BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

Transcription

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]
2Sciences, Museum Victoria, GPO Box 666, Melbourne, Vic 3001, Australia
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 planktonic stages, spawning characteristics and duration of planktonic life seem to play an important
role in their dispersal capacities. Duration of the hatching period of a single egg mass can range
from 2 days to 11 wk, while duration of the planktonic stage can range from 3 wk to half a year,
depending on the species and temperature. Thus these paralarvae possess considerable potential
for dispersal. In some species, individuals reach relatively large sizes while living as part of the
micronekton of oceanic, epipelagic waters. Such forms appear to delay settlement for an unknown
period that is suspected to be longer than for paralarvae in more coastal, neritic waters. During the
planktonic period, paralarval octopuses feed on crustaceans as their primary prey. In addition to
the protein, critical to the protein-based metabolism of octopuses (and all cephalopods), the lipid
and copper contents of the prey also appear important in maintaining normal growth. Littoral and
oceanic fishes are their main predators and defence behaviours may involve fast swimming speeds,
use of ink decoys, dive responses and camouflage. Sensory systems of planktonic stages include
photo-, mechano- and chemoreceptors controlled by a highly evolved nervous system that follows
the general pattern described for adult cephalopods. On settlement, a major metamorphosis occurs
in morphology, physiology and behaviour. Morphological changes associated with the settlement
process include positive allometric arm growth; chromatophore, iridophore and leucophore genesis;
development of skin sculptural components and a horizontal pupillary response. At the same time,
animals lose the 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 paralarvae comes from studies of just two species (Octopus vulgaris and Enteroctopus
dofleini) and knowledge of the vast majority of benthic octopus species with planktonic stages is
considered rudimentary or non-existent. Research is needed in a variety of fields, from taxonomy
to ecology. Studies of feeding and nutrition are critical in order to develop the nascent aquaculture
of key species and ageing studies are necessary to understand planktonic population dynamics,
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ROGER VILLANUEVA & MARK D. NORMAN
particularly in commercially valuable species targeted by fisheries. Current and potential anthropogenic impacts on these early life stages of octopuses, such as pollution, overfishing and global
warming, are also identified.
Introduction
Amongst the cephalopods, one of the most familiar groups is the bottom-dwelling or benthic octopuses of the family Octopodidae. This large family contains over 200 species (Norman & Hochberg
2005a), which range in size from pygmy taxa mature at <1 g (e.g., Octopus wolfi) to giant forms
exceeding 100 kg (e.g., Enteroctopus dofleini) (Norman 2000). Member species occupy all marine
habitats from tropical intertidal reefs to polar latitudes and into the deep sea to nearly 4000 m (Voss
1988). Benthic octopuses adopt two major life-history strategies (Boletzky 1977a, 1992). The first
is production of relatively few, large eggs resulting in well-developed hatchlings that resemble the
adults and rapidly adopt the benthic habit of their parents (Figure 1C,D). The second strategy is
production of numerous small eggs that hatch into distinctive free-swimming, planktonic and semitransparent hatchlings occupying ecological niches distinct from those of the adults (Figure 1A,B).
This latter category of hatchling typically has poorly developed limbs, few suckers, simple chromatophores and transparent musculature.
This marked contrast between the morphology and ecology of the planktonic stages of cephalopods and their adult form led to the coining of the term ‘cephalopod paralarva’. Young & Harman
(1988, p. 202) defined paralarva as “a cephalopod of the first post-hatching growth stage that is
pelagic in near-surface waters during the day and that has a distinctly different mode-of-life from
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 paralarvae. (Reproduced with permission from Miske &
Kirchhauser 2006.) Female Octopus berrima at the time of hatching in the laboratory with a benthic juvenile
hatchling (total length ~20 mm) in foreground (C) and within 10 min of hatching (D) showing well-developed
arms and chromatic and sculptural components of the skin. (Photos: David Paul.)
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BIOLOGY OF THE PLANKTONIC STAGES OF BENTHIC OCTOPUSES
that of older conspecific individuals”. This term alludes to the metamorphic transformations seen in
arthropods and fishes from a larval juvenile form to a morphologically distinct adult form. As the
transformation in cephalopod species with planktonic young is less dramatic, the term ‘paralarva’
was considered appropriate. Octopus paralarvae can be considered members of the meroplankton
because these young octopuses live as plankton for only a part of their life cycle. According to their
size (in total length), most planktonic octopuses can be considered mesoplankton (0.2–20 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 benthic hatchlings while eggs <10% of ML produce planktonic hatchlings. Table 1 lists those octopus
species known or likely to have planktonic paralarvae. It comprises three classes of information —
species for which planktonic paralarvae have been described; species that produce small-type eggs
(<10% of ML; sensu Boletzky, 1977a); and species for which only submature material is available
and eggs in the submature ovary are numerous and appear to be of the small-type category.
After residence in the plankton of varying duration, octopus paralarvae undergo a dramatic
morphological and ecological transition from a free-swimming pelagic animal to the predominantly benthic life of the juvenile stage. The end of the paralarval period varies, dependent on the
species and/or the environmental context. Some species such as Octopus vulgaris have a relatively
short presettlement period during which they rapidly become benthic in habit. Other paralarvae
have an expanded, transitional presettlement phase split between periods of swimming in the water
column and benthic crawling. There is a third category of a prolonged/suspended paralarval state
in which some paralarvae reach considerable sizes in epipelagic waters. At the start of this pelagic
period, these relatively large, actively swimming young octopuses (<2 cm total length) can be considered planktonic (sensu Omori & Ikeda 1984) because their power of locomotion is insufficient to
prevent them from being passively transported by currents. At the end of this phase, however, they
are clearly micronektonic (sensu Pearcy 1983, animals 2–10 cm in total length), attaining the ability
to swim freely without being overly affected by currents.
Most of our knowledge of octopus paralarvae comes from studies of just two species, O. vulgaris and Enteroctopus dofleini, potentially due to both their fisheries value and their proximity to
major centres of scientific research in the Northern Hemisphere. At this stage, knowledge of the
vast majority of benthic octopus species with planktonic stages is considered rudimentary or nonexistent. This is despite references to octopus paralarvae dating back more than 2300 yr. Probably
referring to Octopus vulgaris paralarvae of the Mediterranean Sea, Aristotle noted that “the creature is extraordinarily prolific, for the number of individuals that come from the spawn is something
incalculable” and “they are so small and helpless that the greater number perish”. Hochberg et al.
(1992) drew together published and unpublished data on identification of octopus paralarvae and
proposed both a suite of taxonomic characters and a standardized format for morphological description. This work remains the seminal study on identification of octopus paralarva over a wide range
of taxa. Boletzky (2003) reviewed recent literature on the early stages of cephalopods, particularly
issues of yolk absorption and biological adaptations throughout these early growth stages.
A note of caution must be made on species identifications for octopus paralarvae treated in the
literature. Considerable historical confusion surrounds the taxonomy of adult benthic octopuses (see
Norman & Hochberg 2005a). Similarly, the absence of detailed morphological descriptions for all
paralarval species and the lack of appropriate taxonomic tools mean that taxonomic identifications
for many studies (particularly those based on wild-caught paralarvae) must be taken as tentative.
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Table 1 Species of Octopodidae known (or likely) to possess planktonic paralarvae: maximum
values of egg length (ELmax, in mm) and egg length index (ELImax, egg length as percentage
of mantle length)
Species
ELmax
ELImax
Abdopus abaculus
Abdopus aculeatus
Abdopus tonganus
Amphioctopus aegina
2.4
3
2.8
2.4
7.9
7.2
Amphioctopus arenicola
2.7
~4
Amphioctopus burryi
Amphioctopus exannulatus
Amphioctopus kagoshimensis
Amphioctopus cf kagoshimensis
2.5
3.9
1.8
3.8
Amphioctopus marginatus
Amphioctopus mototi
Amphioctopus neglectus
3
6
Amphioctopus ovulum
Amphioctopus rex
3
3
Amphioctopus robsoni
Amphioctopus siamensis
5.2
1.7
8.8
Amphioctopus varunae
Aphrodoctopus schultzei
Callistoctopus aspilosomatis
Callistoctopus lechenaultii
Callistoctopus luteus
2
7.5
3.3
7
Small type
Small type
0.8
Callistoctopus macropus
Callistoctopus nocturnus
2.5
Callistoctopus ornatus
Cistopus indicus
3.5
4.5
2.7
3.8
Eledone cirrhosa
Enteroctopus dofleini
7.5
8
Small type
Small type
Enteroctopus magnificus
Enteroctopus megalocyathus
Euaxoctopus panamensis
Hapalochlaena lunulata
Macroctopus maorum
Macrotritopus defilippi
Octopus alecto
Octopus berenice
7
12
1.4
3.5
7
2.1
2.5
1.5
1.9
0.2
1
4
7.3
8.3
4.3
7.8
7
6.5
Small type
2.7
Reference
Norman & Finn 2001
Norman & Finn 2001
Norman & Finn 2001
Norman unpubl. data
Huffard & Hochberg
2005
Hochberg et al. 1992
Norman 1992a
Norman unpubl. data
Norman & Kubodera
2006
Norman 1992b
Norman 1992a
Nateewathana &
Norman 1999
Sasaki 1929
Nateewathana &
Norman 1999
Norman 1992a
Nateewathana &
Norman 1999
Norman 1992a
Smith 1999
Norman 1992c
Norman unpubl. data
Norman & Sweeney
1997
Mangold 1998
Norman & Sweeney
1997
Norman 1993
Norman & Sweeney
1997
Boyle 1983
Hochberg 1998
Villanueva et al. 1991
Ortiz et al. 2006
Voss 1971
Stranks 1996
Mangold 1998
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Paralarvae hatched in laboratory
Eibl-Eibesfeldt & Scheer 1962,
Ignatius & Srinivasan 2006
Forsythe & Hanlon 1985
Boletzky et al. 2001
Mangold et al. 1971
Gabe 1975, Okubo 1979, 1980,
Marliave 1981, Snyder 1986a,b,
and others
Ortiz et al. 2006
Overath & Boletzky 1974
Batham 1957
Hanlon et al. 1985
Table 1 (continued) Species of Octopodidae known (or likely) to possess planktonic paralarvae:
maximum values of egg length (ELmax, in mm) and egg length index (ELImax, egg length as
percentage of mantle length)
Species
ELmax
ELImax
Reference
Paralarvae hatched in laboratory
Norman & Sweeney
1997
O’Shea 1999
Norman 1991
Norman unpubl. data
Voss & Toll 1998
O’Shea 1999
Ambrose 1981
Octopus bimaculatus
Octopus bocki
4
2
Octopus campbelli
Octopus cyanea
Octopus favonius
Octopus filosus
Octopus hawiiensis
Octopus hummelincki
Octopus huttoni
1.7
2.5
Octopus joubini
Octopus laqueus
Octopus mimus
4.8
2.8
3
Small type
Small type
Small type
Voss & Toll 1998
Kaneko et al. 2006
Cortez et al. 1995a
Octopus parvus
Octopus rubescens
Octopus salutii
Octopus selene
Octopus tetricus
Octopus ‘tetricus’ West
Australia
Octopus veligero
Octopus vitiensis
Octopus vulgaris
1.8
4
6
1.6
2.5
2.4
Small type
Sasaki 1929
Voss 1971
Norman unpubl. data
Octopus warringa
Octopus wolfi
Pteroctopus tetracirrhus
Robsonella fontanianus
Scaeurgus jumeau
Scaeurgus nesisi
Scaeurgus patiagatus
Scaeurgus tuber
Scaeurgus unicirrhus
Thaumoctopus mimicus
3
Wunderpus photogenicus
3.6
9.5
Small type
1.7
Small type
1.8
3
3
3.1
5
3.2
Small type
2
2.7
8.3
5
2.6
1.7
2.5
2.7
2.5
Small type
Small type
9
Small type
11
3.6
6.2
Small type
10.1
Hochberg unpubl. data
Norman unpubl. data
Norman 2000
Norman unpubl. data
Boletzky 1981
Norman et al. 2005
Norman et al. 2005
Norman et al. 2005
Norman & Hochberg
2005b
Van Heukelem 1973
Brough 1965 (as Robsonella
australis)
Forsythe & Toll 1991
Kaneko et al. 2006
Zúñiga et al. 1997, Warnke 1999,
Baltazar et al. 2000, Montoya 2002
Mangold-Wirz et al. 1976
Joll 1976, 1978
Naef 1928, Vevers 1961, Itami et al.
1963 and others
Norman 2000
González et al. 2006
Boletzky 1984
Miske & Kirchhauser 2006
Note: The list includes (1) species that produce small-type eggs (ELI < 10, sensu Boletzky 1977a), (2) species for which
only submature material is available and eggs in the submature ovary are numerous and appear to be of the small-type
category and (3) species for which planktonic paralarvae have been described from laboratory hatched individuals.
For such samples that are not directly linked to spawning adult females, there is potential for misidentification or oversimplification of the diversity of taxa represented in a region. As Hochberg
et al. (1992, p. 245) state, their work: “is a preliminary study whose sole purpose is to summarize
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the current status of our knowledge. … It should not be used as an identification manual without
considerable reservation and without further critical study”.
A number of other octopod families have a completely pelagic life cycle that includes planktonic hatchlings. These include the families Amphitretidae, Vitreledonellidae, Bolitaenidae and the
superfamily Argonautoida (Alloposidae, Tremoctopodidae, Ocythoidae and Argonautidae). These
octopods are represented by approximately 21 species (Sweeney & Roper 1998) and have not been
included in the present review. Their origins and links to paralarval strategies are discussed in the
section ‘Permanent paralarvae: neoteny and holopelagic octopuses’, p. 182. The aim of the current
work is to review available knowledge on all aspects of octopus paralarvae of the benthic octopuses
(family Octopodidae) and encompasses their diversity, spawning characteristics, morphology, sensory systems, diet, biochemical composition, growth, behaviour, predators, distribution, settlement,
biogeography and evolution. This review is also presented as a vehicle for identifying gaps in our
knowledge and candidates for future research.
Spawning and hatching characteristics of benthic octopuses
with planktonic paralarvae and implications for dispersal
Egg care and duration of embryonic development
In all species of incirrate octopuses (including the benthic octopuses, family Octopodidae), the
eggs are highly vulnerable to predation (see ‘Predators on egg masses and paralarvae’, p. 170). The
eggs of these octopus groups only have the chorionic membrane protecting the ovum. They lack
the additional protective membranes, capsules or jelly masses found in other cephalopod groups
(Budelmann et al. 1997, Boletzky 1998). These additional outer layers appear to convey physical
and/or chemical protections that enable nautilus, cuttlefish, squid and cirrate octopuses to deposit
eggs that require no parental care. All female incirrate octopuses must guard their eggs throughout
the developmental period, after which the females die. The female must continuously clean the
egg surfaces with her suckers, ventilate the eggs with water flushes from the funnel and protect
the eggs from potential predators. The eggs of these octopuses possess a stalk of varying length
(the ‘chorion stalk’) that is used to attach the egg directly to a hard substratum or can be joined
together to form egg strings or festoons (i.e., Cosgrove 1993, Huffard & Hochberg 2005). The
eggs are typically attached to hard surfaces in protected shelters such as caves, crevices or mollusc
shells but in some groups can be carried directly within the webs of the female (i.e., as in some
pygmy species, Forsythe & Hanlon 1985; genus Wunderpus, Miske & Kirchhauser 2006; genus
Hapalochlaena, Norman 2000; and genus Amphioctopus, Huffard & Hochberg 2005). Females of
wholly pelagic octopus families also carry the eggs in a variety of manners: within the arm crown
(families Bolitaenidae, Vitreledonellidae, Amphitretidae, Alloposidae), within greatly elongated
distal oviducts (family Ocythoidae), attached to small mineralized rods (family Tremoctopodidae)
or within an encased shell-like capsule (family Argonautidae) (Young 1972, Nesis 1987).
Eggs laid by octopuses with planktonic hatchlings typically number in the thousands but can
reach as high as 500,000 in Octopus vulgaris (Mangold 1983) and 700,000 eggs in O. cyanea
(Van Heukelem 1983). However, lower numbers of eggs can also be produced by certain species
with planktonic hatchlings (i.e., 450 for Wunderpus photogenicus; Miske & Kirchhauser 2006).
Body size constraints for pygmy octopus species that produce planktonic young also make it likely
that egg production for such species would be in the hundreds not thousands of eggs. Within each
species-specific range, temperature is the main factor regulating the development of the octopod
embryos, which is faster at higher temperatures. For small-egg species of the family Octopodidae,
the fastest embryo development is found in tropical species. Examples of rapid development are
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 physiological mechanism(s) that promote the hatching process are unknown. A natural tranquillizer
described in the perivitelline fluid of loliginid squid prevents premature hatching (Marthy et al.
1976); however, its presence in octopus eggs has not been assessed. Mechanical stimulation provided by the brooding female may aid or regulate the timing of hatching but no quantitative studies
have been done on this subject. During hatching, brooding females sometimes forcibly expel water
through the funnel over the eggs (Sarvesan 1969, Kaneko et al. 2006). This turbulence may act as a
stimulus to instigate hatching. During laboratory incubation of eggs without female care, hatching
predominantly occurred after agitation as has been observed for Octopus cf tetricus (Joll 1978 as
O. tetricus) and Enteroctopus dofleini (Snyder 1986a).
Mechanics of hatching
Laboratory observations on Octopus bimaculatus showed prehatching individuals pumping energetically in their egg cases prior to hatching (Ambrose 1981). To escape the chorion membrane, rapid
mantle contractions by the embryo may mechanically put pressure on the chorion membrane or it
may ensure that the hatching gland is pressed firmly against the inner wall of the chorion to ensure
direct application of the enzymatic solution released from this gland (see description p. 118). Active
use of the arms and suckers has also been observed in some species such as Scaeurgus unicirrhus
(Boletzky 1984). After the enzymatic secretions of the hatching gland dissolve and hence perforate
the chorion membrane, the Kölliker organs also probably help to prevent the retraction of the emerging octopus back into the egg capsule during hatching (Naef 1923, Boletzky 1966) (see ‘Surface epithelia and integumentary structures’, p. 116). The hatching period can take up to 44 min to complete
under laboratory conditions in Octopus tetricus (Le Souef & Allan 1937 as O. cyanea). A schematic
drawing of the hatching process is given in Figure 2.
Timing of hatching
In situ observations found that hatching occurred at night or in darkened conditions in egg masses of
Enteroctopus dofleini at 17–24 m depth (Cosgrove 1993), whereas daytime hatching was observed
for paralarvae of Octopus bimaculatus, swimming upwards and reaching depths of 1–5 m below the
surface (Ambrose 1981). Under laboratory conditions, paralarvae of O. cyanea hatch only at night
(Van Heukelem 1973) and both day and night hatching has been observed in O. cf tetricus (Joll
1978). In addition to embryonic rhythms, species-specific differences in the timing of hatching may
be influenced by adult rhythms. Mechanical stimulation provided by the brooding female on the egg
mass may differ between nocturnal and diurnal species, making maternal activity an unquantified
factor in the hatching process. Under laboratory conditions, non-brooding adult O. vulgaris prefer
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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.)
nocturnal activity patterns (Brown et al. 2006) and for this species most hatching events occur at
night (R. Villanueva personal observation).
Paralarval hatching in cephalopod species without maternal care, as in the squid Loligo vulgaris,
is influenced by the transition from light to dark, which seems to function as a ‘zeitgeber’ or synchronizer, stimulating hatching (Paulij et al. 1990). The attraction of visual fish predators to the brooding
octopus site may prevent major hatching during daytime, selecting for night hatching to avoid predation (Van Heukelem 1973), as has been observed in other invertebrate larvae such as the hatching of
decapod crustacean zoeae (Forward 1987, Ziegler & Forward 2005, 2006). The tendency for sunset
and nocturnal hatching in octopus paralarvae needs to be confirmed and quantified, with the influence of tidal and lunar rhythms taken into account. Similarly, the roles of external synchronizers and
circadian rhythms in adult octopuses are poorly known (Houck 1982, Wells et al. 1983a, Cobb et al.
1995a,b, Brown et al. 2006, Meisel et al. 2006) but future research on this field may shed light on the
potential links between female brooding behaviour and the timing of hatching.
Hatching duration within an egg mass
The hatching period from a single egg mass can be rapid (i.e., hours), continue over a few days or
for weeks, influenced by factors such as the duration over which the eggs were laid, the incubation
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temperature and the species. Egg laying under aquarium conditions in temperate and tropical species 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 egglaying periods a single octopus egg mass can contain eggs in different developmental stages.
The duration of the hatching period of a single egg mass observed under laboratory conditions
ranges from 2 days at 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-lightlevel videography may be a promising avenue for investigating natural hatching processes.
Morphological characteristics of planktonic octopus paralarvae
At hatching, the external attributes of octopus paralarvae are distinctive and often markedly different from that of post-settlement juveniles and the first growth stages of species with benthic
hatchlings. All inner organs of planktonic octopus paralarvae are well differentiated at hatching
except for the reproductive system. However, there are few data on the development of the digestive, circulatory, respiratory, excretory and muscular systems after hatching and prior to settlement.
Most information comes from embryological studies on prehatching and hatchling individuals and
has been reviewed by Boletzky (1989). The surface epithelia, integumentary structures, nervous and
sensory systems of the paralarvae also have been the object of research and the present knowledge is
reviewed. The order of morphological and anatomical characters in this section follows Budelmann
et al. (1997).
Body form and musculature
One of the most evident attributes of octopus paralarvae is their largely transparent form. All musculature is transparent including those of the mantle, head, arms, webs and suckers. This transparency is not visible in preserved material as the musculature becomes opaque on fixation. This
transparency matches the planktonic lifestyle of the paralarvae, minimizing their silhouette, and
hence visibility, to predators (and prey) below. No studies have examined the microscopic structure
of the transparent musculature of octopus paralarvae. The mantle musculature of some holopelagic
octopods contains thin outer layers of longitudinal and circular muscle enclosing a thick layer of
transparent gelatinous matrix supported by narrow strands of radial muscle (e.g., Amphitretus,
113
Table 2 Duration of hatching period from a single egg mass in Octopodidae species with
planktonic hatchlings
Temperature
(°C) during
hatching
Laboratory
or field
observation
3
Np
Laboratory
3
28–30
Laboratory
10
39
Laboratory
Laboratory
49
23–24
12.5–15.3,
mean 13.9
4–7
78
10–12.8
Laboratory
30
27
45
14
Np
9–13
Laboratory
Laboratory
Laboratory
Macroctopus maorum
Octopus laqueus
<7
10
2–9
Np
Np
26
Field
Laboratory
Laboratory
Octopus mimus
14
16, 20 and
24
Laboratory
Octopus cf tetricus
28
6
10
8–15
19
21
22.6
20
Laboratory
Octopus huttoni
6–12
3–8
5
21
22–23
21–27
17–19
Np
Laboratory
Laboratory
Field
Laboratory
3
26
Laboratory
Species
Amphioctopus aegina
Amphioctopus burryi
Octopus vulgaris
Hatching
duration
(days)
Comments
Eggs incubated
without female
Laboratory
Laboratory
Eggs incubated
without female
Eggs incubated
without female
75% hatched in 1 h
of the same day
No differences
between
temperatures
Reference
Sarvesan 1969 (as
Octopus dollfusi)
Ignatius & Srinivasan
2006
Forsythe & Hanlon 1985
Okubo 1973
Ruggieri & Rosenberg
1974
Gabe 1975
Okubo 1979
Okubo 1980
Snyder 1986a,
unpublished
Cosgrove 1993
Batham 1957
Kaneko et al. 2006
Warnke 1999
Joll 1976
Eggs incubated with
and without female
Joll 1978
Vevers 1961
Caverivière et al. 1999
Caverivière et al. 1999
Brough 1965 (as
Robsonella australis)
Miske & Kirchhauser
2006
Note: Np, not provided.
