryological studies on prehatching and hatchling individuals and has been reviewed by Boletzky (1989). The surface epithelia, integumentary structures, nervous and sensory systems of the paralarvae also have been the object of research and the present knowledge is reviewed. The order of morphological and anatomical characters in this section follows Budelmann et al. (1997).
Body form and musculature

one of the most evident attributes of octopus paralarvae is their largely transparent form. All musculature is transparent including those of the mantle, head, arms, webs and suckers. This transparency is not visible in preserved material as the musculature becomes opaque on fixation. This transparency matches the planktonic lifestyle of the paralarvae, minimizing their silhouette, and hence visibility, to predators (and prey) below. No studies have examined the microscopic structure of the transparent musculature of octopus paralarvae. The mantle musculature of some holopelagic octopods contains thin outer layers of longitudinal and circular muscle enclosing a thick layer of transparent gelatinous matrix supported by narrow strands of radial muscle (e.g., Amphitretus,
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RoGER VillANuEVA & MARk D. NoRMAN Table 2 Duration of hatching period from a single egg mass in octopodidae species with planktonic hatchlings
hatching duration (days) 3 3 Amphioctopus burryi Enteroctopus dofleini 10 39 49 78 30 27 45 <7 10 29 14 Temperature (c) during hatching Np 2830 2324 12.515.3, mean 13.9 47 1012.8 14 Np 913 Np Np 26 16, 20 and 24 19 21 22.6 20 2223 2127 1719 Np 26 laboratory or field observation laboratory laboratory laboratory laboratory laboratory laboratory laboratory laboratory laboratory Field laboratory laboratory laboratory Eggs incubated without female
species Amphioctopus aegina
comments
Reference sarvesan 1969 (as Octopus dollfusi) ignatius & srinivasan 2006 Forsythe & hanlon 1985 okubo 1973 Ruggieri & Rosenberg 1974 Gabe 1975 okubo 1979 okubo 1980 snyder 1986a, unpublished cosgrove 1993 Batham 1957 kaneko et al. 2006 Warnke 1999
Eggs incubated without female
Eggs incubated without female
Macroctopus maorum Octopus laqueus Octopus mimus
75% hatched in 1 h of the same day No differences between temperatures
Octopus cf tetricus
28 6 10 815 612 38 5 21 3
laboratory
Joll 1976
laboratory laboratory laboratory Field laboratory laboratory
Eggs incubated with and without female
Joll 1978 Vevers 1961 caverivire et al. 1999 caverivire et al. 1999 Brough 1965 (as Robsonella australis) Miske & kirchhauser 2006
Octopus vulgaris
Octopus huttoni Wunderpus photogenicus Note: Np, not provided.
Haliphron, Mangold et al. 1989). A similar arrangement is likely to be present in octopus paralarvae but as yet the histological structure of the musculature of these animals has not been examined. General body proportions of octopus paralarvae vary throughout paralarval growth (Figure 3) and between species. At hatching, planktonic octopuses are squat with arms shorter than Ml. see hatchlings in Figures 1B, 3A, 17A,D, 26, 27 and 41. A smaller proportion of species have paralarvae with arms longer than Ml, particularly micronektonic paralarval stages (Figure 4). The relative length of different arm pairs also varies between some species and can be diagnostic at a generic level (hochberg et al. 1992). For example, some paralarvae have arms of equivalent length (Figure 3, 6A),
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Figure 3 (see also colour Figure 3 in the insert.) individuals of Octopus vulgaris from hatching to settlement obtained from rearing experiments described in Villanueva (1995). images not to scale. Age (days) and mantle length (Ml) of the individuals measured fresh are (A) 0 days, 2.0 mm Ml; (B) 20 days, 3.0 mm Ml; (c) 30 days, 4.3 mm Ml; (D) 42 days, 5.9 Ml; (E) 50 days, 6.6 mm Ml; (F) 60 days, 8.5 mm Ml. octopuses from this experiment settled between 47 and 54 days. individuals were photographed under anaesthesia (2% ethanol) potentially causing chromatophore contraction in some cases. (photos by Jean lecomte, observatoire ocanologique de Banyuls, cNRs. Reproduced with permission from Villanueva et al. 1995, modified.)
those of the genus Callistoctopus possess longer dorsal arm pairs (Figure 4A,B), the second pair is the longest in Euaxoctopus (Figure 5), whereas Macrotritopus defilippi paralarvae possess a longer third arm pair (Figure 6, right), as do certain unidentified paralarvae (Figure 4B,c). sucker number, arrangement and relative size can also be used to separate species (hochberg et al. 1992). At hatching there are typically few suckers (three or four) present in a single straight row. During growth suckers are added, with the double row gradually becoming apparent for genera such as Octopus, Enteroctopus and Callistoctopus. Genera such as Eledone retain the single row of suckers into adulthood. The body form and transparency of octopus paralarvae show strong parallels with a number of holopelagic octopuses (families Bolitaenidae, Vitreledonellidae and Amphitretidae) and squids (family cranchiidae) (see permanent paralarvae: neoteny and holopelagic octopuses, p. 182).
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Figure 4 (see also colour Figure 4 in the insert.) Micronektonic octopus paralarvae. Top, unidentified paralarva of the genus Callistoctopus from the coral sea, Australia, showing longer dorsal arm pair. (photos: David paul.) centre, unidentified paralarva (Macrotritopus sp.?) from hawaii showing long arms relative to body length, particularly the third pair. (photos: chris Newbert.) Bottom, unidentified paralarva from hawaii. (photos: Jeffrey Rotman.)
Surface epithelia and integumentary structures

Chromatic elements As with many other cephalopods, octopuses possess three major chromatic elements within the skin chromatophores, iridophores and leucophores that produce the different chromatic patterns that play such important roles in octopus behaviour (packard & hochberg 1977, hanlon & Messenger 1996, Messenger 2001). chromatophores are the primary chromatic element present in the skin of octopus paralarvae. These organs are flexible pigment pouches surrounded by radiating musculature. in the relaxed state, the elastic pigment sacs are tiny and effectively invisible within the transparent musculature (Figure 7, left). contraction of the radial muscles surrounding the pigment sac causes it to expand significantly, resulting in display of a relatively large visible disc of colour (Figure 7, right). in adult cephalopods, chromatophores of up to five colours are present in the skin at densities of up to 200 mm2 (packard & sanders 1969), enabling presentation of complex
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs chromatic displays (hanlon & Messenger 1996). in octopus paralarvae, chromatophore numbers are typically low and they are relatively large in proportion to body size. chromatophores of just one or two colours (red and black) are typically present, enabling expression of relatively simple colour patterns, that is, uniform colour versus transparency (contracted chromatophores). At hatching, octopus paralarvae possess a low number of large chromatophores, present in fixed arrangements. They are known as founder chromatophores and their mode of growth and development is described in packard (1985). patterns and positions of these founder chromatophores can have taxonomic value and Figure 5 Euaxoctopus panamensis, 11-mm mantle enable species identification (hochberg et al. length (Ml). Note the large second arm pair, measur- 1992). The number and distribution of chroing 32 mm long. collected using isaacs-kidd midwater matophores on the skin over the arms, funnel, trawls (ikMT) between 0 and 500 m depth, 09N 90W, eyes, head, mantle and perivisceral epithelium off costa Rica, eastern pacific. (Reproduced with per- (i.e., chromatophore fields) of octopus paramission from Nesis & Nikitina 1991, modified.) larvae can be used to separate species (young et al. 1989, hochberg et al. 1992) (Figure 8). Founder chromatophores remain relatively unchanged throughout ontogenetic growth and are still visible subdermally in post-settlement animals in the same patterns of dark and dense chromatophores. These chromatophores are particularly evident in adults of pygmy octopus species and can be diagnostic to species level (i.e., Octopus bocki and O. wolfi) (Norman & sweeney 1997). Reflective tissues (iridophores) are not typically evident in the skin of octopus paralarvae, particularly in the earliest stages. They are present, however, in the membranes enclosing the eyes and viscera, providing a reflective surface to these opaque body organs as an additional ambient light reflector appropriate for a pelagic environment (Figure 4 bottom). small spots of dermal iridescence are evident in some paralarvae, potentially produced from the bristles of the klliker organs (described in the section klliker organs, p. 120) (e.g., unknown species; Figure 9). in some late-stage paralarvae, potentially close to settlement, iridescence is visible in the position of the ocellus that is found in ocellate species (e.g., unidentified Amphioctopus sp.; Figure 9). leucophores are white-reflecting components of cephalopod skin. They are not typically evident in the skin of octopus paralarvae.
Figure 6 (see also colour Figure 6 in the insert.) unidentified paralarva from the coral sea, Australia, showing arms of equivalent length (left). (photo: David paul.) paralarva of Macrotritopus defilippi from caribbean sea showing longer third arm pair (right). (photo: Raymond hixon.) 117
Figure 7 (see also colour Figure 7 in the insert.) chromatophores contracted (left) or expanded (right) on the head of paralarvae. The left image corresponds to an unidentified paralarva of unknown genus and the right image is from an unidentified paralarva of the genus Callistoctopus. Both individuals from coral sea, Australia. (photos: David paul.)
A AB F AVM VH DE DH
ADM V DM
VM A PC
Figure 8 Distribution of chromatophore fields in octopodidae. (A) left lateral view, optical section; (B) dorsal view; (c) ventral view. superficial or tegumental chromatophores are represented by stippled spots. A, arm; AB*, arm base; ADM, anterior margin of dorsal mantle; AVM, anterior margin of ventral mantle; DE*, dorsal eye; Dh*, dorsal head; DM, dorsal mantle; F, funnel; pc, posterior cap; V*, visceral; Vh*, ventral head; VM, ventral mantle. Extrategumental chromatophores are indicated by (*). (Reproduced with permission from hochberg et al. 1992.)
As with iridophores, these structures may be evident in paralarvae close to settlement. The simple chromatic capacities of planktonic octopus paralarvae show a stark contrast with the complex skin and capacities of the benthic hatchlings of octopus species with large eggs (e.g., Hapalochlaena maculosa, Figure 10). Hatching gland The hatching gland or hoyles organ is located at the posterior tip of the mantle (Figure 2). The enzymatic action of this gland helps the octopus during the hatching process by dissolving the apical pole of the chorion membrane. it is assumed that there is a protease hatching enzyme similar to that described in squids (paulij et al. 1992) although its presence in octopods has not been investigated.
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Figure 9 (see also colour Figure 9 in the insert.) iridescence in octopus paralarvae. left, unidentified paralarva showing scattered points of iridescence, potentially from klliker organs in skin. Right, Amphioctopus sp. paralarva showing iridescent tissue in location of ocelli of ocellate octopuses. Both individuals collected while night diving on a moonless night at ~10 m deep over a seafloor depth of 450 m at osprey Reef, coral sea, Australia. photographs taken in shipboard aquaria immediately after capture. (photos: M.D. Norman.)
Figure 10 (see also colour Figure 10 in the insert.) Hapalochlaena maculosa hatchling, a direct benthic species, showing well-developed skin colour and sculpture. (photo: David paul.)
in embryos that do not execute the second reversion (Boletzky & Fioroni 1990), the hatching gland also helps the animal to hatch via the opposite pole, adjacent to the egg stalk (Boletzky 1966). in incirrate octopods, the glandular cells of the hatching gland are limited to a narrow transverse band (orelli 1959, Fioroni 1978, Boletzky 19781979, Boletzky 1982). The two different cell types and structure described for the hatching gland of loliginid squids (Arnold & singley 1989, paulij & Denuc 1990) have not been observed. in addition to the chemical effects of the hatching gland enzymes, the hatching process is aided by mechanical effort through powerful stroke movements of the mantle that enables the animal to free itself from the chorion membrane (Figure 2). Active movements of the arms and suckers have also been observed for Scaeurgus unicirrhus (Boletzky 1977b, 1984). There are no quantified
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RoGER VillANuEVA & MARk D. NoRMAN studies on the duration of the hatching process. in Octopus tetricus individuals can take up to 44 min to hatch under laboratory conditions (le souef & Allan 1937, as O. cyanea). The hatching gland is a transitory organ. soon after hatching the gland is shed along with the rest of the embryonic epidermis and its many ciliated cells (Budelmann et al. 1997). Klliker organs klliker organs are bristle-like structures present on the surface of the head, arms, funnel and mantle of embryos, paralarvae and recently settled octopus individuals, giving the animals a punctate appearance (Figures 11 and 12). These organs are only found in incirrate octopods, including individuals of some octopus species with direct benthic hatchlings such as Eledone moschata (Naef 1923, Boletzky 1973). First described by klliker (1844) from Argonauta embryos, they have also been described by other authors (Querner 1927, Naef 1928, Adam 1939, Fioroni 1962, Boletzky 19781979, Joll 1978). Detailed description of the histology and ultrastructure of the klliker organs can be found in Boletzky (1973) and Brocco et al. (1974). These organs consist of three structural components (Figure 13): (1) an ectodermal follicle of specialized cells, (2) an extracellular fascicle of cannular rodlets secreted by the basal chaetoblast and (3) mesodermal muscles. These muscles presumably help to evaginate the fascicle and spread the rodlets (Figure 13A). The length of the klliker organs is relatively constant in preserved specimens (3040 m) for species with very different hatchling size, representing 4% of the Ml in Argonauta argo and 0.4% in Eledone moschata. Their density in planktonic paralarvae is, however, higher than in benthic juveniles (Boletzky 1973). in paralarvae of some species, high densities of klliker organs have been found on the ventral surface of the head (young et al. 1989). During hatching, the combined effect of mantle movements and the presence of klliker organs help the animal to move in one direction and exit the chorion membrane (Naef 1923, Boletzky 1966, 19781979). This does not seem to be the sole function of these organs. For captive-reared Octopus vulgaris, klliker organs have been recorded from hatchling through to settlement, and on the distal portion of the arms in pre- and post-settlement paralarvae, indicating the addition of new organs after hatching and during the entire planktonic phase (Villanueva 1995) (Figure 11Fh). After hatching, the primary function of the klliker organs during the planktonic phase remains unknown and many hypotheses have been proposed for these amazing structures. As klliker organs in the expanded form can increase the body surface of the animal, it has been hypothesized that they may help in some passive mode of planktonic transport (Naef 1923, Boletzky 1973); however this use seems doubtful in large planktonic animals due to the small size of the organs relative to body size. Alternatively, due to the shining appearance of the everted fascicles in live individuals observed under a binocular microscope (R. Villanueva personal observation), it is possible that light reflection could produce defensive counter-shading or crypsis in the water column. klliker organs are transitory structures because there are no reports of their presence in subadult and adult benthic octopuses and it is unknown how they are transformed and/or degenerate in the octopus skin after settlement. Naef (1923) suggests that klliker organs form the basis for the formation of the juvenile and adult skin warts or skin papillae. klliker organs have been reported in subadult pelagic octopods Bolitaena and Eledonella (chun 1902 in Adam 1939), suggesting that these organs may have a function related to a planktonic/pelagic lifestyle (see permanent paralarvae: neoteny and holopelagic octopuses, p. 182). Integumental pores and glandular cells pores of different diameter have been observed on the epidermis of the arms, head, funnel and mantle of hatchling paralarvae and these appear related to glandular cells (young et al. 1989, lenz et al. 1995). in laboratory-hatched individuals of Octopus cyanea, densities of these pores (5 m
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs A B
Figure 11 klliker organs in Octopus vulgaris throughout planktonic stage. scanning electron microscope images of individuals collected during rearing experiments described in Villanueva (1995). (A) oral view of 19-day-old individual 3 mm mantle length (Ml) measured fresh. Note the porcupine aspect of the body due to the emerged fascicles of the klliker organs on the skin. (B) left ventrolateral view of 30-day-old individual, 4.8 mm Ml (fresh). Note the density of klliker organs on the mantle. The hole near the mantle margin is due to handling using forceps. (c) left lateral and (D) ventral views of 50-day-old individual, 7.3 mm Ml (fresh). Note the density of emerged klliker organs radiated on the ventral mantle, mantle margin, funnel and near the eye. (E) Right lateral view of 50-day-old individual, 6.5 mm Ml (fresh), showing klliker organs near the tip of the fourth right arm (F), on the middle of third right arm (G) and a radiated fascicle near the tip of the left third arm (h). Both individuals aged 50 days were in presettlement stage. All individuals were killed following anaesthesia in 2% ethanol and lowered water temperature (34c), then fixed in 5% buffered formalin. original.
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RoGER VillANuEVA & MARk D. NoRMAN A B
Figure 12 klliker organs in Enteroctopus megalocyathus hatchling paralarvae. individuals collected during rearing experiments described in ortiz et al. (2006). scanning electron microscope images from ventral (A) and lateral (B) views. Note the density of klliker organs on the mantle, head and arms and the ventral mantle. (c) skin surface of the ventral mantle showing klliker organs and cilia (D) observed inside the rectangle. (E) klliker organs from ventral mantle in different degrees of expansion. (specimens kindly provided by N. ortiz, centro Nacional patagnico, coNicET.) original.
in diameter) represented 10% of the skin surface for some areas but these high densities were not observed in field-collected specimens (young et al. 1989). The pores have small spheres in the apertures that may be the secretory products of these potential mucus-secreting cells (Figure 14). Sucker surfaces in hatchling octopus paralarvae the main features of the outer surface of the suckers resemble that of the adults (Nixon & Dilly 1977, kier & smith 1990). The infundibulum of the suckers has numerous flattened pegs that are already endowed with minute pores (Figure 15) (schmidtberg 1997, 1999). pegs may provide friction to aid the suckers in attaining suction adhesion. however, as observed in hatchlings of Octopus vulgaris (schmidtberg 1999) and O. cyanea (young et al. 1989), the infundibulum is encircled by a plain rim and lacks the circumferential marginal folds that surround the infundibulum in suckers of adult individuals or hatchlings of direct benthic species such as Eledone moschata (schmidtberg 1997, 1999). These circumferential marginal folds may aid formation of a tight seal (Nixon & Dilly 1977, kier & smith 2002), suggesting that the suction process in hatchling octopus paralarvae is not as effective as in adults or hatchlings of directly benthic species (schmidtberg 1997, 1999). Sculptural components Adult benthic octopuses are renowned for their camouflage and background-matching abilities. Beyond chromatic components, this disguise is aided by sculptural components: papillae (branched
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E C A B C
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Figure 13 klliker organ from the skin of Octopus sp. hatchling paralarvae. (A) scanning electron microscope image of a radiated fascicle showing the rodlets and three new fascicles (white arrows) beginning to emerge. scale 30 m. (B) longitudinal section of an emerged fascicle, transmission electron microscope image. scale 5 m. inset, section through a microvillus of the chaetoblast that inserts into the basal end of a rodlet. inset scale 0.5 m. (c) Diagram of an everted fascicle. c, chaetoblast; E, epidermal cell; l, lateral follicular cell; M, obliquely striated muscle; R, rodlet. (Reproduced with permission from Brocco et al. 1974.)
Figure 14 integumetal pores and glandular cells. scanning electron microscope images of Octopus cyanea hatchlings showing (left) the pores on the arm tips (scale 0.1 mm) and (right) the oral surface of the arm showing the pores and the secretory spherules (scale 0.01 mm). (Reproduced with permission from young et al. 1989.)
or unbranched), skin flaps and raised ridges (i.e., lateral mantle ridge) (Figure 16). in stark contrast to benthonic hatchlings (Figures 1D and 10) and adults, octopus paralarvae lack any evidence of these components, even in the largest forms (Figure 4). Loose skin film in some species, an unpigmented, transparent, loose skin layer has been observed to cover the body of the whole animal (Figure 17). hatchlings of Enteroctopus megalocyathus observed under a binocular microscope show a transparent skin film densely surrounded by klliker organs and covering the mantle, funnel, head, arms and eyes (ortiz et al. 2006) (Figure 17D). observations using scanning electron microscopy (sEM) do not reveal this layer, instead showing the direct surface of the skin (Figures 12 and 23). This may be an artefact of the fixative process required for electron
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Figure 15 sucker structure of Octopus vulgaris hatchling paralarvae. (A) sagittal section of the sucker, stained with haematoxylin and eosin. scanning electron microscope images showing the whole suckers (B) and infundibulum (c). c, cuticle; i, infundibulum; p, peg or projection of cuticular process of infundibulum; R, rim. (Reproduced with permission: (A) from Nixon & Mangold 1996, (B) and (c) from schmidtberg 1997.)
Figure 16 (see also colour Figure 16 in the insert.) Adult Octopus cyanea in camouflage display amongst soft corals, puerto Galera, philippine islands. (photo: Gunther Deichmann.)
microscopy. The presence of a similar loose skin structure has also been reported for laboratoryhatched E. dofleini by Green (1973, p. 39), noting that The lateral sides of each arm were outlined with a transparent web. kubodera & okutani (1981, p. 149) noted that wild paralarvae of the same species had a body all covered with gelatinous tissue which is more prominent in smaller specimens. kubodera (1991) also showed that this loose skin layer is not only related to the hatchling stage but also present during paralarval growth (Figure 17B). in addition to the genus Enteroctopus,
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Figure 17 skin film in Enteroctopus. (A) Dorsal views of E. dofleini hatchling (scale 1 mm) and (B) a 14 mm mantle length individual (scale 5 mm). (c) lateral view, scale 1 mm. (D) Ventral view of newly hatched E. megalocyathus after preservation in formaldehyde showing the skin film covering the whole animal (scale 2 mm). (Reproduced with permission: (A) from Green 1973, (B) from kubodera & okutani 1981, (c) from kubodera 1991, (D) from ortiz et al. 2006.)
the loose skin film also seems to be present in Octopus bimaculatus from the eastern north pacific (from drawings of hochberg et al. 1992; their Figure 257) and in the Macrotritopus defilippi species complex from hawaiian waters (hochberg et al. 1992; their Figures 260 and 261). Diekmann et al. (2002) drew this structure for Argonauta argo and for an undetermined species of Octopus sp. collected in the subtropical eastern north Atlantic. A parallel supradermal skin layer is also found in three families of oceanic squids: octopoteuthidae, cycloteuthidae and Bathyteuthidae (Voight et al. 1994). A number of other soft-bodied pelagic cephalopods possess a gelatinous subdermal layer within the skin. These taxa include pelagic octopods such as Amphitretus, Haliphron and the deep-sea cirrate octopods, and squids including Mesonychoteuthis and Chiroteuthis (Mangold et al. 1989). The function of such a gelatinous layer (supra- or subdermal) is unknown but it is possible that its gelatinous matrix is more buoyant than seawater (as in scyphozoans) or contains buoyant ammonia solution. it is possible that such layers are used to attain neutral buoyancy, potentially aiding passive paralarval dispersion. The bristles of the klliker organs in octopus paralarvae may also play a role in anchoring the loose skin film to the body surfaces. The microscopic structure of this loose skin film in octopus paralarvae and its relationship to the integument needs to be examined in detail and its characteristics described in live animals. live animals should be observed and killed under controlled conditions to avoid possible premortem stress and/or fixative artefacts that may influence the general skin attributes in the preserved animal.
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Sensory systems
Central nervous system The nervous system of paralarvae matches the general pattern described for adults (young 1971, Wells 1978) but it is comparatively larger by volume. The brain, penetrated by the oesophagus, consists of two large components, the supra- and the suboesophageal masses, each subdivided into brain lobes (Figure 18). The brain of Octopus vulgaris hatchlings has been estimated to weigh 0.2 mg (20% of the total body weight of the animal); addition of the eight brachial ganglia and eyes results in the nervous system representing approximately one quarter of the paralarval fresh weight (packard & Albergoni 1970). The relative proportions of the lobes of the paralarval brain are markedly different from those of juveniles or adults. in O. vulgaris and Eledone cirrhosa these differences have been related to morphological development and changes in mode of life (Frsch 1971, Marquis 1989, Nixon & Mangold 1996, 1998, Nixon & young 2003). For example, at hatching the buccal and basal lobes are larger than in juveniles, while the brachial lobes are smaller. Brachial lobes, which represent 8% of the total volume of the brain, increase to 13% at settlement, coinciding with the rapid growth of the arms and suckers and the development of the tactile sense that is characteristic of the octopuss benthic life, reaching 18% in the adult (Nixon & Mangold 1996). The reduced brachial lobe seems to be an attribute of octopod planktonic life because Amphioctopus ocellatus, a species with direct benthic hatchlings, has a brachial lobe that represents 15% of the brain volume at hatching (yamazaki et al. 2002). in general terms, the sensory systems of octopus paralarvae show adult-like characteristics, with the exception of the lateral line system, the presence of which has not been reported for adult octopods. The main sensory system components are treated individually below. Photoreceptors Eye photoreceptors The eyes of octopodid paralarvae are located laterally and directed slightly forward. During the planktonic stage there is a relatively slight increase in eye diameter relative to the head and mantle in reared Octopus vulgaris (Villanueva 1995). Adult octopuses are blind to colour (Messenger 1977) and sensitive to polarized light (Moody & parriss 1961, shashar & cronin 1996). These attributes can probably be extended to paralarvae but no experimentation has been done in this respect. Eye receptors of young octopus have been described for species with benthic hatchlings, including O. australis and O. pallidus (Wentworth & Muntz 1992), showing that by the time of hatching all relevant components of the visual system are recognizable in their essentially adult form (see reviews by Budelmann et al. 1997, Nixon & young 2003). however, further differentiation and growth takes place. There is little information on the vision of planktonic octopuses. unpublished observations (A. Bozzano, institut de cincies del Mar) showed that the eyes of
DG SM
ST
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Figure 18 sagittal section of hatchling Octopus vulgaris. DG, digestive gland; F, funnel; s, sucker; sM, supraoesophageal mass; sT, statocyst. (Reproduced with permission from Nixon & Mangold 1996, modified.) 126
l L LB
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Figure 19 Transversal section of the eye of Octopus vulgaris hatchling, stained with toluidine blue. BM, basal membrane; i, iris; l, lens; lB, lentigenetic body; p, photoreceptors; pl, plexiform layer; pN, photoreceptor nuclei; sN, supporting cell nuclei. photo courtesy of Anna Bozzano.
Octopus vulgaris are also completely formed at hatching and the retina already shows all the adult differentiated retinal layers (Figure 19). in the hatchling eye, it is possible to distinguish the iris and the lentigenic body as well as the fully developed lens. The photosensitive retina consists only of rod-like photoreceptors and supporting cells. A basement membrane separates the supporting cell nuclei from the photoreceptor nuclei. The plexiform layer, posterior to the photoreceptor nuclei, contains the synaptic processes of the photoreceptors and the efferent fibres from the brain lobes. These structures contribute to the formation of the optic nerve collecting fibres at the back of the eye. Photosensitive vesicles in addition to the normal retinal photoreceptors of the eyes, most cephalopods have small groups of photoreceptors located external to the eyes; these have been termed the extraocular photoreceptors or photosensitive vesicles (Mauro 1977). in adult stages of benthic and pelagic octopods the photosensitive vesicles consist of a single pair of organs located inside the mantle cavity (Nishioka et al. 1962, young 1978). Each organ is a spherical vesicle attached to the posterior margin of each stellate ganglion, recognizable as an orange spot in Eledone cirrhosa (cobb et al. 1995a,b) and colourless in Octopus vulgaris (Mauro 1977). The presence of photosensitive vesicles has been recorded in developed embryos of O. vulgaris (Marquis 1989) but their development throughout planktonic life is unknown. The function of these vesicles remains enigmatic in benthic octopods although it seems to be related to regulation of circadian activity (cobb et al. 1995a,b, cobb & Williamson 1998, 1999). Mechanoreceptors Statocysts and statoliths The two sphere-like, membranous statocysts are situated in cavities of the cranial cartilage. They consist of fluid-filled spaces each containing a mineralized statolith borne on receptor hairs. Their mechanoreceptors respond to mechanical stress caused by a relative movement between receptor hair cells, the statoliths and the surrounding medium (Budelmann et al. 1997). The octopod statocyst has been the subject of detailed research in adult individuals (young 1960, Budelmann et al. 1973, Budelmann 1977, Budelmann & young 1984, Budelmann et al. 1987). statocysts in O. vulgaris hatchlings are relatively large and their anterior-posterior length represents 32% of Ml in fixed specimens, then decreasing to 11% of Ml after settlement (Nixon & Mangold 1996) (Figure 18). Octopus vulgaris hatchling statocysts were analysed histologically by Bllow &
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Figure 20 statoliths of Octopus vulgaris paralarvae. scanning electron microscopic images from anterolateral (A) and posterior (c) views of hatchling statoliths with their respective crystalline surface structure presented inside the rectangles (B, D). in paralarvae aged 30 days, statolith growth is observed on the posterior side of the statolith (E, F). The crystalline structure of the surface observed inside the lower (G) and upper (h) rectangle of the image F is also indicated. individuals obtained from rearing experiments described in Villanueva et al. (2004). original.
Fioroni (1989) indicating that, in comparison with the adult statocysts, the cartilaginous capsules lack the detached epithelium that probably lies within the cartilaginous layer. The crista statica is divided into three parts and the anticristae are absent. colmers et al. (1984) describe neuroepithelial structures of the statocyst and statoliths of species with benthic hatchlings in O. maya and O. sp. (reported as O. joubini). The statoliths of O. vulgaris hatchlings (Figure 20AD) have a hemispherical shape that corresponds to the knob present on the peak of the limpet-shaped statoliths of adult individuals of octopodidae, as observed in O. vulgaris (young 1960, sakaguchi 2006), Eledone cirrhosa (clarke 1978), Enteroctopus magnificus (Villanueva et al. 1991) and E. dofleini (ikeda et al. 1999). The hatchling or natal statolith can be recognized externally on the adult statolith as its size is nearly constant and is independent of the sizes of the adult body or statolith (sakaguchi 2006). After hatching, statolith growth takes place on the posterior side of the statolith, as observed in laboratory-reared O. vulgaris paralarvae aged 1 month (Figure 20Eh). Lateral line system ciliated primary sensory hair cells, sensitive to local water movements, are arranged in epidermal lines located on the arms, head, anterior part of the dorsal mantle and funnel in O. vulgaris hatchlings (lenz et al. 1995, lenz 1997). The epidermal line runs in an anterioposterior direction. The dorsal, dorsolateral, ventrolateral and ventral lines are paired, occurring on
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VL VLL FL
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Figure 21 Epidermal lines in Octopus vulgaris hatchling paralarvae. (A) schematic drawings showing the course of the epidermal lines (indicated by dotted lines) from dorsal (left), ventrolateral (central) and ventral (right) views. Dl, dorsal line; Dll, dorsolateral line; Fl, funnel line; Vl, ventral line; Vll, ventrolateral line. (B) scanning electron microscope (sEM) image from the lateral view of the head showing the dorsal, dorsolateral and ventral lines. DA, dorsal arm; DlA, dorsolateral arm; VlA, ventrolateral arm. (c) sEM image of the funnel line showing the ciliated cells of the funnel line (black arrow) and the ciliated cells in the immediate neighbourhood of the line (white arrow). (Reproduced with permission from lenz 1997, modified.)
both sides of the head and on the left and right arms but there is only one line along the midline of the funnel (Figure 21A,B). The ciliated cells of these lines have an elongated apical surface bearing up to six long (10-m) cilia and short microvilli. The dorsal lines are the longest. The funnel line has the most complex structure, composed of two parallel rows of ciliated cells and several smaller, accessory non-ciliated cells with long microvilli in the centre of the line (Figure 21c). The epidermal lines found in octopus paralarvae have not been reported in adult octopuses but they
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RoGER VillANuEVA & MARk D. NoRMAN are homologous to those described in adults of sepioid and teuthoid cephalopods. The cells of the epidermal lines are able to perceive hydrodynamic pressure and neurophysiological experiments in adult decapod cephalopods showed that epidermal lines can be considered as an organ analogous to the lateral line system found in fishes (Budelmann & Bleckmann 1988, Bleckmann et al. 1991, Budelmann et al. 1997). Single ciliated cells and group-arranged ciliated cells in addition to the ciliated cells of the epidermal lines, hatchling O. vulgaris have ciliated cells on the epidermis that are randomly scattered over the body surface of arms, suckers, head, funnel and mantle or are in special arrangements on the funnel, external yolk sac and the olfactory organ (lenz et al. 1995, lenz 1997, Wildenburg 1997, see chemoreceptors below). During the embryonic stage, the cilia help during rotation of the embryo (Boletzky & Fioroni 1990), presumably keeping the chorionic fluid in motion and preventing the embryo from sticking to the chorion after rotation has occurred. After hatching their function is unknown. Body surfaces that lack cilia are the growing tips of the arms, cornea, margin of the eyes, funnel aperture and the inner side of the mantle. Sucker mechanoreceptors A variety of presumed mechanoreceptors has been described on the suckers of adult octopuses (Graziadei 1964, Graziadei & Gagne 1976a,b) and their presence in the paralarval suckers can be expected. however, schmidtberg (1999), after studying the hatchling suckers of O. vulgaris, concluded that the ciliated cells present on the suckers are chemosensory receptors rather than mechanoreceptors. The development of sucker mechanoreceptors during paralarval and juvenile growth and its relation to a planktonic or benthic mode of life need to be examined. Chemoreceptors Olfactory organ in O. vulgaris hatchlings, paired oval-shaped olfactory organs are situated on either side of the head, ventrally behind the eye and near the mantle edge (Figure 22). They measure around 3545 m in length (lenz 1997, Wildenburg 1997). in this species the surface of the organ is covered by a brushborder of microvilli and cilia. it is composed of one epithelial cell type, four sensory morphological cell types with a chemosensory function and a fifth, mechanosensitive morphological cell type, suggesting the olfactory organ has both chemical and mechanosensitive functions in planktonic O. vulgaris (Woodhams & Messenger 1974, Wildenburg 1997). in Enteroctopus megalocyathus the organ is larger (Figure 23). in hatchlings of directly benthic octopuses such as Octopus joubini, the olfactory organ resembles that of the adults except in size, and the receptors are smaller (Emery 1976). Electrophysiological and behavioural analyses of the receptor cells from the olfactory organ in adult loliginid squid have proved their chemoreceptor function (Gilly & lucero 1992, lucero et al. 1992, lucero et al. 2000). The same function can be expected in octopuses. Lip chemoreceptors ciliated receptors and sensory cells have been described on the finger-like papillae that distally fold the muscular lip around the beaks in O. joubini (Emery 1975). These receptor cells seem more developed in octopuses than in cuttlefish or squid; their presence in octopus paralarvae has not been assessed. Sucker chemoreceptors in hatchlings of O. vulgaris, primary ciliated, flask-shaped receptor cells of presumed chemoreception function are common on the rim but rare at the lateral regions of the suckers and absent on the epithelium of the infundibulum (schmidtberg 1997, 1999). These chemoreceptor cells seem to correspond with those previously described on the epithelium of the rim sucker of adult octopuses (Graziadei 1962, 1964, 1965, 1971, Graziadei & Gagne 1976b).
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50 m di
5 m
Figure 22 olfactory organ in Octopus vulgaris hatchling paralarvae. scanning electron microscopic images showing (A) the position (arrow) of the olfactory organ and (B) the cilia (arrow) on the organ surface. Transmission electron microscope images showing (c) sensory cells of morphological type 1 with an apical cilia pocket and cell morphological type 2 with a spacious ciliated cavity, and (D) sensory cell of morphological type 5, cell apex with one kinocilium and microvilli (di, dictyosome). scale bar 2 m. (Reproduced with permission from Wildenburg 1997, modified.)
Digestive system
Buccal mass The buccal mass consists of the two jaws of the beak, a radula, salivary papillae and associated musculature. At hatching, the buccal mass is fully formed and functional (Nixon & Mangold 1996). The upper and lower beaks are transparent and have oral denticles (Figures 24 and 25). These denticles are absent in adult octopuses, which have smooth and darkly pigmented beaks. oral denticles have been described in hatchlings of Octopus vulgaris (Boletzky 1971, Nixon & Mangold 1996, Nixon & young 2003), O. mimus (castro-Fuentes et al. 2002), Eledone cirrhosa (Boletzky 1974), as well as in the juvenile stages of the pelagic octopods Argonauta argo and Tremoctopus violaceus (Boletzky 1971) and ctenoglossans (strugnell et al. 2005). see p. 148 for functioning of the buccal mass components. Digestive tract The digestive tract of octopus paralarvae is functional at birth and feeding commences rapidly after hatching (Villanueva et al. 2002, Morote et al. 2005, iglesias et al. 2006). The external yolk sac that is evident within the egg capsule is sometimes visible externally in the earliest hatchling stages, indicating premature hatching (Figure 26). The white of the yolk sac is also visible within
131
2 mm
200 um
Figure 23 olfactory organ in Enteroctopus megalocyathus hatchling paralarvae. specimen collected during rearing experiments described in ortiz et al. (2006). scanning electron microscope images showing the position (left) and the organ (right). Note the large size of the organ in comparison with Octopus vulgaris hatchling (Figure 22). (specimen kindly provided by N. ortiz, centro Nacional patagnico, coNicET.) original.
UB D
LB 50 m 25 m
Figure 24 Buccal mass and denticulation on the beaks of Octopus vulgaris. left, whole mount of a hatchling individual. Right, oral surface of the rostrum of the upper (top) and lower (bottom) beaks showing denticulation in 1-day-old specimen. D, denticles; lB, lower beak; uB, upper beak. (left, modified from Nixon & Mangold 1996; right, from Boletzky 1971 and reproduced with permission.)
the visceral mass in these early hatchling stages (Figure 26). The yolk sac is rapidly devoured or discarded after hatching (see p. 135) and its presence internally does not hamper direct feeding because the digestive tract is immediately capable of ingesting prey (Boletzky 1975).
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Figure 25 Denticulation of beaks in Octopus vulgaris paralarvae. scanning electron microscope images of (A) oral view of hatchling; (B) 50-day-old specimen in presettlement stage, 7.3 mm mantle length (Ml) (fresh) and (c) 60-day-old recently settled individual of 9.3 mm Ml (fresh). Note the broken denticles on the lower beaks of posthatching individuals and the rostral tip of the beak in the settled individual, in transition to the typical adult beak form. individuals obtained from rearing experiments described in Villanueva (1995). original.
Ink sac
For those species that possess an ink sac in the adult form, the ink sac of their paralarvae is functional from birth (yamashita 1974, Gabe 1975, Joll 1978, okubo 1979, kaneko et al. 2006). The positions of this and other organs of the digestive tract are shown in Figure 27. The organ is visible through the body wall in those taxa that lack a reflective iridophore membrane surrounding the viscera (Figure 26).
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Figure 26 (see also colour Figure 26 in the insert.) planktonic paralarva of Octopus warringa within 10 min of hatching in the laboratory showing short arms, transparent musculature, simple chromatophores and external yolk sac (within arm crown). (photo: David paul.)
oo r cv sg fr is g 1 mm bh A B C
Figure 27 Scaeurgus unicirrhus hatchling after fixation. (A) lateral view. (B) Dorsal view. (c) Ventral view after removal of the ventral mantle musculature. bh, branchial heart; cv, cephalic vein lying beside the intestine; fr, funnel retractor; g, gill; is, ink sac; oo, olfactory organ; r, rectum; sg, stellate ganglion. (Reproduced with permission from Boletzky 1984, modified.)
Food, feeding and nutritional requirements

