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Southern Ocean Cephalopods
Martin A. Collins and Paul G. K. Rodhouse
British Antarctic Survey, Natural Environment Research Council,
High Cross, Madingley Road, Cambridge, United Kingdom
1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192
2. Cephalopod Biodiversity and Origins of the
Antarctic Cephalopod Fauna . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195
3. Distribution . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . 201
3.1. Determining distribution . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.2. Octopodids . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . 206
3.3. Decapods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 208
3.4. Geographic migration patterns . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216
3.5. Vertical migration patterns . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216
3.6. Mass strandings . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217
4. Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217
4.1. Methods of measuring growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217
4.2. Rates of growth . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218
5. Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219
5.1. Life-cycle strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . 219
5.2. Fecundity, egg size and development . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . 220
5.3. Maturation and spawning . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . 222
6. Trophic ecology . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . 223
6.1. Role as predators . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
6.2. Role as prey . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . 229
7. Physiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247
8. Commercial exploitation . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247
9. Discussion . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . 248
Acknowledgements. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . 249
References . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . 250
ADVANCES IN MARINE BIOLOGY VOL 50 0065-2881/06 $35.00
#2006 Elsevier Ltd. All rights reserved DOI: 10.1016/S0065-2881(05)50003-8
The Southern Ocean cephalopod fauna is distinctive, with high levels of
endemism in the squid and particularly in the octopodids. Loliginid squid,
sepiids and sepiolids are absent from the Southern Ocean, and all the squid
are oceanic pelagic species. The octopodids dominate the neritic cephalopod
fauna, with high levels of diversity, probably associated with niche separation.
In common with temperate cephalopods, Southern Ocean species appear to be
semelparous, but growth rates are probably lower and longevity greater than
temperate counterparts. Compared with equivalent temperate species, eggs are
generally large and fecundity low, with putative long development times.
Reproduction may be seasonal in the squid but is extended in the octopodids.
Cephalopods play an important role in the ecology of the Southern Ocean,
linking the abundant mesopelagic fish and crustaceans with higher predators
such as albatross, seals and whales. To date Southern Ocean cephalopods have
not been commercially exploited, but there is potential for exploitation of
muscular species of the Family Ommastrephidae.
1. INTRODUCTION
The Southern Ocean, which surrounds the Antarctic continent, consists of
a system of deepsea basins, separated by three systems of ridges: the
Macquarie Ridge (south of New Zealand and Tasmania), the Scotia
Arc (between the Patagonian shelf and the Antarctic Peninsula) and the
Kerguelen Ridge (Carmack, 1990)(Figure 1). It is bounded to the north by
the Antarctic Polar Front (APF) or Antarctic Convergence (Figure 1) and
occupies an area of 38 10
6
km
2
(Carmack, 1990). The location of the
APF, where cold Antarctic surface water meets warmer sub-Antarctic water
flowing southeast, varies temporally and spatially (between 47 and 63 S) and
is characterised by a distinct change in temperature (2–3 C) and other
oceanographic parameters (Carmack, 1990). It acts as a biological barrier,
making the Southern Ocean a largely closed system. The main surface
currents are the Antarctic Circumpolar Current, which flows in an easterly
direction encircling the Antarctic continent, and the east wind drift, which
flows in a westerly direction, close to the Antarctic continent (Lutjeharms
et al., 1985). Seasonal and regional variations in water temperature in the
Southern Ocean are small (þ3to2C). Sea ice covers large areas of the
Southern Ocean, the extent varying seasonally from 10% in summer to
50% of the total area in winter (Carmack, 1990). Within the Southern Ocean,
sub-Antarctic Islands, such as South Georgia, Kerguelen and Heard, are
areas of enhanced productivity and support large populations of higher
predators such as whales, seals and seabirds (Atkinson et al., 2001), as well
as fisheries for toothfish, krill and icefish (Kock, 1992; Agnew, 2004).
192 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
The ecology of the Southern Ocean, particularly in the southwest Atlantic
sector, is dominated by Antarctic krill (Euphausia superba), which is consid-
ered the keystone species linking primary production to the abundant higher
predators. However, evidence from predators such as toothed whales, pen-
guins, albatross and elephant seals has also highlighted the importance of
cephalopods (particularly squid) in the Antarctic system, leading Rodhouse
and White (1995) to propose an alternative oceanic food-web linking plank-
tivorous mesopelagic fish to squid and predators. The abundance of cepha-
lopods in predator stomachs has not been replicated in net samples, which
rarely produce significant quantities of squid, probably as a consequence of
Figure 1 Polar projection of the Antarctic continent to 45 S, showing the ap-
proximate location of the Antarctic Polar Front and the locations of the Scotia
Ridge, Macquarie Ridge and Kerguelen Plateau.
SOUTHERN OCEAN CEPHALOPODS 193
the small size of scientific nets and their avoidance by mobile large squid (see
Clarke, 1977).
Investigations of Southern Ocean cephalopods began with the pio-
neering expeditions of HMS Challenger, the Scottish Antarctic Expedition
on HMS Alert and the German Valdivia cruise (Hoyle, 1886; Odhner, 1923).
Small numbers of cephalopods were collected on these early expeditions,
and many of the early descriptions of Southern Ocean cephalopods were
based on fragments of specimens or remains found in predator stomachs
(Thiele, 1920; Odhner, 1923; Robson, 1925). In the 1960s, Clarke (1962a,b)
developed the use of beaks to identify cephalopod remains in predator
stomachs, and this highlighted the importance of cephalopods in the diet
of many predators, particularly sperm whales. In fact the stomachs of
predators were the main source of cephalopods for many years, with
sperm whales much better samplers of large adult squid than any nets
(Clarke, 1980), but this source of material has been limited since the
cessation of commercial whaling. During the 1960s, the former Soviet
Union began a series of cruises, initially on the purpose-built RV
Academic Knipovitch, to search for new fishery resources in the Scotia Sea.
