2008 Villanueva & Norman 2008 With Colour Plates

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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

RoGER VillANuEVA1 & MARk D. NoRMAN2

1Institut de Ciències del Mar (CSIC), Passeig Marítim de la Barceloneta 37–49, E-08003 Barcelona, Spain

E-mail: [email protected], Museum Victoria, GPO Box 666, Melbourne, Vic 3001, Australia

E-mail: [email protected]

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 para-larvae 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 plank-tonic 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 para larvae 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 para larvae 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 kölliker 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 para larvae 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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particularly in commercially valuable species targeted by fisheries. current and potential anthro-pogenic 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 octo-puses 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 semi-transparent 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 chro-matophores and transparent musculature.

This marked contrast between the morphology and ecology of the planktonic stages of cephalo-pods 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

A B

C D

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 para larvae. (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.)


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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 para larvae 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 (0.2–20 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, 1978–1979) 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 10–12% of mantle length (Ml). Eggs >12% of Ml produce ben-thic hatchlings while eggs <10% of Ml produce planktonic hatchlings. Table 1 lists those octopus species known or likely to have planktonic para larvae. it comprises three classes of information — species for which planktonic para larvae 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 para larvae undergo a dramatic morphological and ecological transition from a free-swimming pelagic animal to the predomi-nantly 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 para larvae 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 para larvae 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 con-sidered 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 2–10 cm in total length), attaining the ability to swim freely without being overly affected by currents.

Most of our knowledge of octopus para larvae comes from studies of just two species, O. vul-garis 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 non- existent. This is despite references to octopus para larvae dating back more than 2300 yr. probably referring to Octopus vulgaris para larvae of the Mediterranean sea, Aristotle noted that “the crea-ture 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 para larvae and proposed both a suite of taxonomic characters and a standardized format for morphological descrip-tion. 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 para larvae 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 para larvae) must be taken as tentative.


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Table 1 species of octopodidae known (or likely) to possess planktonic para larvae: maximum values of egg length (Elmax, in mm) and egg length index (Elimax, egg length as percentage of mantle length)

species Elmax Elimax Reference paralarvae hatched in laboratory

Abdopus abaculus 2.4 7.9 Norman & Finn 2001

Abdopus aculeatus 3 7.2 Norman & Finn 2001

Abdopus tonganus 2.8 Norman & Finn 2001

Amphioctopus aegina 2.4 4 Norman unpubl. data Eibl-Eibesfeldt & scheer 1962, ignatius & srinivasan 2006

Amphioctopus arenicola 2.7 ~4 huffard & hochberg 2005

Amphioctopus burryi 2.5 hochberg et al. 1992 Forsythe & hanlon 1985

Amphioctopus exannulatus 3.9 7.3 Norman 1992a

Amphioctopus kagoshimensis 1.8 Norman unpubl. data

Amphioctopus cf kagoshimensis 3.8 8.3 Norman & kubodera 2006

Amphioctopus marginatus 3 4.3 Norman 1992b

Amphioctopus mototi 6 7.8 Norman 1992a

Amphioctopus neglectus 7 Nateewathana & Norman 1999

Amphioctopus ovulum 3 sasaki 1929

Amphioctopus rex 3 6.5 Nateewathana & Norman 1999

Amphioctopus robsoni 5.2 8.8 Norman 1992a

Amphioctopus siamensis 1.7 Nateewathana & Norman 1999

Amphioctopus varunae 2 3.3 Norman 1992a

Aphrodoctopus schultzei 7.5 7 smith 1999

Callistoctopus aspilosomatis small type Norman 1992c

Callistoctopus lechenaultii small type Norman unpubl. data

Callistoctopus luteus 1 0.8 Norman & sweeney 1997

Callistoctopus macropus 2.5 Mangold 1998 Boletzky et al. 2001

Callistoctopus nocturnus small type Norman & sweeney 1997

Callistoctopus ornatus 3.5 2.7 Norman 1993

Cistopus indicus 4.5 3.8 Norman & sweeney 1997

Eledone cirrhosa 7.5 small type Boyle 1983 Mangold et al. 1971

Enteroctopus dofleini 8 small type hochberg 1998 Gabe 1975, okubo 1979, 1980, Marliave 1981, snyder 1986a,b, and others

Enteroctopus magnificus 7 1.9 Villanueva et al. 1991

Enteroctopus megalocyathus 12 0.2 ortiz et al. 2006 ortiz et al. 2006

Euaxoctopus panamensis 1.4 Voss 1971

Hapalochlaena lunulata 3.5 hochberg et al. 1992 overath & Boletzky 1974

Macroctopus maorum 7 2.7 stranks 1996 Batham 1957

Macrotritopus defilippi 2.1 Mangold 1998 hanlon et al. 1985

Octopus alecto 2.5 hochberg et al. 1992

Octopus berenice 1.5 hochberg et al. 1992


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For such samples that are not directly linked to spawning adult females, there is potential for mis-identification 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

Table 1 (continued) species of octopodidae known (or likely) to possess planktonic para larvae: maximum values of egg length (Elmax, in mm) and egg length index (Elimax, egg length as percentage of mantle length)

species Elmax Elimax Reference paralarvae hatched in laboratory

Octopus bimaculatus 4 hochberg et al. 1992 Ambrose 1981

Octopus bocki 2 9.5 Norman & sweeney 1997

Octopus campbelli 1.7 small type o’shea 1999

Octopus cyanea 2.5 1.7 Norman 1991 Van heukelem 1973

Octopus favonius small type Norman unpubl. data

Octopus filosus 1.8 Voss & Toll 1998

Octopus hawiiensis 3 hochberg et al. 1992

Octopus hummelincki 3 hochberg et al. 1992

Octopus huttoni 3.1 o’shea 1999 Brough 1965 (as Robsonella australis)

Octopus joubini 4.8 small type Voss & Toll 1998 Forsythe & Toll 1991

Octopus laqueus 2.8 small type kaneko et al. 2006 kaneko et al. 2006

Octopus mimus 3 small type cortez et al. 1995a Zúñiga et al. 1997, Warnke 1999, Baltazar et al. 2000, Montoya 2002

Octopus parvus 1.8 small type sasaki 1929

Octopus rubescens 4 hochberg et al. 1992

Octopus salutii 6 5 hochberg et al. 1992 Mangold-Wirz et al. 1976

Octopus selene 1.6 3.2 Voss 1971

Octopus tetricus 2.5 hochberg et al. 1992

Octopus ‘tetricus’ West Australia

2.4 Norman unpubl. data Joll 1976, 1978

Octopus veligero small type hochberg unpubl. data

Octopus vitiensis 2 Norman unpubl. data

Octopus vulgaris 2.7 hochberg et al. 1992 Naef 1928, Vevers 1961, itami et al. 1963 and others

Octopus warringa 3 small type Norman 2000 Norman 2000

Octopus wolfi small type Norman unpubl. data

Pteroctopus tetracirrhus 8.3 9 Boletzky 1981

Robsonella fontanianus 5 small type hochberg et al. 1992 González et al. 2006

Scaeurgus jumeau 2.6 11 Norman et al. 2005

Scaeurgus nesisi 1.7 3.6 Norman et al. 2005

Scaeurgus patiagatus 2.5 hochberg et al. 1992

Scaeurgus tuber 2.7 6.2 Norman et al. 2005

Scaeurgus unicirrhus 2.5 hochberg et al. 1992 Boletzky 1984

Thaumoctopus mimicus small type Norman & hochberg 2005b

Wunderpus photogenicus 3.6 10.1 hochberg et al. 2006 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 para larvae have been described from laboratory hatched individuals.


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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 plank-tonic 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 para larvae: neoteny and holopelagic octopuses’, p. 182. The aim of the current work is to review available knowledge on all aspects of octopus para larvae of the benthic octopuses (family octopodidae) and encompasses their diversity, spawning characteristics, morphology, sen-sory 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 para larvae 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 para larvae’, 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 18–20 days for Amphioctopus aegina incubated at 28–30°c (ignatius & srinivasan 2006), 21 days


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in Octopus cyanea at mean temperature of 27.1°c (Van heukelem 1973), 22–25 days in O. vulgaris at 25°c (Mangold 1983), 22–30 days in O. laqueus at 26°c (kaneko et al. 2006) and 23 days at 26°c 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 9.2–13.9°c when the female tends the eggs (Gabe 1975) and up to 5–6 months at 9.4–13°c when the eggs are incubated experimentally without the female in breeder nets (snyder 1986a, s. snyder unpublished manuscript). For Eledone cirrhosa, 3–4 months at 14–18°c 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 phys-iological 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 pro-vided 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 ener-getically 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 kölliker organs also probably help to prevent the retraction of the emerg-ing octopus back into the egg capsule during hatching (Naef 1923, Boletzky 1966) (see ‘surface epi-thelia 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 17–24 m depth (cosgrove 1993), whereas daytime hatching was observed for para larvae of Octopus bimaculatus, swimming upwards and reaching depths of 1–5 m below the surface (Ambrose 1981). under laboratory conditions, para larvae 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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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 synchro-nizer, 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 preda-tion (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 para larvae needs to be confirmed and quantified, with the influ-ence 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

Figure 2 line drawing showing the hatching process in Octopus vulgaris. The hatching gland (or hoyle’s 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 kölliker organs covering the body surface have been emphasized to show position and orientation. see text for details. (original drawing from Jordi corbera with permission.)


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temperature and the species. Egg laying under aquarium conditions in temperate and tropical spe-cies takes 10 days at 18.2–20°c in Octopus luteus (Arakawa 1962), 4–7 days at 21–27°c (caverivière et al. 1999) and 9 days at 17–19°c in O. vulgaris (iglesias et al. 2004). in cold water species, it takes 14 days at 9.2–10.3°c (Gabe 1975) and 20 days at 15.2°c (yamashita 1974) for Enteroctopus dofleini, and for Eledone cirrhosa, it can take from 8 days (Joubin 1888), to 10–15 days at 14°c (Mangold et al. 1971) or nearly 1 month (Gravely 1908). As a consequence of these diverse egg-laying 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 26°c in Octopus laqueus (kaneko et al. 2006) to 78 days at 10–12.8°c 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-light-level videography may be a promising avenue for investigating natural hatching processes.

Morphological characteristics of planktonic octopus para larvae

At hatching, the external attributes of octopus para larvae are distinctive and often markedly dif-ferent from that of post-settlement juveniles and the first growth stages of species with benthic hatchlings. All inner organs of planktonic octopus para larvae are well differentiated at hatching except for the reproductive system. however, there are few data on the development of the diges-tive, 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 para larvae 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 para larvae is their largely transparent form. All mus-culature is transparent including those of the mantle, head, arms, webs and suckers. This trans-parency is not visible in preserved material as the musculature becomes opaque on fixation. This transparency matches the planktonic lifestyle of the para larvae, minimizing their silhouette, and hence visibility, to predators (and prey) below. No studies have examined the microscopic structure of the transparent musculature of octopus para larvae. The mantle musculature of some holo pelagic 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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Haliphron, Mangold et al. 1989). A similar arrangement is likely to be present in octopus para larvae but as yet the histological structure of the musculature of these animals has not been examined.