Haliphron, Mangold et al. 1989). A similar arrangement is likely to be present in octopus paralarvae
but as yet the histological structure of the musculature of these animals has not been examined.
General body proportions of octopus paralarvae vary throughout paralarval growth (Figure 3)
and between species. At hatching, planktonic octopuses are squat with arms shorter than ML. See
hatchlings in Figures 1B, 3A, 17A,D, 26, 27 and 41. A smaller proportion of species have paralarvae
with arms longer than ML, particularly micronektonic paralarval stages (Figure 4). The relative
length of different arm pairs also varies between some species and can be diagnostic at a generic level
(Hochberg et al. 1992). For example, some paralarvae have arms of equivalent length (Figure 3, 6A),
114
A
B
C
D
E
F
Figure 3 (See also Colour Figure 3 in the insert.) Individuals of Octopus vulgaris from hatching to settlement obtained from rearing experiments described in Villanueva (1995). Images not to scale. Age (days) and
mantle length (ML) of the individuals measured fresh are (A) 0 days, 2.0 mm ML; (B) 20 days, 3.0 mm ML;
(C) 30 days, 4.3 mm ML; (D) 42 days, 5.9 ML; (E) 50 days, 6.6 mm ML; (F) 60 days, 8.5 mm ML. Octopuses
from this experiment settled between 47 and 54 days. Individuals were photographed under anaesthesia (2%
ethanol) potentially causing chromatophore contraction in some cases. (Photos by Jean Lecomte, Observatoire
Océanologique de Banyuls, CNRS. Reproduced with permission from Villanueva et al. 1995, modified.)
those of the genus Callistoctopus possess longer dorsal arm pairs (Figure 4A,B), the second pair is
the longest in Euaxoctopus (Figure 5), whereas Macrotritopus defilippi paralarvae possess a longer
third arm pair (Figure 6, right), as do certain unidentified paralarvae (Figure 4B,C).
Sucker number, arrangement and relative size can also be used to separate species (Hochberg
et al. 1992). At hatching there are typically few suckers (three or four) present in a single straight
row. During growth suckers are added, with the double row gradually becoming apparent for genera such as Octopus, Enteroctopus and Callistoctopus. Genera such as Eledone retain the single
row of suckers into adulthood. The body form and transparency of octopus paralarvae show strong
parallels with a number of holopelagic octopuses (families Bolitaenidae, Vitreledonellidae and
Amphitretidae) and squids (family Cranchiidae) (see ‘Permanent paralarvae: neoteny and holopelagic octopuses’, p. 182).
115
Figure 4 (See also Colour Figure 4 in the insert.) Micronektonic octopus paralarvae. Top, unidentified
paralarva of the genus Callistoctopus from the Coral Sea, Australia, showing longer dorsal arm pair. (Photos:
David Paul.) Centre, unidentified paralarva (Macrotritopus sp.?) from Hawaii showing long arms relative to
body length, particularly the third pair. (Photos: Chris Newbert.) Bottom, unidentified paralarva from Hawaii.
(Photos: Jeffrey Rotman.)
Surface epithelia and integumentary structures
Chromatic elements
As with many other cephalopods, octopuses possess three major chromatic elements within the
skin — chromatophores, iridophores and leucophores — that produce the different chromatic patterns that play such important roles in octopus behaviour (Packard & Hochberg 1977, Hanlon &
Messenger 1996, Messenger 2001). Chromatophores are the primary chromatic element present in
the skin of octopus paralarvae. These organs are flexible pigment pouches surrounded by radiating
musculature. In the relaxed state, the elastic pigment sacs are tiny and effectively invisible within
the transparent musculature (Figure 7, left). Contraction of the radial muscles surrounding the pigment sac causes it to expand significantly, resulting in display of a relatively large visible disc of
colour (Figure 7, right). In adult cephalopods, chromatophores of up to five colours are present in
the skin at densities of up to 200 mm−2 (Packard & Sanders 1969), enabling presentation of complex
116
chromatic displays (Hanlon & Messenger 1996).
In octopus paralarvae, chromatophore numbers
are typically low and they are relatively large in
proportion to body size. Chromatophores of just
one or two colours (red and black) are typically
present, enabling expression of relatively simple
colour patterns, that is, uniform colour versus
transparency (contracted chromatophores).
At hatching, octopus paralarvae possess
a low number of large chromatophores, present in fixed arrangements. They are known as
‘founder chromatophores’ and their mode of
growth and development is described in Packard
(1985). Patterns and positions of these founder
chromatophores can have taxonomic value and
Figure 5 Euaxoctopus panamensis, 11-mm mantle enable species identification (Hochberg et al.
length (ML). Note the large second arm pair, measur- 1992). The number and distribution of chroing 32 mm long. Collected using Isaacs-Kidd midwater matophores on the skin over the arms, funnel,
trawls (IKMT) between 0 and 500 m depth, 09°N 90°W, eyes, head, mantle and perivisceral epithelium
off Costa Rica, eastern Pacific. (Reproduced with per- (i.e., chromatophore fields) of octopus para
mission from Nesis & Nikitina 1991, modified.)
larvae can be used to separate species (Young
et al. 1989, Hochberg et al. 1992) (Figure 8).
Founder chromatophores remain relatively unchanged throughout ontogenetic growth and are still
visible subdermally in post-settlement animals in the same patterns of dark and dense chromatophores. These chromatophores are particularly evident in adults of pygmy octopus species and can be
diagnostic to species level (i.e., Octopus bocki and O. wolfi) (Norman & Sweeney 1997). Reflective
tissues (iridophores) are not typically evident in the skin of octopus paralarvae, particularly in the
earliest stages. They are present, however, in the membranes enclosing the eyes and viscera, providing a reflective surface to these opaque body organs as an additional ambient light reflector appropriate for a pelagic environment (Figure 4 bottom). Small spots of dermal iridescence are evident
in some paralarvae, potentially produced from the bristles of the Kölliker organs (described in the
section ‘Kölliker organs’, p. 120) (e.g., unknown species; Figure 9). In some late-stage paralarvae,
potentially close to settlement, iridescence is visible in the position of the ocellus that is found in
ocellate species (e.g., unidentified Amphioctopus sp.; Figure 9). Leucophores are white-reflecting
components of cephalopod skin. They are not typically evident in the skin of octopus paralarvae.
Figure 6 (See also Colour Figure 6 in the insert.) Unidentified paralarva from the Coral Sea, Australia,
showing arms of equivalent length (left). (Photo: David Paul.) Paralarva of Macrotritopus defilippi from
Caribbean Sea showing longer third arm pair (right). (Photo: Raymond Hixon.)
117
Figure 7 (See also Colour Figure 7 in the insert.) Chromatophores contracted (left) or expanded (right) on
the head of paralarvae. The left image corresponds to an unidentified paralarva of unknown genus and the
right image is from an unidentified paralarva of the genus Callistoctopus. Both individuals from Coral Sea,
Australia. (Photos: David Paul.)
A
AB
DE
DH
F
ADM
VH
AVM
V
DM
VM
A
PC
B
C
Figure 8 Distribution of chromatophore fields in Octopodidae. (A) Left lateral view, optical section; (B) dorsal view; (C) ventral view. Superficial or tegumental chromatophores are represented by stippled spots. A, arm;
AB*, arm base; ADM, anterior margin of dorsal mantle; AVM, anterior margin of ventral mantle; DE*, dorsal
eye; DH*, dorsal head; DM, dorsal mantle; F, funnel; PC, posterior cap; V*, visceral; VH*, ventral head; VM,
ventral mantle. Extrategumental chromatophores are indicated by (*). (Reproduced with permission from
Hochberg et al. 1992.)
As with iridophores, these structures may be evident in paralarvae close to settlement. The simple
chromatic capacities of planktonic octopus paralarvae show a stark contrast with the complex skin
and capacities of the benthic hatchlings of octopus species with large eggs (e.g., Hapalochlaena
maculosa, Figure 10).
Hatching gland
The hatching gland or 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.
118
Figure 9 (See also Colour Figure 9 in the insert.) Iridescence in octopus paralarvae. 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.)
Figure 10 (See also Colour Figure 10 in the insert.) Hapalochlaena maculosa hatchling, a direct benthic
species, showing well-developed skin colour and sculpture. (Photo: David Paul.)
In embryos that do not execute the second reversion (Boletzky & Fioroni 1990), the hatching gland
also helps the animal to hatch via the opposite pole, adjacent to the egg stalk (Boletzky 1966). In
incirrate octopods, the glandular cells of the hatching gland are limited to a narrow transverse band
(Orelli 1959, Fioroni 1978, Boletzky 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
119
studies on the duration of the hatching process. In Octopus tetricus individuals can take up to
44 min to hatch under laboratory conditions (Le Souef & Allan 1937, as O. cyanea). The hatching
gland is a transitory organ. Soon after hatching the gland is shed along with the rest of the embryonic epidermis and its many ciliated cells (Budelmann et al. 1997).
Kölliker organs
Kölliker organs are bristle-like structures present on the surface of the head, arms, funnel and
mantle of embryos, paralarvae and recently settled octopus individuals, giving the animals a punctate appearance (Figures 11 and 12). These organs are only found in incirrate octopods, including
individuals of some octopus species with direct benthic hatchlings such as Eledone moschata (Naef
1923, Boletzky 1973). First described by 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 different hatchling size, representing 4% of the ML in Argonauta argo and 0.4% in Eledone moschata.
Their density in planktonic paralarvae is, however, higher than in benthic juveniles (Boletzky 1973).
In paralarvae of some species, high densities of 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 hatchling 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); however this use seems doubtful in large planktonic animals due to the small size of the organs relative
to body size. Alternatively, due to the shining appearance of the everted fascicles in live individuals
observed under a binocular microscope (R. Villanueva personal observation), it is possible that light
reflection could produce defensive counter-shading or crypsis in the water column. 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 juvenile 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 paralarvae: neoteny and
holopelagic octopuses’, p. 182).
Integumental pores and glandular cells
Pores of different diameter have been observed on the epidermis of the arms, head, funnel and
mantle of hatchling paralarvae and these appear related to glandular cells (Young et al. 1989, Lenz
et al. 1995). In laboratory-hatched individuals of Octopus cyanea, densities of these pores (5 µm
120
A
B
C
D
E
F
G
H
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 individual, 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.
121
A
C
B
D
E
Figure 12 Kölliker organs in Enteroctopus megalocyathus hatchling paralarvae. Individuals collected during rearing experiments described in Ortiz et al. (2006). Scanning electron microscope images from ventral
(A) and lateral (B) views. Note the density of 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 rectangle. (E) Kölliker organs from ventral mantle in different degrees of expansion. (Specimens kindly provided
by N. Ortiz, Centro Nacional Patagónico, CONICET.) Original.
in diameter) represented 10% of the skin surface for some areas but these high densities were not
observed in field-collected specimens (Young et al. 1989). The pores have small spheres in the apertures that may be the secretory products of these potential mucus-secreting cells (Figure 14).
Sucker surfaces
In hatchling octopus paralarvae the main features of the outer surface of the suckers resemble
that of the adults (Nixon & Dilly 1977, Kier & Smith 1990). The infundibulum of the suckers has
numerous flattened pegs that are already endowed with minute pores (Figure 15) (Schmidtberg
1997, 1999). Pegs may provide friction to aid the suckers in attaining suction adhesion. However, as
observed in hatchlings of Octopus vulgaris (Schmidtberg 1999) and O. cyanea (Young et al. 1989),
the infundibulum is encircled by a plain rim and lacks the circumferential marginal folds that surround the infundibulum in suckers of adult individuals or hatchlings of direct benthic species such
as Eledone moschata (Schmidtberg 1997, 1999). These circumferential marginal folds may aid
formation of a tight seal (Nixon & Dilly 1977, Kier & Smith 2002), suggesting that the suction process in hatchling octopus paralarvae is not as effective as in adults or hatchlings of directly benthic
species (Schmidtberg 1997, 1999).
Sculptural components
Adult benthic octopuses are renowned for their camouflage and background-matching abilities.
Beyond chromatic components, this disguise is aided by sculptural components: papillae (branched
122
R
E
C
A
E
L
M
B
C
Figure 13 Kölliker organ from the skin of Octopus sp. hatchling paralarvae. (A) Scanning electron microscope image of a radiated fascicle showing the rodlets and three new fascicles (white arrows) beginning to
emerge. Scale 30 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 follicular cell; M, obliquely striated muscle; R, rodlet. (Reproduced with permission from Brocco et al. 1974.)
Figure 14 Integumetal pores and glandular cells. Scanning electron microscope images of Octopus cyanea
hatchlings showing (left) the pores on the arm tips (scale 0.1 mm) and (right) the oral surface of the arm showing the pores and the secretory spherules (scale 0.01 mm). (Reproduced with permission from Young et al.
1989.)
or unbranched), skin flaps and raised ridges (i.e., lateral mantle ridge) (Figure 16). In stark contrast
to benthonic hatchlings (Figures 1D and 10) and adults, octopus paralarvae lack any evidence of
these components, even in the largest forms (Figure 4).
Loose skin film
In some species, an unpigmented, transparent, loose skin layer has been observed to cover the body
of the whole animal (Figure 17). Hatchlings of Enteroctopus megalocyathus observed under a binocular microscope show a transparent skin film densely surrounded by Kölliker organs and covering the mantle, funnel, head, arms and eyes (Ortiz et al. 2006) (Figure 17D). Observations using
scanning electron microscopy (SEM) do not reveal this layer, instead showing the direct surface of
the skin (Figures 12 and 23). This may be an artefact of the fixative process required for electron
123
C
A
P
R
P
20 µm
B
R
i
100 µm
C
5 µm
Figure 15 Sucker structure of Octopus vulgaris hatchling paralarvae. (A) Sagittal section of the sucker,
stained with haematoxylin and eosin. Scanning electron microscope images showing the whole suckers (B)
and infundibulum (C). C, cuticle; i, infundibulum; P, peg or projection of cuticular process of infundibulum; R,
rim. (Reproduced with permission: (A) from Nixon & Mangold 1996, (B) and (C) from Schmidtberg 1997.)
Figure 16 (See also Colour Figure 16 in the insert.) Adult Octopus cyanea in camouflage display amongst
soft corals, Puerto Galera, Philippine Islands. (Photo: Gunther Deichmann.)
microscopy. The presence of a similar loose skin structure has also been reported for laboratoryhatched E. dofleini by Green (1973, p. 39), noting that “The lateral sides of each arm were outlined
with a transparent web”. Kubodera & Okutani (1981, p. 149) noted that wild paralarvae of the same
species had a “body all covered with gelatinous tissue which is more prominent in smaller specimens”. Kubodera (1991) also showed that this loose skin layer is not only related to the hatchling
stage but also present during paralarval growth (Figure 17B). In addition to the genus Enteroctopus,
124
A
B
C
D
Figure 17 Skin film in Enteroctopus. (A) Dorsal views of E. dofleini hatchling (scale 1 mm) and (B) a 14 mm
mantle length individual (scale 5 mm). (C) Lateral view, scale 1 mm. (D) Ventral view of newly hatched E.
megalocyathus after preservation in formaldehyde showing the skin film covering the whole animal (scale
2 mm). (Reproduced with permission: (A) from Green 1973, (B) from Kubodera & Okutani 1981, (C) from
Kubodera 1991, (D) from Ortiz et al. 2006.)
the loose skin film also seems to be present in Octopus bimaculatus from the eastern north Pacific
(from drawings of Hochberg et al. 1992; their Figure 257) and in the Macrotritopus defilippi species
complex from Hawaiian waters (Hochberg et al. 1992; their Figures 260 and 261). Diekmann et al.
(2002) drew this structure for Argonauta argo and for an undetermined species of Octopus sp. collected in the subtropical eastern north Atlantic.
A parallel supradermal skin layer is also found in three families of oceanic squids: 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 paralarvae may also play a role in anchoring the loose skin film to
the body surfaces. The microscopic structure of this loose skin film in octopus paralarvae and its
relationship to the integument needs to be examined in detail and its characteristics described in
live animals. Live animals should be observed and killed under controlled conditions to avoid possible premortem stress and/or fixative artefacts that may influence the general skin attributes in the
preserved animal.
125
Sensory systems
Central nervous system
The nervous system of paralarvae matches the general pattern described for adults (Young 1971,
Wells 1978) but it is comparatively larger by volume. The brain, penetrated by the oesophagus,
consists of two large components, the supra- and the suboesophageal masses, each subdivided into
brain lobes (Figure 18). The brain of Octopus vulgaris hatchlings has been estimated to weigh
0.2 mg (20% of the total body weight of the animal); addition of the eight brachial ganglia and
eyes results in the nervous system representing approximately one quarter of the paralarval fresh
weight (Packard & Albergoni 1970). The relative proportions of the lobes of the paralarval brain
are markedly different from those of juveniles or adults. In O. vulgaris and Eledone cirrhosa these
differences have been related to morphological development and changes in mode of life (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, coinciding 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
paralarvae show adult-like characteristics, with the exception of the ‘lateral line system’, the presence of which has not been reported for adult octopods. The main sensory system components are
treated individually below.
Photoreceptors
Eye photoreceptors The eyes of octopodid paralarvae are located laterally and directed slightly
forward. During the planktonic stage there is a relatively slight increase in eye diameter relative to
the head and mantle in reared Octopus vulgaris (Villanueva 1995). Adult octopuses are blind to
colour (Messenger 1977) and sensitive to polarized light (Moody & Parriss 1961, Shashar & Cronin
1996). These attributes can probably be extended to paralarvae but no experimentation has been
done in this respect. Eye receptors of young octopus have been described for species with benthic
hatchlings, including O. australis and O. pallidus (Wentworth & Muntz 1992), showing that by the
time of hatching all relevant components of the visual system are recognizable in their essentially
adult form (see reviews by Budelmann et al. 1997, Nixon & Young 2003). However, further differentiation and growth takes place. There is little information on the vision of planktonic octopuses. Unpublished observations (A. Bozzano, Institut de Ciències del Mar) showed that the eyes of
SM
DG
S
ST
200 µm
F
Figure 18 Sagittal section of hatchling Octopus vulgaris. DG, digestive gland; F, funnel; S, sucker; SM,
supraoesophageal mass; ST, statocyst. (Reproduced with permission from Nixon & Mangold 1996, modified.)
126
l
LB
L
20 µm
P
SN
PN
PL
BM
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.
Octopus vulgaris are also completely formed at hatching and the retina already shows all the adult
differentiated retinal layers (Figure 19). In the hatchling eye, it is possible to distinguish the iris and
the lentigenic body as well as the fully developed lens. The photosensitive retina consists only of
rod-like photoreceptors and supporting cells. A basement membrane separates the supporting cell
nuclei from the photoreceptor nuclei. The plexiform layer, posterior to the photoreceptor nuclei, contains the synaptic processes of the photoreceptors and the efferent fibres from the brain lobes. These
structures contribute to the formation of the optic nerve collecting fibres at the back of the eye.
Photosensitive vesicles In addition to the normal retinal photoreceptors of the eyes, most cephalopods have small groups of photoreceptors located external to the eyes; these have been termed
the extraocular photoreceptors or photosensitive vesicles (Mauro 1977). In adult stages of benthic
and pelagic octopods the photosensitive vesicles consist of a single pair of organs located inside
the mantle cavity (Nishioka et al. 1962, Young 1978). Each organ is a spherical vesicle attached to
the posterior margin of each stellate ganglion, recognizable as an orange spot in Eledone cirrhosa
(Cobb et al. 1995a,b) and colourless in Octopus vulgaris (Mauro 1977). The presence of photosensitive vesicles has been recorded in developed embryos of O. vulgaris (Marquis 1989) but their development throughout planktonic life is unknown. The function of these vesicles remains enigmatic
in benthic octopods although it seems to be related to regulation of circadian activity (Cobb et al.
1995a,b, Cobb & Williamson 1998, 1999).
Mechanoreceptors
Statocysts and statoliths The two sphere-like, membranous statocysts are situated in cavities of
the cranial cartilage. They consist of fluid-filled spaces each containing a mineralized statolith
borne on receptor hairs. Their mechanoreceptors respond to mechanical stress caused by a relative
movement between receptor hair cells, the statoliths and the surrounding medium (Budelmann et al.
1997). The octopod statocyst has been the subject of detailed research in adult individuals (Young
1960, Budelmann et al. 1973, Budelmann 1977, Budelmann & Young 1984, Budelmann et al. 1987).
Statocysts in O. vulgaris hatchlings are relatively large and their anterior-posterior length represents
32% of ML in fixed specimens, then decreasing to 11% of ML after settlement (Nixon & Mangold
1996) (Figure 18). Octopus vulgaris hatchling statocysts were analysed histologically by Büllow &
127
Figure 20 Statoliths of Octopus vulgaris paralarvae. Scanning electron microscopic images from anterolateral (A) and posterior (C) views of hatchling statoliths with their respective crystalline surface structure
presented inside the rectangles (B, D). In paralarvae aged 30 days, statolith growth is observed on the posterior side of the statolith (E, F). The crystalline structure of the surface observed inside the lower (G) and
upper (H) rectangle of the image F is also indicated. Individuals obtained from rearing experiments described
in Villanueva et al. (2004). Original.
Fioroni (1989) indicating that, in comparison with the adult statocysts, the cartilaginous capsules
lack the detached epithelium that probably lies within the cartilaginous layer. The crista statica is
divided into three parts and the anticristae are absent. Colmers et al. (1984) describe neuroepithelial
structures of the statocyst and statoliths of species with benthic hatchlings in O. maya and O. sp.