Yolk reserves
After hatching, octopus paralarvae possess available yolk reserves that help the animal during the first hours or days, combining endogenous (yolk) with exogenous (prey) feeding until the yolk is completely absorbed (Boletzky 1975, 1989). in octopods, part of the yolk is enclosed within the hatchling proper and the rest forms an external sac enclosed within a membranous envelope
134
BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs (Figure 26). The yolk can be considered as a unit independent from the digestive system: the paralarvae absorb the yolk directly into the blood as the yolk nutrients flow to the circulatory system, not via the alimentary canal (Boletzky 1975). The amount of yolk in hatchling individuals varies greatly. The reduced volume or absence of the external yolk sac at hatching can be considered a sign of health or competence of the animal, indicating that these reserves have been correctly absorbed. in contrast, a large external sac indicates premature hatching (Boletzky & hanlon 1983, Boletzky 1987) and a quick loss/discarding of this external sac reduces the survival rate of the hatchlings (okubo 1979). observations under experimental conditions show that well-developed, non-premature hatched Octopus vulgaris paralarvae start to feed during the first 24 h after hatching (Villanueva et al. 2002, Morote et al. 2005, iglesias et al. 2006) and that the presence of an inner yolk sac does not apparently interfere with any organ functioning (Boletzky 1975). The amount of yolk is proportional to body weight and the yolk absorption is related to temperature in squid paralarvae (oDor et al. 1986, Vidal et al. 2002, 2005). The same relationship can also be expected for octopus paralarvae. large octopus hatchlings from species adapted to low temperatures, such as Enteroctopus megalocyathus, can survive under starved conditions up to 15 days at 11.5c (ortiz et al. 2006), while species with small hatchlings, such as Octopus cf tetricus, can survive up to 10 days at 20c (Joll 1978 as O. tetricus). under the same temperature conditions, starved O. vulgaris hatchlings lose 16% and 28% of their dry weight after 2 and 4 days, respectively (Villanueva et al. 2004). in O. vulgaris, the maternal diet before spawning (crab or sardine diet) influences the lipid composition of the eggs and hatchlings and has been related to paralarval survival under starvation conditions. starved paralarvae fed a maternal sardine diet had low survival rates and low lipid content, particularly for phosphatidylcholine and phosphatidylethanolamine as well as low content in n-3 and n-6 polyunsaturated fatty acids (puFAs) (Quintana et al. 2005, 2006). Table 3 shows survival of different paralarval species after hatching in the laboratory; some of these results are the product of unsuccessful feeding experiments for which the short survival period suggests that metabolic fuel was provided mostly by the yolk and whole animal reserves. The physiological conditions that enable the first digestion of external prey have not been determined for octopus paralarvae and need further research.
Natural prey
At the moment of prey capture, octopus paralarvae bite and administer salivary products using their beaks and radula. The saliva contains enzymes that predigest the prey, enabling easy removal of the flesh from exo- or endoskeletons. The beak and radula are then used to macerate the predigested flesh, sucking up the edible content of prey such as crustaceans and rejecting their exoskeletons (hernndez-Garca et al. 2000). They sometimes also ingest small pieces of prey carapace (iglesias et al. 2006) (see p. 148). This mode of ingestion makes the study of stomach contents difficult. As a result, there are few reports on the diet of octopus paralarvae in the wild. passarella & hopkins (1991) examined stomach contents of 57 paralarvae (<20 mm Ml) of octopodidae (Macrotritopus defilippi, Octopus sp. and Scaeurgus unicirrhus) collected from eastern Gulf of Mexico at depths between 0 and 900 m and found that the major prey types were euphausiids (53% of the stomachs) and non-cephalopod molluscs (23%), as well as ostracods, hyperiid amphipods, decapod crustaceans and fishes. octopus paralarvae share a preference for crustacean prey with squid paralarvae (passarella & hopkins 1991, Vecchione 1991, Vidal & haimovici 1998), in common with most juvenile cephalopods (Nixon 1987). A wide variety of live and inert prey has been consumed by octopus paralarvae in laboratory experiments (Table 3). Most of the successful or long-term laboratory rearings used decapod crustacean zoeae (Figure 28) as the primary prey for small-sized octopus paralarvae (Octopus vulgaris type) (itami et al. 1963, Forsythe & Toll 1991, Villanueva 1994, 1995, shiraki 1997, carrasco et al.
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Table 3 prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from hatching to settlement of the paralarvae obtained during rearing experiments of octopodidae species with planktonic hatchlings
Temp. (c) survival rate (%) To 16% at 26 d No No growth in Ml NW Atlantic comments 2324 Reared to settlement Geographic area Reference Forsythe & hanlon 1985
species and prey offered
Amphioctopus burryi live wild zooplankton (copepods, larval crustaceans and fishes) and Artemia nauplii Callistoctopus macropus hatchling zoeae of Pagurus prideaux 16 To 6 d No Without food survived 34 d Mediterranean
Boletzky et al. 2001 NE pacific NW pacific Green 1973 okubo 1973
Np To 26 d No
To 7 d
No
Eating not observed
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4% at 135 d To 19 d No presettlement 8.515.6, mean 11.8 1012.8 Np No 7.814.7, mean 10.8 Np 8% at 6 months To 169 d settlement from 100117 d settlement from 88 d
Enteroctopus dofleini Artemia, frozen Calanus, frozen and live zooplankton pieces (25 mm) of prawns (Palaemon pacificus), clam (Ruditapes philippinarum) and crab live mysidaceans, amphipods and pieces of shrimp after 70 d Artemia and hatchlings of greenling fish 10.611.8, mean 11.0 Np
NW pacific NW pacific
okubo 1974 yamashita 1974
Food pieces submerged previously in freshwater to increase floatability individuals reached 33 mm Tl at 115 d Feeding and development not observed
NE pacific
Gabe 1975
only adult Artemia and fry fish accepted as prey; occasionally dead siblings captured by the paralarvae individuals reached 35 mm Tl at 169 d Tank with upwelling water system
NW pacific
okubo 1979
crushed egg yolk, ground shrimp and mussel, live gammarids, Artemia biomass and fry of fish Hemilepidotus hemilepidotus Mysidaceans (515 mm) during first feeding and pieces of shrimp (Palaemon pacificus) after 70 d From hatching to 50 d: dead mysidaceans + amphipods; 5080 d: dead mysidaceans + amphipods + pieces of shrimp; from 80 d: pieces of shrimp
NW pacific
okubo 1980
Artemia biomass, frozen krill (Euphausia pacifica), larval cottid fish (Hemilepidotus hemilepidotus), trout micropellets No The preferred prey was krill; neustonic feeding behaviour described hatchling food size equivalent to octopus head width; developed paralarvae feed on chunks of food 36 25 mm suspended in the tank sW Atlantic slight paralarval growth central E pacific sW pacific NE pacific Growth increase in 0.5 mm Tl; unfed controls died in 5 d Addition of vitamin supplement mixture to the rearing tanks only feeding on pieces of shrimp was observed No Best results with zoeae as food and octopus density of 25 ind l1 No hawaii islands NW Atlantic NE pacific snyder 1986a,b, unpublished manuscript NE pacific Marliave 1981 1111.5 settlement from 5 to 6 months
10
With Artemia: 50% sR at 5 d and maximum to 22 d; with krill: 50% sR at 16 d and maximum to 87 d 4% after 67 months
Frozen or fresh chopped body and muscle of crabs Cancer productus, Pugettia productus, tails of Pandalus danae shrimps, Euphausia pacifica, beef heart and lamb kidney Enteroctopus megalocyathus starved Hapalochlaena lunulata Artemia and small crustaceans 11.5 26 To 7 d No To 15 d No
ortiz et al. 2006 overath & Boletzky 1974 Batham 1957 Ambrose 1981 Van heukelem 1973 Forsythe & Toll 1991
Np Np Np To 21 d No To 6 d No
To 8 d
No
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24 To 10% at 7 d and 0.2% at 23 d settlement from 21 d 26 To 7 d No <22 To 31 d Np To 12 d
Macroctopus maorum starved Octopus bimaculatus Artemia and wild plankton Octopus cyanea crab and mysis zoeae, copepods Promysis orientalis and Lucifer sp. Octopus joubini Wild live zooplankton, zoea of penaeid shrimp, mysidacean shrimp
NW pacific
kaneko et al. 2006 sE pacific Ziga et al. 1997 sE pacific Warnke 1999 (continued on next page)
Octopus laqueus Artemia nauplii, copepods and pieces of shrimp Octopus mimus Artemia metanauplii, zoeae of Leptograpsus variegatus and Cancer setosus, and rotifers hatchling zoeae of Pagurus sp. and Cancer setosus
Table 3 (continued) prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from hatching to settlement of the paralarvae obtained during rearing experiments of octopodidae species with planktonic hatchlings
Temp. (c) survival rate (%) No No sE pacific sE pacific comments Reference 2122 1723 10% at 5 d, maximum survival to 17 d To 23 d Reared to settlement Geographic area
Artemia nauplii
Baltazar et al. 2000 Montoya 2002
Artemia, Brachionus, zoeae of Cancer setosus, Hepatus chiliensis, Emerita analoga and Pleuroncodes monodon and micropellets Octopus tetricus copepods, Artemia, small pieces of fish and mollusca Octopus cf tetricus Artemia and rice powder To 32 To 6 d No All food refused sW pacific Np To 21 d No No growth, no evidence of eating E indian
Dew 1959 (as O. cyanea) Joll 1976
138
Np 23 Mean 24.7 Np To 35 d To 67% at 22 d 25.1 9% at settlement settlement from 33 d No To 12 d To 9 d No No 2528 30% at 25 d 21.2 Np 30% at 29 d 9% to settlement at 47 d Transition to benthic stage Transition to benthic stage settlement from 47 d presettlement
No feeding observed P. serrifer zoeae feed with Artemia nauplii Growth ceased from 25 d Microalgae Nannocloropsis added to the culture tank Tank volume of 20 m3 and microalgae Nannocloropsis added to the tank Food added 5 times per day individuals with 19 suckers at 29 d
Mediterranean NE Atlantic NW pacific Mediterranean NW pacific
Octopus vulgaris Argonauta argo hatchlings harpacticoid copepods, Artemia, ciliates, yeast cells Palaemon serrifer decapod palaemonid zoeae Zoeae of crabs and prawns, Artemia biomass Artemia biomass
Naef 1928 Vevers 1961 itami et al. 1963 Mangold & Boletzky 1973 imamura 1990
Artemia biomass
NW pacific
hamazaki et al. 1991 Mediterranean NW pacific Villanueva 1994, 1995 shiraki 1997
Liocarcinus depurator and Pagurus prideaux decapod crab zoeae Artemia and Portunus trituberculatus crab zoeae
21, 24 and 27 NW pacific hamasaki & Takeuchi 2000 iglesias et al. 2000 1820 To 32 d No NE Atlantic
To 88% at 24 d
No
higher growth and survival with 100400 104 algal cells/ml Best survival with Artemia metanauplii
Artemia biomass (12.7 mm) feed with or without Nannochloropsis algae on the rearing tank Rotifers, fish eggs, micropellets, wild copepods, Artemia nauplii and metanauplii, zoeae of shrimp Palaemon serratus, zoeae of crab Carcinus maenas and Necora puber Artemia biomass (13 mm) and pellets (250500 m) with 6% moisture 2022.5 To 6.7% at 30 d No Fatty acid of cultured octopus reflected that of the food Enriched Artemia increased survival and growth Mediterranean 25 To 45% and 24% at 16 and 20 d, respectively No NW pacific Navarro & Villanueva 2000 hamasaki & Takeuchi 2001
1729
To 62.5% at 40 d
No
highest survival at 21c
NW pacific
hamasaki & Morioka 2002 NE Atlantic Moxica et al. 2002 Mediterranean Villanueva et al. 2002 NE Atlantic NE Atlantic
139
Np To 56 d No 19.422.5 To 4.6% at 30 d No 21.122.2 22.5 31.5% at 40 d 3.4% at 60 d settlement from 52 d settlement from 40 d
Nannochloropsis algae on the rearing tank at 100 104 cells/ml; Artemia biomass (2 mm) not enriched or enriched with yeast or shark egg powder Artemia biomass (1.52 mm) feed with Nannochloropsis algae Octopus vulgaris Artemia biomass and zoeae of Maja squinado
Artemia nauplii and millicapsules of 1.32 mm in , 0.3 mg fresh weight
live and frozen Maja brachydactyla zoeae 13 d old and Artemia biomass Maja brachydactyla zoeae and Artemia biomass (14 mm)
Tank volume of 9 m3 and microalgae Isochrysis, Tetraselmis and Chaetoceros Total proteolytic activity correlated with paralarval weight parabolic tanks with upwelling water system Microalgae (Chlorella sp., Isochrysis galbana and Chaetoceros sp.) added daily to the culture tank
carrasco et al. 2003, 2006 iglesias et al. 2004
(continued on next page)
Table 3 (continued) prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from hatching to settlement of the paralarvae obtained during rearing experiments of octopodidae species with planktonic hatchlings
Temp. (c) survival rate (%) To 12.5% at 30 d No Best survival in trials receiving amino acids Mediterranean comments Reference 19.221.1 Reared to settlement Geographic area
Artemia nauplii and essential amino acids added to the rearing tank
Artemia metanauplii and zoeae of Maja squinado 2122 To 10 d No
20 1
To 26 d
No
central E Atlantic NE Atlantic
Better growth and survival with light intensity of 6000 lux protease activity indicates hatchling condition
Villanueva et al. 2004, Villanueva & Bustamante 2006 Fernndezlpez et al. 2005 Morote et al. 2005
Artemia metanauplii, cladocerans Moina salina, zoeae of Maja brachydactyla and Palaemon serratus, eggs and larvae of fish Solea senegalensis, artificial pellets Artemia nauplii and thawed frozen fish (Ammodytes personatus) flakes 21.224.8 To 45.9% at 32 d 1820 3d Transition to benthic stage No
NW pacific
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2426.9 To 10% at 42 d Transition to benthic stage No No Np 20 1 To 39% at 40 d To 27% at 28 d 20 2d No
okumura et al. 2005a NE Atlantic iglesias et al. 2006 NW pacific kurihara et al. 2006
Artemia biomass of 0.8 and 1.4 mm
Artemia nauplii and defrozen fish (Ammodytes personatus) flakes
Fish flakes effective for improving the DhA content of the paralarvae preference for Artemia 1.4 mm at densities of 0.1 Artemia ml1 Fish flakes improved DhA content of the paralarvae
NE Atlantic sE Atlantic
Octopus vulgaris Artemia metanauplii, Grapsus grapsus and Plagusia depressa zoeae Artemia nauplii supplemented with copepods (Acartia tonsa), juvenile mysids (Metamysidopsis elongata atlantica) and crab zoeae (Callinectes sapidus) Artemia 0.8 mm
Best survival and growth with G. grapsus zoeae Best survival with A. tonsa up to 15 d supplemented with Artemia prey capture higher during light periods, decreasing in the dark
iglesias et al. 2007 iglesias et al. 2007
NE Atlantic
Mrquez et al. 2007
1016
To 34 d
Np
sE pacific
Gonzlez et al. 2006 Boletzky 1984 Miske & kirchhauser 2006
19 26 To 4 d No sW pacific
Robsonella fontanianus Artemia, small crustaceans and micropellets Scaeurgus unicirrhus Artemia biomass Wunderpus photogenicus Artemia naupli, rotifers Brachionus and copepods To 6 d No Mediterranean
Note: DhA, docosahexanoic acid; Ml, mantle length; Np, not provided; sR, survival rate; Tl, total length.
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Figure 28 Decapod crab zoeae hatchlings used as live prey in successful rearing experiments of Octopus vulgaris paralarvae. left to right: Liocarcinus depurator, 0.5 mm carapace length (cl); Pagurus prideaux, 1.2 mm cl (photos: R. Villanueva); Maja brachydactyla, 1.1 mm cl (photo courtesy of Guiomar Rotllant).
2003, 2006, iglesias et al. 2004) or mysidaceans, amphipods and euphausiids for larger-size paralarvae (Enteroctopus type) (okubo 1979, 1980, Marliave 1981). preference for these prey types correlates with the few available field observations. itami (1975) found that during the hatching season of Octopus vulgaris in the Akashi straits, Japan, the presence of paralarvae collected in plankton nets 12 m above the seafloor in coastal waters was associated with areas rich in shrimp and crab zoeae and megalopa. After copepods, decapod crustacean zoeae are the most abundant crustacean group in the meso- and macroplankton (size >1 mm) on the continental shelf of the north-west Mediterranean sea over summer (Razouls & Thiriot 1968), coinciding with the peak hatching season for O. vulgaris in that area (Mangold 1983, Villanueva 1995). Decapod crustacean larvae are probably one of the main natural prey of planktonic O. vulgaris and other species of littoral octopuses although stomach analyses from wild paralarvae need to be examined. in contrast, the ability of planktonic octopuses to feed on inert food, as observed under laboratory conditions (see p. 146), suggests that scavenging activity in the wild is also possible. immunoassay techniques used to analyse stomach contents of squid paralarvae (Venter et al. 1999, hoving et al. 2005) may be useful tools for gaining better insights into the earliest feeding stages of octopus paralarvae.
Prey size and prey density