General body proportions of octopus para larvae 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 para larvae 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 para larvae have arms of equivalent length (Figure 3, 6A),

Table 2 Duration of hatching period from a single egg mass in octopodidae species with planktonic hatchlings

species

hatching duration (days)

Temperature (°c) during

hatching

laboratory or field

observation comments Reference

Amphioctopus aegina 3 Np laboratory sarvesan 1969 (as Octopus dollfusi)

3 28–30 laboratory ignatius & srinivasan 2006

Amphioctopus burryi 10 23–24 laboratory Forsythe & hanlon 1985

Enteroctopus dofleini 39 12.5–15.3, mean 13.9

laboratory Eggs incubated without female

okubo 1973

49 4–7 laboratory Ruggieri & Rosenberg 1974

78 10–12.8 laboratory Eggs incubated without female

Gabe 1975

30 14 laboratory okubo 1979

27 Np laboratory okubo 1980

45 9–13 laboratory Eggs incubated without female

snyder 1986a, unpublished

<7 Np Field cosgrove 1993

Macroctopus maorum 10 Np laboratory Batham 1957

Octopus laqueus 2–9 26 laboratory 75% hatched in 1 h of the same day

kaneko et al. 2006

Octopus mimus 14 16, 20 and 24

laboratory No differences between temperatures

Warnke 1999

Octopus cf tetricus 28 19 laboratory Joll 1976

6 21

10 22.6

8–15 20 laboratory Eggs incubated with and without female

Joll 1978

Octopus vulgaris 6–12 22–23 laboratory Vevers 1961

3–8 21–27 laboratory caverivière et al. 1999

5 17–19 Field caverivière et al. 1999

Octopus huttoni 21 Np laboratory Brough 1965 (as Robsonella australis)

Wunderpus photogenicus 3 26 laboratory Miske & kirchhauser 2006

Note: Np, not provided.


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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 para larvae possess a longer third arm pair (Figure 6, right), as do certain unidentified para larvae (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 gen-era 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 para larvae show strong parallels with a number of holopelagic octopuses (families Bolitaenidae, Vitreledonellidae and Amphitretidae) and squids (family cranchiidae) (see ‘permanent para larvae: neoteny and holope-lagic octopuses’, p. 182).

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Figure 3 (see also colour Figure 3 in the insert.) individuals of Octopus vulgaris from hatching to settle-ment 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 océanologique de Banyuls, cNRs. Reproduced with permission from Villanueva et al. 1995, modified.)


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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 pat-terns 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 para larvae. 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 pig-ment 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 mm−2 (packard & sanders 1969), enabling presentation of complex

Figure 4 (see also colour Figure 4 in the insert.) Micronektonic octopus para larvae. 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.)


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chromatic displays (hanlon & Messenger 1996). in octopus para larvae, 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 para larvae possess a low number of large chromatophores, pres-ent 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 enable species identification (hochberg et al. 1992). The number and distribution of chro-matophores on the skin over the arms, funnel, eyes, head, mantle and peri visceral epithelium (i.e., chromatophore fields) of octopus para-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 chromato-phores. 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 para larvae, particularly in the earliest stages. They are present, however, in the membranes enclosing the eyes and viscera, provid-ing a reflective surface to these opaque body organs as an additional ambient light reflector appro-priate for a pelagic environment (Figure 4 bottom). small spots of dermal iridescence are evident in some para larvae, potentially produced from the bristles of the kölliker organs (described in the section ‘kölliker organs’, p. 120) (e.g., unknown species; Figure 9). in some late-stage para larvae, 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 para larvae.

Figure 5 Euaxoctopus panamensis, 11-mm mantle length (Ml). Note the large second arm pair, measur-ing 32 mm long. collected using isaacs-kidd midwater trawls (ikMT) between 0 and 500 m depth, 09°N 90°W, off costa Rica, eastern pacific. (Reproduced with per-mission from Nesis & Nikitina 1991, modified.)

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.)


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As with iridophores, these structures may be evident in para larvae close to settlement. The simple chromatic capacities of planktonic octopus para larvae 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 hoyle’s 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.

Figure 7 (see also colour Figure 7 in the insert.) chromatophores contracted (left) or expanded (right) on the head of para larvae. 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.)

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Figure 8 Distribution of chromatophore fields in octopodidae. (A) left lateral view, optical section; (B) dor-sal 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.)


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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 1978–1979, Boletzky 1982). The two different cell types and structure described for the hatching gland of loliginid squids (Arnold & singley 1989, paulij & Denucé 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

Figure 9 (see also colour Figure 9 in the insert.) iridescence in octopus para larvae. left, unidentified par-alarva showing scattered points of iridescence, potentially from kölliker 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.)


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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 embry-onic epidermis and its many ciliated cells (Budelmann et al. 1997).

Kölliker organs

kölliker organs are bristle-like structures present on the surface of the head, arms, funnel and mantle of embryos, para larvae and recently settled octopus individuals, giving the animals a punc-tate 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 kölliker (1844) from Argonauta embryos, they have also been described by other authors (Querner 1927, Naef 1928, Adam 1939, Fioroni 1962, Boletzky 1978–1979, Joll 1978). Detailed description of the histology and ultrastructure of the kölliker 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 kölliker organs is relatively constant in preserved specimens (30–40 µm) for species with very dif-ferent hatchling size, representing 4% of the Ml in Argonauta argo and 0.4% in Eledone moschata. Their density in planktonic para larvae is, however, higher than in benthic juveniles (Boletzky 1973). in para larvae of some species, high densities of kölliker 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 kölliker organs help the animal to move in one direction and exit the chorion membrane (Naef 1923, Boletzky 1966, 1978–1979). This does not seem to be the sole function of these organs. For captive-reared Octopus vulgaris, kölliker organs have been recorded from hatch-ling through to settlement, and on the distal portion of the arms in pre- and post-settlement para-larvae, indicating the addition of new organs after hatching and during the entire planktonic phase (Villanueva 1995) (Figure 11F–h).

After hatching, the primary function of the kölliker organs during the planktonic phase remains unknown and many hypotheses have been proposed for these amazing structures. As kölliker 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); how-ever 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. kölliker 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 kölliker organs form the basis for the formation of the juve-nile and adult skin warts or skin papillae. kölliker 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 para larvae: 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 para larvae 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 µm


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Figure 11 kölliker 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 kölliker organs on the skin. (B) left ventrolateral view of 30-day-old indi-vidual, 4.8 mm Ml (fresh). Note the density of kölliker 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 kölliker 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 kölliker 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 (3–4°c), then fixed in 5% buffered formalin. original.


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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 aper-tures that may be the secretory products of these potential mucus-secreting cells (Figure 14).

Sucker surfaces

in hatchling octopus para larvae 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 sur-round 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 pro-cess in hatchling octopus para larvae 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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Figure 12 kölliker organs in Enteroctopus megalocyathus hatchling para larvae. individuals collected dur-ing rearing experiments described in ortiz et al. (2006). scanning electron microscope images from ventral (A) and lateral (B) views. Note the density of kölliker organs on the mantle, head and arms and the ventral mantle. (c) skin surface of the ventral mantle showing kölliker organs and cilia (D) observed inside the rect-angle. (E) kölliker organs from ventral mantle in different degrees of expansion. (specimens kindly provided by N. ortiz, centro Nacional patagónico, coNicET.) original.


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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 para larvae 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 bin-ocular microscope show a transparent skin film densely surrounded by kölliker organs and cover-ing 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 13 kölliker organ from the skin of Octopus sp. hatchling para larvae. (A) scanning electron micro-scope image of a radiated fascicle showing the rodlets and three new fascicles (white arrows) beginning to emerge. scale 30 µm. (B) longitudinal section of an emerged fascicle, transmission electron microscope image. scale 5 µm. inset, section through a microvillus of the chaetoblast that inserts into the basal end of a rodlet. inset scale 0.5 µm. (c) Diagram of an everted fascicle. c, chaetoblast; E, epidermal cell; l, lateral fol-licular 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 show-ing the pores and the secretory spherules (scale 0.01 mm). (Reproduced with permission from young et al. 1989.)


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microscopy. The presence of a similar loose skin structure has also been reported for laboratory-hatched 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 para larvae of the same species had a “body all covered with gelatinous tissue which is more prominent in smaller speci-mens”. 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 15 sucker structure of Octopus vulgaris hatchling para larvae. (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.)


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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. col-lected in the subtropical eastern north Atlantic.

A parallel supradermal skin layer is also found in three families of oceanic squids: octo-poteuthidae, 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 kölliker organs in octopus para larvae 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 para larvae 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 pos-sible premortem stress and/or fixative artefacts that may influence the general skin attributes in the preserved animal.

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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.)


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Sensory systems

Central nervous system

The nervous system of para larvae 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 (Frösch 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, coincid-ing with the rapid growth of the arms and suckers and the development of the tactile sense that is characteristic of the octopus’s 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 para larvae show adult-like characteristics, with the exception of the ‘lateral line system’, the pres-ence 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 para larvae 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 para larvae 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 dif-ferentiation and growth takes place. There is little information on the vision of planktonic octo-puses. unpublished observations (A. Bozzano, institut de ciències del Mar) showed that the eyes of

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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.)


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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, con-tains 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 cephalo-pods 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 photosensi-tive vesicles has been recorded in developed embryos of O. vulgaris (Marquis 1989) but their devel-opment 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 Büllow &

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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, photo-receptor nuclei; sN, supporting cell nuclei. photo courtesy of Anna Bozzano.


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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 20A–D) have a hemispheri-cal 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 para larvae aged 1 month (Figure 20E–h).

‘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 fun-nel in O. vulgaris hatchlings (lenz et al. 1995, lenz 1997). The epidermal line runs in an anterio-posterior direction. The dorsal, dorsolateral, ventrolateral and ventral lines are paired, occurring on

Figure 20 statoliths of Octopus vulgaris para larvae. scanning electron microscopic images from antero-lateral (A) and posterior (c) views of hatchling statoliths with their respective crystalline surface structure presented inside the rectangles (B, D). in para larvae aged 30 days, statolith growth is observed on the pos-terior 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.


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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 bear-ing up to six long (10-µm) 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 para larvae have not been reported in adult octopuses but they

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Figure 21 Epidermal lines in Octopus vulgaris hatchling para larvae. (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.)


130

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 epi-dermal 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 pre-venting 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 suck-ers of O. vulgaris, concluded that the ciliated cells present on the suckers are chemosensory recep-tors 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 35–45 µm 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 mor-phological cell type, suggesting the olfactory organ has both chemical and mechanosensitive func-tions 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 octo-pus para larvae 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).


131

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 den-ticles 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 para larvae 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

A

B C D

2

di

50 µm

5 µm

Figure 22 olfactory organ in Octopus vulgaris hatchling para larvae. 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 morphologi-cal type 5, cell apex with one kinocilium and microvilli (di, dictyosome). scale bar 2 µm. (Reproduced with permission from Wildenburg 1997, modified.)


132

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).

2 mm 200 um

Figure 23 olfactory organ in Enteroctopus megalocyathus hatchling para larvae. specimen collected during rearing experiments described in ortiz et al. (2006). scanning electron microscope images showing the posi-tion (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 patagónico, coNicET.) original.