(reported as O. joubini). The statoliths of O. vulgaris hatchlings (Figure 20A–D) have a hemispherical shape that corresponds to the knob present on the peak of the limpet-shaped statoliths of adult
individuals of Octopodidae, as observed in O. vulgaris (Young 1960, Sakaguchi 2006), Eledone
cirrhosa (Clarke 1978), Enteroctopus magnificus (Villanueva et al. 1991) and E. dofleini (Ikeda
et al. 1999). The hatchling or natal statolith can be recognized externally on the adult statolith as
its size is nearly constant and is independent of the sizes of the adult body or statolith (Sakaguchi
2006). After hatching, statolith growth takes place on the posterior side of the statolith, as observed
in laboratory-reared O. vulgaris paralarvae aged 1 month (Figure 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 funnel in O. vulgaris hatchlings (Lenz et al. 1995, Lenz 1997). The epidermal line runs in an anterioposterior direction. The dorsal, dorsolateral, ventrolateral and ventral lines are paired, occurring on
128
A
DLL
VL
VLL
VL
DL
DLL
VLL
FL
FL
DL
B
DA
DL
DLL
DLA
VLA
VLL
200 µm
C
10 µm
Figure 21 Epidermal lines in Octopus vulgaris hatchling paralarvae. (A) schematic drawings showing the
course of the epidermal lines (indicated by dotted lines) from dorsal (left), ventrolateral (central) and ventral
(right) views. DL, dorsal line; DLL, dorsolateral line; FL, funnel line; VL, ventral line; VLL, ventrolateral
line. (B) Scanning electron microscope (SEM) image from the lateral view of the head showing the dorsal,
dorsolateral and ventral lines. DA, dorsal arm; DLA, dorsolateral arm; VLA, ventrolateral arm. (C) SEM
image of the funnel line showing the ciliated cells of the funnel line (black arrow) and the ciliated cells
in the immediate neighbourhood of the line (white arrow). (Reproduced with permission from Lenz 1997,
modified.)
both sides of the head and on the left and right arms but there is only one line along the midline of
the funnel (Figure 21A,B). The ciliated cells of these lines have an elongated apical surface bearing up to six long (10-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 paralarvae have not been reported in adult octopuses but they
129
are homologous to those described in adults of sepioid and teuthoid cephalopods. The cells of the
epidermal lines are able to perceive hydrodynamic pressure and neurophysiological experiments in
adult decapod cephalopods showed that epidermal lines can be considered as an organ analogous
to the lateral line system found in fishes (Budelmann & Bleckmann 1988, Bleckmann et al. 1991,
Budelmann et al. 1997).
Single ciliated cells and group-arranged ciliated cells In addition to the ciliated cells of the epidermal lines, hatchling O. vulgaris have ciliated cells on the epidermis that are randomly scattered
over the body surface of arms, suckers, head, funnel and mantle or are in special arrangements
on the funnel, external yolk sac and the olfactory organ (Lenz et al. 1995, Lenz 1997, Wildenburg
1997, see ‘Chemoreceptors’ below). During the embryonic stage, the cilia help during rotation of
the embryo (Boletzky & Fioroni 1990), presumably keeping the chorionic fluid in motion and preventing the embryo from sticking to the chorion after rotation has occurred. After hatching their
function is unknown. Body surfaces that lack cilia are the growing tips of the arms, cornea, margin
of the eyes, funnel aperture and the inner side of the mantle.
Sucker mechanoreceptors A variety of presumed mechanoreceptors has been described on the
suckers of adult octopuses (Graziadei 1964, Graziadei & Gagne 1976a,b) and their presence in the
paralarval suckers can be expected. However, Schmidtberg (1999), after studying the hatchling suckers of O. vulgaris, concluded that the ciliated cells present on the suckers are chemosensory receptors rather than mechanoreceptors. The development of sucker mechanoreceptors during paralarval
and juvenile growth and its relation to a planktonic or benthic mode of life need to be examined.
Chemoreceptors
Olfactory organ In O. vulgaris hatchlings, paired oval-shaped olfactory organs are situated on
either side of the head, ventrally behind the eye and near the mantle edge (Figure 22). They measure
around 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 morphological cell type, suggesting the olfactory organ has both chemical and mechanosensitive functions in planktonic O. vulgaris (Woodhams & Messenger 1974, Wildenburg 1997). In Enteroctopus
megalocyathus the organ is larger (Figure 23). In hatchlings of directly benthic octopuses such as
Octopus joubini, the olfactory organ resembles that of the adults except in size, and the receptors are
smaller (Emery 1976). Electrophysiological and behavioural analyses of the receptor cells from the
olfactory organ in adult loliginid squid have proved their chemoreceptor function (Gilly & Lucero
1992, Lucero et al. 1992, Lucero et al. 2000). The same function can be expected in octopuses.
Lip chemoreceptors Ciliated receptors and sensory cells have been described on the finger-like
papillae that distally fold the muscular lip around the beaks in O. joubini (Emery 1975). These
receptor cells seem more developed in octopuses than in cuttlefish or squid; their presence in octopus paralarvae has not been assessed.
Sucker chemoreceptors In hatchlings of O. vulgaris, primary ciliated, flask-shaped receptor cells
of presumed chemoreception function are common on the rim but rare at the lateral regions of
the suckers and absent on the epithelium of the infundibulum (Schmidtberg 1997, 1999). These
chemoreceptor cells seem to correspond with those previously described on the epithelium of the
rim sucker of adult octopuses (Graziadei 1962, 1964, 1965, 1971, Graziadei & Gagne 1976b).
130
A
50 µm
di
2
B
5 µm
C
D
Figure 22 Olfactory organ in Octopus vulgaris hatchling paralarvae. Scanning electron microscopic
images showing (A) the position (arrow) of the olfactory organ and (B) the cilia (arrow) on the organ surface.
Transmission electron microscope images showing (C) sensory cells of morphological type 1 with an apical
cilia pocket and cell morphological type 2 with a spacious ciliated cavity, and (D) sensory cell of morphological type 5, cell apex with one kinocilium and microvilli (di, dictyosome). Scale bar 2 µm. (Reproduced with
permission from Wildenburg 1997, modified.)
Digestive system
Buccal mass
The buccal mass consists of the two jaws of the beak, a radula, salivary papillae and associated
musculature. At hatching, the buccal mass is fully formed and functional (Nixon & Mangold 1996).
The upper and lower beaks are transparent and have oral denticles (Figures 24 and 25). These denticles are absent in adult octopuses, which have smooth and darkly pigmented beaks. Oral denticles
have been described in hatchlings of Octopus vulgaris (Boletzky 1971, Nixon & Mangold 1996,
Nixon & Young 2003), O. mimus (Castro-Fuentes et al. 2002), Eledone cirrhosa (Boletzky 1974),
as well as in the juvenile stages of the pelagic octopods Argonauta argo and Tremoctopus violaceus
(Boletzky 1971) and ctenoglossans (Strugnell et al. 2005). See p. 148 for functioning of the buccal
mass components.
Digestive tract
The digestive tract of octopus paralarvae is functional at birth and feeding commences rapidly
after hatching (Villanueva et al. 2002, Morote et al. 2005, Iglesias et al. 2006). The external yolk
sac that is evident within the egg capsule is sometimes visible externally in the earliest hatchling
stages, indicating premature hatching (Figure 26). The white of the yolk sac is also visible within
131
2 mm
200 um
Figure 23 Olfactory organ in Enteroctopus megalocyathus hatchling paralarvae. Specimen collected during
rearing experiments described in Ortiz et al. (2006). Scanning electron microscope images showing the position (left) and the organ (right). Note the large size of the organ in comparison with Octopus vulgaris hatchling
(Figure 22). (Specimen kindly provided by N. Ortiz, Centro Nacional Patagónico, CONICET.) Original.
UB
D
LB
50 µm
25 µm
Figure 24 Buccal mass and denticulation on the beaks of Octopus vulgaris. Left, whole mount of a hatchling individual. Right, oral surface of the rostrum of the upper (top) and lower (bottom) beaks showing denticulation in 1-day-old specimen. D, denticles; LB, lower beak; UB, upper beak. (Left, modified from Nixon
& Mangold 1996; right, from Boletzky 1971 and reproduced with permission.)
the visceral mass in these early hatchling stages (Figure 26). The yolk sac is rapidly devoured or
discarded after hatching (see p. 135) and its presence internally does not hamper direct feeding
because the digestive tract is immediately capable of ingesting prey (Boletzky 1975).
132
Figure 25 Denticulation of beaks in Octopus vulgaris paralarvae. Scanning electron microscope images
of (A) oral view of hatchling; (B) 50-day-old specimen in presettlement stage, 7.3 mm mantle length (ML)
(fresh) and (C) 60-day-old recently settled individual of 9.3 mm ML (fresh). Note the broken denticles on the
lower beaks of posthatching individuals and the rostral tip of the beak in the settled individual, in transition
to the typical adult beak form. Individuals obtained from rearing experiments described in Villanueva (1995).
Original.
Ink sac
For those species that possess an ink sac in the adult form, the ink sac of their paralarvae is functional from birth (Yamashita 1974, Gabe 1975, Joll 1978, Okubo 1979, Kaneko et al. 2006). The
positions of this and other organs of the digestive tract are shown in Figure 27. The organ is visible
through the body wall in those taxa that lack a reflective iridophore membrane surrounding the
viscera (Figure 26).
133
Figure 26 (See also Colour Figure 26 in the insert.) Planktonic paralarva of Octopus warringa within
10 min of hatching in the laboratory showing short arms, transparent musculature, simple chromatophores
and external yolk sac (within arm crown). (Photo: David Paul.)
oo
r
cv
sg
fr
is
g
1 mm bh
A
B
C
Figure 27 Scaeurgus unicirrhus hatchling after fixation. (A) Lateral view. (B) Dorsal view. (C) Ventral view
after removal of the ventral mantle musculature. bh, branchial heart; cv, cephalic vein lying beside the intestine; fr, funnel retractor; g, gill; is, ink sac; oo, olfactory organ; r, rectum; sg, stellate ganglion. (Reproduced
with permission from Boletzky 1984, modified.)
Food, feeding and nutritional requirements
Yolk reserves
After hatching, octopus paralarvae possess available yolk reserves that help the animal during
the first hours or days, combining endogenous (yolk) with exogenous (prey) feeding until the yolk
is completely absorbed (Boletzky 1975, 1989). In octopods, part of the yolk is enclosed within
the hatchling proper and the rest forms an external sac enclosed within a membranous envelope
134
(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 paralarvae start to feed during the first 24 h after hatching
(Villanueva et al. 2002, Morote et al. 2005, Iglesias et al. 2006) and that the presence of an inner
yolk sac does not apparently interfere with any organ functioning (Boletzky 1975).
The amount of yolk is proportional to body weight and the yolk absorption is related to temperature in squid paralarvae (O’Dor et al. 1986, Vidal et al. 2002, 2005). The same relationship can
also be expected for octopus paralarvae. Large octopus hatchlings from species adapted to low temperatures, such as Enteroctopus megalocyathus, can survive under starved conditions up to 15 days
at 11.5°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 survival under starvation conditions. Starved paralarvae fed a maternal sardine diet had low survival
rates and low lipid content, particularly for phosphatidylcholine and phosphatidylethanolamine as
well as low content in n-3 and n-6 polyunsaturated fatty acids (PUFAs) (Quintana et al. 2005,
2006). Table 3 shows survival of different paralarval species after hatching in the laboratory; some
of these results are the product of unsuccessful feeding experiments for which the short survival
period suggests that metabolic fuel was provided mostly by the yolk and whole animal reserves. The
physiological conditions that enable the first digestion of external prey have not been determined for
octopus paralarvae and need further research.
Natural prey
At the moment of prey capture, octopus paralarvae bite and administer salivary products using their
beaks and radula. The saliva contains enzymes that predigest the prey, enabling easy removal of the
flesh from exo- or endoskeletons. The beak and radula are then used to macerate the predigested
flesh, sucking up the edible content of prey such as crustaceans and rejecting their exoskeletons
(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 paralarvae in the wild. Passarella & Hopkins
(1991) examined stomach contents of 57 paralarvae (<20 mm ML) of Octopodidae (Macrotritopus
defilippi, Octopus sp. and Scaeurgus unicirrhus) collected from eastern Gulf of Mexico at depths
between 0 and 900 m and found that the major prey types were euphausiids (53% of the stomachs)
and non-cephalopod molluscs (23%), as well as ostracods, hyperiid amphipods, decapod crustaceans and fishes. Octopus paralarvae share a preference for crustacean prey with squid paralarvae
(Passarella & Hopkins 1991, Vecchione 1991, Vidal & Haimovici 1998), in common with most
juvenile cephalopods (Nixon 1987).
A wide variety of live and inert prey has been consumed by octopus paralarvae in laboratory
experiments (Table 3). Most of the successful or long-term laboratory rearings used decapod crustacean zoeae (Figure 28) as the primary prey for small-sized octopus paralarvae (Octopus vulgaris
type) (Itami et al. 1963, Forsythe & Toll 1991, Villanueva 1994, 1995, Shiraki 1997, Carrasco et al.
135
136
Crushed egg yolk, ground shrimp and
mussel, live gammarids, Artemia biomass
and fry of fish Hemilepidotus
hemilepidotus
Mysidaceans (5–15 mm) during first
feeding and pieces of shrimp (Palaemon
pacificus) after 70 d
From hatching to 50 d: dead
mysidaceans + amphipods; 50–80 d:
dead mysidaceans + amphipods + pieces
of shrimp; from 80 d: pieces of shrimp
Artemia, frozen Calanus, frozen and live
zooplankton
Pieces (2–5 mm) of prawns (Palaemon
pacificus), clam (Ruditapes
philippinarum) and crab
Live mysidaceans, amphipods and pieces
of shrimp after 70 d
Artemia and hatchlings of greenling fish
Amphioctopus burryi
Live wild zooplankton (copepods, larval
crustaceans and fishes) and Artemia
nauplii
Callistoctopus macropus
Hatchling zoeae of Pagurus prideaux
Species and prey offered
7.8–14.7,
mean
10.8
Np
8.5–15.6,
mean
11.8
10–12.8
To 26 d
10.6–11.8,
mean
11.0
Np
8% at 6 months
To 169 d
Np
To 19 d
4% at 135 d
To 7 d
To 6 d
16
Np
To 16% at 26 d
Survival rate (%)
23–24
Temp.
(°C)
Settlement
from
100–117 d
Settlement
from 88 d
No
No
Presettlement
No
No
No
No
Reared to
settlement
Tank with upwelling water
system
Only adult Artemia and fry
fish accepted as prey;
occasionally dead siblings
captured by the paralarvae
Individuals reached 35 mm TL
at 169 d
Food pieces submerged
previously in freshwater to
increase floatability
Individuals reached 33 mm TL
at 115 d
Feeding and development not
observed
Eating not observed
Without food survived 3–4 d
No growth in ML
Comments
NW Pacific
NW Pacific
NE Pacific
NW Pacific
NW Pacific
NW Pacific
NE Pacific
Mediterranean
NW Atlantic
Geographic
area
Okubo 1980
Okubo 1979
Gabe 1975
Yamashita 1974
Okubo 1974
Okubo 1973
Green 1973
Boletzky et al.
2001
Forsythe &
Hanlon 1985
Reference
Table 3 Prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from hatching to
settlement of the paralarvae obtained during rearing experiments of Octopodidae species with planktonic hatchlings
137
Octopus laqueus
Artemia nauplii, copepods and pieces of
shrimp
Octopus mimus
Artemia metanauplii, zoeae of
Leptograpsus variegatus and Cancer
setosus, and rotifers
Hatchling zoeae of Pagurus sp. and Cancer
setosus
Macroctopus maorum
Starved
Octopus bimaculatus
Artemia and wild plankton
Octopus cyanea
Crab and mysis zoeae, copepods Promysis
orientalis and Lucifer sp.
Octopus joubini
Wild live zooplankton, zoea of penaeid
shrimp, mysidacean shrimp
Frozen or fresh chopped body and muscle
of crabs Cancer productus, Pugettia
productus, tails of Pandalus danae
shrimps, Euphausia pacifica, beef heart
and lamb kidney
Enteroctopus megalocyathus
Starved
Hapalochlaena lunulata
Artemia and small crustaceans
Artemia biomass, frozen krill (Euphausia
pacifica), larval cottid fish (Hemilepidotus
hemilepidotus), trout micropellets
To 7 d
11.5
26
To 31 d
To 12 d
<22
Np
To 10% at 7 d and 0.2% at
23 d
24
To 7 d
To 21 d
Np
26
To 6 d
Np
To 8 d
To 15 d
11–11.5
Np
With Artemia: 50% SR at
5 d and maximum to 22 d;
with krill: 50% SR at 16 d
and maximum to 87 d
4% after 6–7 months
10
No
No
No
Settlement
from 21 d
No
No
No
No
No
Settlement
from 5 to
6 months
No
Best results with zoeae as food
and octopus density of 25 ind
l−1
Only feeding on pieces of
shrimp was observed
Addition of vitamin
supplement mixture to the
rearing tanks
Growth increase in 0.5 mm
TL; unfed controls died in 5 d
Slight paralarval growth
Hatchling food size equivalent
to octopus head width;
developed paralarvae feed on
chunks of food 3–6 × 25 mm
suspended in the tank
The preferred prey was krill;
neustonic feeding behaviour
described
(continued on next page)
Warnke 1999
Zúñiga et al.
1997
SE Pacific
SE Pacific
Kaneko et al.
2006
Forsythe & Toll
1991
Van Heukelem
1973
Ambrose 1981
Batham 1957
Overath &
Boletzky 1974
Ortiz et al. 2006
Snyder 1986a,b,
unpublished
manuscript
Marliave 1981
NW Pacific
NW Atlantic
Hawaii
Islands
NE Pacific
SW Pacific
Central E
Pacific
SW Atlantic
NE Pacific
NE Pacific
138
9% to settlement at 47 d
30% at 29 d
21.2
Np
Liocarcinus depurator and Pagurus
prideaux decapod crab zoeae
Artemia and Portunus trituberculatus crab
zoeae
To 67% at 22 d
25.1
30% at 25 d
To 35 d
25–28
9% at settlement
Mean
24.7
Np
Np
To 12 d
To 9 d
To 21 d
To 32
Np
23
To 6 d
17–23
Survival rate (%)
10% at 5 d, maximum
survival to 17 d
To 23 d
21–22
Temp.
(°C)
Artemia biomass
Octopus vulgaris
Argonauta argo hatchlings
Harpacticoid copepods, Artemia, ciliates,
yeast cells
Palaemon serrifer decapod palaemonid
zoeae
Zoeae of crabs and prawns, Artemia
biomass
Artemia biomass
Artemia, Brachionus, zoeae of Cancer
setosus, Hepatus chiliensis, Emerita
analoga and Pleuroncodes monodon and
micropellets
Octopus tetricus
Copepods, Artemia, small pieces of fish
and mollusca
Octopus cf tetricus
Artemia and rice powder
Artemia nauplii
Transition to
benthic
stage
Transition to
benthic
stage
Settlement
from 47 d
Presettlement
Settlement
from 33 d
No
No
No
No
No
No
No
Reared to
settlement
Individuals with 19 suckers at
29 d
NW Pacific
Tank volume of 20 m3 and
microalgae Nannocloropsis
added to the tank
Food added 5 times per day
NW Pacific
Mediterranean
NW Pacific
Mediterranean
NW Pacific
Mediterranean
NE Atlantic
E Indian
SW Pacific
SE Pacific
SE Pacific
Geographic
area
Microalgae Nannocloropsis
added to the culture tank
P. serrifer zoeae feed with
Artemia nauplii
Growth ceased from 25 d
No feeding observed
No growth, no evidence of
eating
All food refused
Comments
Villanueva
1994, 1995
Shiraki 1997
Hamazaki et al.
1991
Itami et al.
1963
Mangold &
Boletzky 1973
Imamura 1990
Naef 1928
Vevers 1961
Joll 1976
Dew 1959 (as
O. cyanea)
Baltazar et al.
2000
Montoya 2002
Reference
Table 3 (continued) Prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from
hatching to settlement of the paralarvae obtained during rearing experiments of Octopodidae species with planktonic hatchlings
139
3.4% at 60 d
31.5% at 40 d
21.1–22.2
22.5
Live and frozen Maja brachydactyla zoeae
1–3 d old and Artemia biomass
Maja brachydactyla zoeae and Artemia
biomass (1–4 mm)
To 4.6% at 30 d
To 56 d
19.4–22.5
Np
To 62.5% at 40 d
17–29
To 6.7% at 30 d
20–22.5
To 45% and 24% at 16 and
20 d, respectively
To 32 d
18–20
25
To 88% at 24 d
21, 24 and
27
Artemia nauplii and millicapsules of
1.3–2 mm in ∅, 0.3 mg fresh weight
Nannochloropsis algae on the rearing tank
at 100 × 104 cells/ml; Artemia biomass
(2 mm) not enriched or enriched with
yeast or shark egg powder
Artemia biomass (1.5–2 mm) feed with
Nannochloropsis algae
Octopus vulgaris
Artemia biomass and zoeae of Maja
squinado
Artemia biomass (1–2.7 mm) feed with or
without Nannochloropsis algae on the
rearing tank
Rotifers, fish eggs, micropellets, wild
copepods, Artemia nauplii and
metanauplii, zoeae of shrimp Palaemon
serratus, zoeae of crab Carcinus maenas
and Necora puber
Artemia biomass (1–3 mm) and pellets
(250–500 µm) with 6% moisture
Settlement
from 52 d
Settlement
from 40 d
No
No
No
No
No
No
No
Tank volume of 9 m3 and
microalgae Isochrysis,
Tetraselmis and Chaetoceros
Total proteolytic activity
correlated with paralarval
weight
Parabolic tanks with upwelling
water system
Microalgae (Chlorella sp.,
Isochrysis galbana and
Chaetoceros sp.) added daily
to the culture tank
Highest survival at 21°C
Enriched Artemia increased
survival and growth
Fatty acid of cultured octopus
reflected that of the food
Higher growth and survival
with 100–400 × 104 algal
cells/ml
Best survival with Artemia
metanauplii
Carrasco et al.
2003, 2006
Iglesias et al.
2004
Villanueva et al.
2002
Moxica et al.
2002
Hamasaki &
Morioka 2002
Navarro &
Villanueva
2000
Hamasaki &
Takeuchi 2001
Iglesias et al.
2000
Hamasaki &
Takeuchi 2000
NE Atlantic
NE Atlantic
Mediterranean
NE Atlantic
NW Pacific
NW Pacific
Mediterranean
NE Atlantic
NW Pacific
140
To 27% at 28 d
To 39% at 40 d
2d
20 ± 1
20
To 10% at 42 d
3d
Np
24–26.9
Artemia nauplii and defrozen fish
(Ammodytes personatus) flakes
Octopus vulgaris
Artemia metanauplii, Grapsus grapsus and
Plagusia depressa zoeae
Artemia nauplii supplemented with
copepods (Acartia tonsa), juvenile mysids
(Metamysidopsis elongata atlantica) and
crab zoeae (Callinectes sapidus)
Artemia 0.8 mm
18–20
To 45.9% at 32 d
21.2–24.8
Artemia biomass of 0.8 and 1.4 mm
To 10 d
21–22
Artemia metanauplii, cladocerans Moina
salina, zoeae of Maja brachydactyla and
Palaemon serratus, eggs and larvae of fish
Solea senegalensis, artificial pellets
Artemia nauplii and thawed frozen fish
(Ammodytes personatus) flakes
To 26 d
20 ± 1
Artemia metanauplii and zoeae of Maja
squinado
To 12.5% at 30 d
Survival rate (%)
19.2–21.1
Temp.