Cephalopods were not targeted but were often taken as ‘‘by-catch.’’ The
results of the Soviet work are largely in grey literature (and in Russian), but
Filippova (2002) reviewed some of the important findings of the Russian
studies. Since the 1970s, there has been considerable research eVort in the
Southern Ocean, both ship-based research, using scientific and commercial-
scale fishing nets, and land-based studies of predator diets. Whilst few of
these studies have focused specifically on cephalopods, they have yielded
considerable new data on their distribution and ecology in the Southern
Ocean.
In 1982 the Convention on the Conservation of Antarctic Marine Living
Resources (CCAMLR) was established in response to concerns about
the ecosystem eVects of exploitation of Antarctic marine resources. The
focus of CCAMLR has been primarily krill and exploited finfish, but com-
mercial exploitation of cephalopods has also been the subject of interest in
the Southern Ocean, with some exploratory fishing for the squid Martialia
hyadesi having been undertaken around South Georgia (Rodhouse et al.,
1993; Gonzalez et al., 1997; Rodhouse, 1997; Gonzalez and Rodhouse,
1998).
In this review we deal with the biology and ecology of the Southern Ocean
cephalopods including species that spend part of their life cycle south of the
APF. However, considerably more is known about the biology of species
that are also caught north of the APF, such as M. hyadesi and Moroteuthis
ingens than the species that are generally restricted to south of the APF and
this is reflected in the text.
194 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
2. CEPHALOPOD BIODIVERSITY AND ORIGINS OF THE
ANTARCTIC CEPHALOPOD FAUNA
The high-latitude Southern Ocean cephalopod fauna is highly distinctive,
diVering greatly from that of the temperate zone. The fauna includes oegop-
sid squids, cirrate and incirrate octopods, but the sepiids, sepiolids and
loliginid squid, which dominate the cephalopod fauna in the neritic zone
of temperate and tropical regions, are entirely absent. The reasons for this
absence are not clear but could be related to putative long development
times in cold water (Boletzky, 1994), making the relatively unprotected
benthic egg masses of these groups more susceptible to predation and ice
scour. The oegopsid squids, which are present in the Southern Ocean, are
exclusively pelagic or benthopelagic and most have circum-Antarctic pat-
terns of distribution, a consequence of which may be the relatively small
number of species (see later discussion). In contrast, the incirrate octopodids
are highly speciose, with each species typically occupying a rather limited
geographic distribution (see Allcock and Piertney, 2002; Allcock et al.,
2003b; Allcock, 2005). The diVerence in distribution and diversity patterns
between the two groups is probably a result of diVerences in habitat
and reproductive strategy. Adult squid are generally highly mobile, with
planktonic eggs and larvae, permitting a high degree of dispersion. The
octopodids, on the other hand, produce large, direct developing eggs and
the adults are, with the exception of some of the cirrates, benthic, reducing
the opportunity for dispersal.
The distinct Southern Ocean fauna includes high levels of endemism in
both the squid (two endemic families, Psychroteuthidae and Batoteuthidae,
and six endemic genera, Mesonychoteuthis, Psychroteuthis, Kondakovia,
Alluroteuthis, Slosarczykovia and Batoteuthis) and the incirrate octopods
(five endemic genera: Pareledone, Megaleledone, Adelieledone, Prealtus and
Bathypurpurata). The endemic incirrates are thought to have evolved after
the separation of the Antarctic continent and the subsequent formation of
the Antarctic circumpolar current (25–28 my BP) and the APF (22 my BP)
(Allcock and Piertney, 2002), which produced a distinct thermal barrier for
the shallow fauna. This mirrors what is found in the Antarctic fish, where
the notothenioids are largely endemic to the Southern Ocean (Eastman
and Clarke, 1998). There is also evidence that the incirrate octopods have
diversified into species flocks in a similar way to that of the notothenioids
(Allcock and Piertney, 2002).
At present, the extant Southern Ocean octopod fauna (known to science)
includes seven cirrate and 27 incirrate species (Figures 2 and 3;Table 1).
Paraeledone is the most speciose and abundant genus, with 13 species
recognised (Allcock, 2005). It is becoming apparent that the diversity of
SOUTHERN OCEAN CEPHALOPODS 195
Figure 2 Photographs of Southern Ocean cephalopod fauna: (a) Thaumeledone
gunteri: scale bar 50 mm, (b) Pareledone charcoti: scale bar 50 mm (c)
Mesonychoteuthis hamiltoni scale bar 1000 mm (d) Kondakovia longimana, washed
ashore on Signy Island (South Orkneys), (e) Martialia hyadesi: scale bar 100 mm.
196 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
incirrate octopods, particularly the genus Pareledone, is much greater than
previously thought. In common with the endemic notothenioid fish families
(e.g., Channichthyidae, Artididraconidae, Bathydidraconidae), Pareledone
has undergone extensive radiation in the Southern Ocean, probably a
Figure 3 Southern Ocean octopod fauna (a) Pareledone turqueti (b) Graneledone
sp., (c) Thaumeledone gunteri, (d) Stauroteuthis gilchristi and (e) Opisthoteuthis
hardyi.