50 µm

UB

LB

D

25 µm

Figure 24 Buccal mass and denticulation on the beaks of Octopus vulgaris. left, whole mount of a hatch-ling individual. Right, oral surface of the rostrum of the upper (top) and lower (bottom) beaks showing den-ticulation 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.)


133

Ink sac

For those species that possess an ink sac in the adult form, the ink sac of their para larvae is func-tional 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).

Figure 25 Denticulation of beaks in Octopus vulgaris para larvae. 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.


134

Food, feeding and nutritional requirements

Yolk reserves

After hatching, octopus para larvae 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

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.)

oorcv

frisgbh1 mm

A B C

sg

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 intes-tine; fr, funnel retractor; g, gill; is, ink sac; oo, olfactory organ; r, rectum; sg, stellate ganglion. (Reproduced with permission from Boletzky 1984, modified.)


135

(Figure 26). The yolk can be considered as a unit independent from the digestive system: the para-larvae 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 para larvae 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 tem-perature in squid para larvae (o’Dor et al. 1986, Vidal et al. 2002, 2005). The same relationship can also be expected for octopus para larvae. large octopus hatchlings from species adapted to low tem-peratures, such as Enteroctopus megalocyathus, can survive under starved conditions up to 15 days at 11.5°c (ortiz et al. 2006), while species with small hatchlings, such as Octopus cf tetricus, can survive up to 10 days at 20°c (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 sur-vival under starvation conditions. starved para larvae 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 para larvae and need further research.

Natural prey

At the moment of prey capture, octopus para larvae 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 (hernández-García 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 para larvae in the wild. passarella & hopkins (1991) examined stomach contents of 57 para larvae (<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 crusta-ceans and fishes. octopus para larvae share a preference for crustacean prey with squid para larvae (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 para larvae in laboratory experiments (Table 3). Most of the successful or long-term laboratory rearings used decapod crus-tacean zoeae (Figure 28) as the primary prey for small-sized octopus para larvae (Octopus vulgaris type) (itami et al. 1963, Forsythe & Toll 1991, Villanueva 1994, 1995, shiraki 1997, carrasco et al.


136

Tab

le 3

p

rey

offe

red,

rea

ring

tem

pera

ture

, sur

viva

l or

max

imum

age

in d

ays

(d),

and

dura

tion

of th

e pl

ankt

onic

per

iod

from

hat

chin

g to

se

ttle

men

t of

the

para

larv

ae o

btai

ned

duri

ng r

eari

ng e

xper

imen

ts o

f o

ctop

odid

ae s

peci

es w

ith p

lank

toni

c ha

tchl

ings

spec

ies

and

prey

off

ered

Tem

p.

(°c

)su

rviv

al r

ate

(%)

Rea

red

to

settl

emen

tc

omm

ents

Geo

grap

hic

area

Ref

eren

ce

Am

phio

ctop

us b

urry

i

liv

e w

ild z

oopl

ankt

on (

cope

pods

, lar

val

crus

tace

ans

and

fishe

s) a

nd A

rtem

ia

naup

lii

23–2

4To

16%

at 2

6 d

No

No

grow

th in

Ml

NW

Atla

ntic

Fors

ythe

&

han

lon

1985

Cal

list

octo

pus

mac

ropu

s

hat

chlin

g zo

eae

of P

agur

us p

ride

aux

16To

6 d

No

With

out f

ood

surv

ived

3–4

dM

edite

rran

ean

Bol

etzk

y et

al.

2001

Ent

eroc

topu

s do

flein

i

Art

emia

, fro

zen

Cal

anus

, fro

zen

and

live

zoop

lank

ton

Np

To 7

dN

oE

atin

g no

t obs

erve

dN

E p

acifi

cG

reen

197

3

piec

es (

2–5

mm

) of

pra

wns

(Pa

laem

on

paci

ficus

), c

lam

(R

udit

apes

ph

ilip

pina

rum

) an

d cr

ab

10.6

–11.

8,

mea

n 11

.0

To 2

6 d

No

Food

pie

ces

subm

erge

d pr

evio

usly

in f

resh

wat

er to

in

crea

se fl

oata

bilit

y

NW

pac

ific

oku

bo 1

973

liv

e m

ysid

acea

ns, a

mph

ipod

s an

d pi

eces

of

shr

imp

afte

r 70

dN

p4%

at 1

35 d

pres

ettle

men

tin

divi

dual

s re

ache

d 33

mm

Tl

at

115

dN

W p

acifi

co

kubo

197

4

Art

emia

and

hat

chlin

gs o

f gr

eenl

ing

fish

8.5–

15.6

, m

ean

11.8

To 1

9 d

No

Feed

ing

and

deve

lopm

ent n

ot

obse

rved

NW

pac

ific

yam

ashi

ta 1

974

cru

shed

egg

yol

k, g

roun

d sh

rim

p an

d m

usse

l, liv

e ga

mm

arid

s, A

rtem

ia b

iom

ass

and

fry

of fi

sh H

emil

epid

otus

he

mil

epid

otus

10–1

2.8

Np

No

onl

y ad

ult A

rtem

ia a

nd f

ry

fish

acce

pted

as

prey

; oc

casi

onal

ly d

ead

sibl

ings

ca

ptur

ed b

y th

e pa

ra la

rvae

NE

pac

ific

Gab

e 19

75

Mys

idac

eans

(5–

15 m

m)

duri

ng fi

rst

feed

ing

and

piec

es o

f sh

rim

p (P

alae

mon

pa

cific

us)

afte

r 70

d

7.8–

14.7

, m

ean

10.8

To 1

69 d

settl

emen

t fr

om

100–

117

d

indi

vidu

als

reac

hed

35 m

m T

l

at 1

69 d

NW

pac

ific

oku

bo 1

979

Fro

m h

atch

ing

to 5

0 d:

dea

d m

ysid

acea

ns +

am

phip

ods;

50–

80 d

: de

ad m

ysid

acea

ns +

am

phip

ods

+ p

iece

s of

shr

imp;

fro

m 8

0 d:

pie

ces

of s

hrim

p

Np

8% a

t 6 m

onth

ss

ettl

emen

t fr

om 8

8 d

Tank

wit

h up

wel

ling

wat

er

syst

em

NW

pac

ific

oku

bo 1

980


137

Art

emia

bio

mas

s, f

roze

n kr

ill (

Eup

haus

ia

paci

fica)

, lar

val c

ottid

fish

(H

emil

epid

otus

he

mil

epid

otus

), tr

out m

icro

pelle

ts

10W

ith A

rtem

ia: 5

0% s

R a

t 5

d an

d m

axim

um to

22

d;

with

kri

ll: 5

0% s

R a

t 16

d an

d m

axim

um to

87

d

No

The

pre

ferr

ed p

rey

was

kri

ll;

neus

toni

c fe

edin

g be

havi

our

desc

ribe

d

NE

pac

ific

Mar

liave

198

1

Froz

en o

r fr

esh

chop

ped

body

and

mus

cle

of c

rabs

Can

cer

prod

uctu

s, P

uget

tia

prod

uctu

s, ta

ils o

f Pa

ndal

us d

anae

sh

rim

ps, E

upha

usia

pac

ifica

, bee

f he

art

and

lam

b ki

dney

11–1

1.5

4% a

fter

6–7

mon

ths

settl

emen

t fr

om 5

to

6 m

onth

s

hat

chlin

g fo

od s

ize

equi

vale

nt

to o

ctop

us h

ead

wid

th;

deve

lope

d pa

ra la

rvae

fee

d on

ch

unks

of

food

3–6

× 2

5 m

m

susp

ende

d in

the

tank

NE

pac

ific

snyd

er 1

986a

,b,

unpu

blis

hed

man

uscr

ipt

Ent

eroc

topu

s m

egal

ocya

thus

star

ved

11.5

To 1

5 d

No

sW A

tlant

ico

rtiz

et a

l. 20

06

Hap

aloc

hlae

na lu

nula

ta

Art

emia

and

sm

all c

rust

acea

ns26

To 7

dN

osl

ight

par

alar

val g

row

thc

entr

al E

pa

cific

ove

rath

&

Bol

etzk

y 19

74

Mac

roct

opus

mao

rum

star

ved

Np

To 8

dN

osW

pac

ific

Bat

ham

195

7

Oct

opus

bim

acul

atus

Art

emia

and

wild

pla

nkto

nN

pTo

6 d

No

NE

pac

ific

Am

bros

e 19

81

Oct

opus

cya

nea

cra

b an

d m

ysis

zoe

ae, c

opep

ods

Pro

mys

is

orie

ntal

is a

nd L

ucif

er s

p.N

pTo

21

dN

oG

row

th in

crea

se in

0.5

mm

T

l; u

nfed

con

trol

s di

ed in

5 d

haw

aii

isla

nds

Van

heu

kele

m

1973

Oct

opus

joub

ini

Wild

live

zoo

plan

kton

, zoe

a of

pen

aeid

sh

rim

p, m

ysid

acea

n sh

rim

p24

To 1

0% a

t 7 d

and

0.2

% a

t 23

dse

ttlem

ent

from

21

dA

dditi

on o

f vi

tam

in

supp

lem

ent m

ixtu

re to

the

rear

ing

tank

s

NW

Atla

ntic

Fors

ythe

& T

oll

1991

Oct

opus

laqu

eus

Art

emia

nau

plii,

cop

epod

s an

d pi

eces

of

shri

mp

26To

7 d

No

onl

y fe

edin

g on

pie

ces

of

shri

mp

was

obs

erve

dN

W p

acifi

ck

anek

o et

al.

2006

Oct

opus

mim

us

Art

emia

met

anau

plii,

zoe

ae o

f L

epto

grap

sus

vari

egat

us a

nd C

ance

r se

tosu

s, a

nd r

otif

ers

<22

To 3

1 d

No

Bes

t res

ults

with

zoe

ae a

s fo

od

and

octo

pus

dens

ity o

f 25

ind

l−1

sE p

acifi

cZ

úñig

a et

al.

1997

hat

chlin

g zo

eae

of P

agur

us s

p. a

nd C

ance

r se

tosu

sN

pTo

12

dN

osE

pac

ific

War

nke

1999

(con

tinu

ed o

n ne

xt p

age)


138

Tab

le 3

(con

tinu

ed)

pre

y of

fere

d, r

eari

ng te

mpe

ratu

re, s

urvi

val o

r m

axim

um a

ge in

day

s (d

), an

d du

ratio

n of

the

plan

kton

ic p

erio

d fr

om

hatc

hing

to s

ettle

men

t of

the

para

larv

ae o

btai

ned

duri

ng r

eari

ng e

xper

imen

ts o

f o

ctop

odid

ae s

peci

es w

ith p

lank

toni

c ha

tchl

ings

spec

ies

and

prey

off

ered

Tem

p.

(°c

)su

rviv

al r

ate

(%)

Rea

red

to

settl

emen

tc

omm

ents

Geo

grap

hic

area

Ref

eren

ce

Art

emia

nau

plii

21–2

210

% a

t 5 d

, max

imum

su

rviv

al to

17

dN

osE

pac

ific

Bal

taza

r et

al.