in comparison with most carnivorous larval fishes, for which mouth opening diameter limits the size of the prey that are generally ingested whole, planktonic octopuses can capture prey of their own size using their well-developed arms and suckers. prey size and prey density preferences of planktonic octopus have been determined only under experimental conditions. Artemia of 1.11.7 mm (imamura 1990) or 1.52 mm length (hamazaki et al. 1991) have been recommended for rearing Octopus vulgaris hatchlings (3 mm total length). iglesias et al. (2006) also fed hatchlings of the same species with both small (0.8 mm) and large (1.4 mm) Artemia, recording preference (77%) for large Artemia that represented nearly 50% of the total length of the octopus. Octopus vulgaris hatchlings capture a range of live decapod crustacean zoeae, including Liocarcinus depurator, Palaemon serrifer, Pagurus prideaux and Maja brachydactyla (1.3, 2.5, 3.1 and 3.4 mm in total length, respectively), representing 45118% of octopus total length and 232% of octopus fresh weight at hatching (Figure 29). laboratory experiments using these prey obtained high growth and survival rates during the first half of planktonic life, suggesting the suitability of this range of prey sizes (itami et al. 1963, Villanueva 1995, carrasco et al. 2003, 2006, iglesias et al. 2004).
142

140 Prey TW as % of octopus TW Prey TL as % of octopus TL 120 100 80 60 40 20 0 0 5 10 15 Octopus TL (mm) 20 35 30 25 20 15 10 5 0 1 100 10 Octopus TW (mg) 1000
Figure 29 predator-prey size relationships in Octopus vulgaris during the paralarval stage expressed as length (left) and fresh weight (right). octopus data points correspond to reared O. vulgaris aged 0, 10, 20, 30, 42, 50 and 60 days (data from Villanueva 1995). selected prey are hatchling zoeae of Maja brachydactyla (dark circles) used as prey in iglesias et al. (2004) and carrasco et al. (2006); Pagurus prideaux (white circles) and Liocarcinus depurator (white squares) used as prey in Villanueva (1995); adult stages of the copepod Acartia tonsa (diamonds) and Artemia nauplii, AF strain (triangles). Tl, total length; TW, total weight. original.
prey densities in successful cultures using decapod crustacean zoeae ranged from 0.10.3 Pagurus prideaux ml1 (Villanueva 1995) to 0.011 Maja brachydactyla ml1 supplemented with 0.050.8 Artemia ml1 (carrasco et al. 2003, 2006, iglesias et al. 2004). The effect of different prey densities needs to be studied in detail. using Artemia as prey, iglesias et al. (2006) found no significant differences in the number of attacks by Octopus vulgaris hatchlings on Artemia of 1.4 mm length at densities of 0.1, 0.5 and 1 Artemia ml1; however, Mrquez et al. (2007), using Artemia nauplii (0.8 mm length), observed higher consumption rates at 9.4 Artemia ml1 in comparison with 2.3 and 4.7 Artemia ml1. As Octopus vulgaris paralarvae grow in the second half of their planktonic phase, larger prey are required. hatchling decapod zoeae decrease in size relative to presettlement paralarvae (>10 mm total length), representing only 926% of their length and 0.040.7% of their weight (Figure 29). presettlement O. vulgaris-type paralarvae, large Enteroctopus-type paralarval forms and micronektonic paralarvae forms (see p. 182) probably require larger prey. in fact, E. dofleini hatchings (10 mm total length) eat mysidaceans 515 mm in length during the first feeding phases in successful laboratory experiments (okubo 1979). The limited data collected from the field (passarella & hopkins 1991) suggests that euphausiids can be a main prey source for relatively large octopus paralarvae in the wild.
Food searching and prey capture

Experiments with Octopus vulgaris hatchlings showed that light enhanced consumption rates 3-fold in comparison with dark conditions. A higher percentage of non-feeding individuals was also recorded in the dark, suggesting the importance of light (and vision) in predatory behaviour (Mrquez et al. 2007). however, these authors showed that light may not be essential for prey capture as a positive correlation was found between prey density and consumption rates in dark conditions. observations of the swimming paths of O. vulgaris paralarvae in laboratory conditions over 2 months of planktonic life found that paralarval behaviour is affected by the presence of prey individual paralarvae tend to increase their turning rate and reduce swimming speed in the presence of prey (Villanueva et al. 1996). in the sea, both responses may combine to improve the exploitation
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RoGER VillANuEVA & MARk D. NoRMAN of patchy food environments as curvilinear paths and slow swimming speeds increase the probability of residence time in a zooplankton patch, increasing the probability of prey encounters. Capture of live prey in O. vulgaris, prey capture can be predicted by a human observer as the paralarva modifies its routine swimming behaviour in a recognizable behavioural sequence (Boletzky 1987, Villanueva et al. 1996, hernndez-Garca et al. 2000). After a zoea prey is selected, three phases can be identified (Figure 30). The first phase is the attention phase; paralarvae reduce speed and approach the prey, using a range of different manoeuvring movements including forward, backward and lateral swimming. The second phase is the positioning phase; the anterior end of the body is directed towards the prey and an aiming posture is adopted with arms drawn together and pointed anteriorly. The body axis is aligned directly towards the prey. At this time the paralarva is almost immobile, sometimes rotating its position around the prey using jets of water through the flexible funnel, attaining the best position for attack. The third phase is the attack phase; the paralarvae swims forward fast, usually through one (sometimes two) powerful jets from the funnel and the prey is seized with all arms. During the prey capture sequence, a change in chromatophore pattern usually takes place between the second and third phase (hernndez-Garca et al. 2000). During the attention phase, the paralarvae maintain contracted chromatophores, so that the octopus is nearly transparent to a human observer; then, during the positioning phase and/or during the contact with the prey, the chromatophores from the dorsal mantle, head and arms are expanded dramatically. After seizure of the prey the chromatophores are contracted again. This visual signal is suspected to be defensive
A B C D
Figure 30 Behavioral sequences during prey capture in 20-day-old individual of Octopus vulgaris (4.4 mm total length) preying on hatchling zoeae of Pagurus prideaux (3.1 mm total length). After the prey is selected, three phases can be identified: (A) attention, (B) positioning and (c) attack (see text for explanation). Note that during the attention phase, the octopus maintains contracted chromatophores, then, during positioning and contact with the prey, the chromatophores from the dorsal mantle, head and arms are expanded. After seizure of the prey (D), chromatophores are contracted again. The dark oval spot inside the mantle cavity represents the digestive gland. (original drawing from Jordi corbera based on video recordings from Villanueva et al. 1996.) 144
BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs behaviour (see Defences, p. 168). selection of the attack angle probably depends on the type of prey, its size and defences (i.e., many crustacean zoeae possess dorsal spines) (Figure 28). Further research is required on the predatory behaviour of octopus paralarvae, as have been made on loliginid squid paralarvae (chen et al. 1996). such studies may detect ontogenetic changes in predatory behaviour along with behavioural responses specific to different prey types. After prey have been selected, attack distances are usually two to four times the total length of the octopus, or sometimes more. in Amphioctopus burryi paralarvae preying on wild zooplankton, these distances are 1030 mm (Forsythe & hanlon 1985). For Octopus vulgaris aged 30 days (mean octopus total length of 7.4 mm), the reaction distance (R, the maximum predator-prey distance at which the paralarvae notice the prey during the attention phase) was 15.5 mm (Villanueva et al. 1996). using an estimated mean cruising speed of 25.6 mm s1, the estimated water volume searched (Vs) by 30-day-old O. vulgaris paralarvae (Vs = 2/3R2cruising speed; Blaxter & staines 1971) is 5.5 1 min1 (Villanueva et al. 1996). This volume cannot be extrapolated to hour units until daily activity periods are recorded as paralarvae have static periods during which they remain hovering using weaker ventilatory pulses to provide dynamic lift (Boletzky 1977a). Forward swimming is always used to capture prey, while backward jetting is used while subduing and ingesting prey. Mean time taken from striking prey to backwards swimming after subduing the prey is 0.3 s in O. vulgaris (Villanueva et al. 1996) (Figures 31 and 32). As indicated (see sucker surfaces, p. 122), the sucker structure of octopus paralarvae suggests that hydrostatic suction is not as effective in
200 160 120 80 40 Swimming speed (mm s1) 0 160 120 80 40 0 160 120 80 40 0 4 2 0 2 2 Time (in seconds) 0 2 4 E F C D A B
Figure 31 swimming performance during six successful prey captures by 30-day-old Octopus vulgaris paralarvae (4.5 mm mean mantle length), using live Pagurus prideaux hatchling zoeae as prey. Time elapsed before and after capture and swimming speed are indicated at time intervals of 0.04 s. Time 0 indicates the instant when the octopus strikes the prey. Before prey capture, the paralarva can swim forward (), backwards (-----) or laterally (, only observed in example A), and the arms are pointed towards the prey ( at bottom of each graph). The same paths in the same order are used in Figure 32. (Reproduced with permission from Villanueva et al. 1996.) 145

6 5 4 3 2 1 0 40 30 Y (mm) 20 10 0 70 60 50 40 30 20 10 0 0 20 0 60 50 40 30 20 10 5 10 15 20 (C) 0 20 15 10 5 0 30 20 0 10 20 30 40 50 60 (D)
(A)
s e s c
(B)
c e
s e c
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10
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c e S
40 60
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Figure 32 swimming paths of six successful prey capture sequences of 30-day-old Octopus vulgaris paralarvae, 4.5-mm mean mantle length (open circles) and Pagurus prideaux hatchling zoeae as prey (). Each point represents the respective position of the animal at 0.04-s time intervals. c, capture; e, end position; s, starting position. inset of B, path of octopus before attack, represented by (). The same paths are used in the same order in Figure 31. (Reproduced with permission from Villanueva et al. 1996.)
early paralarvae as it is in adults or octopus hatchlings of directly benthic species (schmidtberg 1997, 1999). This may represent an impediment to holding and subduing prey although the gland cells on the epithelium of the sucker rims that secrete mucopolysaccharides probably assist in adherence of paralarval suckers (kier & smith 1990, schmidtberg 1999). Capture of inert prey live prey is not a prerequisite stimulus in provoking attacks by octopus paralarvae. laboratory studies using inert food showed that attacks usually take place when the dead prey or food particle descends in the water column (Boletzky & hanlon 1983). pellets, millicapsules and fish flakes have been used as supplementary food for O. vulgaris paralarvae and are captured when sinking through the water column (Navarro & Villanueva 2000, 2003, okumura et al. 2005a, kurihara et al. 2006). As the escape response of many water column residents of open ocean is to passively and rapidly
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs sink (i.e., pteropod molluscs and gastropod veliger larvae; lalli & Gilmer 1989), capture of sinking food items may not simply be an attempt to capture inert or dead food sources. capture of dead prey from the bottom of rearing tanks has also been reported by itami et al. (1963) for O. vulgaris when live prey were scarce in the water column. okubo (1980) reared Enteroctopus dofleini from hatching to settlement on floating frozen prey (mysidaceans, amphipods, pieces of shrimp), using a tank with an upwelling water system that maintained movement of the food particles. snyder (1986a,b, unpublished manuscript) fed paralarvae of the same species over 56 months exclusively on inert food and pieces of crab and shrimp meal (36 mm wide, 25 mm length) suspended in the tank (Table 3). Marliave (1981) described in detail the neustonic feeding behaviour of paralarval E. dofleini on pieces of floating thawed krill in laboratory conditions. When the mantles of E. dofleini individuals aged 6 days came into contact with floating pieces of krill, the octopuses would turn over and adhere to the surface tension film in an inverted posture with the oral surface of the arms extended towards the surface. on contacting the food with their arm tips, individuals would seize the krill and leave the surface to feed on it within the water column, suggesting chemotactile discrimination of these food sources (Figure 33). The neustonic feeding described by Marliave ceased once the paralarvae reached 1 month old and was replaced by the capture sequences more typical of the smaller Octopus vulgaris. Neustonic feeding was also reported by snyder (unpublished manuscript) for Enteroctopus dofleini and Boletzky (1987) for Octopus vulgaris hatchlings. overall, octopus paralarvae seem to be visual predators but chemical and tactile senses also seem to play important roles during prey searching and require further research. octopuses are blind to colour (Messenger 1977). certain cephalopods have been shown to be polarization sensitive (see among others shashar & cronin 1996, shashar et al. 1996). hatchlings of the squid Loligo pealei attacked planktonic prey under polarized illumination at a 70% greater distance than under depolarized light (shashar et al. 1998). The role of polarization vision in octopus paralarvae is unknown although it is likely to play an important role. As visual predators, octopus paralarvae may target luminescing prey, particularly when feeding in deeper waters and at night. Dinoflagellate bioluminescence has also been proposed to help in locating and capturing non-luminous prey during nocturnal feeding for juvenile cuttlefishes (Fleisher & case 1995). The same may apply for octopus paralarvae.
Figure 33 Neustonic feeding in Enteroctopus dofleini. individuals adhering to the surface film in inverted posture (upper right individual) and normal swimming posture (lower left). Note that reflected glare indicates attachment of the suckers to the water surface and depression of the surface tension film. scale 4 mm. (Reproduced with permission from Marliave 1981, modified.) 147
Buccal mass, denticulate beaks and external digestion