(°C)
Artemia nauplii and essential amino acids
added to the rearing tank
No
No
No
Transition to
benthic
stage
Transition to
benthic
stage
No
No
No
No
Reared to
settlement
Prey capture higher during
light periods, decreasing in
the dark
Best survival and growth with
G. grapsus zoeae
Best survival with A. tonsa up
to 15 d supplemented with
Artemia
Fish flakes effective for
improving the DHA content
of the paralarvae
Preference for Artemia 1.4 mm
at densities of 0.1 Artemia
ml−1
Fish flakes improved DHA
content of the paralarvae
Better growth and survival
with light intensity of
6000 lux
Protease activity indicates
hatchling condition
Best survival in trials receiving
amino acids
Comments
NE Atlantic
SE Atlantic
NE Atlantic
NW Pacific
NE Atlantic
NW Pacific
NE Atlantic
Central E
Atlantic
Mediterranean
Geographic
area
Márquez et al.
2007
Iglesias et al.
2007
Iglesias et al.
2007
Kurihara et al.
2006
Iglesias et al.
2006
Okumura et al.
2005a
Villanueva et al.
2004,
Villanueva &
Bustamante
2006
FernándezLópez et al.
2005
Morote et al.
2005
Reference
Table 3 (continued) Prey offered, rearing temperature, survival or maximum age in days (d), and duration of the planktonic period from
hatching to settlement of the paralarvae obtained during rearing experiments of Octopodidae species with planktonic hatchlings
To 34 d
To 6 d
To 4 d
10–16
19
26
No
No
Np
Note: DHA, docosahexanoic acid; ML, mantle length; Np, not provided; SR, survival rate; TL, total length.
Robsonella fontanianus
Artemia, small crustaceans and
micropellets
Scaeurgus unicirrhus
Artemia biomass
Artemia naupli, rotifers Brachionus and
copepods
SW Pacific
Mediterranean
SE Pacific
Miske &
Kirchhauser
2006
Boletzky 1984
González et al.
2006
141
Figure 28 Decapod crab zoeae hatchlings used as live prey in successful rearing experiments of Octopus
vulgaris paralarvae. Left to right: Liocarcinus depurator, 0.5 mm carapace length (CL); Pagurus prideaux,
1.2 mm CL (photos: R. Villanueva); Maja brachydactyla, 1.1 mm CL (photo courtesy of Guiomar Rotllant).
2003, 2006, Iglesias et al. 2004) or mysidaceans, amphipods and euphausiids for larger-size 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 paralarvae 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 littoral octopuses although stomach analyses from wild paralarvae need to be examined. In contrast,
the ability of planktonic octopuses to feed on inert food, as observed under laboratory conditions
(see p. 146), suggests that scavenging activity in the wild is also possible. Immunoassay techniques
used to analyse stomach contents of squid paralarvae (Venter et al. 1999, Hoving et al. 2005) may be
useful tools for gaining better insights into the earliest feeding stages of octopus paralarvae.
Prey size and prey density
In comparison with most carnivorous larval fishes, for which mouth opening diameter limits the size
of the prey that are generally ingested whole, planktonic octopuses can capture prey of their own
size using their well-developed arms and suckers. Prey size and prey density preferences of planktonic octopus have been determined only under experimental conditions. Artemia of 1.1–1.7 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).
142
35
Prey TW as % of octopus TW
Prey TL as % of octopus TL
140
120
100
80
60
40
20
0
0
5
10
15
Octopus TL (mm)
30
25
20
15
10
5
0
20
1
100
10
Octopus TW (mg)
1000
Figure 29 Predator-prey size relationships in Octopus vulgaris during the paralarval stage expressed as
length (left) and fresh weight (right). Octopus data points correspond to reared O. vulgaris aged 0, 10, 20, 30,
42, 50 and 60 days (data from Villanueva 1995). Selected prey are hatchling zoeae of Maja brachydactyla (dark
circles) used as prey in Iglesias et al. (2004) and Carrasco et al. (2006); Pagurus prideaux (white circles) and
Liocarcinus depurator (white squares) used as prey in Villanueva (1995); adult stages of the copepod Acartia
tonsa (diamonds) and Artemia nauplii, AF strain (triangles). TL, total length; TW, total weight. Original.
Prey densities in successful cultures using decapod crustacean zoeae ranged from 0.1–0.3
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 significant differences in the number of attacks by Octopus vulgaris hatchlings on Artemia of 1.4 mm
length at densities of 0.1, 0.5 and 1 Artemia 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 paralarvae grow in the second half of their planktonic phase, larger prey are required. Hatchling decapod zoeae decrease in size relative to presettlement paralarvae (>10 mm total length), representing only 9–26% of their length and 0.04–0.7%
of their weight (Figure 29). Presettlement O. vulgaris-type paralarvae, large Enteroctopus-type
paralarval forms and micronektonic paralarvae forms (see p. 182) probably require larger prey. In
fact, E. dofleini hatchings (10 mm total length) eat mysidaceans 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 relatively large octopus paralarvae in the wild.
Food searching and prey capture
Experiments with Octopus vulgaris hatchlings showed that light enhanced consumption rates
3-fold in comparison with dark conditions. A higher percentage of non-feeding individuals was
also recorded in the dark, suggesting the importance of light (and vision) in predatory behaviour
(Márquez et al. 2007). However, these authors showed that light may not be essential for prey capture as a positive correlation was found between prey density and consumption rates in dark conditions. Observations of the swimming paths of O. vulgaris paralarvae in laboratory conditions over
2 months of planktonic life found that paralarval behaviour is affected by the presence of prey —
individual paralarvae tend to increase their turning rate and reduce swimming speed in the presence
of prey (Villanueva et al. 1996). In the sea, both responses may combine to improve the exploitation
143
of patchy food environments as curvilinear paths and slow swimming speeds increase the probability of residence time in a zooplankton patch, increasing the probability of prey encounters.
Capture of live prey
In O. vulgaris, prey capture can be predicted by a human observer as the paralarva modifies its routine swimming behaviour in a recognizable behavioural sequence (Boletzky 1987, Villanueva et al.
1996, 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’; paralarvae reduce speed and approach the prey,
using a range of different manoeuvring movements including forward, backward and lateral swimming. The second phase is the ‘positioning phase’; the anterior end of the body is directed towards
the prey and an aiming posture is adopted with arms drawn together and pointed anteriorly. The
body axis is aligned directly towards the prey. At this time the paralarva is almost immobile, sometimes rotating its position around the prey using jets of water through the flexible funnel, attaining
the best position for attack. The third phase is the ‘attack phase’; the paralarvae swims forward fast,
usually through one (sometimes two) powerful jets from the funnel and the prey is seized with all
arms. During the prey capture sequence, a change in chromatophore pattern usually takes place
between the second and third phase (Hernández-García et al. 2000). During the attention phase,
the paralarvae maintain contracted chromatophores, so that the octopus is nearly transparent to
a human observer; then, during the positioning phase and/or during the contact with the prey, the
chromatophores from the dorsal mantle, head and arms are expanded dramatically. After seizure of
the prey the chromatophores are contracted again. This visual signal is suspected to be defensive
A
B
C
D
Figure 30 Behavioral sequences during prey capture in 20-day-old individual of Octopus vulgaris (4.4 mm
total length) preying on hatchling zoeae of Pagurus prideaux (3.1 mm total length). After the prey is selected,
three phases can be identified: (A) attention, (B) positioning and (C) attack (see text for explanation). Note that
during the attention phase, the octopus maintains contracted chromatophores, then, during positioning and
contact with the prey, the chromatophores from the dorsal mantle, head and arms are expanded. After seizure
of the prey (D), chromatophores are contracted again. The dark oval spot inside the mantle cavity represents
the digestive gland. (Original drawing from Jordi Corbera based on video recordings from Villanueva et al.
1996.)
144
behaviour (see ‘Defences’, p. 168). Selection of the attack angle probably depends on the type of
prey, its size and defences (i.e., many crustacean zoeae possess dorsal spines) (Figure 28). Further
research is required on the predatory behaviour of octopus paralarvae, as have been made on loliginid squid paralarvae (Chen et al. 1996). Such studies may detect ontogenetic changes in predatory
behaviour along with behavioural responses specific to different prey types.
After prey have been selected, attack distances are usually two to four times the total length of
the octopus, or sometimes more. In Amphioctopus burryi paralarvae preying on wild zooplankton,
these distances are 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 paralarvae notice the prey during the attention phase) was 15.5 mm (Villanueva et al.
1996). Using an estimated mean cruising speed of 25.6 mm s−1, the estimated water volume searched
(VS) by 30-day-old O. vulgaris paralarvae (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 paralarvae have static periods during which they remain hovering
using weaker ventilatory pulses to provide dynamic lift (Boletzky 1977a). Forward swimming is
always used to capture prey, while backward jetting is used while subduing and ingesting prey.
Mean time taken from striking prey to backwards swimming after subduing the prey is 0.3 s in
O. vulgaris (Villanueva et al. 1996) (Figures 31 and 32). As indicated (see ‘Sucker surfaces’, p. 122),
the sucker structure of octopus paralarvae suggests that hydrostatic suction is not as effective in
200
160
A
B
C
D
E
F
120
80
Swimming speed (mm s–1)
40
0
160
120
80
40
0
160
120
80
40
0
–4
–2
–0
2
–2
Time (in seconds)
0
2
4
Figure 31 Swimming performance during six successful prey captures by 30-day-old Octopus vulgaris
paralarvae (4.5 mm mean mantle length), using live Pagurus prideaux hatchling zoeae as prey. Time elapsed
before and after capture and swimming speed are indicated at time intervals of 0.04 s. Time 0 indicates the
instant when the octopus strikes the prey. Before prey capture, the paralarva can swim forward (———),
backwards (-----) or laterally (·····, only observed in example A), and the arms are pointed towards the prey
(
at bottom of each graph). The same paths in the same order are used in Figure 32. (Reproduced with
permission from Villanueva et al. 1996.)
145
6
60
(A)
5
c
4
3
0
30
10
S
0
5
10
Y (mm)
30
15
c
20
S
0
10
20
30
40 50
e
10
60
(D)
s
15
10
c
5
0
5
10
15
20
70
60
0
0
S
0
20
40
60
e
40
(F)
10
20
10
30
c
e
30
20
s
20
40
10
30
(E)
c
50
0
0
20
(C)
e
20
c
s
20
40
0
e
40
e
2
1
(B)
s
50
80
0
0
10
20
30
X (mm)
Figure 32 Swimming paths of six successful prey capture sequences of 30-day-old Octopus vulgaris para
larvae, 4.5-mm mean mantle length (open circles) and Pagurus prideaux hatchling zoeae as prey (·). Each
point represents the respective position of the animal at 0.04-s time intervals. c, capture; e, end position; s,
starting position. Inset of B, path of octopus before attack, represented by (———). The same paths are used
in the same order in Figure 31. (Reproduced with permission from Villanueva et al. 1996.)
early paralarvae as it is in adults or octopus hatchlings of directly benthic species (Schmidtberg
1997, 1999). This may represent an impediment to holding and subduing prey although the gland
cells on the epithelium of the sucker rims that secrete mucopolysaccharides probably assist in adherence of paralarval suckers (Kier & Smith 1990, Schmidtberg 1999).
Capture of inert prey
Live prey is not a prerequisite stimulus in provoking attacks by octopus paralarvae. Laboratory
studies using inert food showed that attacks usually take place when the dead prey or food particle
descends in the water column (Boletzky & Hanlon 1983). Pellets, millicapsules and fish flakes have
been used as supplementary food for O. vulgaris paralarvae and are captured when sinking through
the water column (Navarro & Villanueva 2000, 2003, Okumura et al. 2005a, Kurihara et al. 2006).
As the escape response of many water column residents of open ocean is to passively and rapidly
146
sink (i.e., pteropod molluscs and gastropod veliger larvae; Lalli & Gilmer 1989), capture of sinking
food items may not simply be an attempt to capture inert or dead food sources.
Capture of dead prey from the bottom of rearing tanks has also been reported by Itami
et al. (1963) for O. vulgaris when live prey were scarce in the water column. Okubo (1980) reared
Enteroctopus dofleini from hatching to settlement on floating frozen prey (mysidaceans, amphipods, pieces of shrimp), using a tank with an upwelling water system that maintained movement
of the food particles. Snyder (1986a,b, unpublished manuscript) fed paralarvae of the same species
over 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 conditions. When the mantles of E. dofleini individuals aged 6 days came into contact with floating
pieces of krill, the octopuses would turn over and adhere to the surface tension film in an inverted
posture with the oral surface of the arms extended towards the surface. On contacting the food with
their arm tips, individuals would seize the krill and leave the surface to feed on it within the water
column, suggesting chemotactile discrimination of these food sources (Figure 33). The neustonic
feeding described by Marliave ceased once the paralarvae reached 1 month old and was replaced
by the capture sequences more typical of the smaller Octopus vulgaris. Neustonic feeding was also
reported by Snyder (unpublished manuscript) for Enteroctopus dofleini and Boletzky (1987) for
Octopus vulgaris hatchlings.
Overall, octopus paralarvae seem to be visual predators but chemical and tactile senses also
seem to play important roles during prey searching and require further research. Octopuses are blind
to colour (Messenger 1977). Certain cephalopods have been shown to be polarization sensitive (see
among others Shashar & Cronin 1996, Shashar et al. 1996). Hatchlings of the squid Loligo pealei
attacked planktonic prey under polarized illumination at a 70% greater distance than under depolarized light (Shashar et al. 1998). The role of polarization vision in octopus paralarvae is unknown
although it is likely to play an important role. As visual predators, octopus paralarvae may target luminescing prey, particularly when feeding in deeper waters and at night. Dinoflagellate bioluminescence
has also been proposed to help in locating and capturing non-luminous prey during nocturnal feeding
for juvenile cuttlefishes (Fleisher & Case 1995). The same may apply for octopus paralarvae.
Figure 33 Neustonic feeding in Enteroctopus dofleini. Individuals adhering to the surface film in inverted
posture (upper right individual) and normal swimming posture (lower left). Note that reflected glare indicates attachment of the suckers to the water surface and depression of the surface tension film. Scale 4 mm.
(Reproduced with permission from Marliave 1981, modified.)
147
Buccal mass, denticulate beaks and external digestion
In comparison with adults, octopus paralarvae have relatively short arms with few suckers and a
large buccal apparatus (containing the beaks and radula) and this apparatus is particularly important
at this life-history stage in subduing and chopping the prey prior to ingestion. At hatching, the diameter of the nearly spherical buccal mass represents 30% of the ML and is innervated by the buccal
lobe of the brain that is also proportionally much larger than in recently settled individuals (Nixon
& Young 2003). After settlement, octopuses have a large arm crown and numerous suckers, representing the main means of prey capture and manipulation. In adult octopuses, buccal mass length
decreases to around 13% of ML (Nixon 1985, Nixon & Mangold 1996, Nixon & Young 2003).
As stated, the posterior salivary gland papilla and radula are well developed and fully functional
at hatching (Nixon & Mangold 1996). Octopus paralarvae beaks possess oral denticles. These denticles have also been observed for paralarvae of loliginid (Boletzky 1971) and ommastrephid squids
(Shigeno et al. 2001) and in hatchlings of octopod species with direct benthic young, although
showing less-developed denticulation in these octopod species with direct benthics (Boletzky 1971,
1977a). They have also been reported in adult pygmy squid, Idiosepius (Adam 1986, Kasugai et al.
2004). The function of these denticles, typically associated with early stages or pygmy species such
as Idiosepius, remains unclear. However, detailed observations on the external digestion and initial
ingestion process (see this section) suggest that denticles may be useful to detach the semidigested
flesh from the exoskeleton of the crustacean prey (Kasugai et al. 2004). Two factors may account
for this dentition. The first is that the radula may be too poorly developed to grip and remove flesh
from the prey. The second is that the dentition may aid gripping the prey in paralarvae with few,
proportionally large (and hence clumsy) suckers. The beaks of presettlement and recently settled
captive-reared Octopus vulgaris individuals show loss of some denticle tips, presumably worn by
their use during feeding on crustacean zoeae larvae (Figure 25B,C). The erosion of the denticles
seems to be a stage in the transition to the thick, darkly pigmented and chitinized beaks of juvenile O. vulgaris that lack denticles and have rostral tips more characteristic of the adult octopus
(Nixon & Mangold 1996).
In octopuses, two categories of glands discharge their secretion into the buccal cavity: (1) diffuse
glands of single or small groups of gland cells on the lips, salivary papilla and buccal epithelium
and (2) five major glands (the single submandibular salivary gland below the radular complex, the
paired anterior salivary glands that lie on the posterior surface of the buccal mass, and the paired
posterior salivary glands that lie adjacent to the swollen crop diverticulum anterior to the digestive
gland) (Boucaud-Camou & Boucher-Rodoni 1983, Budelmann et al. 1997, Nixon & Young 2003).
The posterior salivary glands secrete a mixture of substances, including biologically active amines,
enzymes (particularly proteolytic enzymes) and toxins with venomous, pharmacological, digestive
and haemolytic properties (Grisley & Boyle 1987, Grisley 1993, Key et al. 2002). The adult octopus
cephalotoxin is responsible for the paralysis and killing of crabs (Ghiretti 1959, 1960) and the ability
of octopus saliva to release crab muscle from the carapace prior to ingestion is principally caused by
proteases in the saliva (Grisley & Boyle 1987), injected into the crab by a narrow hole produced in
the carapace or the cornea of the crab (Grisley et al. 1996, 1999). Prey is then disarticulated and the
flesh removed and ingested, leaving the clean exoskeleton, which is discarded by the octopus.
This process is generally known as external digestion (Nixon 1984) and in octopus paralarvae
has been described for O. vulgaris hatchlings feeding in laboratory on recently hatched decapod
crab zoeae Pachygrapsus marmoratus, P. transversus and Eriphia verrucosa (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 appendages. Similar observations have also been reported for 11-day-old loliginid squid paralarvae (Loligo
vulgaris) feeding on mysidacean shrimp in the laboratory (Boletzky 1974) and for adults of the
148
pygmy squid Idiosepius (Kasugai 2001, Kasugai et al. 2004). During external digestion and ingestion, the prey is actively handled with arms, suckers and buccal mass. Boucaud-Camou & Roper
(1995) found chymiotrypsin activity on the sucker surface of Octopus sp. paralarvae and suggested
that this enzymatic activity was probably related to secretions of the posterior salivary glands and
involved in diffusion of the octopus enzymes and venom when handling the prey during the external
digestive processes. In addition to an external digestion that rejects the entire crustacean carapace,
analysis of stomach contents of O. vulgaris hatchlings eating Artemia showed the presence of thoracic appendices (thoracopods) of this prey in the stomach contents (Iglesias et al. 2006). Similarly,
exoskeleton crustacean remains were found in stomach contents of wild paralarvae and juvenile
squids (Vecchione 1991, Vidal & Haimovici 1998), showing that external digestion is not the only
digestive choice for paralarvae. The selection of different modes of ingestion and/or digestion by the
paralarvae is probably related to prey characteristics. The mode of digestion as well as the percentage of prey ingested or rejected require further research.
Daily food ration by octopus paralarvae is also poorly known. Itami et al. (1963) found that
O. vulgaris of 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 vulgaris hatchlings preying on 0.8- to 1.4-mm Artemia ranged from 4 to 10 min (Iglesias et al. 2006).
For 15-day-old paralarvae, the duration was up to 15 min when ingesting 250- to 500-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 caecum, digestive gland and skin. High levels of acid phosphatase activity were found in the digestive
gland and digestive duct appendages and acetyl-glicosaminidase activity on the posterior salivary
glands, digestive gland and stomach. Protease and chymiotrypsin activity were recorded in all parts
of the digestive tract with virtually zero glucoronidase, amylase and cathepsin B activity. The high
proteolitic activity of the digestive gland seems to be related to the carnivorous diet of the 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, recording trypsin activity for only 20% of the individuals analysed. This result suggests that trypsin activity is developed only after active exogenous feeding. In fact, total proteolytic activity, and trypsin
and chymiotrypsin levels in advanced embryos and unfed hatchlings at day 0 show no differences.
However, 5-day-old fasting paralarvae have been shown to decrease their proteolytic activity
(Villanueva et al. 2002). Once external feeding commences, O. vulgaris paralarvae can adjust their
digestive enzymes to different diets and food rations during the first month of life. This adaptation
seems to be positively correlated with paralarval growth by weight. Differences in enzyme activity can be detected after 5 days of rearing at a mean temperature of 20°C under high or low feeding regimes, with higher proteolytic, trypsin and chymiotrypsin activities correlating with higher
growth and feeding ratios. In comparison with carnivorous larval fishes, levels of trypsin activity in
O. vulgaris paralarvae seem to be higher. Zambonino-Infante et al. (1996) reported trypsin activity
149
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 paralarvae the corresponding 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 oesophagus and crop to the stomach for internal digestion, aided by salivary and digestive gland enzymes.
Smaller food particles move into the digestive gland or caecum for further digestion. The caecum
processes fine particles and fluids and is considered the main absorptive organ in adult octopods
(Boucaud-Camou & Boucher-Rodoni 1983, O’Dor et al. 1984). The same role can be expected
for octopus paralarvae although its characteristics have not been studied in detail. R. Villanueva
(unpublished) encapsulated glass ball beads (10–30 µm in diameter) within Artemia nauplii and
offered them as food to 12-day-old Octopus vulgaris paralarvae reared at 20°C. The paralarvae
started to defaecate glass balls after 1 h, suggesting that the duration of digestion in this growth
phase is relatively short.
Skin absorption
A secondary and intriguing absorptive tissue of octopus paralarvae is the integument. Castille &
Lawrence (1978) found that planktonic hatchlings identified as Octopus sp. (probably O. joubini)
uptake radio-labelled amino acids (valine) and hexoses (glucose, mannitol) directly from seawater.
They suggest that this uptake mechanism is more active than diffusion, it is saturable and specific,
and that little of the uptake is due to the bacterial flora associated with the octopod hatchlings.
Radio-labelled amino acid (phenylalanine) uptake from seawater was also recorded in O. vulgaris
aged 0, 7, 14 and 21 days (Villanueva et al. 2004) and has been recorded for adult cuttlefishes, Sepia
officinalis (de Eguileor et al. 2000). In these laboratory experiments, the contribution to absorption
of radio-labelled marker molecules made by microorganisms in both the cephalopod skin and the
seawater could not be ruled out. Further support for this skin absorptive mechanism came from
Boucaud-Camou & Roper (1995), who used histochemical methods to demonstrate high alkaline
phosphatase activity in the skin of wild Octopus sp. paralarvae. They suggest that the presence
of this digestive enzyme indicates active absorption through the skin from seawater during the
paralarval period. A high microbial presence in the skin mucus covering of rhynchoteuthion squid
paralarvae has also been suggested to be a source of food to these paralarvae (Vidal & Haimovici
1998).