2000

Art

emia

, Bra

chio

nus,

zoe

ae o

f C

ance

r se

tosu

s, H

epat

us c

hili

ensi

s, E

mer

ita

anal

oga

and

Ple

uron

code

s m

onod

on a

nd

mic

rope

llets

17–2

3To

23

dN

osE

pac

ific

Mon

toya

200

2

Oct

opus

tetr

icus

cop

epod

s, A

rtem

ia, s

mal

l pie

ces

of fi

sh

and

mol

lusc

aTo

32

To 6

d

No

All

food

ref

used

sW p

acifi

cD

ew 1

959

(as

O. c

yane

a)

Oct

opus

cf

tetr

icus

Art

emia

and

ric

e po

wde

rN

pTo

21

dN

oN

o gr

owth

, no

evid

ence

of

eatin

gE

ind

ian

Joll

1976

Oct

opus

vul

gari

s

Arg

onau

ta a

rgo

hatc

hlin

gsN

pTo

12

dN

oM

edite

rran

ean

Nae

f 19

28

har

pact

icoi

d co

pepo

ds, A

rtem

ia, c

iliat

es,

yeas

t cel

ls23

To 9

dN

oN

o fe

edin

g ob

serv

edN

E A

tlant

icV

ever

s 19

61

Pala

emon

ser

rife

r de

capo

d pa

laem

onid

zo

eae

Mea

n 24

.79%

at s

ettle

men

tse

ttlem

ent

from

33

dP.

ser

rife

r zo

eae

feed

with

A

rtem

ia n

aupl

iiN

W p

acifi

cit

ami e

t al.

1963

Zoe

ae o

f cr

abs

and

praw

ns, A

rtem

ia

biom

ass

Np

To 3

5 d

No

Gro

wth

cea

sed

from

25

dM

edite

rran

ean

Man

gold

&

Bol

etzk

y 19

73

Art

emia

bio

mas

s25

.1To

67%

at 2

2 d

Tra

nsiti

on to

be

nthi

c st

age

Mic

roal

gae

Nan

nocl

orop

sis

adde

d to

the

cultu

re ta

nkN

W p

acifi

cim

amur

a 19

90

Art

emia

bio

mas

s25

–28

30%

at 2

5 d

Tra

nsiti

on to

be

nthi

c st

age

Tank

vol

ume

of 2

0 m

3 an

d m

icro

alga

e N

anno

clor

opsi

s ad

ded

to th

e ta

nk

NW

pac

ific

ham

azak

i et a

l. 19

91

Lio

carc

inus

dep

urat

or a

nd P

agur

us

prid

eaux

dec

apod

cra

b zo

eae

21.2

9% to

set

tlem

ent a

t 47

d se

ttlem

ent

from

47

dFo

od a

dded

5 ti

mes

per

day

Med

iterr

anea

nV

illan

ueva

19

94, 1

995

Art

emia

and

Por

tunu

s tr

itube

rcul

atus

cra

b zo

eae

Np

30%

at 2

9 d

pres

ettle

men

tin

divi

dual

s w

ith 1

9 su

cker

s at

29

dN

W p

acifi

csh

irak

i 199

7


139

Art

emia

bio

mas

s (1

–2.7

mm

) fe

ed w

ith o

r w

ithou

t Nan

noch

loro

psis

alg

ae o

n th

e re

arin

g ta

nk

21, 2

4 an

d 27

To 8

8% a

t 24

dN

oh

ighe

r gr

owth

and

sur

viva

l w

ith 1

00–4

00 ×

104

alga

l ce

lls/m

l

NW

pac

ific

ham

asak

i &

Take

uchi

200

0

Rot

ifer

s, fi

sh e

ggs,

mic

rope

llets

, wild

co

pepo

ds, A

rtem

ia n

aupl

ii an

d m

etan

aupl

ii, z

oeae

of

shri

mp

Pala

emon

se

rrat

us, z

oeae

of

crab

Car

cinu

s m

aena

s an

d N

ecor

a pu

ber

18–2

0To

32

dN

oB

est s

urvi

val w

ith A

rtem

ia

met

anau

plii

NE

Atla

ntic

igle

sias

et a

l. 20

00

Art

emia

bio

mas

s (1

–3 m

m)

and

pelle

ts

(250

–500

µm

) w

ith 6

% m

oist

ure

20–2

2.5

To 6

.7%

at 3

0 d

No

Fatty

aci

d of

cul

ture

d oc

topu

s re

flect

ed th

at o

f th

e fo

odM

edite

rran

ean

Nav

arro

&

Vill

anue

va

2000

Nan

noch

loro

psis

alg

ae o

n th

e re

arin

g ta

nk

at 1

00 ×

104

cells

/ml;

Art

emia

bio

mas

s (2

mm

) no

t enr

iche

d or

enr

iche

d w

ith

yeas

t or

shar

k eg

g po

wde

r

25To

45%

and

24%

at 1

6 an

d 20

d, r

espe

ctiv

ely

No

Enr

iche

d A

rtem

ia in

crea

sed

surv

ival

and

gro

wth

NW

pac

ific

ham

asak

i &

Take

uchi

200

1

Art

emia

bio

mas

s (1

.5–2

mm

) fe

ed w

ith

Nan

noch

loro

psis

alg

ae17

–29

To 6

2.5%

at 4

0 d

No

hig

hest

sur

viva

l at 2

1°c

NW

pac

ific

ham

asak

i &

Mor

ioka

200

2

Oct

opus

vul

gari

s

Art

emia

bio

mas

s an

d zo

eae

of M

aja

squi

nado

Np

To 5

6 d

No

Tank

vol

ume

of 9

m3

and

mic

roal

gae

Isoc

hrys

is,

Tetr

asel

mis

and

Cha

etoc

eros

NE

Atla

ntic

Mox

ica

et a

l. 20

02

Art

emia

nau

plii

and

mill

icap

sule

s of

1.

3–2

mm

in ∅

, 0.3

mg

fres

h w

eigh

t19

.4–2

2.5

To 4

.6%

at 3

0 d

No

Tota

l pro

teol

ytic

act

ivity

co

rrel

ated

with

par

alar

val

wei

ght

Med

iterr

anea

n V

illan

ueva

et a

l. 20

02

liv

e an

d fr

ozen

Maj

a br

achy

dact

yla

zoea

e 1–

3 d

old

and

Art

emia

bio

mas

s21

.1–2

2.2

3.4%

at 6

0 d

settl

emen

t fr

om 5

2 d

para

bolic

tank

s w

ith u

pwel

ling

wat

er s

yste

mN

E A

tlant

icc

arra

sco

et a

l. 20

03, 2

006

Maj

a br

achy

dact

yla

zoea

e an

d A

rtem

ia

biom

ass

(1–4

mm

)22

.531

.5%

at 4

0 d

settl

emen

t fr

om 4

0 d

Mic

roal

gae

(Chl

orel

la s

p.,

Isoc

hrys

is g

alba

na a

nd

Cha

etoc

eros

sp.

) add

ed d

aily

to

the

cultu

re ta

nk

NE

Atla

ntic

igle

sias

et a

l. 20

04

(con

tinu

ed o

n ne

xt p

age)


140

Tab

le 3

(con

tinu

ed)

pre

y of

fere

d, r

eari

ng te

mpe

ratu

re, s

urvi

val o

r m

axim

um a

ge in

day

s (d

), an

d du

ratio

n of

the

plan

kton

ic p

erio

d fr

om

hatc

hing

to s

ettle

men

t of

the

para

larv

ae o

btai

ned

duri

ng r

eari

ng e

xper

imen

ts o

f o

ctop

odid

ae s

peci

es w

ith p

lank

toni

c ha

tchl

ings

spec

ies

and

prey

off

ered

Tem

p.

(°c

)su

rviv

al r

ate

(%)

Rea

red

to

settl

emen

tc

omm

ents

Geo

grap

hic

area

Ref

eren

ce

Art

emia

nau

plii

and

esse

ntia

l am

ino

acid

s ad

ded

to th

e re

arin

g ta

nk19

.2–2

1.1

To 1

2.5%

at 3

0 d

No

Bes

t sur

viva

l in

tria

ls r

ecei

ving

am

ino

acid

sM

edite

rran

ean

Vill

anue

va e

t al.

2004

, V

illan

ueva

&

Bus

tam

ante

20

06

Art

emia

met

anau

plii

and

zoea

e of

Maj

a sq

uina

do20

± 1

To 2

6 d

No

Bet

ter

grow

th a

nd s

urvi

val

with

ligh

t int

ensi

ty o

f 60

00 lu

x

cen

tral

E

Atla

ntic

Fern

ánde

z-l

ópez

et a

l. 20

05

Art

emia

met

anau

plii,

cla

doce

rans

Moi

na

sali

na, z

oeae

of

Maj

a br

achy

dact

yla

and

Pala

emon

ser

ratu

s, e

ggs

and

larv

ae o

f fis

h So

lea

sene

gale

nsis

, art

ifici

al p

elle

ts

21–2

2To

10

dN

opr

otea

se a

ctiv

ity in

dica

tes

hatc

hlin

g co

nditi

onN

E A

tlant

icM

orot

e et

al.

2005

Art

emia

nau

plii

and

thaw

ed f

roze

n fis

h (A

mm

odyt

es p

erso

natu

s) fl

akes

21.2

–24.

8To

45.

9% a

t 32

dT

rans

ition

to

bent

hic

stag

e

Fish

flak

es e

ffec

tive

for

impr

ovin

g th

e D

hA

con

tent

of

the

para

larv

ae

NW

pac

ific

oku

mur

a et

al.

2005

a

Art

emia

bio

mas

s of

0.8

and

1.4

mm

18–2

03d

No

pref

eren

ce f

or A

rtem

ia 1

.4 m

m

at d

ensi

ties

of 0

.1 A

rtem

ia

ml−

1

NE

Atla

ntic

igle

sias

et a

l. 20

06

Art

emia

nau

plii

and

defr

ozen

fish

(A

mm

odyt

es p

erso

natu

s) fl

akes

24–2

6.9

To 1

0% a

t 42

dT

rans

ition

to

bent

hic

stag

e

Fish

flak

es im

prov

ed D

hA

co

nten

t of

the

para

larv

aeN

W p

acifi

ck

urih

ara

et a

l. 20

06

Oct

opus

vul

gari

s

Art

emia

met

anau

plii,

Gra

psus

gra

psus

and

P

lagu

sia

depr

essa

zoe

aeN

pTo

27%

at 2

8 d

No

Bes

t sur

viva

l and

gro

wth

with

G

. gra

psus

zoe

aeN

E A

tlant

icig

lesi

as e

t al.

2007

Art

emia

nau

plii

supp

lem

ente

d w

ith

cope

pods

(A

cart

ia to

nsa)

, juv

enile

mys

ids

(Met

amys

idop

sis

elon

gata

atl

anti

ca)

and

crab

zoe

ae (

Cal

line

ctes

sap

idus

)

20 ±

1To

39%

at 4

0 d

No

Bes

t sur

viva

l with

A. t

onsa

up

to 1

5 d

supp

lem

ente

d w

ith

Art

emia

sE A

tlant

icig

lesi

as e

t al.