SOUTHERN OCEAN CEPHALOPODS 197
Table 1 Bathymetric and geographic distribution of Southern Ocean Octopoda
Family Species Geographic range
Bathymetric range
(m) Sources
Opisthoteuthidae Opisthoteuthis hardyi
Villanueva et al., 2002
South Georgia 1000 Villanueva et al., 2002
Cirroctopus glacialis
Robson, 1930
South Shetlands;
Antarctic Peninsula
>330 Robson, 1930; Hardy, 1963;
Vecchione et al., 1998
Cirroctopus mawsoni
(Berry, 1917)
Indian Ocean sector 526–911 O’Shea, 1999
Cirroctopus antarctica
(Kubodera and Okutani,
1986)
Pacific sector Kubodera and Okutani, 1986;
Vecchione et al., 1998;
O’Shea, 1999
Cirroteuthidae Cirrothauma magna
(Hoyle, 1885)
Prince Edward/Crozet Bathyal Guerra et al., 1998
Cirrothauma murrayi
Chun, 1910
Scotia Sea, Drake
Passage
Bathyal Collins, unpublished; Roper
and Brundage, 1972
Stauroteuthis gilchristi
(Robson, 1930)
South Georgia 1000 Collins and Henriques, 2000
Octopodidae Graneledone antarctica
Voss, 1976
Ross Sea, Antarctic
Peninsula
1500–2341 Voss, 1976; Vecchione et al.,
2005
Graneledone macrotyla
Voss, 1976
Drake Passage 1647–2044 Voss, 1976
Graneledone gonzalezi
Guerra et al., 2000
Kerguelen 510–540 Guerra et al., 2000
Bathypurpurata profunda
Vecchone et al., 2005
South Shetlands 509–565 Vecchione et al., 2005
Pareledone turqueti
(Joubin, 1905)
West Antarctic 25–640 Kuehl, 1988; Allcock, 2005
198 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Pareledone antarctica
(Thiele, 1920)
Probably junior
synonym of
P. harissoni
Lu and Stranks, 1994
Pareledone charcoti
(Joubin, 1905)
Antarctic Peninsula,
South Orkneys,
South Shetlands
Shallow to 392 Allcock, 2005
Pareledone aurorae
(Berry, 1917)
Queen Mary Land 200 Allcock, 2005
Pareledone framensis
Lu and Stranks, 1994
Fram Bank, East
Antarctica
145–319
(2.2 to 2.1 C)
Lu and Stranks, 1994
Pareledone aequipapillae
Allcock, 2005
South Shetlands 110–465 Allcock, 2005
Pareledone albimaculata
(Allcock, 2005)
South Shetlands 190–465 Allcock, 2005
Pareledone aurata
Allcock, 2005
South Shetlands 89–465 Allcock, 2005
Pareledone cornuta
Allcock, 2005
South Shetlands 130–454 Allcock, 2005
Pareledone panchroma
Allcock, 2005
South Shetlands 427–804 Allcock, 2005
Pareledone serperastrata
Allcock, 2005
South Shetlands 130–454 Allcock, 2005
Pareledone subtilis
Allcock, 2005
South Shetlands 190–427 Allcock, 2005
Pareledone prydzensis
Lu and Stranks, 1994
Prydz Bay, East
Antarctica
526–676
(2.1 to 0.6 C)
Lu and Stranks, 1994
Pareledone harrissoni
(Berry, 1917)
East Antarctic 25–743
(2.1 to 0.6 C)
Lu and Stranks, 1994
Adelieledone polymorpha
(Robson, 1930)
West Antarctic 15–862 Kuehl, 1988;
Allcock et al., 2003b
(Continued)
SOUTHERN OCEAN CEPHALOPODS 199
Adelieledone adelieana
(Berry, 1917)
30 E to 90 E 139–680 Lu and Stranks, 1994;
Allcock et al., 2003b
Adelieledone piatkowski
Allcock et al ., 2003
Antarctic Peninsula 612–1510 Allcock et al., 2003b
Thaumeledone gunteri
Robson, 1930
South Georgia only 364–964 possibly
deeper
Yau et al., 2002;
Allcock et al., 2004
Thaumeledone rotunda
(Hoyle, 1885)
Circum-Antarctic 2900–3500 Allcock et al., 2004
Thaumeledone peninsulae
Allcock et al., 2004
Antarctic Peninsula 377–1512 Allcock et al., 2004
Megaleledone setebos
(Robson, 1932)
Circum-Antarctic 32–850;
1.9 to 1.4 C
Lu and Stranks, 1994;
Allcock et al., 2003a
Benthoctopus levis
(Hoyle, 1885)
Heard Island, Weddell
Sea?
140 Piatkowski et al., 1998;
Allcock et al., 2001
Benthoctopus thielei
Robson, 1932
Kerguelen Bustamente et al ., 1998;
Cherel et al ., 2002
Bentheledone albida
(Berry, 1917)
Nomen dubium Allcock et al., 2004
Praealtus paralbida
Allcock et al., 2004
Antarctic Peninsula 2986–3222 Allcock et al., 2004
Table 1 (Continued)
Family Species Geographic range
Bathymetric range
(m) Sources
200 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
consequence of the isolated areas of shelf associated with diVerent island
groups (Allcock et al., 2001; Allcock, 2005). At South Georgia, the only peri-
Antarctic island where the octopod fauna has been extensively studied, there
is just one species of Pareledone, perhaps as this represents the edge of the
range of this genus.
The cirrate octopods, characterised by the presence of cirri on the arms,
paired fins and a well-developed internal shell, are generally deepwater
forms. Endemism is less apparent in the cirrates, with no endemic genera,
which is probably a consequence of the greater mobility of the adults and
their deepwater habitat, to which the polar front is less of a barrier. To date,
the deep waters of the Southern Ocean have been poorly investigated and
further work will probably reveal greater diversity in both the incirrate
and the cirrate octopods.
The 22 species of Southern Ocean squid include representatives of 13
oegopsid families (Figures 2 and 4;Table 2). It is notable that, as well as
the absence of the myopsids from the Southern Ocean, many families of
oegopsids that are abundant in temperate oceanic areas such as the Enoplo-
teuthidae are also absent. The squid fauna can be divided into species that
are entirely Antarctic (Psychroteuthis, Alluroteuthis) and those that span the
APF. The species that cross the APF are either mobile migratory species that
undertake feeding migrations (M. hyadesi, M. ingens) or deepwater species
to which the APF is not such a distinct barrier (Chiroteuthis veranyi). A
number of other squid species have been recorded in the diets of Southern
Ocean predators but were probably taken when predators forage north of
the polar front and are excluded from Table 2.
3. DISTRIBUTION
3.1. Determining distribution
The distribution of Southern Ocean cephalopods has largely been deter-
mined from relatively small scientific nets, which can be opened and closed
and are useful in determining the vertical distribution of species but tend to
catch only juvenile cephalopods. Rodhouse et al. (1996) used a large pelagic
trawl at the APF and caught larger specimens of M. hyadesi, Slosarczykovia
circumantarctica and Galiteuthis glacialis than those caught in scientific nets.