in comparison with adults, octopus paralarvae have relatively short arms with few suckers and a large buccal apparatus (containing the beaks and radula) and this apparatus is particularly important at this life-history stage in subduing and chopping the prey prior to ingestion. At hatching, the diameter of the nearly spherical buccal mass represents 30% of the Ml and is innervated by the buccal lobe of the brain that is also proportionally much larger than in recently settled individuals (Nixon & young 2003). After settlement, octopuses have a large arm crown and numerous suckers, representing the main means of prey capture and manipulation. in adult octopuses, buccal mass length decreases to around 13% of Ml (Nixon 1985, Nixon & Mangold 1996, Nixon & young 2003). As stated, the posterior salivary gland papilla and radula are well developed and fully functional at hatching (Nixon & Mangold 1996). octopus paralarvae beaks possess oral denticles. These denticles have also been observed for paralarvae of loliginid (Boletzky 1971) and ommastrephid squids (shigeno et al. 2001) and in hatchlings of octopod species with direct benthic young, although showing less-developed denticulation in these octopod species with direct benthics (Boletzky 1971, 1977a). They have also been reported in adult pygmy squid, Idiosepius (Adam 1986, kasugai et al. 2004). The function of these denticles, typically associated with early stages or pygmy species such as Idiosepius, remains unclear. however, detailed observations on the external digestion and initial ingestion process (see this section) suggest that denticles may be useful to detach the semidigested flesh from the exoskeleton of the crustacean prey (kasugai et al. 2004). Two factors may account for this dentition. The first is that the radula may be too poorly developed to grip and remove flesh from the prey. The second is that the dentition may aid gripping the prey in paralarvae with few, proportionally large (and hence clumsy) suckers. The beaks of presettlement and recently settled captive-reared Octopus vulgaris individuals show loss of some denticle tips, presumably worn by their use during feeding on crustacean zoeae larvae (Figure 25B,c). The erosion of the denticles seems to be a stage in the transition to the thick, darkly pigmented and chitinized beaks of juvenile O. vulgaris that lack denticles and have rostral tips more characteristic of the adult octopus (Nixon & Mangold 1996). in octopuses, two categories of glands discharge their secretion into the buccal cavity: (1) diffuse glands of single or small groups of gland cells on the lips, salivary papilla and buccal epithelium and (2) five major glands (the single submandibular salivary gland below the radular complex, the paired anterior salivary glands that lie on the posterior surface of the buccal mass, and the paired posterior salivary glands that lie adjacent to the swollen crop diverticulum anterior to the digestive gland) (Boucaud-camou & Boucher-Rodoni 1983, Budelmann et al. 1997, Nixon & young 2003). The posterior salivary glands secrete a mixture of substances, including biologically active amines, enzymes (particularly proteolytic enzymes) and toxins with venomous, pharmacological, digestive and haemolytic properties (Grisley & Boyle 1987, Grisley 1993, key et al. 2002). The adult octopus cephalotoxin is responsible for the paralysis and killing of crabs (Ghiretti 1959, 1960) and the ability of octopus saliva to release crab muscle from the carapace prior to ingestion is principally caused by proteases in the saliva (Grisley & Boyle 1987), injected into the crab by a narrow hole produced in the carapace or the cornea of the crab (Grisley et al. 1996, 1999). prey is then disarticulated and the flesh removed and ingested, leaving the clean exoskeleton, which is discarded by the octopus. This process is generally known as external digestion (Nixon 1984) and in octopus paralarvae has been described for O. vulgaris hatchlings feeding in laboratory on recently hatched decapod crab zoeae Pachygrapsus marmoratus, P. transversus and Eriphia verrucosa (hernndez-Garca et al. 2000). The extraction of the edible content of the zoeae by the octopus paralarva means that the prey remains consist only of a transparent, moult-like exoskeleton with attached appendages. similar observations have also been reported for 11-day-old loliginid squid paralarvae (Loligo vulgaris) feeding on mysidacean shrimp in the laboratory (Boletzky 1974) and for adults of the
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs pygmy squid Idiosepius (kasugai 2001, kasugai et al. 2004). During external digestion and ingestion, the prey is actively handled with arms, suckers and buccal mass. Boucaud-camou & Roper (1995) found chymiotrypsin activity on the sucker surface of Octopus sp. paralarvae and suggested that this enzymatic activity was probably related to secretions of the posterior salivary glands and involved in diffusion of the octopus enzymes and venom when handling the prey during the external digestive processes. in addition to an external digestion that rejects the entire crustacean carapace, analysis of stomach contents of O. vulgaris hatchlings eating Artemia showed the presence of thoracic appendices (thoracopods) of this prey in the stomach contents (iglesias et al. 2006). similarly, exoskeleton crustacean remains were found in stomach contents of wild paralarvae and juvenile squids (Vecchione 1991, Vidal & haimovici 1998), showing that external digestion is not the only digestive choice for paralarvae. The selection of different modes of ingestion and/or digestion by the paralarvae is probably related to prey characteristics. The mode of digestion as well as the percentage of prey ingested or rejected require further research. Daily food ration by octopus paralarvae is also poorly known. itami et al. (1963) found that O. vulgaris of 35 or 68 mm total length ingested respectively 35 or 710 Palaemon serrifer zoeae (23 mm in total length) day1 when reared at a mean temperature of 25c. hatchlings of the same species maintained at 20c ingested up to 10 Artemia nauplii (0.8 mm length) per day (Mrquez et al. 2007). After prey capture, the duration of the ingestion process in Octopus vulgaris hatchlings preying on 0.8- to 1.4-mm Artemia ranged from 4 to 10 min (iglesias et al. 2006). For 15-day-old paralarvae, the duration was up to 15 min when ingesting 250- to 500-m pellets (Navarro & Villanueva 2000).
Digestive enzymes
in octopods, the anterior and posterior salivary glands and the digestive gland are considered the most important sites for digestive enzyme synthesis, with final digestion and absorption taking place in the caecum and digestive gland (Boucaud-camou & Boucher-Rodoni 1983). using histochemical methods Boucaud-camou & Roper (1995) studied enzymes in wild Octopus sp. paralarvae of 1.72.6 mm Ml and found non-specific esterase activity, particularly on the epithelia of the digestive tract (crop, stomach and caecum) and high alkaline phosphatasic activity in the caecum, digestive gland and skin. high levels of acid phosphatase activity were found in the digestive gland and digestive duct appendages and acetyl-glicosaminidase activity on the posterior salivary glands, digestive gland and stomach. protease and chymiotrypsin activity were recorded in all parts of the digestive tract with virtually zero glucoronidase, amylase and cathepsin B activity. The high proteolitic activity of the digestive gland seems to be related to the carnivorous diet of the paralarvae. using fluorometric methods to analyse enzymatic activity in O. vulgaris hatchlings, Morote et al. (2005) obtained variation in hatchling protease activity between different egg masses, recording trypsin activity for only 20% of the individuals analysed. This result suggests that trypsin activity is developed only after active exogenous feeding. in fact, total proteolytic activity, and trypsin and chymiotrypsin levels in advanced embryos and unfed hatchlings at day 0 show no differences. however, 5-day-old fasting paralarvae have been shown to decrease their proteolytic activity (Villanueva et al. 2002). once external feeding commences, O. vulgaris paralarvae can adjust their digestive enzymes to different diets and food rations during the first month of life. This adaptation seems to be positively correlated with paralarval growth by weight. Differences in enzyme activity can be detected after 5 days of rearing at a mean temperature of 20c under high or low feeding regimes, with higher proteolytic, trypsin and chymiotrypsin activities correlating with higher growth and feeding ratios. in comparison with carnivorous larval fishes, levels of trypsin activity in O. vulgaris paralarvae seem to be higher. Zambonino-infante et al. (1996) reported trypsin activity
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RoGER VillANuEVA & MARk D. NoRMAN for Dicentrarchus labrax larvae at days 15, 20, 30 and 40 as 40, 120, 78 and 67 mu/mg1 of protein respectively, with a sharp increase in activity after day 20. in Octopus vulgaris paralarvae the corresponding trypsin activity under a high feeding regime at days 10, 15 and 20 was 370, 460 and 340 mu/mg1 of protein, respectively, with the sharp increase in activity occurring after day 15 (Villanueva et al. 2002).
Nutrient absorption and the importance of the skin

After external digestion and ingestion, food travels through the buccal mass and down the oesophagus and crop to the stomach for internal digestion, aided by salivary and digestive gland enzymes. smaller food particles move into the digestive gland or caecum for further digestion. The caecum processes fine particles and fluids and is considered the main absorptive organ in adult octopods (Boucaud-camou & Boucher-Rodoni 1983, oDor et al. 1984). The same role can be expected for octopus paralarvae although its characteristics have not been studied in detail. R. Villanueva (unpublished) encapsulated glass ball beads (1030 m in diameter) within Artemia nauplii and offered them as food to 12-day-old Octopus vulgaris paralarvae reared at 20c. The paralarvae started to defaecate glass balls after 1 h, suggesting that the duration of digestion in this growth phase is relatively short. Skin absorption A secondary and intriguing absorptive tissue of octopus paralarvae is the integument. castille & lawrence (1978) found that planktonic hatchlings identified as Octopus sp. (probably O. joubini) uptake radio-labelled amino acids (valine) and hexoses (glucose, mannitol) directly from seawater. They suggest that this uptake mechanism is more active than diffusion, it is saturable and specific, and that little of the uptake is due to the bacterial flora associated with the octopod hatchlings. Radio-labelled amino acid (phenylalanine) uptake from seawater was also recorded in O. vulgaris aged 0, 7, 14 and 21 days (Villanueva et al. 2004) and has been recorded for adult cuttlefishes, Sepia officinalis (de Eguileor et al. 2000). in these laboratory experiments, the contribution to absorption of radio-labelled marker molecules made by microorganisms in both the cephalopod skin and the seawater could not be ruled out. Further support for this skin absorptive mechanism came from Boucaud-camou & Roper (1995), who used histochemical methods to demonstrate high alkaline phosphatase activity in the skin of wild Octopus sp. paralarvae. They suggest that the presence of this digestive enzyme indicates active absorption through the skin from seawater during the paralarval period. A high microbial presence in the skin mucus covering of rhynchoteuthion squid paralarvae has also been suggested to be a source of food to these paralarvae (Vidal & haimovici 1998). on the basis of the absorptive and mechanical characteristics of the skin, the addition of small molecules to seawater in the laboratory has been used experimentally to explore the contribution of the skin to paralarval growth and survival. Vitamin supplement mixture was added to aquaria (1 mg 11 every 3 days) containing O. joubini paralarvae in rearing experiments that resulted in successful settlement (Forsythe & Toll 1991). Rearing trials on O. vulgaris paralarvae assessed the contribution of the daily addition of amino acid solution (16 mg 11 of crystalline essential amino acids) to the rearing tanks. survival rates for paralarvae aged 20 days were three times higher for the treated group compared with the control group although the dry weight of the treated paralarvae was equal to or lower than the controls (Villanueva et al. 2004). The findings of these studies combine to suggest that small organic molecules dissolved in seawater are potentially important nutritional sources (directly or indirectly) for metabolic needs during the first feeding period of octopus paralarvae.
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs Respiration in addition to the gills, a high amount of oxygen is obtained by transcutaneous means in cephalopods (prtner 1994). skin respiration provides between 8% and 41% of total oxygen uptake for subadult O. vulgaris (Madan & Wells 1996) and its importance is probably higher in planktonic octopuses due to their high surface/volume ratio. in fact, skin respiration predominates in early ontogenetic stages of fishes, but progressively loses importance as gill gas exchange becomes more efficient and surface-volume ratio declines (Rombough & Moroz 1997). A similar sequence can also be expected in planktonic octopuses, but no data have been published on this subject. one day before hatching, oxygen consumption rates in O. vulgaris ranged from 14 to 17 nmol o2 ind1 h1, increasing three times in unfed hatchlings (53 nmol o2 ind1 h1) (parra et al. 2000). oxygen uptake as measured in the egg 1 day before hatching can be considered a good estimation of the resting metabolism of the hatchling paralarvae, with the difference in oxygen uptake after hatching primarily corresponding to the cost of swimming. By comparing the oxygen uptake of advanced embryos with that of the adults (Wells et al. 1983a,b), the consumption of a medium-size egg mass of O. vulgaris (i.e., 300,000 eggs) can be estimated as being approximately twice that of the brooding female (of 2 kg total weight). Methods for the transport of O. vulgaris hatchlings over a 24-h period were determined by Fuentes et al. (2005), who obtained nearly 100% survival when using transparent 30-l plastic bags filled one third with oxygen-saturated seawater and two thirds with pure oxygen gas. paralarval densities were <3000 ind 11 and temperature was maintained at 14c.
Biochemical profiles of paralarvae and nutritional requirements

Proteins and amino acids proteins are the major organic component of octopus tissue. in contrast to the lipid-based metabolism found in many animal groups (i.e., mammals), cephalopods have a vigorous protein and amino acid metabolism (lee 1994). Due to the rapid growth of octopus paralarvae, there is a large amino acid requirement for maintaining optimal growth and to supply the fuel for energy. Mobilization of muscle protein provides metabolic energy during periods of starvation and the direct use of protein as an energy reserve may account for the lack of major glycogen or lipid reserves in cephalopod tissues (storey & storey 1983, oDor et al. 1984). The total protein content measured as N 6.25 in O. vulgaris hatchlings represents 73% of the dry weight. however, it should be noted that total amino acid and the non-protein nitrogen content represent 44% and 37% of the dry weight, respectively (Villanueva et al. 2004). This high non-protein nitrogen content is of a similar range to that reported for adult cephalopods (Robertson 1965, sikorski & kolodziejska 1986, iida et al. 1992, Ruiz-capillas et al. 2002). Major components of this nitrogen fraction are volatile bases such as ammonia and trimethylamine oxide, creatine, free amino acids, nucleotides, purine bases and urea. lysine, leucine and arginine represented 49% of the total essential amino acids and glutamate and aspartate represented 47% of the non-essential amino acids for O. vulgaris hatchlings (Villanueva et al. 2004) (Figure 34). Fasting experiments in O. vulgaris hatchlings demonstrated mobilization of amino acids as a fuel resource (Villanueva et al. 2004). After 2 days, proline was the first free amino acid to be deleted. This amino acid is involved in oxidative metabolism in cephalopods, showing notable drop in mantle muscle concentrations during exercise in adult squid (storey & storey 1978) and probably is also actively metabolized during the continuous, energetically expensive jet-propelled swimming that is characteristic of octopus paralarvae. After 4 days of fasting, the levels of free non-essential amino acids decreased to nearly half of hatching levels (with the exception of cysteine), the level of essential amino acids decreased in both the total content and free forms, free tyrosine was not detected and animals lost 28% of their dry weight. Reared individuals at 25 days of age showed an
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12 10 8 6 4 2 0 12 10 8 6 4 Amino acid content (mg/100 mg dry weight) 2 0 12 10 8 6 4 2 0 12 10 8 6 4 2 0 12 10 8 6 4 2 Ovary Hatchlings Eggs X-XI H. fasted 2d H. fasted 4d Eggs I-II 0 Thr Phe Val lle Arg 12 10 8 6 4 2 0 12 10 8 6 4 2 0 12 10 8 6 4 2 0 12 10 8 6 4 2 0 50 40 30 20 10 Ovary Eggs X-XI Hatchlings H. fasted 2d H. fasted 4d Eggs I-II 0 EAA Met Lys Leu His
Figure 34 Total amino acid content (mean and standard deviation in mg 100 mg1 of dry weight) of Octopus vulgaris from mature ovary, spawned eggs at stages iii and XXii, hatchlings, and hatchlings fasted for 2 and 4 days. EAA, essential amino acids. (Reproduced with permission from Villanueva et al. 2004.) 152

60 Total amino acid (% DW) 55 50 45 40 15 14 12 11 10 9 8 7 6 0 1 2 3 Dry weight (g) 4 5 Total lipid (% DW) 13
Figure 35 Mean value of total amino acid content (solid circles) and total lipid content (open circles) in Octopus vulgaris hatchlings (0.3 mg dry weight, DW) and five wild, recently settled O. vulgaris juveniles of 814, 1128, 1380, 2189 and 3671 mg DW. (Data obtained from Navarro & Villanueva 2000, 2003 and Villanueva et al. 2004.)
increase in free essential amino acids in comparison with hatchlings, and glutamate was the most abundant free amino acid, followed by arginine and aspartate. These amino acids, with leucine and lysine, were also the most abundant in the total content, although glutamate had the highest levels. For free essential amino acids, arginine reaches the highest levels and represents nearly half of the free essential amino acid pool for hatchlings, 55% after 4 days of fasting, 3859% at 10 days and 3245% at 25 days of rearing (Villanueva et al. 2004). The total amount of amino acids in O. vulgaris paralarvae is lower than in recently settled juveniles. These biochemical changes associated with paralarval and juvenile growth are related to morphometric changes in body proportions, mainly due to the notable growth of the arms (Naef 1923, 1928, Boletzky 1977a, Nixon & Mangold 1996, Villanueva et al. 2004), which continues throughout development because juveniles have arm lengths four to five times shorter than subadult and adult individuals (i.e., O. vulgaris; Villanueva 1995). The development of the protein-rich muscular arm crown is accompanied by a relative decrease in total lipid content (Navarro & Villanueva 2003), this being due to the relative decrease of the visceral mass in which lipids are abundant (oDor et al. 1984) (Figure 35). Lipid and fatty acids octopus paralarvae have relatively low lipid content. lipid represents 1114% of dry weight in O. vulgaris hatchlings and variation in this content throughout paralarval growth (1125%) in rearing experiments seems to be related to diet (Navarro & Villanueva 2000, 2003, Moxica et al. 2002, okumura et al. 2005a). The lipid-rich nervous system of hatchling O. vulgaris paralarvae represents approximately one quarter of the animals fresh weight (packard & Albergoni 1970), suggesting the importance of lipids in the diet to maintain suitable growth during planktonic life. After settlement, the total lipid content of wild juveniles decreases, ranging from 7% to 13% of total dry weight in animals of 453671 mg in dry weight. The lipid content in recently settled octopuses was found to be significantly and negatively correlated with the weight of juveniles due to morphometric changes associated with arm growth (Figure 35) and could be fitted to the following regression equation (Navarro & Villanueva 2003): lipid (%) = 11.436 0.0016 dry weight (mg)
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35 30 % of total lipid 25 20 0 15 10 5 pa/cl mag/pigm chol dag lpc tag sm 0
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Lipid class
Figure 36 lipid class composition as percentage of total lipid in Octopus vulgaris hatchlings (solid bars), Pagurus prideaux hatchling zoeae (grey bars), Artemia biomass enriched with superselco (open bars) and 30-day-old reared O. vulgaris fed with Artemia (bars with transverse lines). Data as mean of four replicates. Error bars are standard deviation. chol, cholesterol; dag; diacylglycerides; ffa, free fatty acids; lpc, lysophosphatidylcholine; mag/pigm, monoacylglycerides/pigments; pa/cl, phosphatidic acid/cardiolipin; pc, phosphatidylcholine; pe, phosphatidylethanolamine; pi, phosphatidylinositol; ps, phosphatidylserine; se, sterol esters; sm, sphingomyelin; tag, triacylglycerides. (Reproduced with permission from Navarro & Villanueva 2000, modified.)
in general, the lipids of hatchling O. vulgaris are rich in cholesterol (24%), phosphatidylcholine (21%), phosphatidylethanolamine (16%), and sterol esters (14%) and are relatively low in triacylglycerides (6%) (Navarro & Villanueva 2000) (Figure 36). Endogenous synthesis of cholesterol is absent in adult cuttlefishes (Zandee 1967), suggesting that cholesterol is an essential dietary nutrient in cephalopods; the cholesterol requirements of octopus paralarvae, however, have been not examined in detail. The use of reserve lipids has been recorded during fasting of hatchling O. vulgaris paralarvae because the animals reduce their content in triacylglycerides and monoene fatty acids after 3 days (Quintana et al. 2006). in hatchlings, fatty acids represent 4.6% of lipids of which 27% were saturated, 14% were monoenes and 49% were puFAs and the majority of the puFAs were n-3 (36%) and longer than 20 c atoms (Navarro & Villanueva 2000). The dietary requirements for n-3 puFA, particularly docosahexaenoic acid (DhA), is critical in early developmental stages of fishes and crustaceans due to their high demand in membrane synthesis, where the n-3 puFAs are incorporated (henderson & sargent 1985). The same role is expected for early stages of cephalopods (Navarro & Villanueva 2000). levels of DhA and eicosapentaenoic acid (EpA) fatty acids in O. vulgaris hatchlings represent 2127% and 1318% of the total fatty acids, respectively (Navarro & Villanueva 2000, okumura et al. 2005a, kurihara et al. 2006). The effect of the fatty acid composition of food is evident in paralarvae within a few days of hatching. it has been suggested that their presence in the diet is critical for the early development of paralarvae because their levels are associated with healthy and normal paralarval growth in rearing experiments (Navarro & Villanueva 2000, 2003, hamasaki & Takeuchi 2001, Moxica et al. 2002, okumura et al. 2005a, kurihara et al. 2006). A ratio of DhA/EpA of approximately 1.5 seems a necessary condition for normal growth and development of O. vulgaris paralarvae. high mortality and poor growth associated with nutritional imbalance in fatty acid profiles has been observed when
154
se
pi
BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs DhA/EpA is <1.5 (Navarro & Villanueva 2000, 2003, okumura et al. 2005a). DhA plays an important role in maintaining the structural and functional integrity of cell membranes in fishes (sargent 1995) and this fatty acid may be even more important for healthy development and survival of the fast-growing, phospholipid-rich octopus paralarvae. Elemental composition The elemental composition of hatchlings, reared paralarvae and recently settled wild juveniles of O. vulgaris was reported by Villanueva & Bustamante (2006) (Figure 37), showing that s, Na, k, p and Mg were the main elements present, and levels of Ag, cu, Mn, Ni and Zn higher compared with other cephalopod hatchlings such as Loligo vulgaris and Sepia officinalis. concentrations of non-essential elements (Ag, Al, Ba, cd, hg, pb) found in hatchlings and reared paralarvae of Octopus vulgaris are lower compared with those found in subadult and adult octopuses (seixas et al.
30000 25000 20000 15000 10000 Elemental content (in g g1 of dry weight) 5000 0 30000 25000 20000 15000 10000 5000 0 30000 25000 20000 15000 10000 5000 octopus wild juveniles M. brachydactyla Artemia-fed octopus Artemia nauplii octopus hatchlings 0 P Mg 400 350 300 250 200 150 100 50 0 400 350 300 250 200 150 100 50 0 400 350 300 250 200 150 100 50 0
As
Cu
Zn
octopus wild juveniles
M. brachydactyla
Figure 37 comparison of mean and standard deviation in elemental content (g g1 dry weight, DW) for some major (s, Mg, p) and minor (As, cu, Zn) essential elements in Octopus vulgaris hatchlings (mean DW 0.34 mg), Artemia-fed 20-day-old O. vulgaris (mean DW 0.68 mg), O. vulgaris wild juveniles (mean DW 1836 mg) and prey (Maja brachydactyla hatchling zoeae and Artemia nauplii). (Reproduced with permission from Villanueva & Bustamante 2006, modified.) 155
Artemia-fed octopus
octopus hatchlings
Artemia nauplii
RoGER VillANuEVA & MARk D. NoRMAN 2005), showing their incorporation during growth. The richness of cu in O. vulgaris hatchlings is remarkable (217 g g1 dry weight) and may indicate a particular nutritional requirement for this element during paralarval growth. copper is of particular interest due to its critical role in haemocyanin, the respiratory pigment that represents 98% of cephalopod blood proteins (Ghiretti 1966, DAniello et al. 1986). Reared 20-day-old O. vulgaris paralarvae that were fed on Artemia nauplii (a prey with relatively low cu content [9.5 g g1] in comparison with natural prey such as Maja brachydactyla zoeae [72.5 g g1]), showed nearly half the cu content of the natural profile for octopus hatchlings or wild juveniles, suggesting a dietary effect (Figure 37). These findings concur with nutritional experiments carried out on recently settled (34 g fresh weight), subadult and adult Octopus vulgaris fed with sardine (low cu content) versus control animals fed with crab (high cu content). in the sardine-fed animals, the cu content in the digestive gland (the main reserve for cu) dropped to 1/10 compared with controls after 3 months of this diet. haemocyanin disappeared from the circulating blood and the octopuses died after 5 months of rearing (Ghiretti & Violante 1964). Zinc content of octopus paralarvae seems to be inversely related to cu content as individuals with low levels of cu (fasted or reared paralarvae) showed significant increases in Zn content compared with hatchlings or juvenile wild octopuses with their higher levels of cu (Villanueva & Bustamante 2006). Zinc can act as a metabolic antagonist of cu because they compete for binding sites on the proteins responsible for mineral absorption and/or synthesis of metalloenzymes (Watanabe et al. 1997, lall 2002, craig & overnell 2003). octopuses are carnivores and the majority of their elemental composition can be assumed to be derived from their diet. however, absorption also takes place directly from seawater, as observed under experimental conditions for strontium and cobalt (hanlon et al. 1989, Miyazaki et al. 2001). strontium is of critical importance for statolith development and thus normal swimming behaviour and survival of hatchling cephalopods, including octopuses. Egg incubation in artificial seawater without strontium produced O. vulgaris hatchlings that showed behavioural defects characterized by swimming in a spinning motion (spinners). statoliths from O. vulgaris spinners were irregular in shape and considerably reduced in size compared with control animals. some strontium-deficient animals lacked one or both statoliths. Normal development of the aragonite statoliths and normal swimming behaviour were obtained when strontium levels reached 8 mg 11 (hanlon et al. 1989). cobalt also seems to be important in the development of adenochrome, the red-violet pigment that confers a characteristic purple colour to the branchial hearts of octopuses, the organs involved in excretion processes. Miyazaki et al. (2001) showed that O. vulgaris hatchlings incorporate radio-labelled cobalt in the digestive gland and the inner side of the branchial hearts within 1 min of immersion in radiolabelled seawater. other organs and tissues were not radiographed. Miyazaki et al. (2001) suggested that adenochrome might be a cobalt-binding substance, in addition to iron, and that the radio-labelled cobalt may indicate the incipient development of adenochrome in the hatchlings.
Growth and duration of the planktonic stage