2007

Art

emia

0.8

mm

202d

No

prey

cap

ture

hig

her

duri

ng

light

per

iods

, dec

reas

ing

in

the

dark

NE

Atla

ntic

Már

quez

et a

l. 20

07


141

Rob

sone

lla

font

ania

nus

Art

emia

, sm

all c

rust

acea

ns a

nd

mic

rope

llets

10–1

6To

34

dN

psE

pac

ific

Gon

zále

z et

al.

2006

Scae

urgu

s un

icir

rhus

Art

emia

bio

mas

s19

To 6

dN

oM

edite

rran

ean

Bol

etzk

y 19

84

Wun

derp

us p

hoto

geni

cus

Art

emia

nau

pli,

rotif

ers

Bra

chio

nus

and

cope

pods

26To

4 d

No

sW p

acifi

cM

iske

&

kir

chha

user

20

06

Not

e:

Dh

A, d

ocos

ahex

anoi

c a

cid;

Ml

, man

tle le

ngth

; Np,

not

pro

vide

d; s

R, s

urvi

val r

ate;

Tl

, tot

al le

ngth

.


142

2003, 2006, iglesias et al. 2004) or mysidaceans, amphipods and euphausiids for larger-size para-larvae (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 para larvae collected in plankton nets 1–2 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 lit-toral octopuses although stomach analyses from wild para larvae 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 para larvae (Venter et al. 1999, hoving et al. 2005) may be useful tools for gaining better insights into the earliest feeding stages of octopus para larvae.

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 plank-tonic octopus have been determined only under experimental conditions. Artemia of 1.1–1.7 mm (imamura 1990) or 1.5–2 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 45–118% of octopus total length and 2–32% 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).

Figure 28 Decapod crab zoeae hatchlings used as live prey in successful rearing experiments of Octopus vulgaris para larvae. 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).


143

prey densities in successful cultures using decapod crustacean zoeae ranged from 0.1–0.3 Pagurus prideaux ml−1 (Villanueva 1995) to 0.01–1 Maja brachydactyla ml−1 supplemented with 0.05–0.8 Artemia ml−1 (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 sig-nificant 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 ml−1; however, Márquez et al. (2007), using Artemia nauplii (0.8 mm length), observed higher consumption rates at 9.4 Artemia ml−1 in comparison with 2.3 and 4.7 Artemia ml−1. As Octopus vulgaris para larvae grow in the second half of their plank-tonic phase, larger prey are required. hatchling decapod zoeae decrease in size relative to presettle-ment para larvae (>10 mm total length), representing only 9–26% of their length and 0.04–0.7% of their weight (Figure 29). presettlement O. vulgaris-type para larvae, large Enteroctopus-type paralarval forms and micronektonic para larvae forms (see p. 182) probably require larger prey. in fact, E. dofleini hatchings (10 mm total length) eat mysidaceans 5–15 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 rela-tively large octopus para larvae 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 (Márquez et al. 2007). however, these authors showed that light may not be essential for prey cap-ture as a positive correlation was found between prey density and consumption rates in dark condi-tions. observations of the swimming paths of O. vulgaris para larvae in laboratory conditions over 2 months of planktonic life found that paralarval behaviour is affected by the presence of prey — individual para larvae 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

0 0 5 10

Octopus TL (mm) 15 20

20

40

60

80

100

120

140

0 1 10 100

Octopus TW (mg) 1000

5

10

15

20

25

30

35 Pr

ey T

L as

% o

f oct

opus

TL

Prey

TW

as %

of o

ctop

us T

W

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.


144

of patchy food environments as curvilinear paths and slow swimming speeds increase the probabil-ity 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 rou-tine swimming behaviour in a recognizable behavioural sequence (Boletzky 1987, Villanueva et al. 1996, hernández-García et al. 2000). After a zoea prey is selected, three phases can be identified (Figure 30). The first phase is the ‘attention phase’; para larvae reduce speed and approach the prey, using a range of different manoeuvring movements including forward, backward and lateral swim-ming. 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, some-times 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 para larvae 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 (hernández-García et al. 2000). During the attention phase, the para larvae 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.)


145

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 para larvae, as have been made on lolig-inid squid para larvae (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 para larvae preying on wild zooplankton, these distances are 10–30 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 para larvae 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 s−1, the estimated water volume searched (Vs) by 30-day-old O. vulgaris para larvae (Vs = 2/3·πR2·cruising speed; Blaxter & staines 1971) is 5.5 1 min−1 (Villanueva et al. 1996). This volume cannot be extrapolated to hour units until daily activity periods are recorded as para larvae 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 para larvae suggests that hydrostatic suction is not as effective in

200

160

120

80

40

0

160

Swim

min

g sp

eed

(mm

s–1)

120

80

40

0

160

120

80

40

0 –4 –2 –0 2

E F

A B

C D

2 4 0 Time (in seconds)

–2

Figure 31 swimming performance during six successful prey captures by 30-day-old Octopus vulgaris para larvae (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.)


146

early para larvae 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 adher-ence of paralarval suckers (kier & smith 1990, schmidtberg 1999).

Capture of inert prey

live prey is not a prerequisite stimulus in provoking attacks by octopus para larvae. 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 para larvae 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

00 0 10 20 30 40 50 605 10 15 20

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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, amphi-pods, pieces of shrimp), using a tank with an upwelling water system that maintained movement of the food particles. snyder (1986a,b, unpublished manuscript) fed para larvae of the same species over 5–6 months exclusively on inert food and pieces of crab and shrimp meal (3–6 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 condi-tions. 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 para larvae 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 para larvae 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 depolar-ized light (shashar et al. 1998). The role of polarization vision in octopus para larvae is unknown although it is likely to play an important role. As visual predators, octopus para larvae may target lumi-nescing 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 para larvae.

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 indi-cates 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.)


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Buccal mass, denticulate beaks and external digestion

in comparison with adults, octopus para larvae 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 diam-eter 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, repre-senting 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 para larvae beaks possess oral denticles. These den-ticles have also been observed for para larvae 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 para larvae 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 juve-nile 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 para larvae has been described for O. vulgaris hatchlings feeding in laboratory on recently hatched decapod crab zoeae Pachygrapsus marmoratus, P. transversus and Eriphia verrucosa (hernández-García 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 append-ages. similar observations have also been reported for 11-day-old loliginid squid para larvae (Loligo vulgaris) feeding on mysidacean shrimp in the laboratory (Boletzky 1974) and for adults of the


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pygmy squid Idiosepius (kasugai 2001, kasugai et al. 2004). During external digestion and inges-tion, 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. para larvae 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 tho-racic appendices (thoracopods) of this prey in the stomach contents (iglesias et al. 2006). similarly, exoskeleton crustacean remains were found in stomach contents of wild para larvae and juvenile squids (Vecchione 1991, Vidal & haimovici 1998), showing that external digestion is not the only digestive choice for para larvae. The selection of different modes of ingestion and/or digestion by the para larvae is probably related to prey characteristics. The mode of digestion as well as the percent-age of prey ingested or rejected require further research.

Daily food ration by octopus para larvae is also poorly known. itami et al. (1963) found that O. vulgaris of 3–5 or 6–8 mm total length ingested respectively 3–5 or 7–10 Palaemon serrifer zoeae (2–3 mm in total length) day−1 when reared at a mean temperature of 25°c. hatchlings of the same species maintained at 20°c ingested up to 10 Artemia nauplii (0.8 mm length) per day (Márquez et al. 2007). After prey capture, the duration of the ingestion process in Octopus vul-garis hatchlings preying on 0.8- to 1.4-mm Artemia ranged from 4 to 10 min (iglesias et al. 2006). For 15-day-old para larvae, the duration was up to 15 min when ingesting 250- to 500-µm 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 histo-chemical methods Boucaud-camou & Roper (1995) studied enzymes in wild Octopus sp. para-larvae of 1.7–2.6 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 cae-cum, 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 para-larvae.

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, record-ing trypsin activity for only 20% of the individuals analysed. This result suggests that trypsin activ-ity 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 para larvae have been shown to decrease their proteolytic activity (Villanueva et al. 2002). once external feeding commences, O. vulgaris para larvae 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 activ-ity can be detected after 5 days of rearing at a mean temperature of 20°c under high or low feed-ing 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 para larvae seem to be higher. Zambonino-infante et al. (1996) reported trypsin activity


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for Dicentrarchus labrax larvae at days 15, 20, 30 and 40 as 40, 120, 78 and 67 mu/mg–1 of protein respectively, with a sharp increase in activity after day 20. in Octopus vulgaris para larvae the cor-responding trypsin activity under a high feeding regime at days 10, 15 and 20 was 370, 460 and 340 mu/mg–1 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 oesopha-gus 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, o’Dor et al. 1984). The same role can be expected for octopus para larvae although its characteristics have not been studied in detail. R. Villanueva (unpublished) encapsulated glass ball beads (10–30 µm in diameter) within Artemia nauplii and offered them as food to 12-day-old Octopus vulgaris para larvae reared at 20°c. The para larvae 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 para larvae 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. para larvae. 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 para larvae has also been suggested to be a source of food to these para larvae (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 1−1 every 3 days) containing O. joubini para larvae in rearing experiments that resulted in successful settlement (Forsythe & Toll 1991). Rearing trials on O. vulgaris para larvae assessed the contribution of the daily addition of amino acid solution (16 mg 1−1 of crystalline essential amino acids) to the rearing tanks. survival rates for para larvae aged 20 days were three times higher for the treated group compared with the control group although the dry weight of the treated para-larvae 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 para larvae.


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Respiration

in addition to the gills, a high amount of oxygen is obtained by transcutaneous means in cephalo-pods (pörtner 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 ind−1 h−1, increasing three times in unfed hatchlings (53 nmol o2 ind−1 h–1) (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 para larvae, with the difference in oxygen uptake after hatching primar-ily 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. vul-garis (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 1−1 and temperature was maintained at 14°c.

Biochemical profiles of para larvae and nutritional requirements

Proteins and amino acids

proteins are the major organic component of octopus tissue. in contrast to the lipid-based metabo-lism 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 para larvae, 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, o’Dor 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, respec-tively (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 para larvae. 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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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, 38–59% at 10 days and 32–45% at 25 days of rearing (Villanueva et al. 2004).

The total amount of amino acids in O. vulgaris para larvae is lower than in recently settled juve-niles. These biochemical changes associated with paralarval and juvenile growth are related to mor-phometric 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 (o’Dor et al. 1984) (Figure 35).

Lipid and fatty acids

octopus para larvae have relatively low lipid content. lipid represents 11–14% of dry weight in O. vulgaris hatchlings and variation in this content throughout paralarval growth (11–25%) in rear-ing 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 para larvae represents approximately one quarter of the animal’s 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 45–3671 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):

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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 triacylglyc-erides (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 para larvae, however, have been not examined in detail. The use of reserve lipids has been recorded during fasting of hatchling O. vulgaris para-larvae 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 eicosa-pentaenoic acid (EpA) fatty acids in O. vulgaris hatchlings represent 21–27% and 13–18% 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 para larvae within a few days of hatching. it has been suggested that their presence in the diet is critical for the early development of para larvae 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 para larvae. high mortality and poor growth associated with nutritional imbalance in fatty acid profiles has been observed when

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DhA/EpA is <1.5 (Navarro & Villanueva 2000, 2003, okumura et al. 2005a). DhA plays an impor-tant 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 para larvae.