Predators, such as seabirds, whales, seals and fish, can also be used to
provide information on the distribution of cephalopods. However, squid
beaks are often retained in predator stomachs for a long time (e.g., sperm
whales), and because some predators have extended foraging ranges, the
SOUTHERN OCEAN CEPHALOPODS 201
Figure 4 Southern Ocean squid fauna: (a) Galiteuthis glacialis, (b) Slosarczykovia
circumantarctica, (c) Martialia hyadesi, (d) Gonatus antarcticus, (e) Kondakovia long-
imana, (f) Psychroteuthis glacialis, (g) Mesonychoteuthis hamiltoni and (h)
Moroteuthis knipovitchi.
202 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Table 2 Bathymetric and geographic distribution of Southern Ocean squid species
Family Species Geographic distribution Sources
Onychoteuthidae Kondakovia longimana
Filippova, 1972
Circumpolar Antarctic Filippova, 1972; Lu and Williams,
1994a,b; Vacchi et al., 1994;
Lynnes and Rodhouse, 2002
Moroteuthis ingens
(Smith, 1881)
Circumpolar sub-Antarctic Massy, 1916; Filippova, 1972;
Filippova and Yukhov, 1979;
Alexeyev, 1994
Moroteuthis knipovitchi
Filippova, 1972
Circumpolar Antarctic Filippova, 1972; Filippova and
Yukhov, 1979; Rodhouse,
1989b; Rodhouse et al., 1996;
Piatkowski et al., 1998
Moroteuthis robsoni
Adam, 1962
Occasional sub-Antarctic Rodhouse, 1990b
Notonykia atricanae
Nesis et al ., 1998
Sub-Antarctic Nesis et al., 1998b
Gonatidae Gonatus antarcticus
Lo
¨nnberg, 1898
Circumpolar sub-Antarctic Kubodera and Okutani, 1986;
Rodhouse et al., 1996; Nesis,
1999a; Anderson and
Rodhouse, 2002
Histioteuthidae Histioteuthis atlantica
(Hoyle, 1885)
Sub-Antarctic Kubodera, 1989; Alexeyev, 1994
Histioteuthis eltaninae
Voss, 1969
Circumpolar sub-Antarctic Lu and Mangold, 1978; Alexeyev,
1994; Piatkowski et al., 1994;
Rodhouse et al., 1996
Batoteuthidae Batoteuthis skolops
Young and Roper, 1968
Circumpolar Antarctic Young, 1968; Filippova and
Yukhov, 1979; Rodhouse et al.,
1992b; Rodhouse et al., 1996;
Anderson and Rodhouse, 2002;
Collins et al., 2004
(Continued)
SOUTHERN OCEAN CEPHALOPODS 203
Psychroteuthidae Psychroteuthis glacialis
Thiele, 1920
Circumpolar Antarctic Filippova, 1972; Filippova and
Yukhov, 1979; Kubodera, 1989;
Rodhouse, 1989b; Piatkowski
et al., 1990, 1994, 1998; Lu and
Williams, 1994a; Anderson and
Rodhouse, 2002; Collins et al.,
2004
Neoteuthidae Alluroteuthis antarcticus
Odhner, 1923
Circumpolar Antarctic Odhner, 1923; Dell, 1959;
Filippova and Yukhov, 1979;
Filippova and Yukhov, 1982;
Rodhouse, 1988; Kubodera,
1989; Anderson and Rodhouse,
2002
Bathyteuthidae Bathyteuthis abyssicola
Hoyle, 1885
Circumpolar Antarctic Hoyle, 1886, 1912; Odhner, 1923;
Roper, 1969; Lu and Mangold,
1978; Lu and Williams, 1994a;
Rodhouse et al., 1996
Brachioteuthidae Slosarczykovia
circumantarctica
Lipinski, 2001
Circumpolar Antarctic Kubodera, 1989; Rodhouse,
1989b, 1996; Piatkowski et al.,
1994; Lipinski, 2001; Anderson
and Rodhouse, 2002; Collins
et al., 2004
Brachioteuthis linkovski
Lipinski, 2001
Occasional sub-Antarctic Lipinski, 2001; Cherel et al., 2004
Table 2 (Continued)
Family Species Geographic distribution Sources
204 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Ommastrephidae Martialia hyadesi
Rochebrune and Mabille,
1887
Circumpolar sub-Antarctic O’Sullivan et al., 1983; Rodhouse
and Yeatman, 1990; Rodhouse,
1991; Piatkowski et al., 1991;
Uozomi et al., 1991; Alexeyev,
1994; Rodhouse et al., 1996;
Gonzalez and Rodhouse, 1998;
Anderson and Rodhouse, 2001
Todarodes filippovae
Adam, 1975
Circumpolar sub-Antarctic Piatkowski et al., 1991; Dunning,
1993; Alexeyev, 1994
Chiroteuthidae Chiroteuthis veranyi
Ferussac, 1825
Occasional sub-Antarctic Alexeyev, 1994; Rodhouse and Lu,
1998
Mastigoteuthidae Mastigoteuthis psychrophila
Nesis, 1977
Circumpolar Antarctic Jackson and Lu, 1994; Lu and
Williams, 1994a; Piatkowski
et al., 1994; Rodhouse et al.,
1996; Cherel et al., 2004
Cranchiidae Galiteuthis glacialis
(Chun, 1906)
Circumpolar Antarctic Chun, 1910; Dell, 1959; Filippova,
1972; Lu and Mangold, 1978;
McSweeney, 1978; Kubodera
and Okutani, 1986; Rodhouse
and Clarke, 1986; Rodhouse,
1989b; Lu and Williams, 1994a;
Piatkowski and Hagen, 1994;
Rodhouse et al., 1996; Nesis
et al., 1998a; Piatkowski et al.,
1998; Anderson and Rodhouse,
2002
Taonius sp (cf pavo) Occasional sub-Antarctic Rodhouse, 1990b
Mesonychoteuthis hamiltoni
(Robson, 1925)
Circumpolar Antarctic McSweeney, 1970; Filippova and
Yukhov, 1979; Rodhouse and
Clarke, 1985
Lepidoteuthidae Pholidoteuthis boschmai
(Adam, 1950)
Scotia Sea Nemoto et al., 1985; OVredo et al.,
1985
SOUTHERN OCEAN CEPHALOPODS 205
beaks may not be indicative of local species. For instance, wandering
albatrosses undertake long foraging migrations that extend well outside
the Southern Ocean but return regularly to feed chicks, often with squid
captured a long way north of the polar front. Xavier et al. (2003b) combined
satellite tracking of wandering and grey-headed albatross with diet studies
on tracked birds to estimate the distribution of some of the prey species. By
utilising fresh cephalopod remains rather than beaks, it is possible to deter-
mine what the albatross was feeding on during its recent foraging trip and
use this to help determine the distribution of the prey species. Diets of fish
species such as patagonian toothfish (Xavier et al., 2002b) and deepwater
sharks (Cherel and Duhamel, 2004) can also give an indication of the depth
range of prey species.