Size at hatching
A comparison of morphometrics of planktonic hatchlings in octopodidae is shown in Table 4. There is a wide range of sizes, from 2.5 to 18.3 mm in total length in fresh individuals, with the larger hatchlings belonging to the largest of the benthic octopuses, genus Enteroctopus. shrinking due to fixation in preserved hatchlings shows that Ml and total length can be 1225% and 1317% shorter (respectively) in preserved specimens compared with fresh (unpreserved) material (Boletzky et al. 2001, ortiz et al. 2006). These differences should be considered when comparing species and data from the literature. The number of suckers per arm also shows a considerable interspecific variation ranging from 3 to 21 (Table 4, Figure 38). The number of suckers is not affected by preservation
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs Table 4 size and sucker number per arm in hatchlings of octopodidae species with planktonic stages
Measured fresh or preserved Np F F p Np Np p Np Np F Np Np F Np p F F Np Np Np Np F F Np F Np F F Np 2.6 1.12.0 Number of suckers per arm 6 2.5 0.08 5.5 4.8 9.3 10 (9.510.1) 68 3.4 8.4 0.7 4.5 2.3 7.1 (6.77.6) 4 3.8 0.1 2.42.6 1.7 0.2 1.9 0.98 1.5 0.1 3.54 6.9 18.3 1.7 1114 1012 4 7 Geographic area indian ocean NW Atlantic Mediterranean
species Amphioctopus aegina Amphioctopus burryi Callistoctopus macropus Enteroctopus dofelini
Ml 3.1 0.1 1.5 0.05 4 3 5.35.5 3.5
Tl
Reference ignatius & srinivasan 2006 Forsythe & hanlon 1985 Boletzky et al. 2001
NW pacific NW pacific NE pacific NE pacific NE pacific sW Atlantic Mediterranean central E pacific sW pacific NE pacific hawaii islands sW pacific NW Atlantic NW pacific sE pacific sE pacific sE pacific Mediterranean sW pacific E indian NW pacific NW pacific Mediterranean NW pacific Mediterranean
Enteroctopus megalocyathus Eledone cirrhosa Hapalochlaena lunulata Macroctopus maorum Octopus bimaculatus Octopus cyanea Octopus huttoni Octopus joubini Octopus laqueus Octopus mimus
21.2 2.7 8 10 78 4 3 4 68 3 3 3 3 4 3
yamashita 1974 okubo 1979 Gabe 1975 snyder 1986a, snyder unpublished hartwick 1983 ortiz et al. 2006 Mangold et al. 1971 overath & Boletzky 1974 Batham 1957 Ambrose 1981 young et al. 1989 Brough 1965 (as Robsonella australis) Forsythe & Toll 1991 kaneko et al. 2006 Warnke 1999 Baltazar et al. 2000 castro-Fuentes et al. 2002 Mangold-Wirz et al. 1976 Dew 1959 (as O. cyanea) Joll 1976 itami et al. 1963 hamazaki et al. 1991 Villanueva 1995 okumura et al. 2005a,b Boletzky 1984
3.3 0.3 2.0.2.4 1.9 3.1 0.1 5.5 2.5 2.5 3.2 (33.5) 2.9
Octopus salutii Octopus tetricus Octopus cf tetricus Octopus vulgaris
2.1 (22.3) 2
3 4 3 3.74 4
Scaeurgus unicirrhus
Note: only species in which individuals hatched in the laboratory from egg masses laid from a previously identified female have been included. F, fresh; Ml, mantle length; Np, not provided; p, preserved; Tl, total length. Measurements in millimetres.
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24 Num. of suckers per arm 21 18 15 12 9 6 3 0 0 2 4 6 ML (mm) 8 10
Figure 38 Relationship between mean number of suckers per arm and mantle length (Ml) for hatchlings of 14 octopodidae species with planktonic stages. The figure only includes species for which individuals hatched in the laboratory from egg masses laid by identified females (see Table 4). Black circles indicate species measured fresh; white circles indicate species measured after fixation (with presumed shrinkage), as well as species for which measurement conditions (fresh or preserved individuals) were not indicated. original.
methods and provides a useful parameter of paralarval size and growth. Distal suckers are usually smaller than the other suckers at hatching, with some exceptions, such as Amphioctopus burryi, which hatch with four suckers per arm with the proximal sucker being considerably smaller (Forsythe & hanlon 1985). intraspecific variation in size and number of suckers at hatching has been reported for species such as Octopus vulgaris from the north-west pacific. Females collected from the same region produced hatchling individuals ranging from 1.1 to 3.2 mg mean fresh weight and three to four suckers per arm (okumura et al. 2005a,b, kurihara et al. 2006). Maternal body size and egg incubation temperature also influence hatchling size in O. vulgaris because female weight is positively correlated with hatchling size (in Ml and mantle width) (r = 0.681) and hatchling size is negatively correlated with the egg incubation temperature (r = 0.381) (sakaguchi et al. 2002, sakaguchi 2006). There is a similar tendency in other cephalopod groups because egg incubation at warmer temperature produces comparatively smaller hatchling sizes in cuttlefish (Bouchaud 1991) and loliginid squids (Villanueva 2000, Gowland et al. 2002, Vidal et al. 2002, pecl et al. 2004).
Ageing and factors influencing growth

The analysis of statolith growth increments, a technique routinely used to estimate age and growth in squids, is not possible in octopods due to the crystallization characteristics of their statoliths loose composites without evident growth increments. As a consequence, other hard structures have been investigated to find periodic depositions of growth. The number of concentric rings in the lateral wall of upper beaks from reared O. vulgaris paralarvae proved to be highly correlated with their age in days during the first month of life (hernndez-lpez et al. 2001). The internal shell remnants (stylets) in the family octopodidae also have growth increments in the form of concentric layers (sousa-Reis & Fernandes 2002, Bizikov 2004) and their deposition proved to be daily under aquarium conditions for a species with direct benthic hatchlings, O. pallidus (Doubleday et al. 2006). The internal shell analysis promises to be a helpful technique to be used in the future in ageing of octopus paralarvae. Fluorochrome alizarin complexone is an effective chemical marker because it is incorporated into the statoliths of O. vulgaris hatchlings (Fuentes et al. 2000) and adults (sakaguchi et al. 2000, sakaguchi 2006), suggesting that this marking technique could potentially be used to identify alizarin-stained octopod paralarvae.
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60
Age at settlement (d)
50
40
30
y = 168566x2.6676 r = 0.9476 16 18 20 22 24 26 28 30
20 Temperature (C)
Figure 39 Relationship between the mean rearing temperature and age at settlement from successful rearing experiments of Octopus vulgaris. Error lines indicate temperature ranges. (Data obtained from itami et al. 1963, Villanueva 1995, iglesias et al. 2004 and carrasco et al. 2006.) Exponential regression line, equation and correlation coefficient indicated. original.
After hatching the main abiotic factor influencing planktonic octopus growth seems to be temperature, as has been observed in other cephalopod paralarvae (Forsythe 1993). hamasaki & Morioka (2002) reared O. vulgaris hatchlings at temperatures of 17c, 19c, 21c, 23c, 25c, 27c and 29c and fed with Artemia prey (1.52 mm in length) over the first 40 days of life. They concluded that growth rate increased with increasing rearing temperature up to 21c, and that temperatures higher than 27c were not suitable for this species. under suitable temperature, food and settlement conditions, it would be expected that age at settlement would be inversely correlated with temperature. in fact, a comparison of successful rearings to settlement using crustacean zoeae as food for O. vulgaris (itami et al. 1963, Villanueva 1995, iglesias et al. 2004, carrasco et al. 2006) shows that warmer rearings produced faster growth and that settlement was observed earlier (Figure 39). Modelling of O. vulgaris settlement patterns according to temperature in temperate latitudes suggests shorter planktonic periods when temperature is increasing (early spring to midsummer) or longer planktonic periods when temperature is decreasing (during autumn and winter) (katsanevakis & Verriopoulos 2006). The duration of the planktonic period in octopodidae seems to be species specific, temperature dependent and, under laboratory conditions, ranges from 3 wk in the pygmy octopus O. joubini to 6 months in the giant octopus Enteroctopus dofleini (Table 3). This is a considerable proportion of the life cycle, taking into account that, under laboratory conditions, life cycle of the same species (including embryonic period) ranges from 6 months to 3.5 yr (Forsythe & Toll 1991, snyder unpublished manuscript). in addition to prey availability, it is reasonable to suspect that behaviour and associated spatial distributions can influence planktonic growth. Vertical migration rhythms and related residence periods in the water column at different temperatures need to be investigated to obtain a more precise view of the expected growth and related duration of planktonic life in octopuses.
Behaviour
Swimming behaviour
The locomotion of octopus paralarvae is based primarily on jet propulsion, the characteristic mode used by most octopods for swimming (Wells 1990). The main exception is fin swimming in the
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Figure 40 schematic line drawing showing differences between the mantle cavities of octopodidae and loliginidae paralarvae. left, Octopus vulgaris (3-mm mantle length [Ml], aged 20 days) with two cavities (ventral and dorsal), compared with Loligo opalescens (7.8-mm Ml, aged 50 days) with only one dorsal mantle cavity (right). individuals not at the same scale. (original drawing from J. corbera.)
semigelatinous deep-sea cirrate octopods (collins & Villanueva 2006). The funnel, pallial aperture and interbrachial webs of octopus paralarvae are proportionally more developed than those of squids. Their arms are also larger, increasing in relative length as the animal grows. During a jetting cycle, the contraction of the mantle and collar muscles produces high hydrostatic pressure inside the mantle cavity, which generates a propulsive jet of water through the funnel, resulting in the displacement of the animal. During the first days after hatching, the volume occupied by the internal yolk reserve in cephalopods probably reduces the effective water volume available for ventilation and jet propulsion. using ultrasonography and optical methods to estimate ventilation volume of Octopus vulgaris paralarvae, Tateno (1993) showed that fraction ejected during the first 2 wk of life increased with growth. swimming in octopus paralarvae differs from other planktonic and pelagic cephalopods due to the particulars of their morphology. octopus paralarvae lack fins and the vanes or keels found on the lateral arms of many decapodiform cephalopods (i.e., ommastrephid squids). The body of planktonic octopus paralarvae tends to be globular and less elongate than in planktonic squids, which typically have a shell (gladius) that guides mantle contraction during jet propulsion. in addition to the ventral mantle cavity, octopuses also have a dorsal cavity, absent in most squids (Figures 40 and 41). The relative percentages of water that occupy the dorsal and ventral cavities during the jetting cycle in octopus paralarvae are still unknown and need to be quantified in order to understand their swimming capacities. cranchiid squids (clarke 1962) and pelagic octopods (packard & Wurtz 1994) have dorsal and ventral mantle cavities that facilitate sophisticated swimming and manoeuvrability through independent control of both cavities. swimming behaviour in octopus paralarvae that hatch at a small size (as in O. vulgaris) modifies as the animal grows from hatching to settlement. These changes are directly related to morphometric changes, primarily the strong development of the muscular arm crown (Villanueva et al. 1996). similarly, differences in swimming behaviour can be expected for different octopus species according to the specifics of their hatchling size and body form. Swimming behaviour of planktonic paralarvae hydrodynamic forces probably dictate the swimming capacities and related behaviour of different species of octopus paralarvae. however, other unknown neurological and/or physiological characteristics may also play roles. The paralarvae of two species groups provide examples of extremes in form and swimming behaviour: (1) small planktonic hatchlings (Ml ~2 mm) with short arms and ~3 suckers per arm (O. vulgaris-type) and (2) large planktonic hatchlings (Ml ~6 mm) with long
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Figure 41 The use of the dorsal and ventral mantle cavities for jet swimming in Enteroctopus dofleini hatchlings. The left individual is shown during the inhalatory phase; note the anterior part of the dorsal mantle and the ventral mantle cavities expanded by the internal water pressure and the relatively flaccid funnel. The right individual is in the expulsive phase; note the contracted dorsal and ventral mantle cavities and the rectilinear funnel due to the expulsion of water from the mantle. (Reproduced with permission from okubo 1973.)
arms and >10 suckers per arm (Enteroctopus-type). There seems to be a continuum between these two extremes. large planktonic hatchlings with short arms have not been described to date. using video-recording techniques, the swimming behaviour in Octopus vulgaris was studied by Villanueva et al. (1996) in groups of individuals aged 1, 15, 30, 42 and 60 days (by which time they had become benthic). Backwards, squid-like swimming is the predominant type of locomotion during routine swimming throughout planktonic life, with forward displacement representing only 1% of swimming (excluding prey capture sequences; see capture of live prey, p. 144). cruising swimming speed increased as animals grew and relative swimming speed in units of octopus length decreased with size (Figure 42). The mean speed and distance covered during a burst jet cycle ranged from 41 to 95 mm s1 and 6 to 23 mm at respective ages of 1 and 60 days. The mean maximum speed reached was 211 mm s1 for individuals aged 30 days and 4.5 mm in Ml. These maximum speed values are similar in range to those observed for hatchling squid paralarvae: 160 mm s1 in Loligo vulgaris (packard 1969), 150250 mm s1 in L. forbesi (Zuev 1964 in Mileikovsky 1973) and 52 mm s1 in Illex illecebrosus (oDor et al. 1986). in captive large octopus paralarvae, such as those of the genus Enteroctopus, constant swimming by jet propulsion is intermittently interspersed by descent to the bottom of the rearing tank for short periods of time, as has been reported for E. dofleini (Gabe 1975, snyder unpublished manuscript). During the first month of life E. dofleini actively use their arms and tactile discrimination to collect floating inert food from the water surface film, described by Marliave (1981) as neustonic feeding (see capture of inert prey, p. 146). one of the most extreme examples in a hatchling considered to be planktonic is that of E. megalocyathus, for which hatchlings have a mean of 21 suckers per arm and can swim slowly with loose arms for several hours at a time in the water column, as well as crawling for short distances on the substratum of the aquaria (ortiz et al. 2006). When disturbed, animals responded in two ways: swimming (sometimes ejecting ink) or crawling on the aquarium substratum with a coordinated action of the arms and displaying expanded chromatophores. ortiz et al. (2006) suggest that E. megalocyathus hatchlings may reside in the water layer close to the seafloor, the hyperbenthos (sensu Mees & Jones 1997), for a short period until they attain a benthic mode of life. Swimming behaviour of micronektonic paralarvae Wild observations of paralarvae on moonless nights over deep water (~1 km) in the coral sea found significant differences in swimming behaviour between different species of paralarvae
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Age (days) 2 10 20 30 40 50 60
100 Cruising speed (mm s1) 90 80 70 60 50 40 30 20 10 0 2 2.9 6.4 4.5 ML (mm) Crawling 8.6
240
imm Sw
ing
220 200 180 160
Figure 42 Mean and standard deviation of cruising swimming speed (in mm s 1) (black squares) and total length index (white squares) versus mantle length (Ml, in mm) and age (in days) of Octopus vulgaris paralarvae. crawling speed of recently settled individuals aged 60 days is also indicated. Data collected from digitized video recordings of groups of five individuals. Top, schematic drawings of O. vulgaris individuals aged 1, 30 and 60 days. (Reproduced with permission from Villanueva et al. 1996.)
(M.D. Norman unpublished data). Those paralarvae with short arms and near-spherical bodies (i.e., Figure 9) showed relatively slow swimming speeds. longer-armed, more elongate species (such as Callistoctopus sp.; Figure 4 top) swam faster and took on an elongate form superficially similar to small ommastrephid squid also occurring in the same environment (Callistoctopus sp.; Figure 43). This body form may partially explain why certain micronektonic paralarvae are able to delay settlement (see prolonged paralarval stages, p. 182). From hydrodynamic and energetic perspectives, these paralarvae may be adopting a squid-like strategy: an elongate mantle that enables more energy-efficient jet swimming. This form of locomotion is not possible as a prolonged mode of swimming for settled, benthic octopuses because their small mantle volume cannot power the displacement of relatively long and heavy muscular arms (Wells et al. 1983b, 1987) (see also The settlement process, p. 176). in addition to jet propulsion, long-armed large paralarvae such as Macrotritopus defilippi have been observed in the wild drifting with all arms spread out radially. The animal seems almost neutrally buoyant, remaining almost stationary with little or no jetting (hanlon et al. 1985). These animals also combined these modes of locomotion with slow backwards jet swimming with the arms trailing in a V and the tips usually curled, but also with fast backwards jets when disturbed by a diver. it is remarkable that these animals were also observed to crawl over a coral substratum and as described by hanlon et al. (1985, p. 238): they spread the arms radially and landed oral surface first. Both animals quickly slid into holes and disappeared from view. it was clear that the substrate was not alien to them. More research is necessary to understand swimming behaviour in octopus paralarvae. some similarities can be expected with the complex slow-swimming behaviour of small squids that employ various fine-scale adjustments, such as manipulating funnel diameter during jetting, altering arm
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Total length index
Figure 43 (see also colour Figure 43 in the insert.) unidentified paralarva of the genus Callistoctopus from the coral sea, Australia, showing elongate form when swimming. photograph taken in situ while night diving on a moonless night at ~10 m deep over a seafloor depth of 450 m at osprey Reef, coral sea, Australia. (photo: M.D. Norman.)
position and swimming in different orientations to increase swimming performance (Bartol et al. 2001). in addition, the proportion of water volume ejected from the mantle is expected to change throughout paralarval stage, as occurs in hatchling squid, for which this volume is proportionally higher compared with later growth stages (Thompson & kier 2001a,b, 2006).
Crawling
crawling behaviour is readily observed in hatchling paralarvae contained in captivity. The physical constraint of aquaria may account for some or all crawling behaviour over aquaria surfaces (i.e., Joll 1978, Ambrose 1981). however, in hatchlings of some species such as Enteroctopus megalocyathus (see p. 161), a combination of swimming and crawling has been reported (ortiz et al. 2006). An adhesion reflex, in which the suckers are pressed against a surface and coordinated crawling takes place, can be experimentally induced in planktonic hatchlings of Scaeurgus unicirrhus by reducing the space available down to a droplet of water (Boletzky 1977b). crawling of octopus paralarvae on hard substrata has also been observed in the wild. paralarvae of at least three species attracted using lights at night over deep water in the coral sea readily adhered to any hard surfaces, particularly ropes, buoys, light traps, divers and camera housings (M.D. Norman personal observation). on several occasions paralarval numbers of one unidentified species were so numerous that thousands of animals completely covered the mooring lines between the ship and a boat tender, while all divers returning from night dives were covered in crawling paralarvae. Rafting behaviour has been reported for both paralarval (smale & Buchan 1981) and adult octopuses by which they attach on floating surface objects. Thiel & Gutow (2005) listed 11 species of cephalopods rafting on wood or macroalgae, including adult Octopus bimaculatus, O. bimaculoides, O. micropyrsus, O. variabilis and O. vulgaris. This may have advantages both as a means of passive transport/energy conservation and as potential food-aggregating structures.
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Responses to light and gravity