Elemental composition

The elemental composition of hatchlings, reared para larvae 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 para larvae of Octopus vulgaris are lower compared with those found in subadult and adult octopuses (seixas et al.

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Figure 37 comparison of mean and standard deviation in elemental content (µg g−1 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.)


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2005), showing their incorporation during growth. The richness of cu in O. vulgaris hatchlings is remarkable (217 µg g−1 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 haemo-cyanin, the respiratory pigment that represents 98% of cephalopod blood proteins (Ghiretti 1966, D’Aniello et al. 1986). Reared 20-day-old O. vulgaris para larvae that were fed on Artemia nauplii (a prey with relatively low cu content [9.5 µg g−1] in comparison with natural prey such as Maja brachydactyla zoeae [72.5 µg g−1]), 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 (3–4 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 para larvae seems to be inversely related to cu content as individuals with low levels of cu (fasted or reared para larvae) 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 ani-mals lacked one or both statoliths. Normal development of the aragonite statoliths and normal swim-ming behaviour were obtained when strontium levels reached 8 mg 1−1 (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 pro-cesses. 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 radio-labelled 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 12–25% and 13–17% 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


157

Table 4 size and sucker number per arm in hatchlings of octopodidae species with planktonic stages

species

Measured fresh or

preserved Ml Tl

Number of suckers per arm

Geographic area Reference

Amphioctopus aegina

Np 3.1 ± 0.1 6 indian ocean ignatius & srinivasan 2006

Amphioctopus burryi F 1.5 ± 0.05 2.5 ± 0.08 4 NW Atlantic Forsythe & hanlon 1985

Callistoctopus macropus

F 4 5.5 7 Mediterranean Boletzky et al. 2001

p 3 4.8

Enteroctopus dofelini

Np 9.3 NW pacific yamashita 1974

Np 5.3–5.5 10 (9.5–10.1) NW pacific okubo 1979

p 3.5 11–14 NE pacific Gabe 1975

Np 6–8 10–12 NE pacific snyder 1986a, snyder unpublished

Np 3.4 6.9 NE pacific hartwick 1983

Enteroctopus megalocyathus

F 8.4 ± 0.7 18.3 ± 1.7 21.2 ± 2.7 sW Atlantic ortiz et al. 2006

Eledone cirrhosa Np 4.5 8 Mediterranean Mangold et al. 1971

Hapalochlaena lunulata

Np 2.3 10 central E pacific

overath & Boletzky 1974

Macroctopus maorum

F 7.1 (6.7–7.6) 7–8 sW pacific Batham 1957

Octopus bimaculatus Np 2.6 4 4 NE pacific Ambrose 1981

Octopus cyanea p 1.1–2.0 3 hawaii islands young et al. 1989

Octopus huttoni F 3.8 ± 0.1 4 sW pacific Brough 1965 (as Robsonella australis)

Octopus joubini F 2.4–2.6 6–8 NW Atlantic Forsythe & Toll 1991

Octopus laqueus Np 1.7 ± 0.2 3.3 ± 0.3 3 NW pacific kaneko et al. 2006

Octopus mimus Np 1.9 2.0–.2.4 3 sE pacific Warnke 1999

Np 0.98 1.9 3 sE pacific Baltazar et al. 2000

Np 1.5 ± 0.1 3.1 ± 0.1 3 sE pacific castro-Fuentes et al. 2002

Octopus salutii F 3.5–4 5.5 4 Mediterranean Mangold-Wirz et al. 1976

Octopus tetricus F 2.5 3 sW pacific Dew 1959 (as O. cyanea)

Octopus cf tetricus Np 2.5 E indian Joll 1976

Octopus vulgaris F 2.1 (2–2.3) 3.2 (3–3.5) 3 NW pacific itami et al. 1963

Np 4 NW pacific hamazaki et al. 1991

F 2 2.9 3 Mediterranean Villanueva 1995

F 3.7–4 NW pacific okumura et al. 2005a,b

Scaeurgus unicirrhus

Np 4 Mediterranean Boletzky 1984

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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methods and provides a useful parameter of paralarval size and growth. Distal suckers are usu-ally smaller than the other suckers at hatching, with some exceptions, such as Amphioctopus bur-ryi, 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 pro-duced 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 tem-perature 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 para larvae proved to be highly correlated with their age in days during the first month of life (hernández-lópez et al. 2001). The internal shell remnants (‘stylets’) in the family octopodidae also have growth increments in the form of concen-tric 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 para larvae. 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 para larvae.

0 0 2 4

ML (mm)

Num

. of s

ucke

rs p

er ar

m

6 8 10

3 6 9

12 15 18 21 24

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 mea-sured fresh; white circles indicate species measured after fixation (with presumed shrinkage), as well as spe-cies for which measurement conditions (fresh or preserved individuals) were not indicated. original.


159

After hatching the main abiotic factor influencing planktonic octopus growth seems to be temperature, as has been observed in other cephalopod para larvae (Forsythe 1993). hamasaki & Morioka (2002) reared O. vulgaris hatchlings at temperatures of 17°c, 19°c, 21°c, 23°c, 25°c, 27°c and 29°c and fed with Artemia prey (1.5–2 mm in length) over the first 40 days of life. They concluded that growth rate increased with increasing rearing temperature up to 21°c, and that temperatures higher than 27°c 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 mid-summer) 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 unpub-lished manuscript). in addition to prey availability, it is reasonable to suspect that behaviour and asso-ciated 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 para larvae 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

2016 18 20 22

y = 168566x–2.6676

r = –0.9476

Temperature (°C)

Age

at se

ttlem

ent (

d)

24 26 28 30

30

40

50

60

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.


160

semigelatinous deep-sea cirrate octopods (collins & Villanueva 2006). The funnel, pallial aper-ture and interbrachial webs of octopus para larvae 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 dis-placement 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 para larvae, Tateno (1993) showed that fraction ejected during the first 2 wk of life increased with growth.

swimming in octopus para larvae differs from other planktonic and pelagic cephalopods due to the particulars of their morphology. octopus para larvae 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 para larvae 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 para larvae 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 swim-ming and manoeuvrability through independent control of both cavities. swimming behaviour in octopus para larvae 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 para larvae

hydrodynamic forces probably dictate the swimming capacities and related behaviour of different species of octopus para larvae. however, other unknown neurological and/or physiological charac-teristics may also play roles. The para larvae 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

Figure 40 schematic line drawing showing differences between the mantle cavities of octopodidae and loliginidae para larvae. 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.)


161

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 s−1 and 6 to 23 mm at respective ages of 1 and 60 days. The mean maxi-mum speed reached was 211 mm s−1 for individuals aged 30 days and 4.5 mm in Ml. These maxi-mum speed values are similar in range to those observed for hatchling squid para larvae: 160 mm s−1 in Loligo vulgaris (packard 1969), 150–250 mm s−1 in L. forbesi (Zuev 1964 in Mileikovsky 1973) and 52 mm s−1 in Illex illecebrosus (o’Dor et al. 1986).

in captive large octopus para larvae, such as those of the genus Enteroctopus, constant swim-ming 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 manu-script). 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 con-sidered to be planktonic is that of E. megalocyathus, for which hatchlings have a mean of 21 suck-ers 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 chromato-phores. 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 para larvae

Wild observations of para larvae on moonless nights over deep water (~1 km) in the coral sea found significant differences in swimming behaviour between different species of para larvae

Figure 41 The use of the dorsal and ventral mantle cavities for jet swimming in Enteroctopus dofleini hatch-lings. 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.)


162

(M.D. Norman unpublished data). Those para larvae 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 para larvae are able to delay settlement (see ‘prolonged paralarval stages’, p. 182). From hydrodynamic and energetic perspec-tives, these para larvae 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 dis-placement 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 para larvae 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 para larvae. 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

10 20 30 40 50 60 70 80 90

100

160

180

200

Tota

l len

gth

inde

x

Crui

sing

spee

d (m

m• s

–1)

220

240

0 2 2.9 4.5

ML (mm)

2 10 20 30 40 50 60 Age (days)

6.4

Crawling

Swimming

8.6

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 para-larvae. 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.)


163

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 para larvae 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 para larvae 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, particu-larly 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 div-ers returning from night dives were covered in crawling para larvae. 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 conserva-tion and as potential food-aggregating structures.

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 div-ing 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.)


164

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 neg-ative 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 1–5 m below the surface (Ambrose 1981). Rising hatchlings can be interpreted as either positive phototaxis (head-ing 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 para larvae towards the surface in the first 6–12 h after hatching. This suggests that negative geotaxis is the stronger factor in this behaviour. similar processes may occur in octopus para larvae.

Migration to surface waters could aid hatchling dispersal because surface currents may carry the para larvae 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, sur-face currents may transport hatchlings away from high-predator reef environments to the compara-tive safety of open ocean, potentially aiding in gene flow between coral reefs and atolls.

positive phototactic behaviour has been used to collect octopus para larvae at night in the field. using light traps, Moltschaniwskyj & Doherty (1995) collected 2066 individual octopus para larvae on the Great Barrier Reef, estimating this number to be around half the total number of plank-tonic cephalopods attracted to their lights. The strong response of octopus para larvae 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 para-larvae 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 para larvae 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 para larvae 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. Fernández-lópez et al. (2005) tested the influence of light intensity (1000, 3000 and 6000 lux) on the survival and growth of captive-reared O. vulgaris para larvae, 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 para larvae was negatively affected by an unstable photoenvironment in captive-bred para larvae 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


165

Tab

le 5

sa

mpl

ing

met

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, num

ber

of in

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118

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te

mpe

ratu

res

of

2.6–

6.7°

c

NW

pac

ific

yam

ashi

ta &

To

risa

wa

1983

con

ical

net

∅

130

cm

hor

izon

tal

surf

ace

Nig

ht59

4M

ean

of 6

–8 in

d by

po

sitiv

e to

ws

col

lect

ed f

rom

ea

rly

June

to

mid

-Aug

ust

Nor

th

paci

fick

ubod

era

1991

Mac

rotr

itop

us

defil

ippi

lig

htu

nder

sea

labo

rato

ry15

–40

Nig

ht16

lar

ge

indi

vidu

als,

7–

15 m

m M

l

NE

Atla

ntic

han

lon

et a

l. 19

80b,

198

5

Mac

rotr

itop

us s

p.

8 m

2 R

MT

an

d a

1-m

2 ri

ng n

et

Ver

tical

0–20

00D

ay a

nd

nigh

t16

196

% in

d co

llect

ed b

etw

een

0 an

d 10

0 m

dur

ing

dayl

ight

Rep

rese

nted

12

% o

f th

e to

tal

ceph

alop

ods

colle

cted

NE

Atla

ntic

lu

& c

lark

e 19

75 (

as

Scae

urgu

s un

icir

rhus

)

Oct

opus

cya

nea

2- a

nd 4

-m2

ring

net

so

bliq

ueFr

om 1

00

to s

urfa

ceD

ay38

882

% c

olle

cted

<50

km

of

fsho

reh

awai

ian

isla

nds

Bow

er e

t al.

1999

Oct

opus

ru

besc

ens

Net

∅ 1

00 c

mh

oriz

onta

l20

–760

Np

197

hig

her

at <

100

m; t

o 0.