3.2. Octopodids
The benthic cephalopod fauna is dominated by the incirrate octopodids but
also includes species of cirrates such as Opisthoteuthis hardyi, Cirroctopus
glacialis and Cirroctopus mawsoni. Two genera Pareledone and Adelieledone
are abundant and widespread in shallow water, with other genera such as
Graneledone, Thaumeledone and Megaleledone typically found deeper.
The genus Pareledone is the most speciose (13 species) and widespread
cephalopod genus in shallow water in the Southern Ocean. Until recently
all papillated specimens of Pareledone were attributed to P. charcoti, but
a detailed examination of material from the Antarctic Peninsula region
(Allcock, 2005) has revealed seven new species. Detailed studies in other
areas may reveal similar diversity (Allcock, 2005). Records of Pareledone oV
the South American coast, however, appear to be misidentifications, with
the genus restricted to the Southern Ocean (Allcock, 2005). Pareledone
charcoti is limited to relatively shallow water (<400 m) around the Antarctic
Peninsula, and records from the eastern Antarctic (e.g., Lu and Stranks,
1994) are not attributable to this species (Allcock, 2005). P. turqueti, which
occurs at South Georgia, Shag Rocks and the South Shetlands, is probably
the best studied species and appears to be widely distributed on the South
Georgia shelf, where it is regularly taken in bottom trawls (Yau et al., 2002).
Adelieledone includes three species, with A. polymorpha and A. adelieana
recently removed from Pareledone, and the newly described A. piatkowski.
Three species of Graneledone (G. antarctica, G. macrotyla and G. gonzalezi)
are known from the Southern Ocean, but Kubodera and Okutani (1994)
found two other, undescribed, species oVthe Palmer Archipelago. Collins
et al. (2004) caught specimens of Graneledone in deep water near South
Georgia that diVered slightly from descriptions of the aforementioned
206 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
species, but too few specimens have been critically examined to distinguish
intraspecific from interspecific variation.
Thaumeledone includes three Southern Ocean deepwater species.
Thaumeledone gunteri is only found at South Georgia, where it is abundant
at depths >300 m (Yau et al., 2002; Allcock et al., 2004; Collins et al., 2004);
previous records from other areas (e.g., Kuehl, 1988) have probably been
misidentifications (Allcock et al., 2004). Thaumeledone rotunda appears to be
circum-Antarctic, whilst T. peninsulae was described from the Antarctic
Peninsula (Allcock et al., 2004). Specimens of Thaumeledone brevis (Hoyle,
1885) have been recorded in the Southern Ocean, but the work of Allcock
et al. (2004) has shown them to be misidentified, with T. brevis known only
from the type locality oVMontevideo (Uruguay).
Two new genera have been described from Southern Ocean octopods.
Bathypurpurata profunda is a pygmy deepwater species from the Antarctic
Peninsula (Vecchione et al., 2005), whilst the genus Praealtus was erected to
accommodate Praealtus paralbida from deep water north of the
South Shetland Islands (Allcock et al., 2004). Praealtus paralbida is very
similar to Bentheledone albida and may be conspecific, but until new material
is found from near the type location, B. albida is considered nomen dubium
(Allcock et al., 2004). Megaleledone setebos (¼M. senoi) is the largest South-
ern Ocean octopod, it is circum-Antarctic in distribution but does not extend
as far north as the sub-Antarctic islands (Allcock et al., 2003a). The genus
Benthoctopus is represented by two Southern Ocean species, Benthoctopus
thielei from Kerguelen and Benthoctopus levis from oVHeard Island, al-
though Piatkowski et al. (1998) found specimens similar to B. levis at the
Antarctic Peninsula.
Seven species (four genera) of cirrate octopods are reported in the Southern
Ocean. Three species of Cirroctopus, C. glacialis, C. antarcticus and C. mawsoni,
are found in the Southern Ocean. C. glacialis was described from a single
specimen trawled near Deception Island (Robson, 1930; Hardy, 1963)
but has subsequently been found abundantly around the Antarctic Peninsula
(Vecchione et al.,1998). The status of C. antarcticus, which was described
from 62 S in the Pacific sector (Kubodera and Okutani, 1986), is unclear.
O’Shea (1999) considered it a junior synonym of C. glacialis, but the description
of the beaks diVers from that of C. glacialis (Vecchione et al.,1998). Cirroctopus
mawsoni is recorded from the Indian Ocean sector (see O’Shea, 1999), and
Voss (1988) mentioned, without describing, another Cirroctopus species from
collections by FS Walther Herwig in the Scotia Sea. Stauroteuthis gilchristi
has been reported from South Georgia (Collins and Henriques, 2000; Collins
et al.,2004) but has also been caught in other parts of the Atlantic sector
(Collins, unpublished) and beaks from toothfish stomachs at Kerguelen have
been attributed to this species (Cherel et al., 2004). Opisthoteuthis hardyi is
known only from the type specimen (Villan ueva et al. , 2002), caught at
SOUTHERN OCEAN CEPHALOPODS 207
South Georgi a. Spe cimen s of the blind octopod Ci rrothaum a murrayi
were cau ght at 4,000 m in the Drake Pas sage ( Roper and Brunda ge,
1972; Voss , 1988 ) and from the Sc otia Sea (Colli ns, unpubl ished). This
specie s has an ap parent circum global distribut ion, but a critical revie w of
existing specimen s may reveal more than one species. Finally, the type
specimen of the rare large Cirrot hauma magna was cau ght between Prince
Edward and Crozet Islan ds ( Hoyle, 1886 ), on the edg e of the Southern
Ocean.