On the basis of the absorptive and mechanical characteristics of the skin, the addition of small
molecules to seawater in the laboratory has been used experimentally to explore the contribution
of the skin to paralarval growth and survival. Vitamin supplement mixture was added to aquaria
(1 mg 1−1 every 3 days) containing O. joubini paralarvae in rearing experiments that resulted in
successful settlement (Forsythe & Toll 1991). Rearing trials on O. vulgaris paralarvae assessed the
contribution of the daily addition of amino acid solution (16 mg 1−1 of crystalline essential amino
acids) to the rearing tanks. Survival rates for paralarvae aged 20 days were three times higher for
the treated group compared with the control group although the dry weight of the treated 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 paralarvae.
150
Respiration
In addition to the gills, a high amount of oxygen is obtained by transcutaneous means in cephalopods (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 paralarvae, with the difference in oxygen uptake after hatching primarily corresponding to the cost of swimming. By comparing the oxygen uptake of advanced embryos
with that of the adults (Wells et al. 1983a,b), the consumption of a medium-size egg mass of O. vulgaris (i.e., 300,000 eggs) can be estimated as being approximately twice that of the brooding female
(of 2 kg total weight). Methods for the transport of O. vulgaris hatchlings over a 24-h period were
determined by Fuentes et al. (2005), who obtained nearly 100% survival when using transparent
30-l plastic bags filled one third with oxygen-saturated seawater and two thirds with pure oxygen
gas. Paralarval densities were <3000 ind 1−1 and temperature was maintained at 14°C.
Biochemical profiles of paralarvae and nutritional requirements
Proteins and amino acids
Proteins are the major organic component of octopus tissue. In contrast to the lipid-based metabolism found in many animal groups (i.e., mammals), cephalopods have a vigorous protein and amino
acid metabolism (Lee 1994). Due to the rapid growth of octopus paralarvae, there is a large amino
acid requirement for maintaining optimal growth and to supply the fuel for energy. Mobilization of
muscle protein provides metabolic energy during periods of starvation and the direct use of protein
as an energy reserve may account for the lack of major glycogen or lipid reserves in cephalopod
tissues (Storey & Storey 1983, 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, respectively (Villanueva et al. 2004). This high non-protein nitrogen content is of a similar range to that
reported for adult cephalopods (Robertson 1965, Sikorski & Kolodziejska 1986, Iida et al. 1992,
Ruiz-Capillas et al. 2002). Major components of this nitrogen fraction are volatile bases such as
ammonia and trimethylamine oxide, creatine, free amino acids, nucleotides, purine bases and urea.
Lysine, leucine and arginine represented 49% of the total essential amino acids and glutamate and
aspartate represented 47% of the non-essential amino acids for O. vulgaris hatchlings (Villanueva
et al. 2004) (Figure 34).
Fasting experiments in O. vulgaris hatchlings demonstrated mobilization of amino acids as
a fuel resource (Villanueva et al. 2004). After 2 days, proline was the first free amino acid to be
deleted. This amino acid is involved in oxidative metabolism in cephalopods, showing notable drop
in mantle muscle concentrations during exercise in adult squid (Storey & Storey 1978) and probably
is also actively metabolized during the continuous, energetically expensive jet-propelled swimming
that is characteristic of octopus paralarvae. After 4 days of fasting, the levels of free non-essential
amino acids decreased to nearly half of hatching levels (with the exception of cysteine), the level
of essential amino acids decreased in both the total content and free forms, free tyrosine was not
detected and animals lost 28% of their dry weight. Reared individuals at 25 days of age showed an
151
12
12
10
8
6
6
4
4
2
2
0
12
0
12
10
6
4
4
2
2
0
0
12
12
10
Val
8
6
4
4
2
2
0
0
12
12
10
Phe
8
Met
8
6
6
4
4
2
2
0
0
12
50
10
Lys
8
6
10
Leu
8
6
10
His
10
lle
8
Thr
EAA
40
8
30
6
H. fasted 4d
Hatchlings
H. fasted 2d
Eggs X-XI
H. fasted 4d
Hatchlings
H. fasted 2d
0
Eggs I-II
0
Eggs X-XI
10
Ovary
2
Ovary
20
4
Eggs I-II
Amino acid content (mg/100 mg dry weight)
10
Arg
8
Figure 34 Total amino acid content (mean and standard deviation in mg 100 mg−1 of dry weight) of Octopus
vulgaris from mature ovary, spawned eggs at stages I–II and X–XII, hatchlings, and hatchlings fasted for 2 and
4 days. EAA, essential amino acids. (Reproduced with permission from Villanueva et al. 2004.)
152
15
14
13
55
12
11
10
50
9
8
45
7
Total lipid (% DW)
Total amino acid (% DW)
60
6
40
0
1
2
3
Dry weight (g)
4
5
Figure 35 Mean value of total amino acid content (solid circles) and total lipid content (open circles) in
Octopus vulgaris hatchlings (0.3 mg dry weight, DW) and five wild, recently settled O. vulgaris juveniles
of 814, 1128, 1380, 2189 and 3671 mg DW. (Data obtained from Navarro & Villanueva 2000, 2003 and
Villanueva et al. 2004.)
increase in free essential amino acids in comparison with hatchlings, and glutamate was the most
abundant free amino acid, followed by arginine and aspartate. These amino acids, with leucine and
lysine, were also the most abundant in the total content, although glutamate had the highest levels.
For free essential amino acids, arginine reaches the highest levels and represents nearly half of the
free essential amino acid pool for hatchlings, 55% after 4 days of fasting, 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 paralarvae is lower than in recently settled juveniles. These biochemical changes associated with paralarval and juvenile growth are related to morphometric changes in body proportions, mainly due to the notable growth of the arms (Naef 1923,
1928, Boletzky 1977a, Nixon & Mangold 1996, Villanueva et al. 2004), which continues throughout
development because juveniles have arm lengths four to five times shorter than subadult and adult
individuals (i.e., O. vulgaris; Villanueva 1995). The development of the protein-rich muscular arm
crown is accompanied by a relative decrease in total lipid content (Navarro & Villanueva 2003),
this being due to the relative decrease of the visceral mass in which lipids are abundant (O’Dor et al.
1984) (Figure 35).
Lipid and fatty acids
Octopus paralarvae 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 rearing experiments seems to be related to diet (Navarro & Villanueva 2000, 2003, Moxica et al. 2002,
Okumura et al. 2005a). The lipid-rich nervous system of hatchling O. vulgaris paralarvae represents
approximately one quarter of the 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):
Lipid (%) = 11.436 − 0.0016 × dry weight (mg)
153
35
% of total lipid
30
25
20
0
15
10
se
tag
ﬀa
chol
dag
mag/pigm
pe
pa/cl
pi
ps
pc
sm
0
lpc
5
Lipid class
Figure 36 Lipid class composition as percentage of total lipid in Octopus vulgaris hatchlings (solid bars),
Pagurus prideaux hatchling zoeae (grey bars), Artemia biomass enriched with SuperSelco (open bars) and
30-day-old reared O. vulgaris fed with Artemia (bars with transverse lines). Data as mean of four replicates.
Error bars are standard deviation. chol, cholesterol; dag; diacylglycerides; ffa, free fatty acids; lpc, lysophosphatidylcholine; mag/pigm, monoacylglycerides/pigments; pa/cl, phosphatidic acid/cardiolipin; pc, phosphatidylcholine; pe, phosphatidylethanolamine; pi, phosphatidylinositol; ps, phosphatidylserine; se, sterol esters;
sm, sphingomyelin; tag, triacylglycerides. (Reproduced with permission from Navarro & Villanueva 2000,
modified.)
In general, the lipids of hatchling O. vulgaris are rich in cholesterol (24%), phosphatidylcholine
(21%), phosphatidylethanolamine (16%), and sterol esters (14%) and are relatively low in triacylglycerides (6%) (Navarro & Villanueva 2000) (Figure 36). Endogenous synthesis of cholesterol is absent
in adult cuttlefishes (Zandee 1967), suggesting that cholesterol is an essential dietary nutrient in
cephalopods; the cholesterol requirements of octopus paralarvae, however, have been not examined
in detail. The use of reserve lipids has been recorded during fasting of hatchling O. vulgaris 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 eicosapentaenoic 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 paralarvae within a few days of
hatching. It has been suggested that their presence in the diet is critical for the early development of
paralarvae because their levels are associated with healthy and normal paralarval growth in rearing
experiments (Navarro & Villanueva 2000, 2003, Hamasaki & Takeuchi 2001, Moxica et al. 2002,
Okumura et al. 2005a, Kurihara et al. 2006). A ratio of DHA/EPA of approximately 1.5 seems a
necessary condition for normal growth and development of O. vulgaris paralarvae. High mortality
and poor growth associated with nutritional imbalance in fatty acid profiles has been observed when
154
DHA/EPA is <1.5 (Navarro & Villanueva 2000, 2003, Okumura et al. 2005a). DHA plays an important role in maintaining the structural and functional integrity of cell membranes in fishes (Sargent
1995) and this fatty acid may be even more important for healthy development and survival of the
fast-growing, phospholipid-rich octopus paralarvae.
Elemental composition
The elemental composition of hatchlings, reared paralarvae and recently settled wild juveniles of
O. vulgaris was reported by Villanueva & Bustamante (2006) (Figure 37), showing that S, Na, K,
P and Mg were the main elements present, and levels of Ag, Cu, Mn, Ni and Zn higher compared
with other cephalopod hatchlings such as Loligo vulgaris and Sepia officinalis. Concentrations
of non-essential elements (Ag, Al, Ba, Cd, Hg, Pb) found in hatchlings and reared paralarvae of
Octopus vulgaris are lower compared with those found in subadult and adult octopuses (Seixas et al.
5000
0
30000
25000
400
350
300
250
200
150
100
50
0
Mg
20000
15000
10000
5000
0
30000
25000
P
20000
15000
10000
Artemia nauplii
Artemia-fed octopus
M. brachydactyla
octopus wild juveniles
0
octopus hatchlings
5000
400
350
300
250
200
150
100
50
0
Cu
Zn
Artemia-fed octopus
Elemental content (in µg g–1 of dry weight)
10000
Artemia nauplii
15000
As
M. brachydactyla
20000
octopus hatchlings
25000
400
350
300
250
200
150
100
50
0
S
octopus wild juveniles
30000
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.)
155
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 haemocyanin, the respiratory pigment that represents 98% of cephalopod blood proteins (Ghiretti 1966,
D’Aniello et al. 1986). Reared 20-day-old O. vulgaris paralarvae that were fed on Artemia nauplii
(a prey with relatively low Cu content [9.5 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 paralarvae seems to be inversely related to Cu content as individuals with
low levels of Cu (fasted or reared paralarvae) showed significant increases in Zn content compared
with hatchlings or juvenile wild octopuses with their higher levels of Cu (Villanueva & Bustamante
2006). Zinc can act as a metabolic antagonist of Cu because they compete for binding sites on the
proteins responsible for mineral absorption and/or synthesis of metalloenzymes (Watanabe et al.
1997, Lall 2002, Craig & Overnell 2003).
Octopuses are carnivores and the majority of their elemental composition can be assumed to be
derived from their diet. However, absorption also takes place directly from seawater, as observed
under experimental conditions for strontium and cobalt (Hanlon et al. 1989, Miyazaki et al. 2001).
Strontium is of critical importance for statolith development and thus normal swimming behaviour
and survival of hatchling cephalopods, including octopuses. Egg incubation in artificial seawater
without strontium produced O. vulgaris hatchlings that showed behavioural defects characterized by
swimming in a spinning motion (‘spinners’). Statoliths from O. vulgaris spinners were irregular in
shape and considerably reduced in size compared with control animals. Some strontium-deficient animals lacked one or both statoliths. Normal development of the aragonite statoliths and normal swimming behaviour were obtained when strontium levels reached 8 mg 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 processes. Miyazaki et al. (2001) showed that O. vulgaris hatchlings incorporate radio-labelled cobalt
in the digestive gland and the inner side of the branchial hearts within 1 min of immersion in radiolabelled seawater. Other organs and tissues were not radiographed. Miyazaki et al. (2001) suggested
that adenochrome might be a cobalt-binding substance, in addition to iron, and that the radio-labelled
cobalt may indicate the incipient development of adenochrome in the hatchlings.
Growth and duration of the planktonic stage
Size at hatching
A comparison of morphometrics of planktonic hatchlings in Octopodidae is shown in Table 4. There
is a wide range of sizes, from 2.5 to 18.3 mm in total length in fresh individuals, with the larger
hatchlings belonging to the largest of the benthic octopuses, genus Enteroctopus. Shrinking due to
fixation in preserved hatchlings shows that ML and total length can be 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
156
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
6
Indian Ocean
Reference
Amphioctopus
aegina
Amphioctopus burryi
Np
3.1 ± 0.1
F
1.5 ± 0.05
2.5 ± 0.08
4
NW Atlantic
Callistoctopus
macropus
F
4
5.5
7
Mediterranean
P
Np
Np
P
Np
3
4.8
9.3
10 (9.5–10.1)
6–8
11–14
10–12
NW Pacific
NW Pacific
NE Pacific
NE Pacific
Np
F
3.4
8.4 ± 0.7
6.9
18.3 ± 1.7
21.2 ± 2.7
NE Pacific
SW Atlantic
Yamashita 1974
Okubo 1979
Gabe 1975
Snyder 1986a, Snyder
unpublished
Hartwick 1983
Ortiz et al. 2006
Np
Np
4.5
2.3
Mangold et al. 1971
Overath & Boletzky
1974
Batham 1957
Ambrose 1981
Young et al. 1989
Brough 1965 (as
Robsonella australis)
Forsythe & Toll 1991
Kaneko et al. 2006
Warnke 1999
Baltazar et al. 2000
Castro-Fuentes et al.
2002
Mangold-Wirz et al.
1976
Dew 1959
(as O. cyanea)
Joll 1976
Itami et al. 1963
Hamazaki et al. 1991
Villanueva 1995
Okumura et al.
2005a,b
Boletzky 1984
Enteroctopus
dofelini
Enteroctopus
megalocyathus
Eledone cirrhosa
Hapalochlaena
lunulata
Macroctopus
maorum
Octopus bimaculatus
Octopus cyanea
Octopus huttoni
5.3–5.5
3.5
F
8
10
7.1 (6.7–7.6)
7–8
Mediterranean
Central E
Pacific
SW Pacific
4
3.8 ± 0.1
4
3
4
NE Pacific
Hawaii Islands
SW Pacific
Np
P
F
2.6
1.1–2.0
Octopus joubini
Octopus laqueus
Octopus mimus
F
Np
Np
Np
Np
2.4–2.6
1.7 ± 0.2
1.9
0.98
1.5 ± 0.1
3.3 ± 0.3
2.0–.2.4
1.9
3.1 ± 0.1
6–8
3
3
3
3
NW Atlantic
NW Pacific
SE Pacific
SE Pacific
SE Pacific
Octopus salutii
F
3.5–4
5.5
4
Mediterranean
Octopus tetricus
F
2.5
3
SW Pacific
Octopus cf tetricus
Octopus vulgaris
Np
F
Np
F
F
3
4
3
3.7–4
E Indian
NW Pacific
NW Pacific
Mediterranean
NW Pacific
4
Mediterranean
Scaeurgus
unicirrhus
2.1 (2–2.3)
2.5
3.2 (3–3.5)
2
2.9
Np
Ignatius & Srinivasan
2006
Forsythe & Hanlon
1985
Boletzky et al. 2001
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.
157
Num. of suckers per arm
24
21
18
15
12
9
6
3
0
0
2
4
6
ML (mm)
8
10
Figure 38 Relationship between mean number of suckers per arm and mantle length (ML) for hatchlings of
14 Octopodidae species with planktonic stages. The figure only includes species for which individuals hatched
in the laboratory from egg masses laid by identified females (see Table 4). Black circles indicate species measured fresh; white circles indicate species measured after fixation (with presumed shrinkage), as well as species for which measurement conditions (fresh or preserved individuals) were not indicated. Original.
methods and provides a useful parameter of paralarval size and growth. Distal suckers are usually smaller than the other suckers at hatching, with some exceptions, such as Amphioctopus burryi, which hatch with four suckers per arm with the proximal sucker being considerably smaller
(Forsythe & Hanlon 1985).
Intraspecific variation in size and number of suckers at hatching has been reported for species
such as Octopus vulgaris from the north-west Pacific. Females collected from the same region produced hatchling individuals ranging from 1.1 to 3.2 mg mean fresh weight and three to four suckers
per arm (Okumura et al. 2005a,b, Kurihara et al. 2006). Maternal body size and egg incubation temperature also influence hatchling size in O. vulgaris because female weight is positively correlated
with hatchling size (in ML and mantle width) (r = 0.681) and hatchling size is negatively correlated
with the egg incubation temperature (r = −0.381) (Sakaguchi et al. 2002, Sakaguchi 2006). There
is a similar tendency in other cephalopod groups because egg incubation at warmer temperature
produces comparatively smaller hatchling sizes in cuttlefish (Bouchaud 1991) and loliginid squids
(Villanueva 2000, Gowland et al. 2002, Vidal et al. 2002, Pecl et al. 2004).
Ageing and factors influencing growth
The analysis of statolith growth increments, a technique routinely used to estimate age and growth
in squids, is not possible in octopods due to the crystallization characteristics of their statoliths —
loose composites without evident growth increments. As a consequence, other hard structures have
been investigated to find periodic depositions of growth. The number of concentric rings in the
lateral wall of upper beaks from reared O. vulgaris paralarvae proved to be highly correlated with
their age in days during the first month of life (Hernández-López et al. 2001). The internal shell
remnants (‘stylets’) in the family Octopodidae also have growth increments in the form of concentric layers (Sousa-Reis & Fernandes 2002, Bizikov 2004) and their deposition proved to be daily
under aquarium conditions for a species with direct benthic hatchlings, O. pallidus (Doubleday
et al. 2006). The internal shell analysis promises to be a helpful technique to be used in the future
in ageing of octopus paralarvae. Fluorochrome alizarin complexone is an effective chemical marker
because it is incorporated into the statoliths of O. vulgaris hatchlings (Fuentes et al. 2000) and adults
(Sakaguchi et al. 2000, Sakaguchi 2006), suggesting that this marking technique could potentially
be used to identify alizarin-stained octopod paralarvae.
158
Age at settlement (d)
60
50
40
30
y = 168566x–2.6676
r = –0.9476
20
16
18
20
22
24
26
28
30
Temperature (°C)
Figure 39 Relationship between the mean rearing temperature and age at settlement from successful rearing
experiments of Octopus vulgaris. Error lines indicate temperature ranges. (Data obtained from Itami et al.
1963, Villanueva 1995, Iglesias et al. 2004 and Carrasco et al. 2006.) Exponential regression line, equation
and correlation coefficient indicated. Original.
After hatching the main abiotic factor influencing planktonic octopus growth seems to be
temperature, as has been observed in other cephalopod paralarvae (Forsythe 1993). Hamasaki &
Morioka (2002) reared O. vulgaris hatchlings at temperatures of 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 midsummer) or longer planktonic periods when temperature is decreasing (during autumn and winter)
(Katsanevakis & Verriopoulos 2006).
The duration of the planktonic period in Octopodidae seems to be species specific, temperature
dependent and, under laboratory conditions, ranges from 3 wk in the pygmy octopus O. joubini to
6 months in the giant octopus Enteroctopus dofleini (Table 3). This is a considerable proportion of
the life cycle, taking into account that, under laboratory conditions, life cycle of the same species
(including embryonic period) ranges from 6 months to 3.5 yr (Forsythe & Toll 1991, Snyder unpublished manuscript). In addition to prey availability, it is reasonable to suspect that behaviour and associated spatial distributions can influence planktonic growth. Vertical migration rhythms and related
residence periods in the water column at different temperatures need to be investigated to obtain a
more precise view of the expected growth and related duration of planktonic life in octopuses.
Behaviour
Swimming behaviour
The locomotion of octopus paralarvae is based primarily on jet propulsion, the characteristic mode
used by most octopods for swimming (Wells 1990). The main exception is fin swimming in the
159
Figure 40 Schematic line drawing showing differences between the mantle cavities of Octopodidae and
Loliginidae paralarvae. Left, Octopus vulgaris (3-mm mantle length [ML], aged 20 days) with two cavities
(ventral and dorsal), compared with Loligo opalescens (7.8-mm ML, aged 50 days) with only one dorsal
mantle cavity (right). Individuals not at the same scale. (Original drawing from J. Corbera.)
semigelatinous deep-sea cirrate octopods (Collins & Villanueva 2006). The funnel, pallial aperture and interbrachial webs of octopus paralarvae are proportionally more developed than those of
squids. Their arms are also larger, increasing in relative length as the animal grows. During a jetting
cycle, the contraction of the mantle and collar muscles produces high hydrostatic pressure inside
the mantle cavity, which generates a propulsive jet of water through the funnel, resulting in the displacement of the animal. During the first days after hatching, the volume occupied by the internal
yolk reserve in cephalopods probably reduces the effective water volume available for ventilation
and jet propulsion. Using ultrasonography and optical methods to estimate ventilation volume of
Octopus vulgaris paralarvae, Tateno (1993) showed that fraction ejected during the first 2 wk of life
increased with growth.
Swimming in octopus paralarvae differs from other planktonic and pelagic cephalopods due
to the particulars of their morphology. Octopus paralarvae lack fins and the vanes or keels found
on the lateral arms of many decapodiform cephalopods (i.e., ommastrephid squids). The body of
planktonic octopus paralarvae tends to be globular and less elongate than in planktonic squids,
which typically have a shell (‘gladius’) that guides mantle contraction during jet propulsion. In
addition to the ventral mantle cavity, octopuses also have a dorsal cavity, absent in most squids
(Figures 40 and 41). The relative percentages of water that occupy the dorsal and ventral cavities
during the jetting cycle in octopus paralarvae are still unknown and need to be quantified in order
to understand their swimming capacities. Cranchiid squids (Clarke 1962) and pelagic octopods
(Packard & Wurtz 1994) have dorsal and ventral mantle cavities that facilitate sophisticated swimming and manoeuvrability through independent control of both cavities. Swimming behaviour in
octopus paralarvae that hatch at a small size (as in O. vulgaris) modifies as the animal grows from
hatching to settlement. These changes are directly related to morphometric changes, primarily the
strong development of the muscular arm crown (Villanueva et al. 1996). Similarly, differences in
swimming behaviour can be expected for different octopus species according to the specifics of
their hatchling size and body form.
Swimming behaviour of planktonic paralarvae
Hydrodynamic forces probably dictate the swimming capacities and related behaviour of different
species of octopus paralarvae. However, other unknown neurological and/or physiological characteristics may also play roles. The paralarvae of two species groups provide examples of extremes in
form and swimming behaviour: (1) small planktonic hatchlings (ML ~2 mm) with short arms and
~3 suckers per arm (O. vulgaris-type) and (2) large planktonic hatchlings (ML ~6 mm) with long
160
Figure 41 The use of the dorsal and ventral mantle cavities for jet swimming in Enteroctopus dofleini hatchlings. The left individual is shown during the inhalatory phase; note the anterior part of the dorsal mantle and
the ventral mantle cavities expanded by the internal water pressure and the relatively flaccid funnel. The right
individual is in the expulsive phase; note the contracted dorsal and ventral mantle cavities and the rectilinear
funnel due to the expulsion of water from the mantle. (Reproduced with permission from Okubo 1973.)
arms and >10 suckers per arm (Enteroctopus-type). There seems to be a continuum between these
two extremes. Large planktonic hatchlings with short arms have not been described to date.