9 in

d h−

1 of

tow

Foun

d at

bot

tom

de

pths

less

than

30

0 m

NE

pac

ific

Gre

en 1

973

Ro

Vin

divi

dual

s ob

serv

ed0–

400

Day

40h

ighe

r be

twee

n 30

0 an

d 40

0 m

; to

0.2

ind

h−1

obse

rved

indi

vidu

als

form

ing

shoa

lsN

E p

acifi

ch

unt 1

996

(con

tinu

ed o

n ne

xt p

age)


166

Tab

le 5

(con

tinu

ed)

sam

plin

g m

etho

ds, n

umbe

r of

indi

vidu

als

coll

ecte

d an

d ab

unda

nces

of

oct

opod

idae

par

a lar

vae

from

the

liter

atur

e

spec

ies

Gea

r

hor

izon

tal

or v

ertic

al

tow

nsD

epth

ra

nge

(m)

Day

/ni

ght

Num

ber

of

indi

vidu

als

colle

cted

Abu

ndan

ces

obs

erva

tions

Geo

grap

hic

area

Ref

eren

ce

Oct

opus

vul

gari

spl

ankt

on n

etN

p0–

100

Np

69A

bnor

mal

hig

h se

a te

mpe

ratu

res

asso

ciat

ed

with

abu

ndan

ce o

n th

e no

rthe

rn s

peci

es r

ange

Foun

d at

bot

tom

de

pths

less

than

15

5 m

NE

Atla

ntic

Ree

s 19

50

100

× 1

00 c

m

squa

re n

eth

oriz

onta

lsu

rfac

e an

d 0.

2–4

from

the

botto

m

Mos

tly

diur

nals

159

No

spec

imen

s co

llect

ed in

su

rfac

e du

ring

the

day;

hi

gher

abu

ndan

ces

insh

ore

at n

ight

and

off

shor

e du

ring

day

; fro

m 0

.03

to

0.21

g 1

000

m−

3

No

diff

eren

ces

in

size

bet

wee

n in

divi

dual

s co

llect

ed in

su

rfac

e or

bo

ttom

laye

rs

NW

pac

ific

Take

da 1

990a

Bon

go n

et ∅

60

cm

hor

izon

tal

surf

ace

Day

and

ni

ght

641

hig

her

at n

ight

; 5–8

7 in

d 10

00 m

−3

Two

hatc

hing

pe

aks:

spr

ing

and

fall,

hig

her

in f

all

NW

pac

ific

saka

guch

i et a

l. 19

99

Bon

go n

et ∅

75

cm

hor

izon

tal

Nea

r th

e bo

ttom

at

35–1

05

Np

96A

bund

ance

dep

endi

ng o

n th

e st

reng

th o

f th

e up

wel

led

wat

er; t

o 8

ind

1000

m−3

NE

Atla

ntic

Gon

zále

z et

al.

2005

Bon

go n

et ∅

75

cm

hor

izon

tal

surf

ace

and

near

th

e bo

ttom

at

36–8

5

Day

and

ni

ght

584

in s

urfa

ce d

urin

g ni

ght,

near

th

e bo

ttom

at d

ay; f

rom

0.

01 to

1 in

d 10

00 m

−3

upw

ellin

g pu

lses

po

sitiv

ely

rela

ted

with

pa

rala

rval

ab

unda

nce

NE

Atla

ntic

ote

ro 2

007

oct

opod

idae

8-m

2 R

MT

an

d B

ongo

60

-cm

∅

obl

ique

0–30

0N

p14

39A

bund

ant i

n co

asta

l bay

so

ctop

odid

ae

repr

esen

ted

60%

of

tota

l ce

phal

opod

s

sW A

tlant

icR

odho

use

et a

l. 19

92

oct

opod

idae

lig

ht tr

apD

rift

ing

and

anch

ored

lig

ht tr

aps

0–20

, few

at

100

Nig

ht,

arou

nd

new

m

oon

2066

hig

her

in s

ubsu

rfac

e of

G

reat

Bar

rier

Ree

f l

agoo

n, lo

w o

n th

e sh

elf;

0.

07–5

.57

ind

h−1

oct

opod

idae

re

pres

ente

d 53

% o

f to

tal

ceph

alop

ods

Gre

at

Bar

rier

R

eef

Mol

tsch

aniw

skyj

&

Doh

erty

19

95

Not

e:

Ml

, man

tle le

ngth

; Np,

not

pro

vide

d; R

MT,

rec

tang

ular

mid

wat

er tr

awl;

Ro

V, r

emot

ely

oper

ated

veh

icle

.


167

Table 6 Examples of large octopodidae individuals collected or observed on the water column or surface

species size

Measured fresh or

preserved Gear Depth (m)Geographic

area Reference

Amphioctopus burryi

13–15 mm Ml F light 21, under surface

NW Atlantic hanlon et al. 1980b

16 mm Ml F light surface NW Atlantic Forsythe & hanlon 1985

Callistoctopus macropus

27 mm Tl p Trawl Np NE Atlantic Rees 1955

Eledone cirrhosa

29 mm Tl p plankton net Np NE Atlantic Rees 1956

Enteroctopus dofleini

To 14 mm Ml p Net ∅ 100 cm 20–760 NE pacific Green 1973

33–73 mm Tl p larval net surface NW pacific yamashita 1974

To 14 mm Ml p conical net ∅ 130 cm

surface N pacific kubodera 1991

Euaxoctopus panamensis

11 mm Ml,~ 43 mm Tl

p ikMT 0–500 central E pacific

Nesis & Nikitina 1991

Macrotritopus defilippi

12–15 mm Ml F light 15–40, under surface

NW Atlantic hanlon et al. 1980b, 1985

1.3–11 mm Ml p Bongo net 0–200 Atlantic and indian oceans

Nesis & Nikitina 1981

Macrotritopus sp.

9–13.5 mm Ml F plankton net 100–300 Mediterranean and Atlantic

Joubin & Robson 1929 (as M. danae)

2.5–10 mm Ml F RMT & ring net

0–100 NE Atlantic lu & clarke 1975 (as Scaeurgus unicirrhus)

127 mm Tl F light 0–38, under surface

hawaiian islands

Brower 1981

Octopus rubescens

15–25 mm Ml p ikMT 0–770 NE pacific young 1972 (as Octopus sp.)

Not measured observed from RoV

60 m in an area of 728 m depth

NE pacific present study, see Figure 44

‘Octopus teuthoides’

To 16 mm Ml p light surface central E pacific

Norman & sweeney 1997

Octopus vulgaris

50 mm Tl F? light surface Mediterranean spartá 1933

octopodidae 14 mm Ml p surface hawaiian islands

Berry 1914

56 mm Tl

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.


168

(unpublished manuscript) in captive-reared Enteroctopus dofleini. light intensity was reduced dur-ing 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 para larvae although light may not be essential for capturing prey in O. vulgaris hatchlings (Márquez et al. 2007). The behaviour and activity patterns of octopus para larvae 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 para larvae are severely limited by the removal of a critical attribute of the natural environment of these animals — a realis-tic water column. Rearing tanks severely limit the capacity of the octopus para larvae 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 reclu-sive 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 pho-totactic behaviour. During the early post-settlement period, spartá (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 num-bers, as for an undescribed species of Callistoctopus in New caledonia (G. Boucher personal com-munication 1997).

Defences

Relatively high swimming speed may prevent paralarval capture by some predators. Bursts of jet swimming in O. vulgaris para larvae can reach a mean swimming speed of 41–95 mm s−1 at age of 0 and 60 days, respectively, covering a mean distance of 6–23 mm, respectively. swimming paths in hatchling O. vulgaris are highly rectilinear in comparison with older para larvae and may maxi-mize dispersion of the individuals from the egg mass and minimize attraction of predators to the hatching site (Villanueva et al. 1996). in large para larvae 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 para larvae 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 para larvae in Monterey Bay, california, in response to the approach of a deep-water remotely operated vehicle (RoV) (hunt 1996) and for unidentified octopus para larvae 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 spe-cific gravity, octopus para larvae use funnel jetting as additional propulsion to aid rapid descent.

When the proportionally large and simple chromatophores of octopus para larvae 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 irido-phores. This combination of transparency and reflective body organs is a camouflage adaptation for


169

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 para larvae 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 para larvae 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 para larvae expand their chromatophores, changing to a dark coloration (hernández-García 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 para larvae 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 trajec-tory may deceive or confuse a visual predator (Boletzky 1987). This behaviour is called a blanch-ink-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 para larvae (M.D. Norman personal observation) in response to the approach of divers.

potential schooling behaviour has been reported for the micronektonic para larvae of one spe-cies, 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 para larvae of this species at depths of 200–400 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 9°c and oxygen concentration 2.66 ml 1−1. No euphausiids were observed on the dive tape. (image and data reproduced with permission from Monterey Bay Aquarium Research institute, ©2003, MBARi.)


170

Predators on egg masses and para larvae

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 70–100% 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 (169–182 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 para larvae. longnose lancetfish (Alepisaurus ferox) actively prey on pelagic cephalopods, including octopus para larvae. stomach contents for this species examined from around the pacific ocean (Rancurel 1970) included seven individuals of Macrotritopus forms (6.5–18 mm Ml) from the south pacific (16°–23° s); three ‘Octopus teuthoides’ forms (18–25 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 8–16 mm Ml and collected mainly during March (okutani & kubota 1976). in total, octopus para larvae (octopodidae) were present in 11% (Rancurel 1970) or 12.5% (okutani & kubota 1976) of the A. ferox stomachs containing cephalopods. octopod para larvae not sorted by families occurred in 3% of the stomachs of this fish in western equato-rial 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 (21–33 mm total length) in localities near cape Finisterre and five Octopus vulgaris (6.5–18 mm total length) collected in the Gascogne Gulf during August and october (Bouxin & legendre 1936). parker et al. (2005) reported unidentified cephalopod para larvae in the diet of oceanic loggerhead sea turtles (Caretta caretta) in the central north pacific. All proved to be octopodid para larvae (D.M. parker personal communication 2006). Ephyra larval stage of jellyfish scyphomedusae has been observed feeding on unidentified octopod para larvae (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 para larvae but, as far as we know, no references on this subject have been published and information only comes from


171

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 10–15 m deep in the Medes islands, north-west Mediterranean (R. coma personal communication 2006); serranid fish (Serranus sp.) at 15 m depth on the Ría 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 para larvae. under laboratory conditions, attacks on conspecifics have been reported for O. vulgaris para larvae (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 para larvae were few and widely scattered in the literature. A number of research-ers such as Berry (1914), chun (1915), Naef (1923), Degner (1925), Robson (1929) and Rees (1954)

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.)