3.3. Decapod s
The Southern Ocean squids are prim arily pelagic species, whi ch are often
associated wi th pa rticular water mass es or frontal zones. Some specie s
have been caught wi th bottom trawls at South Georgi a (Col lins et al. ,
2004 ), but these catches are us ually from deep water with very few squid
taken in bottom trawls on the shelf. Spec ies suc h as G. glaciali s and
Psychrot euthis glacialis are rest ricted to cold Anta rctic waters, whi lst others
are associ ated with waters be tween the APF and the sub-A ntarctic Fron t
(SAF) ( Figures 5–8 ).
The onycho teuthids are large, muscular pelagi c squ ids, possess ing hooke d
tentacles and, in the Sout hern Ocean, are repres ented by the genera
Morot euthis (thr ee sp ecies), Kond akovia (1) and the recent ly descri bed
Notanyk ia (1). Morot euthis kni povitchi was or iginally descri bed from a spec-
imen taken north of South Georgi a ( Filipp ova, 1972 ) and has subseq uently
been report ed in the Scotia Sea (Rod house, 1989b; Rodhouse et al. , 1996 ),
oV Sout h Georgia ( Col lins et al. , 2004 ), and in the diet of seabird s at Croz et
(Cher el and Weim erskirch, 1999 ), an d is prob ably circum -Antarct ic, south
of the APF (Nesi s, 1987 )(Figure 5). M. ingens is also circum -Antarct ic,
further north than M. kni povitchi , typic ally sp anning the Antarcti c Polar
Frontal Zone (APFZ), and has been the subject of several studies around the
Falkland Islands, New Zealand and Kerguelen Island (Jackson, 1993, 1997,
2001; Jackson and Mladenov, 1994; Jackson et al., 1998a,b; Phillips et al.,
2001; Cherel and Duhamel, 2003). Moroteuthis robsoni has been recorded in
the Sc otia Sea (Rodhous e, 1990b) and elsewhere occurs oV the souther n tip
of South Africa and to the south of Australasia (Roper et al., 1984; Nesis,
1987). Kondakovia longimana, which reaches sizes in excess of 1 m ML
(Lynnes and Rodhouse, 2002), was originally described from the Scotia
Sea (Filippova, 1972), and although it is rarely caught in nets, evidence
from predators (Clarke and Prince, 1981; Clarke et al., 1981; OVredo
et al., 1985; Cooper et al., 1992a; Green and Burton, 1993) and strandings
(Lu and Williams, 1994b; Vacchi et al., 1994; Lynnes and Rodhouse, 2002)
208 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Figure 5 Distribution of Kondakovia longimana and Moroteuthis knipovitchi in
relation to the main water masses and fronts. Figures were modified from web pages
developed by Xavier et al. (1999). Red dots represent records of each species and
relate to references in Table 2. STF: sub-tropical front, SAF: sub-Antarctic front,
APF: Antarctic Polar Front, SACCF: Southern Antarctic Circumpolar Current
Front, SACCB: Southern Antarctic Circumpolar Current Boundary.
SOUTHERN OCEAN CEPHALOPODS 209
Figure 6 Distribution of Martialia hyadesi and Gonatus antarcticus in relation to
the main water masses and fronts. Figures were modified from web pages developed
by Xavier et al. (1999). Red dots represent records of each species and relate to
references in Table 2.
210 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Figure 8 Distribution of Psychroteuthis glacialis and Slosarczykovia circuman-
tarctica in relation to the main water masses and fronts. Figures were modified from
web pages developed by Xavier et al. (1999). Red dots represent records of each
species and relate to references in Table 2.
212 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
indicates a widespread circumpolar distribution, occurring as far south as
74 S in the Ross Sea (Figure 5). The recently described Notanykia africanae
(Nesis et al., 1998b) occurs in the sub-Antarctic region and is probably
circumpolar.
Two ommastrephid species Megaleledone hyadesi and Todarodes filippo-
vae are more northerly species that are periodically caught south of the APF.
As with other ommastrephids, they are muscular, reach relatively large size
and have been considered potential fishery targets (Rodhouse, 1989a, 1998;
Rodhouse et al., 1993). M. hyadesi has a circum-Antarctic distribution
typically associated with the APFZ (Figure 6) and is important in the diets
of many predators, particularly grey-headed albatross, whilst T. filippovae is
also circumpolar, usually between the APF and STF (Figure 6). The biology
of M. hyadesi has been studied in more detail than most Antarctic cepha-
lopods, with studies undertaken on adult distribution with respect to
oceanography, age, growth and diet (Rodhouse, 1990, 1991; Rodhouse
et al., 1992a; Gonzalez et al., 1997; Gonzalez and Rodhouse, 1998; Dickson
et al., 2004), but patterns of migration, spawning areas and paralarval
distribution remain largely unknown. Xavier et al. (2002a) reported the
presence of another ommastrephid squid, Illex argentinus, in the diets of
grey-headed and black-browed albatross at South Georgia and considered
that these were taken close to South Georgia. I. argentinus has been caught
in small numbers near the APF (Rodhouse, 1991) but is also the bait used by
toothfish long-liners at South Georgia, from which albatross frequently
scavenge, and this may be the source of these specimens.
The gonatids are typically high-latitude, cold water, oceanic, pelagic
squids and are represented in the Southern Ocean by Gonatus antarcticus.