Using video-recording techniques, the swimming behaviour in Octopus vulgaris was studied
by Villanueva et al. (1996) in groups of individuals aged 1, 15, 30, 42 and 60 days (by which time
they had become benthic). Backwards, squid-like swimming is the predominant type of locomotion
during routine swimming throughout planktonic life, with forward displacement representing only
1% of swimming (excluding prey capture sequences; see ‘Capture of live prey’, p. 144). Cruising
swimming speed increased as animals grew and relative swimming speed in units of octopus length
decreased with size (Figure 42). The mean speed and distance covered during a burst jet cycle
ranged from 41 to 95 mm s−1 and 6 to 23 mm at respective ages of 1 and 60 days. The mean maximum speed reached was 211 mm s−1 for individuals aged 30 days and 4.5 mm in ML. These maximum speed values are similar in range to those observed for hatchling squid paralarvae: 160 mm 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 paralarvae, such as those of the genus Enteroctopus, constant swimming by jet propulsion is intermittently interspersed by descent to the bottom of the rearing tank for
short periods of time, as has been reported for E. dofleini (Gabe 1975, Snyder unpublished manuscript). During the first month of life E. dofleini actively use their arms and tactile discrimination
to collect floating inert food from the water surface film, described by Marliave (1981) as neustonic
feeding (see ‘Capture of inert prey’, p. 146). One of the most extreme examples in a hatchling considered to be planktonic is that of E. megalocyathus, for which hatchlings have a mean of 21 suckers per arm and can swim slowly with loose arms for several hours at a time in the water column,
as well as crawling for short distances on the substratum of the aquaria (Ortiz et al. 2006). When
disturbed, animals responded in two ways: swimming (sometimes ejecting ink) or crawling on the
aquarium substratum with a coordinated action of the arms and displaying expanded chromatophores. Ortiz et al. (2006) suggest that E. megalocyathus hatchlings may reside in the water layer
close to the seafloor, the hyperbenthos (sensu Mees & Jones 1997), for a short period until they
attain a benthic mode of life.
Swimming behaviour of micronektonic paralarvae
Wild observations of paralarvae on moonless nights over deep water (~1 km) in the Coral Sea
found significant differences in swimming behaviour between different species of paralarvae
161
Age (days)
2
10
20
30
40
50
60
240
90
80
ing
70
imm
Sw
60
200
50
40
180
30
20
160
10
0
220
Total length index
Cruising speed (mm• s–1)
100
Crawling
2
2.9
6.4
4.5
ML (mm)
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.)
(M.D. Norman unpublished data). Those paralarvae with short arms and near-spherical bodies (i.e.,
Figure 9) showed relatively slow swimming speeds. Longer-armed, more elongate species (such as
Callistoctopus sp.; Figure 4 top) swam faster and took on an elongate form superficially similar to
small ommastrephid squid also occurring in the same environment (Callistoctopus sp.; Figure 43).
This body form may partially explain why certain micronektonic paralarvae are able to delay
settlement (see ‘Prolonged paralarval stages’, p. 182). From hydrodynamic and energetic perspectives, these paralarvae may be adopting a squid-like strategy: an elongate mantle that enables more
energy-efficient jet swimming. This form of locomotion is not possible as a prolonged mode of
swimming for settled, benthic octopuses because their small mantle volume cannot power the displacement of relatively long and heavy muscular arms (Wells et al. 1983b, 1987) (see also ‘The
settlement process’, p. 176).
In addition to jet propulsion, long-armed large paralarvae such as Macrotritopus defilippi have
been observed in the wild drifting with all arms spread out radially. The animal seems almost
neutrally buoyant, remaining almost stationary with little or no jetting (Hanlon et al. 1985). These
animals also combined these modes of locomotion with slow backwards jet swimming with the
arms trailing in a V and the tips usually curled, but also with fast backwards jets when disturbed
by a diver. It is remarkable that these animals were also observed to crawl over a coral substratum
and as described by Hanlon et al. (1985, p. 238): “…they spread the arms radially and landed oral
surface first. Both animals quickly slid into holes and disappeared from view. It was clear that the
substrate was not alien to them.”
More research is necessary to understand swimming behaviour in octopus paralarvae. Some
similarities can be expected with the complex slow-swimming behaviour of small squids that employ
various fine-scale adjustments, such as manipulating funnel diameter during jetting, altering arm
162
Figure 43 (See also Colour Figure 43 in the insert.) Unidentified paralarva of the genus Callistoctopus from
the Coral Sea, Australia, showing elongate form when swimming. Photograph taken in situ while night diving on a moonless night at ~10 m deep over a seafloor depth of 450 m at Osprey Reef, Coral Sea, Australia.
(Photo: M.D. Norman.)
position and swimming in different orientations to increase swimming performance (Bartol et al.
2001). In addition, the proportion of water volume ejected from the mantle is expected to change
throughout paralarval stage, as occurs in hatchling squid, for which this volume is proportionally
higher compared with later growth stages (Thompson & Kier 2001a,b, 2006).
Crawling
Crawling behaviour is readily observed in hatchling paralarvae contained in captivity. The physical
constraint of aquaria may account for some or all crawling behaviour over aquaria surfaces (i.e., Joll
1978, Ambrose 1981). However, in hatchlings of some species such as Enteroctopus megalocyathus
(see p. 161), a combination of swimming and crawling has been reported (Ortiz et al. 2006). An
adhesion reflex, in which the suckers are pressed against a surface and coordinated crawling takes
place, can be experimentally induced in planktonic hatchlings of Scaeurgus unicirrhus by reducing
the space available down to a droplet of water (Boletzky 1977b). Crawling of octopus paralarvae
on hard substrata has also been observed in the wild. Paralarvae of at least three species attracted
using lights at night over deep water in the Coral Sea readily adhered to any hard surfaces, particularly ropes, buoys, light traps, divers and camera housings (M.D. Norman personal observation). On
several occasions paralarval numbers of one unidentified species were so numerous that thousands
of animals completely covered the mooring lines between the ship and a boat tender, while all divers returning from night dives were covered in crawling paralarvae. Rafting behaviour has been
reported for both paralarval (Smale & Buchan 1981) and adult octopuses by which they attach on
floating surface objects. Thiel & Gutow (2005) listed 11 species of cephalopods rafting on wood or
macroalgae, including adult Octopus bimaculatus, O. bimaculoides, O. micropyrsus, O. variabilis
and O. vulgaris. This may have advantages both as a means of passive transport/energy conservation and as potential food-aggregating structures.
163
Responses to light and gravity
Positive phototaxis seems to be a common response to light in octopus hatchlings as well as in
some later paralarval stages. Under laboratory conditions, positive phototaxis has been reported
for hatchlings of several species, including Amphioctopus burryi (Forsythe & Hanlon 1985),
Enteroctopus dofleini (Ruggieri & Rosenberg 1974, Yamashita 1974, Okubo 1979), Macroctopus
maorum (Batham 1957), Octopus bimaculatus (Ambrose 1981), O. cyanea (Dew 1959), O. mimus
(Montoya 2002), O. vulgaris (Vevers 1961, Villanueva 1995, Nixon & Mangold 1998), O. huttoni (as
Robsonella australis) (Brough 1965) and Wunderpus photogenicus (Miske & Kirchhauser 2006).
In contrast, negative phototaxis and an avoidance of strong light intensity has only been observed
for hatchlings of one species, Octopus cf tetricus (Joll 1976) — interesting behaviour that requires
further research.
In interpreting some hatchling behaviours, discrimination between positive phototaxis and negative geotaxis can be difficult. Laboratory-hatched Enteroctopus dofleini that were transported to a
hatching site in the field immediately began swimming up towards the surface (High 1976). Octopus
bimaculatus hatched in the field during the daytime also swam upwards to depths of 1–5 m below
the surface (Ambrose 1981). Rising hatchlings can be interpreted as either positive phototaxis (heading towards surface light) or negative geotaxis (resisting gravity and rising towards surface waters).
Newly hatched squid Loligo pealei also rise to surface waters. Sidie & Holloway (1999) found use
of lights at the bottom of experimental tanks could not prevent the vertical movement of the squid
paralarvae towards the surface in the first 6–12 h after hatching. This suggests that negative geotaxis
is the stronger factor in this behaviour. Similar processes may occur in octopus paralarvae.
Migration to surface waters could aid hatchling dispersal because surface currents may carry
the paralarvae beyond the natal environments. Movement to surface waters may also enable access
to neustonic prey such as crustacean zoeae. For tropical octopus species on isolated coral reefs, surface currents may transport hatchlings away from high-predator reef environments to the comparative safety of open ocean, potentially aiding in gene flow between coral reefs and atolls.
Positive phototactic behaviour has been used to collect octopus paralarvae at night in the field.
Using light traps, Moltschaniwskyj & Doherty (1995) collected 2066 individual octopus paralarvae
on the Great Barrier Reef, estimating this number to be around half the total number of planktonic cephalopods attracted to their lights. The strong response of octopus paralarvae towards light
may be higher than for other planktonic cephalopods. Light attracts not only hatchlings, such as
Enteroctopus dofleini collected on surface waters (Packard 1985), but also relatively large 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 paralarvae collected using lights at night.
Under laboratory conditions, positive phototaxis appears to be strongest at the time of hatching
and can be used to concentrate paralarvae within rearing tanks (i.e., feeding or transferring them
to other reservoirs). Positive phototaxis appears to decrease as the paralarval octopus approaches
settlement (Villanueva 1995). However, there are no quantified studies on this subject. FernándezLópez et al. (2005) tested the influence of light intensity (1000, 3000 and 6000 lux) on the survival
and growth of captive-reared O. vulgaris paralarvae, obtaining the best results with the highest light
intensity treatments during daylight periods. Okumura et al. (2005a) suggest that the survival rate
of O. vulgaris paralarvae was negatively affected by an unstable photoenvironment in captive-bred
paralarvae exposed to variable intensities of natural light (due to cloud drift and intermittent full
sun). Changes in light tolerance throughout the planktonic stage were also observed by S. Snyder
164
165
Horizontal
Undersea
laboratory
Vertical
Oblique
Net ∅ 130 cm
Conical net ∅
130 cm
Light
8 m2 RMT
and a 1-m2
ring net
2- and 4-m2
ring nets
Net ∅ 100 cm
Enteroctopus
dofleini
Macrotritopus
defilippi
Macrotritopus sp.
Octopus cyanea
Octopus
rubescens
ROV
Horizontal
Net ∅ 100 cm
Enteroctopus
dofleini
Individuals
observed
Horizontal
Horizontal
and
oblique
towns
Horizontal
Variety of
plankton
nets
Eledone cirrhosa
Np
Gear
Plankton net
Species
Horizontal
or vertical
towns
0–400
From 100
to surface
20–760
0–2000
15–40
0–20 over
depths of
20–200
Surface
20–760
0–200
0–200
Depth
range (m)
Day
Np
Day
Day and
night
Night
Night
Day and
night
Np
Np
Np
Day/
night
40
197
388
161
16
594
17
790
62
118
Number of
individuals
collected
Higher between 300 and
400 m; to 0.2 ind h−1
observed
82% collected <50 km
offshore
Higher at <100 m; to 0.9
ind h−1 of tow
96% ind collected between
0 and 100 m during
daylight
Absent on the surface,
captured between 9 and
21 m subsurface
Mean of 6–8 ind by
positive tows
Higher at <100 m; to 0.9
ind h−1 of tow
Midwater or near the
bottom, rarely at surface
Largest individuals near to
the seafloor
Abundances
Found at bottom
depths less than
300 m
Individuals
forming shoals
Found at bottom
depths less than
400 m
Collected in
temperatures of
2.6–6.7°C
Collected from
early June to
mid-August
Large
individuals,
7–15 mm ML
Represented
12% of the total
cephalopods
collected
Higher from
May to August
Higher from
May to June
Observations
Hunt 1996
NE Pacific
Hawaiian
Islands
NE Pacific
Lu & Clarke
1975 (as
Scaeurgus
unicirrhus)
Bower et al.
1999
Green 1973
Hanlon et al.
1980b, 1985
Kubodera 1991
Yamashita &
Torisawa 1983
Green 1973
Collins et al.
2002
Stephen 1944
Reference
NE Atlantic
NE Atlantic
North
Pacific
NW Pacific
NE Pacific
NE Atlantic
NE Atlantic
Geographic
area
Table 5 Sampling methods, number of individuals collected and abundances of Octopodidae paralarvae from the literature
166
Drifting
and
anchored
light traps
0–20, few
at 100
Near the
bottom at
35–105
Surface
and near
the
bottom at
36–85
0–300
Night,
around
new
moon
Np
Day and
night
Np
Day and
night
Mostly
diurnals
Np
Day/
night
2066
1439
584
96
641
159
69
Number of
individuals
collected
Higher in subsurface of
Great Barrier Reef
Lagoon, low on the shelf;
0.07–5.57 ind h−1
Abundant in coastal bays
Abundance depending on
the strength of the upwelled
water; to 8 ind 1000 m−3
In surface during night, near
the bottom at day; from
0.01 to 1 ind 1000 m−3
Abnormal high sea
temperatures associated
with abundance on the
northern species range
No specimens collected in
surface during the day;
higher abundances inshore
at night and offshore
during day; from 0.03 to
0.21 g 1000 m−3
Higher at night; 5–87 ind
1000 m−3
Abundances
Note: ML, mantle length; Np, not provided; RMT, rectangular midwater trawl; ROV, remotely operated vehicle.
Light trap
Octopodidae
Oblique
Horizontal
Bongo net ∅
75 cm
8-m2 RMT
and Bongo
60-cm ∅
Horizontal
Horizontal
Bongo net ∅
60 cm
Bongo net ∅
75 cm
Surface
and
0.2–4
from the
bottom
Horizontal
100 × 100 cm
square net
Surface
0–100
Np
Depth
range (m)
Plankton net
Gear
Octopodidae
Octopus vulgaris
Species
Horizontal
or vertical
towns
Upwelling pulses
positively
related with
paralarval
abundance
Octopodidae
represented
60% of total
cephalopods
Octopodidae
represented
53% of total
cephalopods
NW Pacific
No differences in
size between
individuals
collected in
surface or
bottom layers
Two hatching
peaks: spring
and fall, higher
in fall
Great
Barrier
Reef
SW Atlantic
NE Atlantic
NE Atlantic
NW Pacific
NE Atlantic
Geographic
area
Found at bottom
depths less than
155 m
Observations
Moltschaniwskyj
& Doherty
1995
Rodhouse et al.
1992
Otero 2007
González et al.
2005
Sakaguchi et al.
1999
Takeda 1990a
Rees 1950
Reference
Table 5 (continued) Sampling methods, number of individuals collected and abundances of Octopodidae paralarvae from the literature
Table 6 Examples of large Octopodidae individuals collected or observed on the water column
or surface
Measured
fresh or
preserved
Species
Size
Amphioctopus
burryi
13–15 mm ML
F
Light
16 mm ML
F
27 mm TL
Callistoctopus
macropus
Eledone
cirrhosa
Enteroctopus
dofleini
Euaxoctopus
panamensis
Macrotritopus
defilippi
Macrotritopus
sp.
Octopus
rubescens
Depth (m)
Geographic
area
Reference
NW Atlantic
Light
21, under
surface
Surface
P
Trawl
Np
NE Atlantic
Hanlon et al.
1980b
Forsythe &
Hanlon 1985
Rees 1955
29 mm TL
P
Plankton net
Np
NE Atlantic
Rees 1956
To 14 mm ML
33–73 mm TL
To 14 mm ML
P
P
P
20–760
Surface
Surface
NE Pacific
NW Pacific
N Pacific
Green 1973
Yamashita 1974
Kubodera 1991
11 mm ML,
~ 43 mm TL
12–15 mm ML
P
Net ∅ 100 cm
Larval net
Conical net ∅
130 cm
IKMT
0–500
F
Light
1.3–11 mm ML
P
Bongo net
15–40, under
surface
0–200
Central E
Pacific
NW Atlantic
Nesis & Nikitina
1991
Hanlon et al.
1980b, 1985
Nesis & Nikitina
1981
9–13.5 mm ML
F
Plankton net
100–300
2.5–10 mm ML
F
RMT & ring
net
0–100
NE Atlantic
127 mm TL
F
Light
15–25 mm ML
P
IKMT
0–38, under
surface
0–770
Hawaiian
Islands
NE Pacific
NE Pacific
Not measured
‘Octopus
teuthoides’
Octopus
vulgaris
Octopodidae
Gear
Observed
from ROV
To 16 mm ML
P
Light
60 m in an
area of
728 m depth
Surface
50 mm TL
F?
Light
Surface
14 mm ML
P
Surface
56 mm TL
NW Atlantic
Atlantic and
Indian
Oceans
Mediterranean
and Atlantic
Joubin &
Robson 1929
(as M. danae)
Lu & Clarke
1975 (as
Scaeurgus
unicirrhus)
Brower 1981
Young 1972
(as Octopus sp.)
Present study,
see Figure 44
Central E
Pacific
Mediterranean
Norman &
Sweeney 1997
Spartá 1933
Hawaiian
Islands
Berry 1914
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.
167
(unpublished manuscript) in captive-reared Enteroctopus dofleini. Light intensity was reduced during the second half of the planktonic phase because high light levels resulted in premature settlement
for a large number of individuals. Light seems to play an important role in the predatory behaviour of
octopus paralarvae although light may not be essential for capturing prey in O. vulgaris hatchlings
(Márquez et al. 2007). The behaviour and activity patterns of octopus paralarvae in the absence of
light (or in low light levels) are practically unknown and require detailed research. Tateno (1993)
suggested that ultrasonography can be used in the laboratory as a non-invasive technique to record
octopus paralarval activity in total darkness. This technique may offer new insights.
It must be noted that all behavioural observations of captive octopus paralarvae are severely
limited by the removal of a critical attribute of the natural environment of these animals — a realistic water column. Rearing tanks severely limit the capacity of the octopus paralarvae to adjust their
depth in response to experimental factors such as changing light levels, prey, predators and tidal or
lunar cycles. For example, natural variability in light levels may be at significantly lower levels than
in experimental situations such as full sunlight on shallow rearing tanks.
Immediately following settlement, octopuses show strong negative phototaxis and reclusive behaviour, as observed under laboratory conditions in Octopus vulgaris (Itami et al. 1963,
Villanueva 1995) and O. cyanea (Wells & Wells 1970), a behaviour that is more typical of adult
benthic octopuses. There are exceptions, however, because some octopuses possess ambiguous phototactic behaviour. During the early post-settlement period, 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 numbers, as for an undescribed species of Callistoctopus in New Caledonia (G. Boucher personal communication 1997).
Defences
Relatively high swimming speed may prevent paralarval capture by some predators. Bursts of jet
swimming in O. vulgaris paralarvae can reach a mean swimming speed of 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 paralarvae and may maximize dispersion of the individuals from the egg mass and minimize attraction of predators to the
hatching site (Villanueva et al. 1996). In large paralarvae of Macrotritopus defilippi, inking and fast
backward jetting have been observed as a response to the approach of divers, with 0.5-m traverses
per jet outswimming a diver over 3 m of distance, followed by slow backward swimming to the
seafloor (Hanlon et al. 1985).
In the open ocean, the most common form of defence by octopus paralarvae is likely to be a
dive response, into the relative safety of deeper darker waters. Such behaviour has been observed
in Macrotritopus defilippi (Hanlon et al. 1985), en masse for large Octopus rubescens paralarvae
in Monterey Bay, California, in response to the approach of a deep-water remotely operated vehicle
(ROV) (Hunt 1996) and for unidentified octopus paralarvae in the Coral Sea (M.D. Norman personal
observation). This escape response is common to many pelagic, shelled molluscs (both veliger larvae
and holopelagic pteropods) (Lalli & Gilmer 1989). In these molluscs, retraction of locomotory wings
or ciliated podia combines with shell weight to enable rapid sinking. Because they have a lower specific gravity, octopus paralarvae use funnel jetting as additional propulsion to aid rapid descent.
When the proportionally large and simple chromatophores of octopus paralarvae are contracted,
the animals become nearly transparent, all except for the eyes, ink sac and visceral mass. These
opaque organs are typically bound within a silvery membranous layer containing reflective iridophores. This combination of transparency and reflective body organs is a camouflage adaptation for
168
life in the water column of open ocean where animals are vulnerable to visual predators that detect
prey by looking for silhouettes or outlines. Transparency is a remarkable characteristic of many
oceanic zooplankton, an attribute uncommon in other aquatic habitats. It is generally accepted that
transparency is a successful form of camouflage from visual predators and/or prey in the optically
featureless pelagic environment (Johnsen 2001).
Behavioural responses of planktonic Octopodidae to predators have not been recorded in the
field or laboratory. Chromatophores and ink sac are fully functional in octopus paralarvae from
hatching. Chromatophore patterns may be used in concert with ink release to distract potential
predators, as occurs in adult octopuses (Hanlon & Messenger 1996). Octopus paralarvae are likely
to be particularly vulnerable to predation during prey capture because their motion is slowed and
their attention is focused on prey. At this time, detection of potential predators may be lessened
or suspended. During prey capture sequences, octopus paralarvae expand their chromatophores,
changing to a dark coloration (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 paralarvae to predators (see Figure 30).
Dark colouration may be used in concert with ink injection. As a series of ink decoys is released
by a fleeing dark paralarva, rapid transformation to a transparent form with a rapid shift in trajectory may deceive or confuse a visual predator (Boletzky 1987). This behaviour is called a blanchink-jet manoeuvre and is found in many cephalopods (Hanlon & Messenger 1996). A pursuing
predator continues the chase trajectory and finds itself in empty water. Functional ink ejection has
been observed in captive hatchlings, such as Enteroctopus dofleini (Yamashita 1974, Gabe 1975,
Okubo 1979), Octopus cf tetricus (Joll 1978) and O. laqueus (Kaneko et al. 2006) and in the wild for
Macrotritopus defilippi (Hanlon et al. 1985) and in unidentified paralarvae (M.D. Norman personal
observation) in response to the approach of divers.
Potential schooling behaviour has been reported for the micronektonic paralarvae of one species, Octopus rubescens, off Monterey Bay, California (Hanlon & Messenger 1996). Figure 44
shows such an aggregation, photographed from a deep-water ROV in this region. Hunt (1996)
reports high densities of paralarvae of this species at depths of 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.)
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Predators on egg masses and paralarvae
As brooding females of most octopus species continually guard their eggs at a fixed permanent site,
Ambrose (1988) proposed that they are more susceptible to predation. As the duration of brooding
and embryonic development increases with decreasing temperatures, winter-brooding females thus
have an even higher vulnerability to predation. Ambrose recorded 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 paralarvae. Longnose
lancetfish (Alepisaurus ferox) actively prey on pelagic cephalopods, including octopus paralarvae.