positive phototaxis seems to be a common response to light in octopus hatchlings as well as in some later paralarval stages. under laboratory conditions, positive phototaxis has been reported for hatchlings of several species, including Amphioctopus burryi (Forsythe & hanlon 1985), Enteroctopus dofleini (Ruggieri & Rosenberg 1974, yamashita 1974, okubo 1979), Macroctopus maorum (Batham 1957), Octopus bimaculatus (Ambrose 1981), O. cyanea (Dew 1959), O. mimus (Montoya 2002), O. vulgaris (Vevers 1961, Villanueva 1995, Nixon & Mangold 1998), O. huttoni (as Robsonella australis) (Brough 1965) and Wunderpus photogenicus (Miske & kirchhauser 2006). in contrast, negative phototaxis and an avoidance of strong light intensity has only been observed for hatchlings of one species, Octopus cf tetricus (Joll 1976) interesting behaviour that requires further research. in interpreting some hatchling behaviours, discrimination between positive phototaxis and negative geotaxis can be difficult. laboratory-hatched Enteroctopus dofleini that were transported to a hatching site in the field immediately began swimming up towards the surface (high 1976). Octopus bimaculatus hatched in the field during the daytime also swam upwards to depths of 15 m below the surface (Ambrose 1981). Rising hatchlings can be interpreted as either positive phototaxis (heading towards surface light) or negative geotaxis (resisting gravity and rising towards surface waters). Newly hatched squid Loligo pealei also rise to surface waters. sidie & holloway (1999) found use of lights at the bottom of experimental tanks could not prevent the vertical movement of the squid paralarvae towards the surface in the first 612 h after hatching. This suggests that negative geotaxis is the stronger factor in this behaviour. similar processes may occur in octopus paralarvae. Migration to surface waters could aid hatchling dispersal because surface currents may carry the paralarvae beyond the natal environments. Movement to surface waters may also enable access to neustonic prey such as crustacean zoeae. For tropical octopus species on isolated coral reefs, surface currents may transport hatchlings away from high-predator reef environments to the comparative safety of open ocean, potentially aiding in gene flow between coral reefs and atolls. positive phototactic behaviour has been used to collect octopus paralarvae at night in the field. using light traps, Moltschaniwskyj & Doherty (1995) collected 2066 individual octopus paralarvae on the Great Barrier Reef, estimating this number to be around half the total number of planktonic cephalopods attracted to their lights. The strong response of octopus paralarvae towards light may be higher than for other planktonic cephalopods. light attracts not only hatchlings, such as Enteroctopus dofleini collected on surface waters (packard 1985), but also relatively large paralarvae such as those of the Macrotritopus defilippi species complex (hanlon et al. 1980b, Brower 1981, hanlon et al. 1985) and Amphioctopus burryi (hanlon et al. 1980b, Forsythe & hanlon 1985). some octopus taxa are only known from material attracted to lights in surface waters at night the unresolved paralarval form Octopus teuthoides is only known from a handful of micronektonic specimens (Robson 1929, Voss 1963, Norman & sweeney 1997). Tables 5 and 6 list planktonic and micronektonic octopus paralarvae collected using lights at night. under laboratory conditions, positive phototaxis appears to be strongest at the time of hatching and can be used to concentrate paralarvae within rearing tanks (i.e., feeding or transferring them to other reservoirs). positive phototaxis appears to decrease as the paralarval octopus approaches settlement (Villanueva 1995). however, there are no quantified studies on this subject. Fernndezlpez et al. (2005) tested the influence of light intensity (1000, 3000 and 6000 lux) on the survival and growth of captive-reared O. vulgaris paralarvae, obtaining the best results with the highest light intensity treatments during daylight periods. okumura et al. (2005a) suggest that the survival rate of O. vulgaris paralarvae was negatively affected by an unstable photoenvironment in captive-bred paralarvae exposed to variable intensities of natural light (due to cloud drift and intermittent full sun). changes in light tolerance throughout the planktonic stage were also observed by s. snyder
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Table 5
sampling methods, number of individuals collected and abundances of octopodidae paralarvae from the literature
species 0200 0200 Np 62 NE Atlantic Np 118 Midwater or near the bottom, rarely at surface largest individuals near to the seafloor higher from May to August higher from May to June NE Atlantic
Gear
horizontal or vertical towns Depth range (m) Abundances observations Reference stephen 1944 collins et al. 2002 Day/ night Geographic area
Number of individuals collected
Eledone cirrhosa
plankton net
Np
Variety of plankton nets 20760 Np 790 higher at <100 m; to 0.9 ind h1 of tow NE pacific
Enteroctopus dofleini Day and night Night 594 17
Net 100 cm
horizontal and oblique towns horizontal
Green 1973
Enteroctopus dofleini
Net 130 cm
horizontal
NW pacific
yamashita & Torisawa 1983 North pacific NE Atlantic kubodera 1991
conical net 130 cm 1540 Night 16
horizontal
020 over depths of 20200 surface
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02000 Day and night 161 96% ind collected between 0 and 100 m during daylight Day Np 197 388 From 100 to surface 20760 82% collected <50 km offshore higher at <100 m; to 0.9 ind h1 of tow 40 higher between 300 and 400 m; to 0.2 ind h1 observed 0400 Day
Absent on the surface, captured between 9 and 21 m subsurface Mean of 68 ind by positive tows
Macrotritopus defilippi
light
undersea laboratory
hanlon et al. 1980b, 1985 NE Atlantic
Macrotritopus sp.
8 m2 RMT and a 1-m2 ring net
Vertical
Found at bottom depths less than 400 m collected in temperatures of 2.66.7c collected from early June to mid-August large individuals, 715 mm Ml Represented 12% of the total cephalopods collected
Octopus cyanea
oblique
Octopus rubescens
2- and 4-m2 ring nets Net 100 cm
horizontal
hawaiian islands NE pacific
lu & clarke 1975 (as Scaeurgus unicirrhus) Bower et al. 1999 Green 1973
RoV
individuals observed
Found at bottom depths less than 300 m individuals forming shoals
NE pacific
hunt 1996
(continued on next page)
Table 5 (continued)
sampling methods, number of individuals collected and abundances of octopodidae paralarvae from the literature
species 0100 Found at bottom depths less than 155 m NW pacific NE Atlantic Np 69
Gear
horizontal or vertical towns Depth range (m) Abundances observations Reference Rees 1950 Day/ night Geographic area
Number of individuals collected
Octopus vulgaris
plankton net
Np
100 100 cm square net
horizontal
surface and 0.24 from the bottom surface Day and night 641
Mostly diurnals
159
Takeda 1990a
Bongo net 60 cm
horizontal
Abnormal high sea temperatures associated with abundance on the northern species range No specimens collected in surface during the day; higher abundances inshore at night and offshore during day; from 0.03 to 0.21 g 1000 m3 higher at night; 587 ind 1000 m3 No differences in size between individuals collected in surface or bottom layers Two hatching peaks: spring and fall, higher in fall NW pacific
sakaguchi et al. 1999
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Np 96 Day and night 584 Abundance depending on the strength of the upwelled water; to 8 ind 1000 m3 in surface during night, near the bottom at day; from 0.01 to 1 ind 1000 m3 Near the bottom at 35105 surface and near the bottom at 3685 0300 Np 1439 Abundant in coastal bays 020, few at 100 Night, around new moon 2066 higher in subsurface of Great Barrier Reef lagoon, low on the shelf; 0.075.57 ind h1
Bongo net 75 cm
horizontal
NE Atlantic
Gonzlez et al. 2005 NE Atlantic otero 2007
Bongo net 75 cm
horizontal
octopodidae
8-m2 RMT and Bongo 60-cm
oblique
sW Atlantic
Rodhouse et al. 1992
octopodidae
light trap
Drifting and anchored light traps
upwelling pulses positively related with paralarval abundance octopodidae represented 60% of total cephalopods octopodidae represented 53% of total cephalopods
Great Barrier Reef
Moltschaniwskyj & Doherty 1995
Note: Ml, mantle length; Np, not provided; RMT, rectangular midwater trawl; RoV, remotely operated vehicle.
BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs Table 6 Examples of large octopodidae individuals collected or observed on the water column or surface
Measured fresh or preserved F F p p p p p p F p Geographic area NW Atlantic NW Atlantic NE Atlantic NE Atlantic NE pacific NW pacific N pacific central E pacific NW Atlantic Atlantic and indian oceans Mediterranean and Atlantic NE Atlantic
species Amphioctopus burryi
size 1315 mm Ml 16 mm Ml
Gear light light Trawl plankton net Net 100 cm larval net conical net 130 cm ikMT light Bongo net
Depth (m) 21, under surface surface Np Np 20760 surface surface 0500 1540, under surface 0200
Reference hanlon et al. 1980b Forsythe & hanlon 1985 Rees 1955 Rees 1956 Green 1973 yamashita 1974 kubodera 1991 Nesis & Nikitina 1991 hanlon et al. 1980b, 1985 Nesis & Nikitina 1981 Joubin & Robson 1929 (as M. danae) lu & clarke 1975 (as Scaeurgus unicirrhus) Brower 1981 young 1972 (as Octopus sp.) present study, see Figure 44 Norman & sweeney 1997 spart 1933 Berry 1914
Callistoctopus macropus Eledone cirrhosa Enteroctopus dofleini
27 mm Tl 29 mm Tl To 14 mm Ml 3373 mm Tl To 14 mm Ml 11 mm Ml, ~ 43 mm Tl 1215 mm Ml 1.311 mm Ml
Euaxoctopus panamensis Macrotritopus defilippi
Macrotritopus sp.
913.5 mm Ml
plankton net
100300
2.510 mm Ml
RMT & ring net
0100
127 mm Tl Octopus rubescens 1525 mm Ml Not measured
F p
light ikMT observed from RoV
038, under surface 0770 60 m in an area of 728 m depth surface surface surface
hawaiian islands NE pacific NE pacific
Octopus teuthoides Octopus vulgaris octopodidae
To 16 mm Ml 50 mm Tl 14 mm Ml 56 mm Tl
p F? p
light light
central E pacific Mediterranean hawaiian islands
Note: F, measured fresh; ikMT, isaacs-kidd midwater trawl; Ml, mantle length; Np, not provided; p, measured preserved; RMT, rectangular midwater trawl; RoV, remotely operated vehicle; Tl, total length.
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RoGER VillANuEVA & MARk D. NoRMAN (unpublished manuscript) in captive-reared Enteroctopus dofleini. light intensity was reduced during the second half of the planktonic phase because high light levels resulted in premature settlement for a large number of individuals. light seems to play an important role in the predatory behaviour of octopus paralarvae although light may not be essential for capturing prey in O. vulgaris hatchlings (Mrquez et al. 2007). The behaviour and activity patterns of octopus paralarvae in the absence of light (or in low light levels) are practically unknown and require detailed research. Tateno (1993) suggested that ultrasonography can be used in the laboratory as a non-invasive technique to record octopus paralarval activity in total darkness. This technique may offer new insights. it must be noted that all behavioural observations of captive octopus paralarvae are severely limited by the removal of a critical attribute of the natural environment of these animals a realistic water column. Rearing tanks severely limit the capacity of the octopus paralarvae to adjust their depth in response to experimental factors such as changing light levels, prey, predators and tidal or lunar cycles. For example, natural variability in light levels may be at significantly lower levels than in experimental situations such as full sunlight on shallow rearing tanks. immediately following settlement, octopuses show strong negative phototaxis and reclusive behaviour, as observed under laboratory conditions in Octopus vulgaris (itami et al. 1963, Villanueva 1995) and O. cyanea (Wells & Wells 1970), a behaviour that is more typical of adult benthic octopuses. There are exceptions, however, because some octopuses possess ambiguous phototactic behaviour. During the early post-settlement period, spart (1933) collected relatively large juveniles of O. vulgaris (50 mm in total length) at night using surface lights in the strait of Messina, Mediterranean sea. Adult benthic octopuses will also swim towards surface lights at night, as has been observed for Callistoctopus aspilosomatis on the Great Barrier Reef (R. Fitzpatrick personal communication 2005, A. harcourt personal communication 2007) and sometimes in large numbers, as for an undescribed species of Callistoctopus in New caledonia (G. Boucher personal communication 1997).
Defences
Relatively high swimming speed may prevent paralarval capture by some predators. Bursts of jet swimming in O. vulgaris paralarvae can reach a mean swimming speed of 4195 mm s1 at age of 0 and 60 days, respectively, covering a mean distance of 623 mm, respectively. swimming paths in hatchling O. vulgaris are highly rectilinear in comparison with older paralarvae and may maximize dispersion of the individuals from the egg mass and minimize attraction of predators to the hatching site (Villanueva et al. 1996). in large paralarvae of Macrotritopus defilippi, inking and fast backward jetting have been observed as a response to the approach of divers, with 0.5-m traverses per jet outswimming a diver over 3 m of distance, followed by slow backward swimming to the seafloor (hanlon et al. 1985). in the open ocean, the most common form of defence by octopus paralarvae is likely to be a dive response, into the relative safety of deeper darker waters. such behaviour has been observed in Macrotritopus defilippi (hanlon et al. 1985), en masse for large Octopus rubescens paralarvae in Monterey Bay, california, in response to the approach of a deep-water remotely operated vehicle (RoV) (hunt 1996) and for unidentified octopus paralarvae in the coral sea (M.D. Norman personal observation). This escape response is common to many pelagic, shelled molluscs (both veliger larvae and holopelagic pteropods) (lalli & Gilmer 1989). in these molluscs, retraction of locomotory wings or ciliated podia combines with shell weight to enable rapid sinking. Because they have a lower specific gravity, octopus paralarvae use funnel jetting as additional propulsion to aid rapid descent. When the proportionally large and simple chromatophores of octopus paralarvae are contracted, the animals become nearly transparent, all except for the eyes, ink sac and visceral mass. These opaque organs are typically bound within a silvery membranous layer containing reflective iridophores. This combination of transparency and reflective body organs is a camouflage adaptation for
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs life in the water column of open ocean where animals are vulnerable to visual predators that detect prey by looking for silhouettes or outlines. Transparency is a remarkable characteristic of many oceanic zooplankton, an attribute uncommon in other aquatic habitats. it is generally accepted that transparency is a successful form of camouflage from visual predators and/or prey in the optically featureless pelagic environment (Johnsen 2001). Behavioural responses of planktonic octopodidae to predators have not been recorded in the field or laboratory. chromatophores and ink sac are fully functional in octopus paralarvae from hatching. chromatophore patterns may be used in concert with ink release to distract potential predators, as occurs in adult octopuses (hanlon & Messenger 1996). octopus paralarvae are likely to be particularly vulnerable to predation during prey capture because their motion is slowed and their attention is focused on prey. At this time, detection of potential predators may be lessened or suspended. During prey capture sequences, octopus paralarvae expand their chromatophores, changing to a dark coloration (hernndez-Garca et al. 2000), and perform a range of different swimming motions when focusing on the prey (Villanueva et al. 1996). These behaviours may increase the visibility of the paralarvae to predators (see Figure 30). Dark colouration may be used in concert with ink injection. As a series of ink decoys is released by a fleeing dark paralarva, rapid transformation to a transparent form with a rapid shift in trajectory may deceive or confuse a visual predator (Boletzky 1987). This behaviour is called a blanchink-jet manoeuvre and is found in many cephalopods (hanlon & Messenger 1996). A pursuing predator continues the chase trajectory and finds itself in empty water. Functional ink ejection has been observed in captive hatchlings, such as Enteroctopus dofleini (yamashita 1974, Gabe 1975, okubo 1979), Octopus cf tetricus (Joll 1978) and O. laqueus (kaneko et al. 2006) and in the wild for Macrotritopus defilippi (hanlon et al. 1985) and in unidentified paralarvae (M.D. Norman personal observation) in response to the approach of divers. potential schooling behaviour has been reported for the micronektonic paralarvae of one species, Octopus rubescens, off Monterey Bay, california (hanlon & Messenger 1996). Figure 44 shows such an aggregation, photographed from a deep-water RoV in this region. hunt (1996) reports high densities of paralarvae of this species at depths of 200400 m. it is unclear whether this is a potential defensive behaviour, an artefact of water column aggregations within the layer of vertically migrating zooplankton known as the scattering layer (see p. 175) or offers some enhanced feeding success.
Figure 44 (see also colour Figure 44 in the insert.) A dense swarm of Octopus rubescens with the jellyfish (Phacellophora camtschatica) photographed 26 June 2003 at 1115h local time from the RoV Ventana at a depth of about 60 m in 728 m of water in the Monterey submarine canyon, north-east pacific. Temperature 9c and oxygen concentration 2.66 ml 11. No euphausiids were observed on the dive tape. (image and data reproduced with permission from Monterey Bay Aquarium Research institute, 2003, MBARi.) 169
Predators on egg masses and paralarvae

As brooding females of most octopus species continually guard their eggs at a fixed permanent site, Ambrose (1988) proposed that they are more susceptible to predation. As the duration of brooding and embryonic development increases with decreasing temperatures, winter-brooding females thus have an even higher vulnerability to predation. Ambrose recorded 70100% mortality of brooding O. bimaculatus females monitored in the wild during winter off southern california. Moray eels (Gymnothorax mordax) were presumed to be the primary predators. The fate of the egg masses was unknown. The egg masses of Enteroctopus dofleini females that died prior to paralarval hatching on the British columbia coast, north-east pacific, were eaten by the crab species Chorilia longipes, Scyra acutifrons and Oregonia gracilis (cosgrove 1993). Two egg strings of the same species were also consumed by the seastar Evasterias troschelii in the presence of the live brooding female at 19 m depth in the same area (J.A. cosgrove personal communication 2006). Nesis & Nigmatullin (1981) reported egg masses of Eledone caparti from stomach contents of three blue sharks Prionace glauca (169182 cm length), collected off Dakar and cabo Verde. under aquarium conditions, eggs of Macroctopus maorum have been preyed on by the fissurellid gastropod, Scutus breviculus (Batham 1957). Brooding females of octopus species that carry their egg masses, such as Hapalochlaena (Dew 1959, Tranter & Augustine 1973, Norman 2000), Wunderpus photogenicus (Miske & kirchhauser 2006), Amphioctopus burryi (Forsythe & hanlon 1985) and Macrotritopus defilippi (hanlon et al. 1985) may be able to escape or hide from predators, suggesting a possible advantage over species that attach egg strings at a permanent site. however, in order to protect egg masses and themselves from predators, brooding females can partially or completely barricade the permanent spawning shelter with rocks or shells (Wodinsky 1972, Ambrose 1988, Anderson 1997) or close bivalve shells from within (Eibl-Eibesfeldt & scheer 1962). in open oceanic waters, pelagic fishes are the main predators of octopus paralarvae. longnose lancetfish (Alepisaurus ferox) actively prey on pelagic cephalopods, including octopus paralarvae. stomach contents for this species examined from around the pacific ocean (Rancurel 1970) included seven individuals of Macrotritopus forms (6.518 mm Ml) from the south pacific (1623 s); three Octopus teuthoides forms (1825 mm Ml) from East Tonga islands, south-west pacific and one individual of the same species (28 mm Ml) from West Midway islands, north-west pacific; and six unidentified and unmeasured planktonic octopodidae. stomach analysis of Alepisaurus ferox from suruga Bay, north-west pacific, found 68 individuals of Octopus sp, ranging in size from 7 to 23 mm Ml, of which 69% were 816 mm Ml and collected mainly during March (okutani & kubota 1976). in total, octopus paralarvae (octopodidae) were present in 11% (Rancurel 1970) or 12.5% (okutani & kubota 1976) of the A. ferox stomachs containing cephalopods. octopod paralarvae not sorted by families occurred in 3% of the stomachs of this fish in western equatorial indian ocean (potier et al. 2007). The albacore (Thunnus alalunga) is an active predator of pelagic and planktonic cephalopods. stomach contents of this species collected in the north-east Atlantic during July and october included seven young Eledone cirrhosa (2133 mm total length) in localities near cape Finisterre and five Octopus vulgaris (6.518 mm total length) collected in the Gascogne Gulf during August and october (Bouxin & legendre 1936). parker et al. (2005) reported unidentified cephalopod paralarvae in the diet of oceanic loggerhead sea turtles (Caretta caretta) in the central north pacific. All proved to be octopodid paralarvae (D.M. parker personal communication 2006). Ephyra larval stage of jellyfish scyphomedusae has been observed feeding on unidentified octopod paralarvae (Figure 45) from plankton samples collected off lizard island, Great Barrier Reef (p. parks personal communication 2007). in littoral waters, fishes are also expected to be the main predators of octopus paralarvae but, as far as we know, no references on this subject have been published and information only comes from
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Figure 45 (see also colour Figure 45 in the insert.) Ephyra larval stage of jellyfish scyphomedusa feeding on unidentified octopod paralarva. specimens collected using a plankton net at about 180 m depth, off lizard island, Great Barrier Reef. (Data and image reproduced with permission from peter parks/imagequestmarine. com.)
opportunistic personal observations. Fishes are attracted to octopus egg masses during hatching and have been observed during daytime at a short distance from the egg mass, preying on Octopus vulgaris individuals that have hatched seconds or minutes before, as has been observed for the Mediterranean dusky grouper (Epinephelus marginatus) at 1015 m deep in the Medes islands, north-west Mediterranean (R. coma personal communication 2006); serranid fish (Serranus sp.) at 15 m depth on the Ra de Vigo, north-east Atlantic (A. Guerra personal communication 2007); and the sand smelt (Atherina presbyter) that preyed on hatchlings from egg masses placed in floating cages for Octopus vulgaris ongrowing aquaculture in the Ria de Vigo, north-east Atlantic (J. iglesias personal communication 2007). cannibalism has not been observed in captive rearing of octopus paralarvae. under laboratory conditions, attacks on conspecifics have been reported for O. vulgaris paralarvae (Boletzky 1987, Villanueva 1995). however, these attacks do not result in cannibalism, as has been observed for juvenile and subadult benthic stages of some octopus species (i.e., itami et al. 1963, DeRusha et al. 1987, Aronson 1989, cortez et al. 1995b).
Species identification and diversity