G. antarcticus is a circumpolar species, primarily occurring between the
APF and the SAF, where it is locally abundant (Nesis, 1999a), but has
been caught south of the APF in the western part of the Atlantic sector
(Kubodera and Okutani, 1986; Rodhouse et al., 1996). The absence of
G. antarcticus from areas further south, such as Prydz Bay (Lu and Williams,
1994a), suggests that it is principally a sub-Antarctic species (Figure 6),
although beaks have been found in predator stomachs from further south
(e.g., Clarke and MacLeod, 1982a).
The cranchids (Galiteuthis, Mesonychoteuthis and Taonius) are generally
considered sluggish planktonic squids, but Mesonychoteuthis hamiltoni is
muscular, growing to extremely large size (Young, 2003). G. glacialis and
M. hamiltoni are both circum-Antarctic in distribution (Figure 7), whilst
Taonius pavo has only occasionally been found in the Southern Ocean. Like
many other Southern Ocean squid, M. hamiltoni was first described from the
remains in a predator stomach, in this case a sperm whale at the South
Shetlands (Robson, 1925). Juveniles were subsequently described by
McSweeney (1970) from collections in the Atlantic and Pacific sectors,
SOUTHERN OCEAN CEPHALOPODS 213
with others taken in Prydz Bay (Indian Ocean Sector) (Lu and Williams,
1994a) and the Atlantic sector (Rodhouse and Clarke, 1985). A large 2.5 m
ML specimen was captured at the surface in the Ross Sea, suggesting that
they can reach sizes in excess of the true giant squid (Architeuthis)(Young,
2003). G. glacialis is one of the most abundant and widely distributed
of the Antarctic squids, occurring only sporadically north of the APF
(McSweeney, 1978; Rodhouse and Clarke, 1986; Nesis et al., 1998a). A
single specimen preliminarily identified as Taonius pavo was caught near
South Georgia (Rodhouse, 1990), and beaks from this species have been
reported in the diets of toothfish (Xavier et al., 2002b) and grey-headed
albatross (Rodhouse et al., 1990) at South Georgia. Another species of
Taonius has also been identified from predators at Crozet and Kerguelen
(Cherel and Duhamel, 2004; Cherel et al., 2004).
Brachioteuthids are probably the most abundant squid in the upper
layers of pelagic waters of the Southern Ocean, where they are taken as
by-catch in krill trawls (Filippova, 2002); however, the taxonomy of the
family (Brachioteuthidae) is highly confused. Until recently, Brachioteuthis
specimens from the Southern Ocean were referred to either as B. ?picta
(Piatkowski et al., 1994; Rodhouse et al., 1996), B. ?riisii (Filippova, 1972)
or simply Brachioteuthis sp., although evidence from predators indicated the
presence of two species of Brachioteuthidae in the Southern Ocean (Cherel
et al., 2004). Lipinski (2001), albeit briefly, described two new species
of brachioteuthid, Slosarczykovia circumantarctica and Brachioteuthis
linkovskyi, and suggested that the former is widespread in the Southern
Ocean. Subsequently Collins et al. (2004) found specimens of S. circuman-
tarctica in waters around South Georgia and many previous records of
brachioteuthids in the Southern Ocean may be attributable to this species
(see Figure 7). Cherel et al. (2004) examined the beaks of the type specimens
of Lipinski’s new species and clarified previous identifications of
Brachioteuthis beaks. The lower beak of B. linkovskyi possesses a distinct
ridge, which is absent in the beak of S. circumantarctica. Beaks of S. circu-
mantarctica were previously described as Brachioteuthis ?picta (Rodhouse
et al., 1990, 1992c, 1998; Reid, 1995; Reid and Arnould, 1996; Berrow and
Croxall, 1999; Croxall et al., 1999; Daneri et al., 1999, 2000; Xavier et al.,
2002b,2003c), Brachioteuthis ?riisei (Cherel et al., 1996, 2002a,b,d; Catard
et al., 2000; Lea et al.,2002)orBrachioteuthis sp. (Clarke and MacLeod,
1982b). Beaks of B. linkovskyi were identified as Brachioteuthis ‘‘B’’ (Xavier
et al., 2002b, 2003c)orBrachioteuthis sp. (Cherel et al., 1996). However, a full
review of previously collected material has yet to be undertaken and the
family Brachioteuthidae remains in need of detailed revision.
P. glacialis (Psychroteuthidae) was originally described from fragments
found in the stomach contents of Weddell seals and penguins (Thiele, 1920).
Subsequently, Filippova (1972) provided a full description from intact
214 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
specimens that were caught in the Scotia Sea. P. glacialis is circumpolar,
extending to the Antarctic continent (Figure 8), with adults (max. reported
size 380 mm ML (Gro
¨ger et al., 2000) probably living near the bottom at the
shelf break area (300–1000 m) (Lu and Williams, 1994a; Collins et al., 2004).
Data from predators (OVredo et al., 1985; Lake et al., 2003) suggest that
P. glacialis is abundant in high Antarctic areas and extends as far north as
South Georgia in the Atlantic sector, but not beyond the APF. Despite the
importance of this species to predators (see later discussion), little is known
about the biology.
Alluroteuthis antarcticus (Family Neoteuthidae) is also circumpolar, hav-
ing been caught in the Atlantic (Rodhouse, 1988, 1989b; Anderson and
Rodhouse, 2002), and the Indian Ocean (Kubodera, 1989; Filippova and
Pakhomov, 1994; Lu and Williams, 1994a) sectors from the Antarctic conti-
nent to the APF. It grows to sizes in excess of 200 mm ML (Lu and Williams,
1994a), but the vast majority of captured specimens have been smaller than
50 mm. Beaks from larger specimens (lower rostral length up to 11 mm) have
been found in predator stomachs (Xavier et al., 2003c).
The family Batoteuthidae is monotypic, and Batoteuthis skolops is a
mesopelagic or bathypelagic species that was first described from four speci-
mens captured at RV Eltanin stations in the Pacific and Atlantic sectors
(Young, 1968). Subsequently, a small number of additional specimens have
been taken in midwater trawls in the Scotia Sea (Rodhouse et al., 1996;
Anderson and Rodhouse, 2002) and in bottom trawls at 700 m around
South Georgia (Collins et al., 2004).