Stomach contents for this species examined from around the Pacific Ocean (Rancurel 1970) included
seven individuals of Macrotritopus forms (6.5–18 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 paralarvae (Octopodidae) were present in 11% (Rancurel 1970)
or 12.5% (Okutani & Kubota 1976) of the A. ferox stomachs containing cephalopods. Octopod
paralarvae not sorted by families occurred in 3% of the stomachs of this fish in western equatorial Indian Ocean (Potier et al. 2007). The albacore (Thunnus alalunga) is an active predator of
pelagic and planktonic cephalopods. Stomach contents of this species collected in the north-east
Atlantic during July and October included seven young Eledone cirrhosa (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 paralarvae in the diet of oceanic loggerhead sea turtles (Caretta
caretta) in the central north Pacific. All proved to be octopodid paralarvae (D.M. Parker personal
communication 2006). Ephyra larval stage of jellyfish scyphomedusae has been observed feeding
on unidentified octopod paralarvae (Figure 45) from plankton samples collected off Lizard Island,
Great Barrier Reef (P. Parks personal communication 2007).
In littoral waters, fishes are also expected to be the main predators of octopus paralarvae but, as
far as we know, no references on this subject have been published and information only comes from
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Figure 45 (See also Colour Figure 45 in the insert.) Ephyra larval stage of jellyfish scyphomedusa feeding
on unidentified octopod paralarva. Specimens collected using a plankton net at about 180 m depth, off Lizard
Island, Great Barrier Reef. (Data and image reproduced with permission from Peter Parks/imagequestmarine.
com.)
opportunistic personal observations. Fishes are attracted to octopus egg masses during hatching
and have been observed during daytime at a short distance from the egg mass, preying on Octopus
vulgaris individuals that have hatched seconds or minutes before, as has been observed for the
Mediterranean dusky grouper (Epinephelus marginatus) at 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 paralarvae. Under laboratory
conditions, attacks on conspecifics have been reported for O. vulgaris paralarvae (Boletzky 1987,
Villanueva 1995). However, these attacks do not result in cannibalism, as has been observed for
juvenile and subadult benthic stages of some octopus species (i.e., Itami et al. 1963, DeRusha et al.
1987, Aronson 1989, Cortez et al. 1995b).
Species identification and diversity
Prior to the review paper of Hochberg et al. (1992), morphological descriptions and identification
tools for octopus paralarvae were few and widely scattered in the literature. A number of researchers such as Berry (1914), Chun (1915), Naef (1923), Degner (1925), Robson (1929) and Rees (1954)
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along with subsequent researchers in the 1970s and 1980s described individual paralarvae amongst
regional or broader treatments of the family. Hochberg et al. (1992) were the first to compile a suite
of diagnostic characters such as founder chromatophore patterns, sucker attributes, arm formulae
and body shape.
Table 1 lists those species of the family Octopodidae that are known (or presumed) to produce
planktonic paralarvae. Three categories of species are listed: (1) those for which planktonic 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 paralarvae are described. The second category typically comes from studies
of preserved material for which laid eggs or mature ovarian eggs form the basis of the egg-type
discrimination (sensu Boletzky 1977a, 1978–1979). The third category comes from dissection of
preserved submature females as the only material available to provide any indication of early lifehistory strategy.
In only a few studies have paralarval forms been successfully raised through to settlement,
enabling identification of the post-settlement form. A good example is the ‘Macrotritopus’ problem. In 1922, a distinctive paralarval form with greatly elongated third arms formed the basis of
the generic name Macrotritopus Grimpe, 1922. On the basis of apparent left-handed male sexual
modification (hectocotylization) in one specimen, Rees (1954) attributed all reports of this paralarval form to the seamount and continental slope genus, Scaeurgus. In parallel studies in the United
States (Hanlon et al. 1980a, 1985) and Soviet Union (Nesis & Nikitina 1981), Macrotritopus-type
paralarvae were raised to adulthood and identified as the long-armed species Octopus defilippi
(now treated as Macrotritopus defilippi; see Norman & Hochberg 2005a). As representatives of this
distinctive paralarval form have been found in the Pacific and Indian Oceans, where M. defiliippi is
not reported, it is possible that this distinctive paralarval form may represent more than one species
(Hochberg et al. 1992).
Other historical conundrums also await resolution. Octopus teuthoides Robson, 1929 was coined
for a distinctive elongate paralarval form that received considerable attention in subsequent literature (see Norman & Sweeney 1997, Toll & Voss 1998). The adult form, however, still awaits identification. At least 10 other octopodid taxa have been formally described on the basis of paralarval
or juvenile material (Norman & Hochberg 2005a). For many species of benthic octopuses, nothing
is known of egg size or juvenile stages. In combination with the many species yet to be described
by science, particularly in the tropical Indo-Pacific region (Norman & Hochberg 2005a), we can
be confident that the number of known paralarval species is far outweighed by the forms yet to be
defined/described. In regions with well-known faunas or lower diversity in octopodid species, 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
paralarvae in material collected around the Hawaiian Islands. At that stage, only eight species of
benthic octopus were recorded from these islands, with some of these species being large-egg type
(see Norman & Hochberg 2005a). Hence the estimates of species number in the region appeared
to be a significant underestimate. Subsequent studies have found new small-egg species in the
region, such as Amphioctopus arenicola (Huffard & Hochberg 2005), and more await description
(F.G. Hochberg unpublished data).
A revolution is brewing, however, for the identification, description and discrimination of paralarval forms. With the advent of cheap, reliable and accurate DNA sequencing technologies and
sequence databases such as GenBank, it will be possible to definitively identify paralarvae. In
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combination with high-resolution and accurate photography, it will enable development of comprehensive species identification keys for octopus paralarvae. The capacity to identify paralarval stages
will also enable a much more thorough understanding of development and morphometric changes
associated with growth and life in the plankton. Until this process is under way, some caution must
be taken with taxonomic identifications of wild-caught paralarvae because there is potential for
misidentification or oversimplification of the diversity of taxa represented in such samples.
Distribution patterns
Sampling methods
Most benthic octopus species with planktonic stages spawn in shallow, rocky or coral substratum areas and consequently hatchlings can be abundant near the coast. Surveys targeting octopus
paralarvae such as Octopus vulgaris have been done in shallow bays and littoral waters (Takeda
1990a, Sakaguchi et al. 1999, González et al. 2005, Otero 2007). Oceanic plankton sampling is usually rich in oegopsid squid paralarvae and poor in octopuses, with some exceptions. For example,
oceanic surveys in the north Pacific sampled large volumes of water and captured large numbers
of Enteroctopus dofleini paralarvae (Green 1973, Kubodera 1991). Table 5 shows literature records
of the depth ranges and different sampling methods, primarily nets and light traps, used to collect
octopus paralarvae.
Classic bongo nets, conical nets of different sizes, Isaacs-Kidd midwater trawls (IKMTs) and
rectangular midwater trawls (RMTs) have been used to collect octopus paralarvae (see Table 5).
Piatkowski (1998) reviewed the advantages of targeted sampling using modern opening/closing nets
and discussed problems such as net speed and net avoidance by cephalopod paralarvae. The strong
positive phototaxis of octopus paralarvae (see ‘Responses to light and gravity’, p. 163) has been used
during night surveys to attract and collect large paralarvae inhabiting surface or near-surface waters
(see Table 6). Light traps proved to be a powerful method for collecting large numbers of octopus
paralarvae (Moltschaniwskyj & Doherty 1995) but little is known of their sampling efficiency, sampling bias due to water clarity and species-specific capture selectivity. An advantage of this method
is the collection of live animals in excellent conditions for experimental work. For example, Hanlon
et al. (1980a, 1985) resolved the ‘Macrotritopus’ taxonomic problem (see also Nesis & Nikitina
1981) by collecting live ‘Macrotritopus’ paralarvae individuals using light and rearing them to the
adult stage in the laboratory, where they were identified as Macrotritopus defilippi.
Geographic range
Total geographic range of paralarvae of benthic octopuses is poorly known for most species. As
for many attributes of octopus paralarvae, it is probably best known for Octopus vulgaris and
Enteroctopus dofleini (see Table 5). Taxonomic problems for the family Octopodidae are sufficient that accurate distributions for adult octopuses are not available for most species (Norman &
Hochberg 2005a), let alone for paralarvae. Greater resolution may become possible when molecular
tools enable accurate species identifications and hence collation of accurate geographic distributional data.
The greatest geographic range for octopus paralarvae is likely to occur for widely distributed
Indo-West Pacific coral-reef species such as Octopus cyanea and Callistoctopus ornatus. These
small-egg species have distributions spanning two thirds of the globe’s circumference (Norman
1991, 1993). Van Heukelem (1973) reported captive Octopus cyanea paralarvae that lasted in the
water column for 21 days before dying. Norman (1991) suggested that the paralarval stage would
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have to be significantly longer for this species (up to months, as has been recorded for the similar
O. vulgaris paralarvae; see Table 3) to explain the gene flow necessary between the widely spaced
coral-reef habitats in the tropical Indian and Pacific Oceans.
At this stage, there are no reports of octopus paralarvae from polar regions. Benthic octopuses
at these high latitudes exclusively produce large-egg hatchlings as in Benthoctopus (Nesis 2001),
Bathypolypus (Muus 2002, Barratt et al. 2007) and Pareledone (Allcock 2005), as do many other
polar marine invertebrates that show high parental investment in a few, large and well-developed
young (i.e., Poulin & Feral 1996). The largest planktonic hatchlings in the family Octopodidae
belong to the genus Enteroctopus (see Table 4), cold-adapted species distributed in high latitudes.
E. dofleini is distributed from littoral depths to more than 1500 m (Hartwick 1983, Hochberg 1998)
and Kubodera (1991) collected E. dofleini paralarvae in the north Pacific at almost 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 paralarvae’, p. 161). In
common with the Octopodidae of high latitudes, deep-sea benthic octopuses produce large eggs and
have benthic hatchlings (Voss 1988). The notable exceptions appear to be members of the middepth
genera Scaeurgus and Pteroctopus (Table 1), which have small-type egg sizes and for which little is
known of their paralarvae (Bello 2004).
Horizontal dispersal
Horizontal movement dictated by oceanographic conditions in upwelling areas has been suggested
to be of great importance in the distributions of Octopus vulgaris paralarvae (Demarcq & Faure
2000, Faure et al. 2000, 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
paralarvae by limiting offshore paralarval dispersion. Faure et al. (2000) suggested that offshore
paralarval dispersion can be a negative factor in paralarval survival due to the wind-induced breakdown of the retention areas during autumn.
These hypotheses were partially corroborated by González et al. (2005) and Otero (2007), who
found that high abundances of O. vulgaris paralarvae were correlated with high upwelling retention
indices in the north-west Iberian coast, the northern limit of the Canary current. However, nearly
all paralarvae collected by these authors were individuals with three suckers per arm, suggesting
that they were hatchlings incorporated into the relatively low-turbulence water mass. The effect
of upwelling intensity on fish and invertebrate larval distributions varies with the behaviours and
vertical distributions of the larvae, and careful sampling is necessary to determine the contribution
of upwelling to the offshore transport of larvae as a cause of variations in larval settlement levels
(Shanks & Eckert 2005, Shanks & Brink 2005).
The paralarvae of species with large hatchlings such as Enteroctopus dofleini seem to be distributed in both shallow and oceanic waters, having been found off shore in the north-east Pacific
Ocean in higher abundances between the surface and 100 m over bottom depths of <200 m (Green
1973), as well as over the continental shelf in the north-west Pacific Ocean (Yamashita & Torisawa
1983). However, significant numbers of E. dofleini paralarvae have also been encountered in more
distant offshore waters (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 paralarvae, as has been
observed in other shallow-water and bottom-spawning cephalopods such as loliginid paralarvae
(Zeidberg & Hamner 2002).
Vertical distribution and abundances
Few studies have recorded vertical daily cycles of octopus paralarvae, most being focused on
Octopus vulgaris. In shallow coastal waters, paralarvae of this species are nearly absent from the
sea surface during daytime and present from the seafloor to the surface at night, with higher abundances of hatchlings (easily recognized by their three suckers per arm) found near the surface
at night (Takeda 1990a, Sakaguchi et al. 1999, Otero 2007) (Table 5). The hatchling individuals
probably come directly from egg masses in the rocky substrata of the shallow waters sampled. Diel
changes in the open ocean and for older paralarvae are practically unknown and need to be investigated through use of high-resolution discrete-depth sampling.
Sampling between 0 and 2000 m depth in the north-east Atlantic, Clarke & Lu (1975) collected the highest number known to date of Macrotritopus paralarvae (n = 161). Most (73%) of
Macrotritopus sp. collected were concentrated between 0 and 50 m depth and no diel migration was
detected. However, some vertical movements to deep waters may exist because Rees (1954) reported
a Macrotritopus individual collected between 800 and 1500 m, Clarke (1969) noted an individual
collected between 460 and 510 m and Clarke & Lu (1975) recorded one specimen between 1000
and 1250 m depth.
Qualitative observations of paralarval numbers at night in the open ocean of the Coral Sea
found much higher numbers of octopus paralarvae on moonless nights compared with moonlit
nights (M.D. Norman personal observation). Hunt (1996) found that Octopus rubescens paralarvae
were most abundant at depths of 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 paralarvae over settled areas
like seamounts for deeper-water species such as Scaeurgus unicirrhus. Paralarvae presumably
belonging to this species have been collected from the Great Meteor Seamount, north-east Atlantic,
the only cephalopod paralarvae related to bottom-dwelling adults collected over this seamount
(Diekmann et al. 2006). Endemism and seamount associations of members of this genus have been
discussed elsewhere (Norman et al. 2005).
Factors influencing differences in abundances between hatchlings and older paralarvae are
poorly known. Only 7% of 643 Octopus vulgaris paralarvae collected by Sakaguchi et al. (1999)
had more than three suckers per arm (= sucker number at hatching; see Table 4), and only 4% of 780
Enteroctopus dofleini individuals collected by Green (1973) in oceanic waters were >6 mm ML. In
the first instance, the abundance of small animals suggests that mortality rates are higher during
the early paralarval stages. However, other factors cannot be discounted. Diversity in sizes may be a
product of cohorts with differing growth rates, as has been observed in same-age cohorts of several
octopus species (Van Heukelem 1976, Forsythe 1984). Horizontal displacement of older paralarvae
and/or net avoidance by these larger paralarvae with faster swimming speeds and higher sensory
development may also be a factor.
The potential influence of sensory systems on paralarval distributions is unknown. For example, the use of sound by cephalopod paralarvae as an orientation cue in relation to reefs cannot be
excluded, as has been observed for reef fishes and crustacean larvae (Montgomery et al. 2006), potentially influencing their settlement distribution. Octopuses have well-developed mechanoreceptors
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analogous to the receptors of fishes (see ‘Sensory systems’ section, p. 126), capable of detecting low
frequencies; however several studies suggest that cephalopods cannot detect underwater sound or
vibrational stimuli much above 100 Hz (Packard et al. 1990, Budelmann et al. 1997).
Relationships between paralarval and adult populations
Seasonal reproduction patterns of each species will dictate the presence of the different paralarvae
in the plankton throughout the year. Maximum abundances of Octopus vulgaris paralarvae are
recorded during summer and autumn (Rees 1950, Rees & Lumby 1954, Takeda 1990a, Sakaguchi
et al. 1999, 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 paralarvae of this species will practically
disappear from the plankton during winter and spring.
Variability in life span and growth in benthic octopuses with or without planktonic stages is
influenced by many factors, of which temperature is probably the most important (Semmens et al.
2004). In benthic octopuses with planktonic stages, under laboratory conditions, the duration of the
life cycle including embryonic development ranges from 6 to 12 months in pygmy octopuses such
as O. joubini (Forsythe & Toll 1991), nearly 1 yr in O. vulgaris (Iglesias et al. 2004) and 3.5 yr in
the large cold-adapted species Enteroctopus dofleini (S. Snyder unpublished manuscript). In the
short-lived species, pulses of recruitment can be related directly between young stages and adults
of the following year. For a few species, there is some support for a relationship between the success of the paralarval population and adult abundances. After a 6-yr field study, Ambrose (1988)
concluded that the primary regulatory processes of a subtidal population of Octopus bimaculatus
in the north-east Pacific Ocean appeared to take place in the paralarval and juvenile stages. The
importance of early stages was supported in Ambrose’s study by heavy recruitment of settled individuals in 1 yr leading to unusually high adult octopus densities in the subsequent year. Relatively
large O. vulgaris paralarvae (to 6 mm ML) were collected by Rees (1950) and Rees & Lumby (1954)
in the English Channel. These authors concluded that periodic ‘plagues’ of O. vulgaris during warm
years along the south coast of England (the northern limit of distribution of the species in the northeast Atlantic) resulted from the transport of the paralarvae during the summer months across the
English Channel from southern hatching areas. In coastal upwelling areas of West Africa, catches
of adult O. vulgaris during summer are significantly correlated with the upwelling intensity during
the previous winter, indicating the influence of oceanographic conditions on octopus paralarvae and
juveniles and the subsequent effects on the fished adult populations (Caverivière & Demarcq 2002).
In the same region, exceptional oceanographic conditions favouring paralarval and juvenile survival also seem to be the origin of demographic explosions of O. vulgaris (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
paralarvae (Vecchione 1999, Zeidberg & Hamner 2002).
The settlement process
After a period of constant swimming that ranges from 3 wk to 6 months (depending on the species; see
Table 3), planktonic octopuses undergo a transitional period from a pelagic lifestyle to the predominantly benthic life of the juvenile stage. The end of the planktonic paralarval period in octopuses is not
always abrupt as it is in many other benthic invertebrates with planktonic larval forms. There seem to
be three presettlement strategies, dependent on the species and/or the environmental context:
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1.Species with a short presettlement period. After a short period in contact with hard surfaces
and benthos, paralarvae of these species definitively settle to the seafloor at relatively small
sizes. These young octopuses, considered as juveniles from this point onwards (sensu Young
& Harman 1988), live on the benthos and have similar habits to that of the adults. From an
ecological point of view, at this stage the young animals are equivalent to the hatchlings
of large-egg octopus species that immediately adopt a benthic habit on hatching. A typical
example of such species is O. vulgaris (Villanueva 1995, Nixon & Mangold 1996).
2.Species with an expanded, transitional presettlement period. In these species, a strict
benthic life is gradually adopted, split between swimming and benthic crawling. These
paralarvae can reach a relatively large size in the water column and the animals seem
to live in contact with both the benthos and the water column, as has been suggested for
Macrotritopus defilippi in the western Atlantic (Hanlon et al. 1985) and for Amphioctopus
burryi (Forsythe & Hanlon 1985).
3.Species with a prolonged/suspended paralarval state. Certain paralarvae reach considerable sizes, particularly those occurring in oceanic epipelagic waters. Due to their size
and swimming capacities they can be considered micronektonic paralarvae. These para
larvae have been described as ‘extended pelagic stages’ (Rees 1954) or ‘super-paralarvae’
(Strugnell et al. 2004) and have been suggested to be individuals that delay settlement
due to the absence of suitable habitat, i.e., shallow reefs (see ‘Prolonged paralarval stages:
micronektonic paralarvae’, p. 182). It is also possible that the swimming capacities, behaviour, and the well-developed sensory systems of these micronektonic paralarvae may be
used to actively remain in the epipelagic realm, effectively delaying settlement in order to
exploit resources in this habitat.
The physiological processes and environmental cues that govern the settlement metamorphosis have not yet been described. Only external morphology and behavioural characters have been
reported for this period of dramatic ecological change.
Morphological characteristics at settlement
Major external morphological changes associated with the settlement process are positive allometric arm growth, the addition of new suckers, chromatophore, iridophore and leucophore genesis, the
development of skin sculptural components and a horizontal pupillary response. At the same time,
animals appear to lose the 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 paralarvae have a squid-like form that
gradually changes to the typical octopus form after settlement, due primarily to the notable arm
growth. Benthic juveniles and adult octopods have a relatively small mantle cavity volume and have
to produce high ventilation pressures to generate the necessary thrust for locomotion when they
swim. These morphological constraints appear gradually throughout the planktonic phase and it
is expected that they would progressively dictate the locomotion capacities of the paralarvae and
juveniles. As proposed by Wells (1990), cephalopods will try to escape using jet locomotion whenever possible, particularly adult octopus. During jet propulsion, Wells et al. (1983b, 1987) found
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that the hearts of benthic octopuses cease beating, resulting in oxygen debt, as the venous system
is incapable of retuning blood against the gradients produced by the rise in internal mantle pressure. This makes jet swimming impossible as a regular mode of locomotion for benthic octopuses.
At the end of the planktonic phase, the growth of the arm crown and the expected increase in the
internal mantle pressure necessary for jet swimming have been suggested as factors that may instigate settlement in Octopus vulgaris (Villanueva et al. 1995, 1996). For micronektonic forms such
as Callistoctopus sp., this energetic problem may be solved by adopting the hydrodynamic form of
squids with an elongate, large mantle that enables locomotion by jet swimming in the epipelagic
realm, potentially delaying settlement (see Figure 43).
Under laboratory conditions, presettlement reflexes of Octopus vulgaris paralarvae commence
when ML reaches 50% or less of the total length (Villanueva 1995). This relationship is similar in
Enteroctopus dofleini as settlement takes place when ML and arm length represent approximately 45%
and 55% of total length, respectively (Okubo 1979) (Figures 46 and 47). It is interesting to note that total
length of Octopus vulgaris at settlement (11–13 mm) is not dissimilar to that of the length of Enteroctopus
dofleini paralarvae at hatching (10 mm), a species that under laboratory conditions will settle at total
lengths of approximately 30 mm (Okubo 1979, 1980) (see Figure 48 for species comparisons).
Morphological transformations at settlement are less well known for long-armed paralarvae,
such as members of the genus Callistoctopus (e.g., Figures 4 and 43), Euaxoctopus (Nesis &
Nikitina, 1991) (Figure 5) and Macrotritopus (Rees 1954) (Figure 6). These paralarvae can develop
markedly long arms, particularly one arm pair that can reach up to three times the length of the
others (i.e., for Euaxoctopus, Nesis & Nikitina 1991). This longest arm pair corresponds to the first
pair in Callistoctopus, the second in Euaxoctopus and the third in Macrotritopus (see Figures 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 composition of these expanded arms and body musculature may be an interesting subject for further
research because the arms may be buoyant in a comparable fashion to the elongate ammonia-buoyant arm pairs of squids in the family Chiroteuthidae (Voight et al. 1994). An alternative explanation
may be that this longer arm pair act as analogues of the elongate feeding tentacle pair of squids
and cuttlefishes. Further research on how octopus paralarvae use their two mantle cavities (dorsal
and ventral) (see examples in Figures 1B, 26, 40, 41, and 43) during the jet propulsion cycle may
80
ML as % of TL
70
60
50
40
30
0
20
40
60
80 100 120 140 160 180 200
Age (days)
Figure 46 Relative decrease of mantle length (ML) as percentage of total length (TL) from hatching to
settlement during experimental rearings of Enteroctopus dofleini and Octopus vulgaris. (Data for E. dofleini
obtained from Okubo 1979 (dark circles) and data for O. vulgaris obtained from Villanueva 1995 (white
circles).) Initial settlement periods are indicated for both species: E. dofleini, black arrow; O. vulgaris, white
arrow. Original.