172

along with subsequent researchers in the 1970s and 1980s described individual para larvae 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 para larvae. Three categories of species are listed: (1) those for which planktonic para-larvae 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 para larvae 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, 1978–1979). The third category comes from dissection of preserved submature females as the only material available to provide any indication of early life-history 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’ prob-lem. 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 paralar-val 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 para larvae 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 litera-ture (see Norman & sweeney 1997, Toll & Voss 1998). The adult form, however, still awaits iden-tification. 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, para-larvae 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 para larvae 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 par-alarval 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 para larvae. in


173

combination with high-resolution and accurate photography, it will enable development of compre-hensive species identification keys for octopus para larvae. 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 para larvae 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 substra-tum areas and consequently hatchlings can be abundant near the coast. surveys targeting octopus para larvae such as Octopus vulgaris have been done in shallow bays and littoral waters (Takeda 1990a, sakaguchi et al. 1999, González et al. 2005, otero 2007). oceanic plankton sampling is usu-ally rich in oegopsid squid para larvae 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 para larvae (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 para larvae.

classic bongo nets, conical nets of different sizes, isaacs-kidd midwater trawls (ikMTs) and rectangular midwater trawls (RMTs) have been used to collect octopus para larvae (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 para larvae. The strong positive phototaxis of octopus para larvae (see ‘Responses to light and gravity’, p. 163) has been used during night surveys to attract and collect large para larvae inhabiting surface or near-surface waters (see Table 6). light traps proved to be a powerful method for collecting large numbers of octopus para larvae (Moltschaniwskyj & Doherty 1995) but little is known of their sampling efficiency, sam-pling 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’ para larvae 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 para larvae of benthic octopuses is poorly known for most species. As for many attributes of octopus para larvae, it is probably best known for Octopus vulgaris and Enteroctopus dofleini (see Table 5). Taxonomic problems for the family octopodidae are suffi-cient that accurate distributions for adult octopuses are not available for most species (Norman & hochberg 2005a), let alone for para larvae. Greater resolution may become possible when molecular tools enable accurate species identifications and hence collation of accurate geographic distribu-tional data.

The greatest geographic range for octopus para larvae 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 globe’s circumference (Norman 1991, 1993). Van heukelem (1973) reported captive Octopus cyanea para larvae that lasted in the water column for 21 days before dying. Norman (1991) suggested that the paralarval stage would


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have to be significantly longer for this species (up to months, as has been recorded for the similar O. vulgaris para larvae; 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 para larvae 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 para larvae in the north pacific at almost 57°N 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 para larvae’, 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 para larvae (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 para larvae (Demarcq & Faure 2000, Faure et al. 2000, González 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 para larvae 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 break-down of the retention areas during autumn.

These hypotheses were partially corroborated by González et al. (2005) and otero (2007), who found that high abundances of O. vulgaris para larvae were correlated with high upwelling retention indices in the north-west iberian coast, the northern limit of the canary current. however, nearly all para larvae 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 para larvae of species with large hatchlings such as Enteroctopus dofleini seem to be dis-tributed 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 para larvae have also been encountered in more distant offshore waters (200–300 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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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 para larvae, as has been observed in other shallow-water and bottom-spawning cephalopods such as loliginid para larvae (Zeidberg & hamner 2002).

Vertical distribution and abundances

Few studies have recorded vertical daily cycles of octopus para larvae, most being focused on Octopus vulgaris. in shallow coastal waters, para larvae of this species are nearly absent from the sea surface during daytime and present from the seafloor to the surface at night, with higher abun-dances 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 para larvae are practically unknown and need to be investi-gated through use of high-resolution discrete-depth sampling.

sampling between 0 and 2000 m depth in the north-east Atlantic, clarke & lu (1975) col-lected the highest number known to date of Macrotritopus para larvae (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 para larvae on moonless nights compared with moonlit nights (M.D. Norman personal observation). hunt (1996) found that Octopus rubescens para larvae were most abundant at depths of 200–400 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 para larvae 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 para larvae 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 para larvae are poorly known. only 7% of 643 Octopus vulgaris para larvae 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 para larvae and/or net avoidance by these larger para larvae 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 exam-ple, the use of sound by cephalopod para larvae 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), poten-tially influencing their settlement distribution. octopuses have well-developed mechanoreceptors


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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 para larvae in the plankton throughout the year. Maximum abundances of Octopus vulgaris para larvae are recorded during summer and autumn (Rees 1950, Rees & lumby 1954, Takeda 1990a, sakaguchi et al. 1999, González 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 para larvae 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 suc-cess 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 Ambrose’s study by heavy recruitment of settled indi-viduals in 1 yr leading to unusually high adult octopus densities in the subsequent year. Relatively large O. vulgaris para larvae (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 north-east Atlantic) resulted from the transport of the para larvae 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 para larvae and juveniles and the subsequent effects on the fished adult populations (caverivière & Demarcq 2002). in the same region, exceptional oceanographic conditions favouring paralarval and juvenile sur-vival also seem to be the origin of demographic explosions of O. vulgaris (caverivière 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 para larvae (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 predomi-nantly 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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1. species with a short presettlement period. After a short period in contact with hard surfaces and benthos, para larvae 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 para larvae 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 para larvae reach consider-able sizes, particularly those occurring in oceanic epipelagic waters. Due to their size and swimming capacities they can be considered micronektonic para larvae. These para-larvae have been described as ‘extended pelagic stages’ (Rees 1954) or ‘super-para larvae’ (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 para larvae’, p. 182). it is also possible that the swimming capacities, behav-iour, and the well-developed sensory systems of these micronektonic para larvae 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 metamorpho-sis 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 allomet-ric 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 kölliker 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 para larvae 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 para larvae and juveniles. As proposed by Wells (1990), cephalopods will try to escape using jet locomotion when-ever possible, particularly adult octopus. During jet propulsion, Wells et al. (1983b, 1987) found


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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 pres-sure. 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 insti-gate 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 para larvae 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 (11–13 mm) is not dissimilar to that of the length of Enteroctopus dofleini para larvae 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 para larvae, 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 para larvae 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 4–6). 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 com-position 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-buoy-ant 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 para larvae use their two mantle cavities (dorsal and ventral) (see examples in Figures 1B, 26, 40, 41, and 43) during the jet propulsion cycle may

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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.


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also shed light on the poorly known hydrodynamic and energetic adaptations of swimming in these long-armed para larvae.

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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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.

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Figure 48 Growth in total length from hatching to settlement during experimental rearings of Enteroctopus dofleini and Octopus vulgaris para larvae. (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.


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served during the transparent planktonic phase.” All the founder chromatophores of para larvae 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. kölliker 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 kölliker 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 leu-cophores. 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 transforma-tion 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 para larvae 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 ben-thic individuals older than 8–9 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 para larvae that are still present in the micronekton has only been observed in several live photographs of larger animals (e.g., Figure 4 bottom). The pres-ence 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 para larvae’, 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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(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 para larvae, 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 0.8–1.2 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 para larvae 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 para larvae (11 mm Ml) have been col-lected 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 prefer-ence 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 post- settlement, benthic juveniles. settled individuals also begin to direct fluxes of water from their fun-nel 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 4–10 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 para larvae 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 sedi-ments 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 octo-pus 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 para larvae

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 para larvae (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-para larvae’ to refer to these peculiar, often long-armed, para larvae. For Macrotritopus-type para larvae, Rees (1954) discussed the impact of ocean currents sweeping indi-viduals off shore over very deep water. For these para larvae, Rees (1954, p. 69), proposed that settle-ment was delayed and that they could attain “nearly twice the normal size for metamorphosis”. he coined the term ‘extended pelagic stages’ for such para larvae. in relation to Macrotritopus defilippi, Nesis & Nikitina (1981, p. 847) pointed out that: “The macrotritopuses are able to delay their set-tling to the bottom and may have a chance to cross the Atlantic”.

The prevalence of micronektonic para larvae, 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 (15–25 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. young’s 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 para-larvae close to settlement, or a transitional stage with both micronektonic and benthic behaviours.

Permanent para larvae: neoteny and holopelagic octopuses

Extended pelagic phases in oceanic para larvae may have played a role in the evolution of cer-tain 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 (0–200 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 para-larvae and ctenoglossans supported the hypothesis that the latter group evolved from para larvae 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-para larvae’ concept (discussed in ‘prolonged paralarval stages: micronektonic para larvae’, p. 182) may have been the critical stage that enabled


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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 octo-puses 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, act-ing 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 (Gutiérrez-pajares et al. 2003). subadult and adult octo-puses can be used as bioindicator species in polluted areas (Butty & holdway 1997) and are sensi-tive 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 applica-tion of chemical dispersants to oil spills (long & holdway 2002). scheel (2002) noted that densities of Enteroctopus dofleini recorded during 1995–1998, after the 1989 Exxon Valdez oil spill, were only 1–50% 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, Balguerías et al. 2000, caverivière et al. 2002, Rocha & Vega 2003). since 1950, octopus captures have been constantly increasing (Jereb & Roper 2005) and in recent years (1997–2003) world captures of octopodidae have ranged from 290,000 to 409,000 tonnes, with the single species Octopus vulgaris representing 11–18% 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 & caverivière 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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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 (pörtner et al. 2004). At this stage, the direct physiologi-cal 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 para larvae 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. tet-ricus, 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 rap-idly) 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 para larvae and their differences in lifestyle from that of their par-ents 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, settle-ment 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 para larvae, 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 sequenc-ing 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 para larvae of diverse species in detail through all growth stages. use of high-resolution photography and standardised morpho-logical 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 understand-ing 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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3. Rearing techniques. Rearing of para larvae requires innovative approaches to better simu-late natural conditions for para larvae, 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 para larvae for taxonomic and experimental studies.

4. Growth, development and nutrition. With access to healthy para larvae 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 develop-ment 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 fur-ther investigation.

5. hatching and settlement processes. All aspects of the cues, timing, duration and mechan-ics 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 para larvae applying to just two species, Octopus vul-garis 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 morphologi-cal, 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 Fortuño (institut de ciències 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 Fernández and Marta Ezpeleta, provided valuable literature related to planktonic octopuses; Nicolás ortiz (centro Nacional patagónico) provided hatchlings of Enteroctopus megalocyathus for sEM analysis and Erica Vidal (universidade Federal do paraná) provided images of Loligo opalescens para larvae 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. Villanueva’s recent research into planktonic octopus was funded by the fol-lowing research projects: Xarxa de Referència de Recerca i Desenvolupament en Aqüicultura de la Generalitat de catalunya; programa para Movilidad de investigadores, secretaría de Estado de universidades e investigación del Ministerio de Educación y ciencia; planes Nacionales de cultivos Marinos, JAcuMAR, secretaría General de pesca Marítima, Ministerio de pesca, Agricultura y Alimentación, spain; and by the concerted Action cEphsTock from the commission of the European communities. M.D. Norman’s research was funded by Australian Biological Resources study, the Australian Research council and the hermon slade Foundation.


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A B

C D

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 para larvae. (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.)

A B

C D

E F

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 anaes-thesia (2% ethanol) potentially causing chromatophore contraction in some cases. (Photos by Jean Lecomte, Observatoire Océanologique de Banyuls, CNRS. Reproduced with permission from Villanueva et al. 1995, modified.)

Colour Figure 4 (Villanueva & Norman) Micronektonic octopus para larvae. 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 7 (Villanueva & Norman) Chromatophores contracted (left) or expanded (right) on the head of para larvae. 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 para larvae. Left, unidentified paralarva showing scattered points of iridescence, potentially from Kölliker 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 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 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 cor-als, 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 9°C and oxygen concentration 2.66 ml 1−1. 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.)