prior to the review paper of hochberg et al. (1992), morphological descriptions and identification tools for octopus paralarvae were few and widely scattered in the literature. A number of researchers such as Berry (1914), chun (1915), Naef (1923), Degner (1925), Robson (1929) and Rees (1954)
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RoGER VillANuEVA & MARk D. NoRMAN along with subsequent researchers in the 1970s and 1980s described individual paralarvae amongst regional or broader treatments of the family. hochberg et al. (1992) were the first to compile a suite of diagnostic characters such as founder chromatophore patterns, sucker attributes, arm formulae and body shape. Table 1 lists those species of the family octopodidae that are known (or presumed) to produce planktonic paralarvae. Three categories of species are listed: (1) those for which planktonic paralarvae have been described from laboratory-hatched individuals, (2) those with small-type eggs (i.e., egg length typically less than 10% of Ml), and (3) species for which the eggs in the submature ovary can be estimated as being of the small-egg type produced in large numbers (versus large-type eggs produced in low numbers). The first category typically results from captive studies in which eggs hatch and young paralarvae are described. The second category typically comes from studies of preserved material for which laid eggs or mature ovarian eggs form the basis of the egg-type discrimination (sensu Boletzky 1977a, 19781979). The third category comes from dissection of preserved submature females as the only material available to provide any indication of early lifehistory strategy. in only a few studies have paralarval forms been successfully raised through to settlement, enabling identification of the post-settlement form. A good example is the Macrotritopus problem. in 1922, a distinctive paralarval form with greatly elongated third arms formed the basis of the generic name Macrotritopus Grimpe, 1922. on the basis of apparent left-handed male sexual modification (hectocotylization) in one specimen, Rees (1954) attributed all reports of this paralarval form to the seamount and continental slope genus, Scaeurgus. in parallel studies in the united states (hanlon et al. 1980a, 1985) and soviet union (Nesis & Nikitina 1981), Macrotritopus-type paralarvae were raised to adulthood and identified as the long-armed species Octopus defilippi (now treated as Macrotritopus defilippi; see Norman & hochberg 2005a). As representatives of this distinctive paralarval form have been found in the pacific and indian oceans, where M. defiliippi is not reported, it is possible that this distinctive paralarval form may represent more than one species (hochberg et al. 1992). other historical conundrums also await resolution. Octopus teuthoides Robson, 1929 was coined for a distinctive elongate paralarval form that received considerable attention in subsequent literature (see Norman & sweeney 1997, Toll & Voss 1998). The adult form, however, still awaits identification. At least 10 other octopodid taxa have been formally described on the basis of paralarval or juvenile material (Norman & hochberg 2005a). For many species of benthic octopuses, nothing is known of egg size or juvenile stages. in combination with the many species yet to be described by science, particularly in the tropical indo-pacific region (Norman & hochberg 2005a), we can be confident that the number of known paralarval species is far outweighed by the forms yet to be defined/described. in regions with well-known faunas or lower diversity in octopodid species, paralarvae are slightly better known (i.e., Mediterranean sea and eastern pacific off North America). in some cases, paralarval diversity can be a clue to total species diversity of benthic octopuses in a geographic region. F.G. hochberg & R.E. young (unpublished data) recognized 16 species of paralarvae in material collected around the hawaiian islands. At that stage, only eight species of benthic octopus were recorded from these islands, with some of these species being large-egg type (see Norman & hochberg 2005a). hence the estimates of species number in the region appeared to be a significant underestimate. subsequent studies have found new small-egg species in the region, such as Amphioctopus arenicola (huffard & hochberg 2005), and more await description (F.G. hochberg unpublished data). A revolution is brewing, however, for the identification, description and discrimination of paralarval forms. With the advent of cheap, reliable and accurate DNA sequencing technologies and sequence databases such as GenBank, it will be possible to definitively identify paralarvae. in
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs combination with high-resolution and accurate photography, it will enable development of comprehensive species identification keys for octopus paralarvae. The capacity to identify paralarval stages will also enable a much more thorough understanding of development and morphometric changes associated with growth and life in the plankton. until this process is under way, some caution must be taken with taxonomic identifications of wild-caught paralarvae because there is potential for misidentification or oversimplification of the diversity of taxa represented in such samples.
Distribution patterns
Sampling methods
Most benthic octopus species with planktonic stages spawn in shallow, rocky or coral substratum areas and consequently hatchlings can be abundant near the coast. surveys targeting octopus paralarvae such as Octopus vulgaris have been done in shallow bays and littoral waters (Takeda 1990a, sakaguchi et al. 1999, Gonzlez et al. 2005, otero 2007). oceanic plankton sampling is usually rich in oegopsid squid paralarvae and poor in octopuses, with some exceptions. For example, oceanic surveys in the north pacific sampled large volumes of water and captured large numbers of Enteroctopus dofleini paralarvae (Green 1973, kubodera 1991). Table 5 shows literature records of the depth ranges and different sampling methods, primarily nets and light traps, used to collect octopus paralarvae. classic bongo nets, conical nets of different sizes, isaacs-kidd midwater trawls (ikMTs) and rectangular midwater trawls (RMTs) have been used to collect octopus paralarvae (see Table 5). piatkowski (1998) reviewed the advantages of targeted sampling using modern opening/closing nets and discussed problems such as net speed and net avoidance by cephalopod paralarvae. The strong positive phototaxis of octopus paralarvae (see Responses to light and gravity, p. 163) has been used during night surveys to attract and collect large paralarvae inhabiting surface or near-surface waters (see Table 6). light traps proved to be a powerful method for collecting large numbers of octopus paralarvae (Moltschaniwskyj & Doherty 1995) but little is known of their sampling efficiency, sampling bias due to water clarity and species-specific capture selectivity. An advantage of this method is the collection of live animals in excellent conditions for experimental work. For example, hanlon et al. (1980a, 1985) resolved the Macrotritopus taxonomic problem (see also Nesis & Nikitina 1981) by collecting live Macrotritopus paralarvae individuals using light and rearing them to the adult stage in the laboratory, where they were identified as Macrotritopus defilippi.
Geographic range
Total geographic range of paralarvae of benthic octopuses is poorly known for most species. As for many attributes of octopus paralarvae, it is probably best known for Octopus vulgaris and Enteroctopus dofleini (see Table 5). Taxonomic problems for the family octopodidae are sufficient that accurate distributions for adult octopuses are not available for most species (Norman & hochberg 2005a), let alone for paralarvae. Greater resolution may become possible when molecular tools enable accurate species identifications and hence collation of accurate geographic distributional data. The greatest geographic range for octopus paralarvae is likely to occur for widely distributed indo-West pacific coral-reef species such as Octopus cyanea and Callistoctopus ornatus. These small-egg species have distributions spanning two thirds of the globes circumference (Norman 1991, 1993). Van heukelem (1973) reported captive Octopus cyanea paralarvae that lasted in the water column for 21 days before dying. Norman (1991) suggested that the paralarval stage would
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RoGER VillANuEVA & MARk D. NoRMAN have to be significantly longer for this species (up to months, as has been recorded for the similar O. vulgaris paralarvae; see Table 3) to explain the gene flow necessary between the widely spaced coral-reef habitats in the tropical indian and pacific oceans. At this stage, there are no reports of octopus paralarvae from polar regions. Benthic octopuses at these high latitudes exclusively produce large-egg hatchlings as in Benthoctopus (Nesis 2001), Bathypolypus (Muus 2002, Barratt et al. 2007) and Pareledone (Allcock 2005), as do many other polar marine invertebrates that show high parental investment in a few, large and well-developed young (i.e., poulin & Feral 1996). The largest planktonic hatchlings in the family octopodidae belong to the genus Enteroctopus (see Table 4), cold-adapted species distributed in high latitudes. E. dofleini is distributed from littoral depths to more than 1500 m (hartwick 1983, hochberg 1998) and kubodera (1991) collected E. dofleini paralarvae in the north pacific at almost 57N in the Bering sea. Enteroctopus megalocyathus of south America has the largest planktonic hatchlings described and their morphometrics and behaviours are ambiguous between pelagic and benthic modes of life (ortiz et al. 2006) (see swimming behaviour of planktonic paralarvae, p. 161). in common with the octopodidae of high latitudes, deep-sea benthic octopuses produce large eggs and have benthic hatchlings (Voss 1988). The notable exceptions appear to be members of the middepth genera Scaeurgus and Pteroctopus (Table 1), which have small-type egg sizes and for which little is known of their paralarvae (Bello 2004).
Horizontal dispersal
horizontal movement dictated by oceanographic conditions in upwelling areas has been suggested to be of great importance in the distributions of Octopus vulgaris paralarvae (Demarcq & Faure 2000, Faure et al. 2000, Gonzlez et al. 2005, otero 2007). upwelling intensity may act as a limiting factor, generating periods of coastal water retention, potentially beneficial for nutrient enrichment processes. These periods generate low, horizontal larval dispersion off shore in some zoological groups (cury & Roy 1989). using oceanographic models, Demarcq & Faure (2000) and Faure et al. (2000) hypothesised that in the Arguin Bank, influenced by the West African coastal upwelling system, the periods of high retention indices generated during spring benefits planktonic O. vulgaris paralarvae by limiting offshore paralarval dispersion. Faure et al. (2000) suggested that offshore paralarval dispersion can be a negative factor in paralarval survival due to the wind-induced breakdown of the retention areas during autumn. These hypotheses were partially corroborated by Gonzlez et al. (2005) and otero (2007), who found that high abundances of O. vulgaris paralarvae were correlated with high upwelling retention indices in the north-west iberian coast, the northern limit of the canary current. however, nearly all paralarvae collected by these authors were individuals with three suckers per arm, suggesting that they were hatchlings incorporated into the relatively low-turbulence water mass. The effect of upwelling intensity on fish and invertebrate larval distributions varies with the behaviours and vertical distributions of the larvae, and careful sampling is necessary to determine the contribution of upwelling to the offshore transport of larvae as a cause of variations in larval settlement levels (shanks & Eckert 2005, shanks & Brink 2005). The paralarvae of species with large hatchlings such as Enteroctopus dofleini seem to be distributed in both shallow and oceanic waters, having been found off shore in the north-east pacific ocean in higher abundances between the surface and 100 m over bottom depths of <200 m (Green 1973), as well as over the continental shelf in the north-west pacific ocean (yamashita & Torisawa 1983). however, significant numbers of E. dofleini paralarvae have also been encountered in more distant offshore waters (200300 miles from the coast) and collected 1 h after sunset in surface waters along the Aleutian islands and southern Bering sea (kubodera 1991). selective tidal transport
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs can also influence the distributions and densities of prey such as crustacean zoeae (Forward & Tankersley 2001) and is expected to influence the distributions of octopus paralarvae, as has been observed in other shallow-water and bottom-spawning cephalopods such as loliginid paralarvae (Zeidberg & hamner 2002).
Vertical distribution and abundances

Few studies have recorded vertical daily cycles of octopus paralarvae, most being focused on Octopus vulgaris. in shallow coastal waters, paralarvae of this species are nearly absent from the sea surface during daytime and present from the seafloor to the surface at night, with higher abundances of hatchlings (easily recognized by their three suckers per arm) found near the surface at night (Takeda 1990a, sakaguchi et al. 1999, otero 2007) (Table 5). The hatchling individuals probably come directly from egg masses in the rocky substrata of the shallow waters sampled. Diel changes in the open ocean and for older paralarvae are practically unknown and need to be investigated through use of high-resolution discrete-depth sampling. sampling between 0 and 2000 m depth in the north-east Atlantic, clarke & lu (1975) collected the highest number known to date of Macrotritopus paralarvae (n = 161). Most (73%) of Macrotritopus sp. collected were concentrated between 0 and 50 m depth and no diel migration was detected. however, some vertical movements to deep waters may exist because Rees (1954) reported a Macrotritopus individual collected between 800 and 1500 m, clarke (1969) noted an individual collected between 460 and 510 m and clarke & lu (1975) recorded one specimen between 1000 and 1250 m depth. Qualitative observations of paralarval numbers at night in the open ocean of the coral sea found much higher numbers of octopus paralarvae on moonless nights compared with moonlit nights (M.D. Norman personal observation). hunt (1996) found that Octopus rubescens paralarvae were most abundant at depths of 200400 m in Monterey Bay, california. This may correspond to the daytime depth ranges of the vertically migrating gelatinous zooplankton layer, visible on ship depth sounders and defined as the scattering layer by Eyring et al. (1948). Vertical movements are suspected to be important for retention of paralarvae over settled areas like seamounts for deeper-water species such as Scaeurgus unicirrhus. paralarvae presumably belonging to this species have been collected from the Great Meteor seamount, north-east Atlantic, the only cephalopod paralarvae related to bottom-dwelling adults collected over this seamount (Diekmann et al. 2006). Endemism and seamount associations of members of this genus have been discussed elsewhere (Norman et al. 2005). Factors influencing differences in abundances between hatchlings and older paralarvae are poorly known. only 7% of 643 Octopus vulgaris paralarvae collected by sakaguchi et al. (1999) had more than three suckers per arm (= sucker number at hatching; see Table 4), and only 4% of 780 Enteroctopus dofleini individuals collected by Green (1973) in oceanic waters were >6 mm Ml. in the first instance, the abundance of small animals suggests that mortality rates are higher during the early paralarval stages. however, other factors cannot be discounted. Diversity in sizes may be a product of cohorts with differing growth rates, as has been observed in same-age cohorts of several octopus species (Van heukelem 1976, Forsythe 1984). horizontal displacement of older paralarvae and/or net avoidance by these larger paralarvae with faster swimming speeds and higher sensory development may also be a factor. The potential influence of sensory systems on paralarval distributions is unknown. For example, the use of sound by cephalopod paralarvae as an orientation cue in relation to reefs cannot be excluded, as has been observed for reef fishes and crustacean larvae (Montgomery et al. 2006), potentially influencing their settlement distribution. octopuses have well-developed mechanoreceptors
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RoGER VillANuEVA & MARk D. NoRMAN analogous to the receptors of fishes (see sensory systems section, p. 126), capable of detecting low frequencies; however several studies suggest that cephalopods cannot detect underwater sound or vibrational stimuli much above 100 hz (packard et al. 1990, Budelmann et al. 1997).
Relationships between paralarval and adult populations

seasonal reproduction patterns of each species will dictate the presence of the different paralarvae in the plankton throughout the year. Maximum abundances of Octopus vulgaris paralarvae are recorded during summer and autumn (Rees 1950, Rees & lumby 1954, Takeda 1990a, sakaguchi et al. 1999, Gonzlez et al. 2005, otero 2007), corresponding to spawning peaks of O. vulgaris in temperate regions that are in spring and early autumn (Mangold 1983). The warm coastal waters in autumn accelerate embryonic development (see Egg care and duration of embryonic development, p. 110) for the last of the spawnings, after which young paralarvae of this species will practically disappear from the plankton during winter and spring. Variability in life span and growth in benthic octopuses with or without planktonic stages is influenced by many factors, of which temperature is probably the most important (semmens et al. 2004). in benthic octopuses with planktonic stages, under laboratory conditions, the duration of the life cycle including embryonic development ranges from 6 to 12 months in pygmy octopuses such as O. joubini (Forsythe & Toll 1991), nearly 1 yr in O. vulgaris (iglesias et al. 2004) and 3.5 yr in the large cold-adapted species Enteroctopus dofleini (s. snyder unpublished manuscript). in the short-lived species, pulses of recruitment can be related directly between young stages and adults of the following year. For a few species, there is some support for a relationship between the success of the paralarval population and adult abundances. After a 6-yr field study, Ambrose (1988) concluded that the primary regulatory processes of a subtidal population of Octopus bimaculatus in the north-east pacific ocean appeared to take place in the paralarval and juvenile stages. The importance of early stages was supported in Ambroses study by heavy recruitment of settled individuals in 1 yr leading to unusually high adult octopus densities in the subsequent year. Relatively large O. vulgaris paralarvae (to 6 mm Ml) were collected by Rees (1950) and Rees & lumby (1954) in the English channel. These authors concluded that periodic plagues of O. vulgaris during warm years along the south coast of England (the northern limit of distribution of the species in the northeast Atlantic) resulted from the transport of the paralarvae during the summer months across the English channel from southern hatching areas. in coastal upwelling areas of West Africa, catches of adult O. vulgaris during summer are significantly correlated with the upwelling intensity during the previous winter, indicating the influence of oceanographic conditions on octopus paralarvae and juveniles and the subsequent effects on the fished adult populations (caverivire & Demarcq 2002). in the same region, exceptional oceanographic conditions favouring paralarval and juvenile survival also seem to be the origin of demographic explosions of O. vulgaris (caverivire 1990, Diallo et al. 2002). A similar relationship between upwelling intensity and adult catches has been found in the north-west iberian coast (otero 2007). These data suggest that populations of planktonic octopuses may benefit from particular oceanographic conditions, as has been observed for loliginid paralarvae (Vecchione 1999, Zeidberg & hamner 2002).
The settlement process

After a period of constant swimming that ranges from 3 wk to 6 months (depending on the species; see Table 3), planktonic octopuses undergo a transitional period from a pelagic lifestyle to the predominantly benthic life of the juvenile stage. The end of the planktonic paralarval period in octopuses is not always abrupt as it is in many other benthic invertebrates with planktonic larval forms. There seem to be three presettlement strategies, dependent on the species and/or the environmental context:
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs 1. species with a short presettlement period. After a short period in contact with hard surfaces and benthos, paralarvae of these species definitively settle to the seafloor at relatively small sizes. These young octopuses, considered as juveniles from this point onwards (sensu young & harman 1988), live on the benthos and have similar habits to that of the adults. From an ecological point of view, at this stage the young animals are equivalent to the hatchlings of large-egg octopus species that immediately adopt a benthic habit on hatching. A typical example of such species is O. vulgaris (Villanueva 1995, Nixon & Mangold 1996). 2. species with an expanded, transitional presettlement period. in these species, a strict benthic life is gradually adopted, split between swimming and benthic crawling. These paralarvae can reach a relatively large size in the water column and the animals seem to live in contact with both the benthos and the water column, as has been suggested for Macrotritopus defilippi in the western Atlantic (hanlon et al. 1985) and for Amphioctopus burryi (Forsythe & hanlon 1985). 3. species with a prolonged/suspended paralarval state. certain paralarvae reach considerable sizes, particularly those occurring in oceanic epipelagic waters. Due to their size and swimming capacities they can be considered micronektonic paralarvae. These paralarvae have been described as extended pelagic stages (Rees 1954) or super-paralarvae (strugnell et al. 2004) and have been suggested to be individuals that delay settlement due to the absence of suitable habitat, i.e., shallow reefs (see prolonged paralarval stages: micronektonic paralarvae, p. 182). it is also possible that the swimming capacities, behaviour, and the well-developed sensory systems of these micronektonic paralarvae may be used to actively remain in the epipelagic realm, effectively delaying settlement in order to exploit resources in this habitat. The physiological processes and environmental cues that govern the settlement metamorphosis have not yet been described. only external morphology and behavioural characters have been reported for this period of dramatic ecological change.
Morphological characteristics at settlement

Major external morphological changes associated with the settlement process are positive allometric arm growth, the addition of new suckers, chromatophore, iridophore and leucophore genesis, the development of skin sculptural components and a horizontal pupillary response. At the same time, animals appear to lose the klliker organs that cover the body surface and the lateral line system formed by the epidermal lines located on the arms, head, anterior part of dorsal mantle and funnel. These structures have not been reported for adult benthic octopuses (Budelmann et al. 1997). A more minor morphological change is the loss of the oral denticles of the beaks. This transformation is also reflected in changes in the relative sizes of the various lobes of the paralarval and juvenile brain (see central nervous system, p. 126). Positive allometric arm growth From a hydrodynamic point of view, hatchling octopus paralarvae have a squid-like form that gradually changes to the typical octopus form after settlement, due primarily to the notable arm growth. Benthic juveniles and adult octopods have a relatively small mantle cavity volume and have to produce high ventilation pressures to generate the necessary thrust for locomotion when they swim. These morphological constraints appear gradually throughout the planktonic phase and it is expected that they would progressively dictate the locomotion capacities of the paralarvae and juveniles. As proposed by Wells (1990), cephalopods will try to escape using jet locomotion whenever possible, particularly adult octopus. During jet propulsion, Wells et al. (1983b, 1987) found
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RoGER VillANuEVA & MARk D. NoRMAN that the hearts of benthic octopuses cease beating, resulting in oxygen debt, as the venous system is incapable of retuning blood against the gradients produced by the rise in internal mantle pressure. This makes jet swimming impossible as a regular mode of locomotion for benthic octopuses. At the end of the planktonic phase, the growth of the arm crown and the expected increase in the internal mantle pressure necessary for jet swimming have been suggested as factors that may instigate settlement in Octopus vulgaris (Villanueva et al. 1995, 1996). For micronektonic forms such as Callistoctopus sp., this energetic problem may be solved by adopting the hydrodynamic form of squids with an elongate, large mantle that enables locomotion by jet swimming in the epipelagic realm, potentially delaying settlement (see Figure 43). under laboratory conditions, presettlement reflexes of Octopus vulgaris paralarvae commence when Ml reaches 50% or less of the total length (Villanueva 1995). This relationship is similar in Enteroctopus dofleini as settlement takes place when Ml and arm length represent approximately 45% and 55% of total length, respectively (okubo 1979) (Figures 46 and 47). it is interesting to note that total length of Octopus vulgaris at settlement (1113 mm) is not dissimilar to that of the length of Enteroctopus dofleini paralarvae at hatching (10 mm), a species that under laboratory conditions will settle at total lengths of approximately 30 mm (okubo 1979, 1980) (see Figure 48 for species comparisons). Morphological transformations at settlement are less well known for long-armed paralarvae, such as members of the genus Callistoctopus (e.g., Figures 4 and 43), Euaxoctopus (Nesis & Nikitina, 1991) (Figure 5) and Macrotritopus (Rees 1954) (Figure 6). These paralarvae can develop markedly long arms, particularly one arm pair that can reach up to three times the length of the others (i.e., for Euaxoctopus, Nesis & Nikitina 1991). This longest arm pair corresponds to the first pair in Callistoctopus, the second in Euaxoctopus and the third in Macrotritopus (see Figures 46). hanlon et al. (1985) postulated that the long, slender arms may be aids to flotation because they represent a large proportion of the surface area of the animal. chemical and morphological composition of these expanded arms and body musculature may be an interesting subject for further research because the arms may be buoyant in a comparable fashion to the elongate ammonia-buoyant arm pairs of squids in the family chiroteuthidae (Voight et al. 1994). An alternative explanation may be that this longer arm pair act as analogues of the elongate feeding tentacle pair of squids and cuttlefishes. Further research on how octopus paralarvae use their two mantle cavities (dorsal and ventral) (see examples in Figures 1B, 26, 40, 41, and 43) during the jet propulsion cycle may
80 70 ML as % of TL 60 50 40 30 0 20 40 60 80 100 120 140 160 180 200 Age (days)
Figure 46 Relative decrease of mantle length (Ml) as percentage of total length (Tl) from hatching to settlement during experimental rearings of Enteroctopus dofleini and Octopus vulgaris. (Data for E. dofleini obtained from okubo 1979 (dark circles) and data for O. vulgaris obtained from Villanueva 1995 (white circles).) initial settlement periods are indicated for both species: E. dofleini, black arrow; O. vulgaris, white arrow. original. 178

80 Arm length as % of TL 70 60 50 40 30 20 10 0 0 20 40 60 80 100 120 140 160 180 200 Age (days)
Figure 47 Relative increase of arm length as percentage of total length (Tl) from hatching to settlement during experimental rearings of Enteroctopus dofleini and Octopus vulgaris. (Data for E. dofleini obtained from okubo 1979 (dark circles) and data for O. vulgaris obtained from Villanueva 1995 (white circles).) initial settlement periods are indicated for both species: E. dofleini (black arrow); O. vulgaris (white arrow). original.
80 70 Total length (mm) 60 50 40 30 20 10 0 0 20 40 60 80 100 120 140 160 180 200 Age (days)
Figure 48 Growth in total length from hatching to settlement during experimental rearings of Enteroctopus dofleini and Octopus vulgaris paralarvae. (Data for E. dofleini obtained from okubo 1979 (black circles) and okubo 1980 (black squares). Data for Octopus vulgaris obtained from itami et al. 1963 (white squares) and Villanueva 1995 (white circles).) initial settlement periods are indicated for both species: E. dofleini, black arrows; O. vulgaris, white arrows. original.
also shed light on the poorly known hydrodynamic and energetic adaptations of swimming in these long-armed paralarvae. Chromatophore genesis and new skin sculptural components After a nearly transparent life in the plankton, recently settled octopuses develop a dense net of chromatophores, particularly on the dorsal surfaces, which help the animal in camouflage on the seafloor and that develop into body patterns resembling those of the adults. As noted by packard (1985, p. 293): The dorsal spurt in chromatophore genesis at the end of the planktonic phase is so dramatic as to hint at something like metamorphosis. it is as if the skin were waiting for its owner to settle on the seafloor before bringing out the fine-grain dress that is going to serve for the rest of its life, and replace the coarse-grain set of extra-tegument spots (on the surface of the viscera) that
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RoGER VillANuEVA & MARk D. NoRMAN served during the transparent planktonic phase. All the founder chromatophores of paralarvae can be identified in recently settled individuals and are assumed to remain functional. however, they were never expanded during the extensive photographic surveys of packard, who suggested that they may belong to planktonic, rather than benthic, camouflage patterns. klliker organs are present on the skin of recently settled individuals (Villanueva 1995) and probably disappear relatively quickly. it is unknown at which stage these animals completely lose the klliker organs. The presence of these organs has not been reported in the literature for later-stage juveniles or adult octopuses. At settlement, other chromatic components also develop, including epidermal iridophores and leucophores. This transformation has not been described in detail and requires further research. For many species, the sculptural components of the skin also undertake a dramatic transformation from the relatively smooth paralarva to highly sculptured, benthic animals (Figure 16). papillae, flaps, ridges, patch and groove skin texture, and the lateral mantle ridge are all sculptural features of post-settlement juveniles and adults. in some species, papillae in the skin can be dramatically raised (complete with side branches) to form a rugose or even hairy appearance, as occurs in members of the genus Abdopus (Norman & Finn 2001). Horizontal pupillary response in line with many pelagic cephalopods, octopus paralarvae possess a circular pupil (see examples in Figures 1B, 3, 4 centre, 26, 41). in contrast, adult benthic octopuses have a horizontal pupillary response to light intensities: when exposed to bright light the pupil forms a horizontal slit, while the dark-adapted pupil is close to circular, as observed in Octopus vulgaris and Eledone cirrhosa (Muntz 1977, Douglas et al. 2005) (see also Figure 1c). A horizontal pupil is present in octopus hatchlings of directly benthic species (see Figure 1c,D). The horizontal shape of the pupil correlates with the longest rhabdomes found in the central retina, where they form an equatorial strip (young 1963). This adaptation may be related to a benthic mode of life so that objects in the seafloor/water interface can be better discriminated (Muntz 1977). in other cephalopods that live in the water column, such as Loligo pealei, the central retinal strip is absent (young 1963). in Enteroctopus dofleini reared from planktonic hatchlings, the horizontal slit of the pupil was observed only in benthic individuals older than 89 months (s. snyder unpublished manuscript). Quantification of these observations is necessary, however, because the constant circular pupils of planktonic octopuses contrast with the alternative choices of circular or horizontal shapes depending on light intensities, observed when individuals move to the substratum after settlement. The presence of a horizontal pupil in paralarvae that are still present in the micronekton has only been observed in several live photographs of larger animals (e.g., Figure 4 bottom). The presence of this feature may represent animals close to settlement, animals in a transitional phase during which they are spending time split between swimming and benthic crawling, or be an attribute of delayed settlement (see prolonged paralarval stages: micronektonic paralarvae, p. 182).
Behavioural and ecological characteristics at settlement