178
Arm length as % of TL
80
70
60
50
40
30
20
10
0
0
20
40
60
80 100 120 140 160 180 200
Age (days)
Figure 47 Relative increase of arm length as percentage of total length (TL) from hatching to settlement
during experimental rearings of Enteroctopus dofleini and Octopus vulgaris. (Data for E. dofleini obtained
from Okubo 1979 (dark circles) and data for O. vulgaris obtained from Villanueva 1995 (white circles).)
Initial settlement periods are indicated for both species: E. dofleini (black arrow); O. vulgaris (white arrow).
Original.
80
Total length (mm)
70
60
50
40
30
20
10
0
0
20
40
60
80 100 120 140 160 180 200
Age (days)
Figure 48 Growth in total length from hatching to settlement during experimental rearings of Enteroctopus
dofleini and Octopus vulgaris paralarvae. (Data for E. dofleini obtained from Okubo 1979 (black circles) and
Okubo 1980 (black squares). Data for Octopus vulgaris obtained from Itami et al. 1963 (white squares) and
Villanueva 1995 (white circles).) Initial settlement periods are indicated for both species: E. dofleini, black
arrows; O. vulgaris, white arrows. Original.
also shed light on the poorly known hydrodynamic and energetic adaptations of swimming in these
long-armed paralarvae.
Chromatophore genesis and new skin sculptural components
After a nearly transparent life in the plankton, recently settled octopuses develop a dense net of
chromatophores, particularly on the dorsal surfaces, which help the animal in camouflage on the
seafloor and that develop into body patterns resembling those of the adults. As noted by Packard
(1985, p. 293): “The dorsal spurt in chromatophore genesis at the end of the planktonic phase is so
dramatic as to hint at something like metamorphosis. It is as if the skin were waiting for its owner
to settle on the seafloor before bringing out the fine-grain dress that is going to serve for the rest of
its life, and replace the coarse-grain set of extra-tegument spots (on the surface of the viscera) that
179
served during the transparent planktonic phase.” All the founder chromatophores of paralarvae can
be identified in recently settled individuals and are assumed to remain functional. However, they
were never expanded during the extensive photographic surveys of Packard, who suggested that they
may belong to planktonic, rather than benthic, camouflage patterns. 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 leucophores. This transformation has not been described in detail and requires further research.
For many species, the sculptural components of the skin also undertake a dramatic transformation from the relatively smooth paralarva to highly sculptured, benthic animals (Figure 16). Papillae,
flaps, ridges, patch and groove skin texture, and the lateral mantle ridge are all sculptural features of
post-settlement juveniles and adults. In some species, papillae in the skin can be dramatically raised
(complete with side branches) to form a rugose or even hairy appearance, as occurs in members of
the genus Abdopus (Norman & Finn 2001).
Horizontal pupillary response
In line with many pelagic cephalopods, octopus paralarvae possess a circular pupil (see examples
in Figures 1B, 3, 4 centre, 26, 41). In contrast, adult benthic octopuses have a horizontal pupillary
response to light intensities: when exposed to bright light the pupil forms a horizontal slit, while
the dark-adapted pupil is close to circular, as observed in Octopus vulgaris and Eledone cirrhosa
(Muntz 1977, Douglas et al. 2005) (see also Figure 1C). A horizontal pupil is present in octopus
hatchlings of directly benthic species (see Figure 1C,D). The horizontal shape of the pupil correlates
with the longest rhabdomes found in the central retina, where they form an equatorial strip (Young
1963). This adaptation may be related to a benthic mode of life so that objects in the seafloor/water
interface can be better discriminated (Muntz 1977). In other cephalopods that live in the water
column, such as Loligo pealei, the central retinal strip is absent (Young 1963). In Enteroctopus
dofleini reared from planktonic hatchlings, the horizontal slit of the pupil was observed only in benthic individuals older than 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 paralarvae that are still present in the micronekton has
only been observed in several live photographs of larger animals (e.g., Figure 4 bottom). The presence of this feature may represent animals close to settlement, animals in a transitional phase during
which they are spending time split between swimming and benthic crawling, or be an attribute of
delayed settlement (see ‘Prolonged paralarval stages: micronektonic paralarvae’, p. 182).
Behavioural and ecological characteristics at settlement
The shift from a planktonic to a benthic life implies that the adaptations necessary for this change
are attained by the octopuses over a relatively short time. It is also assumed that octopuses settle to
the seafloor. However, they have also been found to use other hard surfaces, including the underside
of buoys set over 64 m of water (Wells & Wells 1970), surface flotsam (Smale & Buchan 1981) and
have taken on a role as epifauna covering floating cages for fish culture at more than 25 m deep
in the Mediterranean Sea (R. Villanueva personal observation). Most descriptions of settlement
behaviour come from laboratory experiments. These are typically characterized by high peaks of
mortality during these periods, at least for Octopus vulgaris (Villanueva 1995, Iglesias et al. 2004,
Carrasco et al. 2006), for which cannibalism has also been observed immediately after settlement
180
(Itami et al. 1963). These findings indicate that laboratory settlement requirements are poorly
understood and need to be improved. The natural settlement process is probably modified under
laboratory conditions, potentially accelerating settlement through factors such as (1) the physical
limits imposed by the size of normal rearing tanks, preventing possible movement within the water
column, (2) light intensity and (3) the prior feeding history of the reared paralarvae, which are
usually indirectly trained to receive food during laboratory daylight periods. Octopuses collected
from floating structures in the wild (Wells & Wells 1970) or from ROVs in the water column (Hunt
1996) become exclusively benthic when transferred to rearing tanks. However, in some species
such as Amphioctopus burryi, relatively large individuals of 0.8–1.2 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 paralarvae have also been found to be benthic during the day and pelagic at
night (Hanlon et al. 1985). This behaviour is suspected to be common in many species. Kanamaru
(1964) reported a mix of planktonic and benthic organisms (shrimp and crab larvae and flatfish
remains) in the gut contents of a juvenile Enteroctopus dofleini, 51 mm in total length, suggesting
this migratory capacity. Relatively large Octopus vulgaris paralarvae (11 mm ML) have been collected from the plankton (Degner 1925, Rees 1953).
In laboratory experiments, presettlement individuals tend to remain attached to the surfaces of
the tanks for the majority of the time, only swimming to capture food in the water column (Itami
et al. 1963, Forsythe & Toll 1991, Villanueva 1995). Recently settled individuals show a preference for dark or shady areas of tanks and have reclusive behaviour, using holes, provided shelters
or gastropod shells as refuges. At this stage, individuals search for food on the floor of the aquaria
rather than in the water column. To identify individuals as presettlement or post-settlement can be
difficult. To discern between planktonic or benthic individuals, a behavioural criterion was used
by Villanueva (1995): when settled individuals are disturbed (i.e., gently touched with the tip of
a pipette) and respond by crawling, rather than swimming away, they are considered to be postsettlement, benthic juveniles. Settled individuals also begin to direct fluxes of water from their funnel to the origin of the disturbance.
Ambrose (1988) developed a means of assessing the population dynamics of recently settled
octopus individuals. The densities of recently settled and juvenile O. bimaculatus were estimated
by sampling the holdfasts of the giant kelp, Macrocystis pyrifera, 15 times over 2 yr consecutively
at 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 paralarvae settled throughout
the year, with the highest octopus densities recorded in early summer, indicating the peak period of
settlement. In the Bay of Naples, Mediterranean Sea, Naef (1928, p. 292) found that recently settled
individuals of Octopus vulgaris are “dredged up with sand, gravel and all sorts of detritus and are
easy raised on a corresponding substratum in the aquarium. They always bury deeply in such sediments or hide in narrow cavities, coming to the sediment surface only at night to forage.”
On reaching the benthos, recently settled octopuses still possess symbionts remaining from
their planktonic stage. Chromidinid ciliates of the genus Chromidia typically infect renal organs
of oceanic cephalopods with a pelagic distribution. However they are also found in benthic octopus species, but only those with a planktonic paralarval stage, such as Eledone cirrhosa, Octopus
salutii, O. vulgaris and Scaeurgus unicirrhus (Hochberg 1982, 1983). It has been suggested that
these symbionts are acquired through association with crustaceans living in the water column and
are transported to the seafloor when octopuses settle (Hochberg 1982, 1983). It is not known how the
ciliates reach the renal organs and they appear to do no harm to the tissues of their host cephalopods
(Furuya et al. 2004).
181
Prolonged paralarval stages: micronektonic paralarvae
There may be a third octopus paralarval strategy that appears peculiar to animals present in the
water column over deep waters. In these habitats, large octopus paralarvae (some more than 100
mm in total length) have been encountered in plankton nets, attracted by lights or observed from
ROVs (see Table 6). Due to the large size and swimming capacities of these individuals that live
in epipelagic waters, they can be considered as part of the micronekton. Strugnell et al. (2004)
coined the term ‘super-paralarvae’ to refer to these peculiar, often long-armed, paralarvae. For
Macrotritopus-type paralarvae, Rees (1954) discussed the impact of ocean currents sweeping individuals off shore over very deep water. For these paralarvae, Rees (1954, p. 69), proposed that settlement was delayed and that they could attain “nearly twice the normal size for metamorphosis”. He
coined the term ‘extended pelagic stages’ for such paralarvae. In relation to Macrotritopus defilippi,
Nesis & Nikitina (1981, p. 847) pointed out that: “The macrotritopuses are able to delay their settling to the bottom and may have a chance to cross the Atlantic”.
The prevalence of micronektonic paralarvae, their identities and the circumstances under which
they exist are poorly known. They reach large sizes and still exhibit the characteristic paralarval
features of nearly transparent musculature, large and simple chromatophores and round pupils. The
nature of the settlement process for these forms is unknown, as is discriminating between whether
this is an accidental process or whether such species have actively delayed settlement to exploit
resources of the epipelagic realm. As discussed (see ‘Defences’ section, p. 168), schools or shoals of
young Octopus rubescens have been reported in midwater in Monterey Bay, California (Figure 44).
Young (1972) captured large individuals of this species (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 paralarvae: neoteny and holopelagic octopuses
Extended pelagic phases in oceanic paralarvae may have played a role in the evolution of certain holopelagic octopuses. Octopus families that have completely pelagic life cycles fall into
two major groups. The ctenoglossans (tribe Ctenoglossa) contain three families (Amphitretidae,
Vitreledonellidae and Bolitaenidae), which are typically relatively small (typically <20 cm in total
length, largest <50 cm), semigelatinous and transparent residents of oceanic midwater depths between
around 200 and 800 m. The second group, the argonautoids (superfamily Argonautida), includes
the argonauts, blanket octopuses and their relatives (families Argonautidae, Tremoctopodidiae,
Alloposidae and Ocythoidae). These octopuses tend to be larger (up to 2 m or more in total length),
more muscular, non-transparent pelagic octopuses, typically residing in shallower, neritic waters
(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 paralarvae
that never ‘returned to earth’. Prolonged residence in the pelagic realm and acquisition of sexual
maturity (and activity) in the water column are suggested as the mechanisms by which this group
became wholly pelagic. The micronektonic or ‘super-paralarvae’ concept (discussed in ‘Prolonged
paralarval stages: micronektonic paralarvae’, p. 182) may have been the critical stage that enabled
182
the evolution of the ctenoglossans. The origin of the other major group of holopelagic octopuses, the
argonautoids, remains unknown.
Anthropogenic impacts on early stages of octopuses
Pollution
Most octopodid species with planktonic paralarval stages live in shallow waters and can be affected
by the many pollutants introduced to the sea by human activities. These pollutants can affect octopuses from the early stages of development. Eggs of incirrate octopods lack an egg capsule so
that the chorion is in direct contact with the seawater. It is expected that contaminants can have
a deleterious effect on octopuses compared with those cephalopod species that have a protecting
egg capsule. For example, cuttlefishes predominantly absorb metals into the outer egg capsule, acting as an effective shield that limits exposure of the embryos to soluble metals (Bustamante et al.
2002, 2004). Compared with recently spawned eggs, developing Octopus vulgaris eggs have higher
concentrations of most essential elements and also of some non-essential elements (i.e., Ag and Pb)
due to the absorption of these elements from seawater during embryonic development (Villanueva
& Bustamante 2006). Due to chronic exposure to organophosphorus pesticides such as parathion,
abnormal embryo gastrulation and arrested development has been observed in O. mimus embryos
at pesticide concentrations of over 0.4 mM (Gutiérrez-Pajares et al. 2003). Subadult and adult octopuses can be used as bioindicator species in polluted areas (Butty & Holdway 1997) and are sensitive to marine pollutants such as ethylene dibromide and mercuric chloride (Adams et al. 1989).
Hatchlings of O. pallidus (a directly benthic species) are more sensitive to exposure to petroleum
hydrocarbon toxicants such as 4-chlorophenol compared with other aquatic invertebrates tested,
such as Daphnia magna or Hydra species, and do not appear to be adversely affected by the application of chemical dispersants to oil spills (Long & Holdway 2002). Scheel (2002) noted that densities
of Enteroctopus dofleini recorded during 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
183
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 physiological effects of seawater acidification on planktonic stages of cephalopods are unknown and further
research is required. It is suspected that indirect effects of climate change may severely affect adult
octopus populations. An example was provided by a prolonged harmful algal bloom (HAB) lasting
nearly 2 months, which appears to have nearly eliminated the once-ubiquitous population of O. cf.
mercatoris (a direct benthic species) in St. Joseph Bay, Florida (Tiffany et al. 2006). HABs seem to
be increasing in frequency, duration and severity worldwide, influenced by anthropogenic impact
and coinciding with trends in global warming (Van Dolah 2000). Such episodes may affect littoral
octopus populations in the future.
As with all marine life, climate change will also affect biogeographic boundaries that are
dictated by seawater temperature. This effect may manifest itself in two ways. Firstly, octopus
taxa geographically associated with land masses that do not extend into higher latitudes will run
out of available habitat and be unable to shift to higher latitudes. Secondly, octopus paralarvae
from warmer latitudes may be amongst the vanguards of invasions into previously cooler habitats.
Qualitative evidence comes from reports of an Australian warm-temperate octopus species, O. tetricus, which has been found outside its typical warmer geographic range in the cool temperate
waters of Victoria, Australia (L. Altoff personal observation 2007). As this species preys on other
octopuses (M.D. Norman unpublished data), it may act as an invasive species, effectively (and rapidly) displacing resident octopus taxa, some of which are endemic/restricted in distribution. Further
research is required into the potential scale of such impacts.
Concluding remarks
The distinctive form of octopus paralarvae and their differences in lifestyle from that of their parents make them enigmatic and fascinating creatures. Their numbers, diversity and wide geographic
range make them important predatory members of planktonic assemblages. The duration of their
planktonic phase varies significantly between species — laboratory studies recording ranges of
3 wk to 6 months. This period is a significant proportion of the total life cycle of these animals, with
various studies reporting lifespans of between 6 months and 3.5 yr. For some species, the duration
of the pelagic period seems to be considerably extended and young octopuses can reach relatively
large sizes as part of the micronekton of epipelagic, oceanic waters. For these individuals, settlement appears to be delayed for an unknown period, potentially in order to enhance dispersal and/or
exploit food resources in this pelagic realm.
Preliminary information is available for many attributes of octopus paralarvae, particularly for
two species, Octopus vulgaris and Enteroctopus dofleini. However, many opportunities exist for
new and exciting research. The most pressing research areas fall into five categories:
1. Accurate taxonomy and development of identification tools. Use of molecular sequencing techniques will enable concrete species identification, linked with databases such as
GenBank and potentially programs such as Barcode (see Strugnell & Lindgren 2007).
This will greatly expand the capacity to describe paralarvae of diverse species in detail
through all growth stages. Use of high-resolution photography and standardised morphological descriptions will be critical to this process.
2. Faunal surveys and biogeography. Equipped with better knowledge of paralarval species
discrimination, surveys of regional faunas can be undertaken to gain a better understanding of the ranges, timing and abundances of the various paralarval taxa. These data can
then be analysed in relation to biogeography and oceanography.
184
3.Rearing techniques. Rearing of paralarvae requires innovative approaches to better simulate natural conditions for paralarvae, particularly in relation to the water column, water
quality and turbulence, prey and light regimes. Specialized treatment of brooding adult
females will also enable provision of healthy paralarvae for taxonomic and experimental
studies.
4.Growth, development and nutrition. With access to healthy paralarvae of all growth stages,
research can be undertaken into morphology, physiology and behaviour during growth and
development. A greater understanding of all aspects of nutrition is critical to the development of aquaculture for key species and needs further study, including aspects of feeding
requirements and nutrient absorption through the skin. Morphological transformations
throughout the paralarval period, particularly in skin components, are also worthy of further investigation.
5.Hatching and settlement processes. All aspects of the cues, timing, duration and mechanics of the hatching and settlement processes require more detailed research. Assessment
of the total duration of paralarval period is also required in order to assess the dispersal
capacities of different species. Development of accurate ageing techniques would be a
valuable tool in these studies.
With most of our knowledge of octopus paralarvae applying to just two species, Octopus vulgaris and Enteroctopus dofleini, there is considerable scope for further research. The total number
of benthic octopus species with planktonic stages is likely to be high (there are at least 68 named
species and many more are yet to be described). It is clear that many new and exciting morphological, physiological and behavioural adaptations await discovery.
Acknowledgements
We wish to gratefully acknowledge Eric Hochberg (Santa Barbara Museum of Natural History) for his
support and advice on all aspects of octopus natural history; Mitsuo Sakai and Toshie Wakabayashi
(National Research Institute of Far Seas Fisheries) for their considerable efforts in translating many
Japanese articles on planktonic octopuses into English; Jose Manuel 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 paralarvae as the basis for Figure 40. Sincere
thanks to the many photographers who contributed live animal photographs, particularly David
Paul. M.D. Norman would like to thank Julian Finn, John Ahern, David Paul and the staff of
the Undersea Explorer for invaluable field and laboratory assistance with planktonic and broader
cephalopod research. R. Villanueva’s recent research into planktonic octopus was funded by the following 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.
185
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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 paralarvae. (Reproduced with permission from Miske & Kirchhauser 2006.) Female Octopus
berrima at the time of hatching in the laboratory with a benthic juvenile hatchling (total length ~20 mm) in
foreground (C) and within 10 min of hatching (D) showing well-developed arms and chromatic and sculptural
components of the skin. (Photos: David Paul.)
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 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.)
Colour Figure 4 (Villanueva & Norman) Micronektonic octopus paralarvae. Top, unidentified paralarva
of the genus Callistoctopus from the Coral Sea, Australia, showing longer dorsal arm pair. (Photos: David
Paul.) Centre, unidentified paralarva (Macrotritopus sp.?) from Hawaii showing long arms relative to body
length, particularly the third pair. (Photos: Chris Newbert.) Bottom, unidentified paralarva from Hawaii.
(Photos: Jeffrey Rotman.)
Colour Figure 6 (Villanueva & Norman) Unidentified paralarva from the Coral Sea, Australia, showing
arms of equivalent length (left). (Photo: David Paul.) Paralarva of Macrotritopus defilippi from Caribbean Sea
showing longer third arm pair (right). (Photo: Raymond Hixon.)
Colour Figure 7 (Villanueva & Norman) Chromatophores contracted (left) or expanded (right) on the head
of paralarvae. The left image corresponds to an unidentified paralarva of unknown genus and the right image
is from an unidentified paralarva of the genus Callistoctopus. Both individuals from Coral Sea, Australia.
(Photos: David Paul.)
Colour Figure 9 (Villanueva & Norman) Iridescence in octopus paralarvae. Left, unidentified paralarva
showing scattered points of iridescence, potentially from 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 10 (Villanueva & Norman) Hapalochlaena maculosa hatchling, a direct benthic species,
showing well-developed skin colour and sculpture. (Photo: David Paul.)
Colour Figure 16 (Villanueva & Norman) Adult Octopus cyanea in camouflage display amongst soft corals, Puerto Galera, Philippine Islands. (Photo: Gunther Deichmann.)
Colour Figure 26 (Villanueva & Norman) Planktonic paralarva of Octopus warringa within 10 min of
hatching in the laboratory showing short arms, transparent musculature, simple chromatophores and external
yolk sac (within arm crown). (Photo: David Paul.)
Colour Figure 43 (Villanueva & Norman) Unidentified paralarva of the genus Callistoctopus from the
Coral Sea, Australia, showing elongate form when swimming. Photograph taken in situ while night diving on
a moonless night at ~10 m deep over a seafloor depth of 450 m at Osprey Reef, Coral Sea, Australia. (Photo:
M.D. Norman.)
Colour Figure 44 (Villanueva & Norman) A dense swarm of Octopus rubescens with the jellyfish
(Phacellophora camtschatica) photographed 26 June 2003 at 1115h local time from the ROV Ventana at a
depth of about 60 m in 728 m of water in the Monterey Submarine Canyon, north-east Pacific. Temperature
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.)
Erratum to “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
2Sciences, Museum Victoria, GPO Box 666, Melbourne, Vic 3001, Australia
Refers to: Villanueva, R. & Norman, M.D. 2008. Biology of the planktonic stages of benthic octopuses. Oceanography and Marine Biology: An Annual Review 46, 105–202.
The publisher regrets the error introduced after proofreading in the scales of Figures 20 and 25 in
the above paper. The corrected figures are reproduced as follows:
ix
© 2009 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon
Erratum to “Biology of the planktonic stages of benthic octopuses”
A
B
C
E
10µm
50µm
50µm
D
10µm
F
H
G
50µm
5µm
5µm
5µm
Figure 20 Statoliths of Octopus vulgaris paralarvae. Scanning electron micrographic images from anterolateral (A) and posterior (C) views of hatchling statoliths with their respective crystalline surface structure
presented inside the rectangles (B, D). In paralarvae aged 30 days, statolith growth is observed on the posterior
side of the statolith (E, F). The crystalline structure of the surface observed inside the lower (G) and upper
(H) rectangle of the image F is also indicated. Individuals obtained from rearing experiments described in
Villanueva et al. (2004). Original.
x
A
B
C
Figure 25 Denticulation of beaks in Octopus vulgaris paralarvae. Scanning electron micrographic 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.
xi
References
Villanueva, R. 1995. Experimental rearing and growth of planktonic Octopus vulgaris from hatching to settlement. Canadian Journal of Fisheries and Aquatic Sciences 52, 2639–2650.
Villanueva, R., Riba, J., Ruiz-Capillas, C., González, A.V. & Baeta, M. 2004. Amino acid composition of
early stages of cephalopods and effect of amino acid dietary treatments on Octopus vulgaris paralarvae.
xii

BioloGy oF ThE plANkToNic sTAGEs oF BENThic ocTopusEs

Transcription

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