The shift from a planktonic to a benthic life implies that the adaptations necessary for this change are attained by the octopuses over a relatively short time. it is also assumed that octopuses settle to the seafloor. however, they have also been found to use other hard surfaces, including the underside of buoys set over 64 m of water (Wells & Wells 1970), surface flotsam (smale & Buchan 1981) and have taken on a role as epifauna covering floating cages for fish culture at more than 25 m deep in the Mediterranean sea (R. Villanueva personal observation). Most descriptions of settlement behaviour come from laboratory experiments. These are typically characterized by high peaks of mortality during these periods, at least for Octopus vulgaris (Villanueva 1995, iglesias et al. 2004, carrasco et al. 2006), for which cannibalism has also been observed immediately after settlement
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs (itami et al. 1963). These findings indicate that laboratory settlement requirements are poorly understood and need to be improved. The natural settlement process is probably modified under laboratory conditions, potentially accelerating settlement through factors such as (1) the physical limits imposed by the size of normal rearing tanks, preventing possible movement within the water column, (2) light intensity and (3) the prior feeding history of the reared paralarvae, which are usually indirectly trained to receive food during laboratory daylight periods. octopuses collected from floating structures in the wild (Wells & Wells 1970) or from RoVs in the water column (hunt 1996) become exclusively benthic when transferred to rearing tanks. however, in some species such as Amphioctopus burryi, relatively large individuals of 0.81.2 g wet weight collected from the sea surface at night showed both pelagic and benthic behaviour in the laboratory, swimming in the water column at night and living on the substratum by day (Forsythe & hanlon 1985). large Macrotritopus-type paralarvae have also been found to be benthic during the day and pelagic at night (hanlon et al. 1985). This behaviour is suspected to be common in many species. kanamaru (1964) reported a mix of planktonic and benthic organisms (shrimp and crab larvae and flatfish remains) in the gut contents of a juvenile Enteroctopus dofleini, 51 mm in total length, suggesting this migratory capacity. Relatively large Octopus vulgaris paralarvae (11 mm Ml) have been collected from the plankton (Degner 1925, Rees 1953). in laboratory experiments, presettlement individuals tend to remain attached to the surfaces of the tanks for the majority of the time, only swimming to capture food in the water column (itami et al. 1963, Forsythe & Toll 1991, Villanueva 1995). Recently settled individuals show a preference for dark or shady areas of tanks and have reclusive behaviour, using holes, provided shelters or gastropod shells as refuges. At this stage, individuals search for food on the floor of the aquaria rather than in the water column. To identify individuals as presettlement or post-settlement can be difficult. To discern between planktonic or benthic individuals, a behavioural criterion was used by Villanueva (1995): when settled individuals are disturbed (i.e., gently touched with the tip of a pipette) and respond by crawling, rather than swimming away, they are considered to be postsettlement, benthic juveniles. settled individuals also begin to direct fluxes of water from their funnel to the origin of the disturbance. Ambrose (1988) developed a means of assessing the population dynamics of recently settled octopus individuals. The densities of recently settled and juvenile O. bimaculatus were estimated by sampling the holdfasts of the giant kelp, Macrocystis pyrifera, 15 times over 2 yr consecutively at 410 m depth at catalina island, california. up to three individuals were collected from a single holdfast, ranging in size from recently settled animals of 5 mm Ml to juveniles of 50 mm Ml. individuals <10 mm Ml were collected in all months, indicating that paralarvae settled throughout the year, with the highest octopus densities recorded in early summer, indicating the peak period of settlement. in the Bay of Naples, Mediterranean sea, Naef (1928, p. 292) found that recently settled individuals of Octopus vulgaris are dredged up with sand, gravel and all sorts of detritus and are easy raised on a corresponding substratum in the aquarium. They always bury deeply in such sediments or hide in narrow cavities, coming to the sediment surface only at night to forage. on reaching the benthos, recently settled octopuses still possess symbionts remaining from their planktonic stage. chromidinid ciliates of the genus Chromidia typically infect renal organs of oceanic cephalopods with a pelagic distribution. however they are also found in benthic octopus species, but only those with a planktonic paralarval stage, such as Eledone cirrhosa, Octopus salutii, O. vulgaris and Scaeurgus unicirrhus (hochberg 1982, 1983). it has been suggested that these symbionts are acquired through association with crustaceans living in the water column and are transported to the seafloor when octopuses settle (hochberg 1982, 1983). it is not known how the ciliates reach the renal organs and they appear to do no harm to the tissues of their host cephalopods (Furuya et al. 2004).
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Prolonged paralarval stages: micronektonic paralarvae

There may be a third octopus paralarval strategy that appears peculiar to animals present in the water column over deep waters. in these habitats, large octopus paralarvae (some more than 100 mm in total length) have been encountered in plankton nets, attracted by lights or observed from RoVs (see Table 6). Due to the large size and swimming capacities of these individuals that live in epipelagic waters, they can be considered as part of the micronekton. strugnell et al. (2004) coined the term super-paralarvae to refer to these peculiar, often long-armed, paralarvae. For Macrotritopus-type paralarvae, Rees (1954) discussed the impact of ocean currents sweeping individuals off shore over very deep water. For these paralarvae, Rees (1954, p. 69), proposed that settlement was delayed and that they could attain nearly twice the normal size for metamorphosis. he coined the term extended pelagic stages for such paralarvae. in relation to Macrotritopus defilippi, Nesis & Nikitina (1981, p. 847) pointed out that: The macrotritopuses are able to delay their settling to the bottom and may have a chance to cross the Atlantic. The prevalence of micronektonic paralarvae, their identities and the circumstances under which they exist are poorly known. They reach large sizes and still exhibit the characteristic paralarval features of nearly transparent musculature, large and simple chromatophores and round pupils. The nature of the settlement process for these forms is unknown, as is discriminating between whether this is an accidental process or whether such species have actively delayed settlement to exploit resources of the epipelagic realm. As discussed (see Defences section, p. 168), schools or shoals of young Octopus rubescens have been reported in midwater in Monterey Bay, california (Figure 44). young (1972) captured large individuals of this species (1525 mm Ml) using ikMT plankton trawls off california. These individuals possessed developed skin sculpture, including papillae on the head and mantle, supraocular papillae and a granulated skin texture. youngs largest specimen had a hectocotylized arm with a short, broad and incompletely formed ligula and lacked a calamus. it is unknown whether these larger individuals constitute micronektonic juveniles, late-stage paralarvae close to settlement, or a transitional stage with both micronektonic and benthic behaviours.
Permanent paralarvae: neoteny and holopelagic octopuses

Extended pelagic phases in oceanic paralarvae may have played a role in the evolution of certain holopelagic octopuses. octopus families that have completely pelagic life cycles fall into two major groups. The ctenoglossans (tribe ctenoglossa) contain three families (Amphitretidae, Vitreledonellidae and Bolitaenidae), which are typically relatively small (typically <20 cm in total length, largest <50 cm), semigelatinous and transparent residents of oceanic midwater depths between around 200 and 800 m. The second group, the argonautoids (superfamily Argonautida), includes the argonauts, blanket octopuses and their relatives (families Argonautidae, Tremoctopodidiae, Alloposidae and ocythoidae). These octopuses tend to be larger (up to 2 m or more in total length), more muscular, non-transparent pelagic octopuses, typically residing in shallower, neritic waters (0200 m) (Norman 2000). strugnell et al. (2004) used molecular sequencing data to demonstrate that the closest relatives of the ctenoglossans are two genera of benthic octopuses from the family octopodidae, Pareledone and Graneledone. in this study, molecular data and parallels in morphology between octopus paralarvae and ctenoglossans supported the hypothesis that the latter group evolved from paralarvae that never returned to earth. prolonged residence in the pelagic realm and acquisition of sexual maturity (and activity) in the water column are suggested as the mechanisms by which this group became wholly pelagic. The micronektonic or super-paralarvae concept (discussed in prolonged paralarval stages: micronektonic paralarvae, p. 182) may have been the critical stage that enabled
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs the evolution of the ctenoglossans. The origin of the other major group of holopelagic octopuses, the argonautoids, remains unknown.
Anthropogenic impacts on early stages of octopuses

Pollution
Most octopodid species with planktonic paralarval stages live in shallow waters and can be affected by the many pollutants introduced to the sea by human activities. These pollutants can affect octopuses from the early stages of development. Eggs of incirrate octopods lack an egg capsule so that the chorion is in direct contact with the seawater. it is expected that contaminants can have a deleterious effect on octopuses compared with those cephalopod species that have a protecting egg capsule. For example, cuttlefishes predominantly absorb metals into the outer egg capsule, acting as an effective shield that limits exposure of the embryos to soluble metals (Bustamante et al. 2002, 2004). compared with recently spawned eggs, developing Octopus vulgaris eggs have higher concentrations of most essential elements and also of some non-essential elements (i.e., Ag and pb) due to the absorption of these elements from seawater during embryonic development (Villanueva & Bustamante 2006). Due to chronic exposure to organophosphorus pesticides such as parathion, abnormal embryo gastrulation and arrested development has been observed in O. mimus embryos at pesticide concentrations of over 0.4 mM (Gutirrez-pajares et al. 2003). subadult and adult octopuses can be used as bioindicator species in polluted areas (Butty & holdway 1997) and are sensitive to marine pollutants such as ethylene dibromide and mercuric chloride (Adams et al. 1989). hatchlings of O. pallidus (a directly benthic species) are more sensitive to exposure to petroleum hydrocarbon toxicants such as 4-chlorophenol compared with other aquatic invertebrates tested, such as Daphnia magna or Hydra species, and do not appear to be adversely affected by the application of chemical dispersants to oil spills (long & holdway 2002). scheel (2002) noted that densities of Enteroctopus dofleini recorded during 19951998, after the 1989 Exxon Valdez oil spill, were only 150% of densities recorded in British columbia in the late 1970s and early 1980s. scheel suggested that the presence of the highest octopus densities in the intertidal and shallowest subtidal areas made populations in these habitats highly vulnerable to human impacts.
Overfishing
coastal species of benthic octopuses represent an important fishery resource in different areas of the world (see, among others, Takeda 1990b, lang & hochberg 1997, Balgueras et al. 2000, caverivire et al. 2002, Rocha & Vega 2003). since 1950, octopus captures have been constantly increasing (Jereb & Roper 2005) and in recent years (19972003) world captures of octopodidae have ranged from 290,000 to 409,000 tonnes, with the single species Octopus vulgaris representing 1118% of these captures (FAo 2005). protection of spawning activity by closing fishing during peak spawning periods has been proposed to protect Octopus vulgaris populations (itami 1975, Jouffre & caverivire 2005). itami reviewed O. vulgaris restocking strategies used by Japanese fishing associations in hyogo prefecture since 1929. he proposes the provision of thousands of specially designed clay pots in which females could spawn. he suggests that these be located on sandy and muddy substrata on fishing grounds rich in zooplankton (particularly crustacean zoeae) to ensure sufficient prey densities are available for the planktonic octopus hatchlings.
Global warming
A picture of how climate change will affect marine plankton dynamics is slowly emerging (hays et al. 2005, sommer et al. 2007) but how this will affect planktonic octopuses is uncertain. Due to
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RoGER VillANuEVA & MARk D. NoRMAN their high metabolic rate and extremely ph-sensitive blood oxygen transport, oceanic cephalopods are amongst the most sensitive of marine groups exposed to the ocean acidification that is predicted to result from elevated seawater co2 levels (prtner et al. 2004). At this stage, the direct physiological effects of seawater acidification on planktonic stages of cephalopods are unknown and further research is required. it is suspected that indirect effects of climate change may severely affect adult octopus populations. An example was provided by a prolonged harmful algal bloom (hAB) lasting nearly 2 months, which appears to have nearly eliminated the once-ubiquitous population of O. cf. mercatoris (a direct benthic species) in st. Joseph Bay, Florida (Tiffany et al. 2006). hABs seem to be increasing in frequency, duration and severity worldwide, influenced by anthropogenic impact and coinciding with trends in global warming (Van Dolah 2000). such episodes may affect littoral octopus populations in the future. As with all marine life, climate change will also affect biogeographic boundaries that are dictated by seawater temperature. This effect may manifest itself in two ways. Firstly, octopus taxa geographically associated with land masses that do not extend into higher latitudes will run out of available habitat and be unable to shift to higher latitudes. secondly, octopus paralarvae from warmer latitudes may be amongst the vanguards of invasions into previously cooler habitats. Qualitative evidence comes from reports of an Australian warm-temperate octopus species, O. tetricus, which has been found outside its typical warmer geographic range in the cool temperate waters of Victoria, Australia (l. Altoff personal observation 2007). As this species preys on other octopuses (M.D. Norman unpublished data), it may act as an invasive species, effectively (and rapidly) displacing resident octopus taxa, some of which are endemic/restricted in distribution. Further research is required into the potential scale of such impacts.
Concluding remarks
The distinctive form of octopus paralarvae and their differences in lifestyle from that of their parents make them enigmatic and fascinating creatures. Their numbers, diversity and wide geographic range make them important predatory members of planktonic assemblages. The duration of their planktonic phase varies significantly between species laboratory studies recording ranges of 3 wk to 6 months. This period is a significant proportion of the total life cycle of these animals, with various studies reporting lifespans of between 6 months and 3.5 yr. For some species, the duration of the pelagic period seems to be considerably extended and young octopuses can reach relatively large sizes as part of the micronekton of epipelagic, oceanic waters. For these individuals, settlement appears to be delayed for an unknown period, potentially in order to enhance dispersal and/or exploit food resources in this pelagic realm. preliminary information is available for many attributes of octopus paralarvae, particularly for two species, Octopus vulgaris and Enteroctopus dofleini. however, many opportunities exist for new and exciting research. The most pressing research areas fall into five categories: 1. Accurate taxonomy and development of identification tools. use of molecular sequencing techniques will enable concrete species identification, linked with databases such as GenBank and potentially programs such as Barcode (see strugnell & lindgren 2007). This will greatly expand the capacity to describe paralarvae of diverse species in detail through all growth stages. use of high-resolution photography and standardised morphological descriptions will be critical to this process. 2. Faunal surveys and biogeography. Equipped with better knowledge of paralarval species discrimination, surveys of regional faunas can be undertaken to gain a better understanding of the ranges, timing and abundances of the various paralarval taxa. These data can then be analysed in relation to biogeography and oceanography.
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BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs 3. Rearing techniques. Rearing of paralarvae requires innovative approaches to better simulate natural conditions for paralarvae, particularly in relation to the water column, water quality and turbulence, prey and light regimes. specialized treatment of brooding adult females will also enable provision of healthy paralarvae for taxonomic and experimental studies. 4. Growth, development and nutrition. With access to healthy paralarvae of all growth stages, research can be undertaken into morphology, physiology and behaviour during growth and development. A greater understanding of all aspects of nutrition is critical to the development of aquaculture for key species and needs further study, including aspects of feeding requirements and nutrient absorption through the skin. Morphological transformations throughout the paralarval period, particularly in skin components, are also worthy of further investigation. 5. hatching and settlement processes. All aspects of the cues, timing, duration and mechanics of the hatching and settlement processes require more detailed research. Assessment of the total duration of paralarval period is also required in order to assess the dispersal capacities of different species. Development of accurate ageing techniques would be a valuable tool in these studies. With most of our knowledge of octopus paralarvae applying to just two species, Octopus vulgaris and Enteroctopus dofleini, there is considerable scope for further research. The total number of benthic octopus species with planktonic stages is likely to be high (there are at least 68 named species and many more are yet to be described). it is clear that many new and exciting morphological, physiological and behavioural adaptations await discovery.
Acknowledgements
We wish to gratefully acknowledge Eric hochberg (santa Barbara Museum of Natural history) for his support and advice on all aspects of octopus natural history; Mitsuo sakai and Toshie Wakabayashi (National Research institute of Far seas Fisheries) for their considerable efforts in translating many Japanese articles on planktonic octopuses into English; Jose Manuel Fortuo (institut de cincies del Mar, icM) for assistance and advice in obtaining sEM images; Anna Bozzano (icM) for advice on cephalopod vision and unpublished observations on the eye morphology of planktonic Octopus vulgaris; James A. cosgrove (Royal British columbia Museum), yuzuru ikeda (university of the Ryukyus), Tsunemi kubodera (National science Museum), Richard E. young (university of hawaii) and the librarians of the icM Dolors Fernndez and Marta Ezpeleta, provided valuable literature related to planktonic octopuses; Nicols ortiz (centro Nacional patagnico) provided hatchlings of Enteroctopus megalocyathus for sEM analysis and Erica Vidal (universidade Federal do paran) provided images of Loligo opalescens paralarvae as the basis for Figure 40. sincere thanks to the many photographers who contributed live animal photographs, particularly David paul. M.D. Norman would like to thank Julian Finn, John Ahern, David paul and the staff of the undersea Explorer for invaluable field and laboratory assistance with planktonic and broader cephalopod research. R. Villanuevas recent research into planktonic octopus was funded by the following research projects: Xarxa de Referncia de Recerca i Desenvolupament en Aqicultura de la Generalitat de catalunya; programa para Movilidad de investigadores, secretara de Estado de universidades e investigacin del Ministerio de Educacin y ciencia; planes Nacionales de cultivos Marinos, JAcuMAR, secretara General de pesca Martima, Ministerio de pesca, Agricultura y Alimentacin, spain; and by the concerted Action cEphsTock from the commission of the European communities. M.D. Normans research was funded by Australian Biological Resources study, the Australian Research council and the hermon slade Foundation.
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Colour Figure 1 (Villanueva & Norman) Planktonic and benthic hatchlings in Octopodidae. Adult female Wunderpus photogenicus 26 mm ML in laboratory carrying egg strings with developing embryos within the arms (A) and hatchling (total length ~3.5 mm) from same egg mass (B). Note the well-developed dorsal mantle cavity of the paralarvae. (Reproduced with permission from Miske & Kirchhauser 2006.) Female Octopus berrima at the time of hatching in the laboratory with a benthic juvenile hatchling (total length ~20 mm) in foreground (C) and within 10 min of hatching (D) showing well-developed arms and chromatic and sculptural components of the skin. (Photos: David Paul.)
Colour Figure 3 (Villanueva & Norman) Individuals of Octopus vulgaris from hatching to settlement obtained from rearing experiments described in Villanueva (1995). Images not to scale. Age (days) and mantle length (ML) of the individuals measured fresh are (A) 0 days, 2.0 mm ML; (B) 20 days, 3.0 mm ML; (C) 30 days, 4.3 mm ML; (D) 42 days, 5.9 ML; (E) 50 days, 6.6 mm ML; (F) 60 days, 8.5 mm ML. Octopuses from this experiment settled between 47 and 54 days. Individuals were photographed under anaesthesia (2% ethanol) potentially causing chromatophore contraction in some cases. (Photos by Jean Lecomte, Observatoire Ocanologique de Banyuls, CNRS. Reproduced with permission from Villanueva et al. 1995, modified.)
Colour Figure 4 (Villanueva & Norman) Micronektonic octopus paralarvae. Top, unidentified paralarva of the genus Callistoctopus from the Coral Sea, Australia, showing longer dorsal arm pair. (Photos: David Paul.) Centre, unidentified paralarva (Macrotritopus sp.?) from Hawaii showing long arms relative to body length, particularly the third pair. (Photos: Chris Newbert.) Bottom, unidentified paralarva from Hawaii. (Photos: Jeffrey Rotman.)
Colour Figure 6 (Villanueva & Norman) Unidentified paralarva from the Coral Sea, Australia, showing arms of equivalent length (left). (Photo: David Paul.) Paralarva of Macrotritopus defilippi from Caribbean Sea showing longer third arm pair (right). (Photo: Raymond Hixon.)
Colour Figure 7 (Villanueva & Norman) Chromatophores contracted (left) or expanded (right) on the head of paralarvae. The left image corresponds to an unidentified paralarva of unknown genus and the right image is from an unidentified paralarva of the genus Callistoctopus. Both individuals from Coral Sea, Australia. (Photos: David Paul.)
Colour Figure 9 (Villanueva & Norman) Iridescence in octopus paralarvae. Left, unidentified paralarva showing scattered points of iridescence, potentially from Klliker organs in skin. Right, Amphioctopus sp. paralarva showing iridescent tissue in location of ocelli of ocellate octopuses. Both individuals collected while night diving on a moonless night at ~10 m deep over a seafloor depth of 450 m at Osprey Reef, Coral Sea, Australia. Photographs taken in shipboard aquaria immediately after capture. (Photos: M.D. Norman.)
Colour Figure 10 (Villanueva & Norman) Hapalochlaena maculosa hatchling, a direct benthic species, showing well-developed skin colour and sculpture. (Photo: David Paul.)
Colour Figure 16 (Villanueva & Norman) Adult Octopus cyanea in camouflage display amongst soft corals, Puerto Galera, Philippine Islands. (Photo: Gunther Deichmann.)
Colour Figure 26 (Villanueva & Norman) Planktonic paralarva of Octopus warringa within 10 min of hatching in the laboratory showing short arms, transparent musculature, simple chromatophores and external yolk sac (within arm crown). (Photo: David Paul.)
Colour Figure 43 (Villanueva & Norman) Unidentified paralarva of the genus Callistoctopus from the Coral Sea, Australia, showing elongate form when swimming. Photograph taken in situ while night diving on a moonless night at ~10 m deep over a seafloor depth of 450 m at Osprey Reef, Coral Sea, Australia. (Photo: M.D. Norman.)
Colour Figure 44 (Villanueva & Norman) A dense swarm of Octopus rubescens with the jellyfish (Phacellophora camtschatica) photographed 26 June 2003 at 1115h local time from the ROV Ventana at a depth of about 60 m in 728 m of water in the Monterey Submarine Canyon, north-east Pacific. Temperature 9C and oxygen concentration 2.66 ml 11. No euphausiids were observed on the dive tape. (Image and data reproduced with permission from Monterey Bay Aquarium Research Institute, 2003, MBARI.)
Colour Figure 45 (Villanueva & Norman) Ephyra larval stage of jellyfish scyphomedusa feeding on unidentified octopod paralarva. Specimens collected using a plankton net at about 180 m depth, off Lizard Island, Great Barrier Reef. (Data and image reproduced with permission from Peter Parks/imagequestmarine. com.)

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Oceanography and Marine Biology: An Annual Review, 2008, 46, 105-202 R. N. Gibson, R. J. A. Atkinson, and J. D. M.

. Gordon, Editors Taylor & Francis

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

Eibl-Eibesfeldt & scheer 1962, ignatius & srinivasan 2006

Forsythe & hanlon 1985

7.3 8.3 4.3 7.8 7

3 3 5.2 1.7 2 7.5

3.3 7 small type small type 0.8

Boletzky et al. 2001

7 12 1.4 3.5 7 2.1 2.5 1.5

Van heukelem 1973

Mangold-Wirz et al. 1976

Joll 1976, 1978

Gonzlez et al. 2006

Miske & kirchhauser 2006

The hatching process and dispersal

RoGER VillANuEVA & MARk D. NoRMAN

Morphological characteristics of planktonic octopus paralarvae

Body form and musculature

species Amphioctopus aegina

Eggs incubated without female

Eggs incubated without female

Macroctopus maorum Octopus laqueus Octopus mimus

75% hatched in 1 h of the same day No differences between temperatures

laboratory laboratory laboratory Field laboratory laboratory

Eggs incubated with and without female

Octopus huttoni Wunderpus photogenicus Note: Np, not provided.

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

RoGER VillANuEVA & MARk D. NoRMAN

Surface epithelia and integumentary structures

RoGER VillANuEVA & MARk D. NoRMAN

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs A B

RoGER VillANuEVA & MARk D. NoRMAN A B

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

RoGER VillANuEVA & MARk D. NoRMAN

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

RoGER VillANuEVA & MARk D. NoRMAN

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

RoGER VillANuEVA & MARk D. NoRMAN

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

VLA VLL 200 m

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

RoGER VillANuEVA & MARk D. NoRMAN

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

RoGER VillANuEVA & MARk D. NoRMAN

Food, feeding and nutritional requirements

species and prey offered

Boletzky et al. 2001 NE pacific NW pacific Green 1973 okubo 1973

Eating not observed

RoGER VillANuEVA & MARk D. NoRMAN

okubo 1974 yamashita 1974

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

species and prey offered

Baltazar et al. 2000 Montoya 2002

Dew 1959 (as O. cyanea) Joll 1976

RoGER VillANuEVA & MARk D. NoRMAN

Mediterranean NE Atlantic NW pacific Mediterranean NW pacific

highest survival at 21c

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

Artemia nauplii and millicapsules of 1.32 mm in , 0.3 mg fresh weight

carrasco et al. 2003, 2006 iglesias et al. 2004

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2008 Villanueva & Norman 2008 With Colour Plates

2008 Villanueva & Norman 2008 With Colour Plates