The mastigoteuthids are bathypelagic squids. Lu and Williams (1994a)
caught 41 specimens (77–129 mm ML) of Mastigoteuthis psychrophila in pelagic
trawls in Prydz Bay and a small number have been caught in scientific midwater
trawls near South Georgia (Rodhouse, 1990; Rodhouse and Piatkowski, 1995;
Rodhouse et al.,1996; Collins, unpublished). In both Prydz Bay and north
of South Georgia, the majority of specimens have been taken at depths of
800–1000 m over deep water (Lu and Williams 1994a; Collins, unpublished).
The Histioteuthidae are mesopelagic and bathypelagic squids, found
throughout the world’s oceans, but only Histioteuthis eltaninae has been
recorded south of the APF (Rodhouse and Piatkowski, 1995; Rodhouse
et al., 1996; Collins et al., 2004), although Histioteuthis atlantica has been
reported in the diets of predators (Cherel and Duhamel, 2004; Cherel et al.,
2004). Three species of apparently widespread bathypelagic squids are
reported from the Southern Ocean. Chiroteuthis veranyi (Chiroteuthidae)
has been caught in closing nets fished to 1000 m and 2000 m in the Scotia Sea
(Rodhouse and Lu, 1998). Elsewhere, this species is found in the equatorial
Atlantic and Mediterranean and the species may be present throughout
the deep parts of the Southern Ocean. Bathyteuthis abyssicola occurs in the
Atlantic, Pacific and Indian Oceans (Roper, 1969). In the Southern Ocean, it
SOUTHERN OCEAN CEPHALOPODS 215
has been recorded in Pr ydz Bay (Lu and William s, 1994a ) an d at the APF
near Sout h Georgi a ( Rodho use et al. , 1996 ). Pholid oteuthis boschm ai has
been repo rted in the Sc otia Se a (Nemot o et al ., 1985 ) and possibly in the
diets of e mperor pe nguins from Adelie Land ( O Vredo et al., 19 85 ).
3.4. Geograph ic migra tion patte rns
Extensive migrations are common among the oceanic squids, particularly
the families Ommastrephidae and Onychoteuthidae. Typically, a passive mi-
gration takes eggs and paralarvae downstream in ocean currents, and juveniles
and a du lt s m ay the n mig ra te towa rd s fee ding grounds , wi th a n up st re am
migration to the spawning area completing the life cycle. These migrations are
linked to the ma jo r c ur re nt s ys te ms a nd the s ucc es s of a g en er at io n influenc ed
by oceanographic variability (O’ Do r, 19 92; Ander son and R odhous e, 2 00 1).
The m ig ra tions of M. hyadesi are not fully understood, and this species occa-
sionally appears on the eastern edge of the Patagonian shelf (Gonzalez et al. ,
19 97 ; Ande rs on and Rodhous e, 20 01) and ha s b e en take n at the APF (south-
wes t A tla nt ic) and northwe st of South G eo r gia (R odhous e et al ., 1996). Xavier
et al . ( 2 00 3a ,c ) ha ve shown inte ra nnual va ri abili ty in the av ail ab ili ty of
M. hyadesi t o pr ed a tors a t South Ge or gi a, whi ch m ay b e a conse que nce
of oc eanogr aphic va ria bilit y influenc ing m igr at ion pa tte rns. H ow ev er , insu Y-
cient data have been collected on the seasonal distribution of any Antarctic
spec ie s to de te rmi ne or de sc ribe s ea sonal c hang es in distr ibution p a tte rn s.
3.5. Vertical migr ation patterns
Many tempe rate planktoni c and ne ktonic anima ls, includi ng cephalopo ds,
are known to unde rtake daily , season al and ontog enetic verti cal migratio ns.
Diurn al vertical migr ation (DVM ) usually involv es anima ls migr ating from
deep wat er to the surface at night, althoug h revers e migran ts are known .
Various hypo theses ha ve been propo sed to e xplain DV M, including a void-
ance of visual predators and the energetic advantage of being in cool water
during the day. In the largely unstratified Southern Ocean, there will be
little energetic advantage in vertically migrating, so predator avoidance is
probably the principal reason for migrations (Robison, 2003). Studies with
opening and closing nets have revealed distinct patterns of DVM in
Slosarczykovia circumantarctica, which is generally deeper than 400 m by
day and migrates towards surface at night (Piatkowski et al., 1994). Juvenile
and subadult Gonatus antarcticus also migrate between 525 and 1000 m by
day to 60–200 m at night (Nesis, 1999a). Other species may also vertically
migrate, but the data are too scarce for any patterns to emerge.
216 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Ontogenetic shifts in bathymetric distribution are reported in many oce-
anic squid species (Clarke, 1966), typically with juveniles found in the
surface waters and adults deeper, although mature females of some species
migrate to the surface. Many Antarctic squids appear to follow this pattern,
although data from nets are rather limited, as scientific nets tend only to
catch the juveniles, with the adults able to avoid the nets, making inferences
from opening and closing nets diYcult to interpret. Russian data suggest
that Gonatus antarcticus undergo an ontogenetic descent, with larvae and
early juveniles in the surface 200 m layer, with growing squids gradually
moving deeper (Nesis, 1999a) and with juveniles and adults undertaking
diurnal vertical migrations. Mature squid are thought to be at 1000–2000
m(Nesis, 1999a). In G. glacialis (Rodhouse and Clarke, 1986)andA.
antarcticus (Rodhouse, 1988), there is also clear evidence of ontogenetic
descent. In G. glacialis, juveniles occur at depths of 200–400 m, with larger
specimens found deeper, concentrated in the 800–1000 m layer, with some
vertical spreading during the night. In other species, such as M. hamiltoni,
there is no evidence of ontogenetic descent, but the size range of specimens
caught is limited. M. hamiltoni juveniles (5–27 mm) were mostly caught
between 20 and 500 m, concentrated in the warm deep water, directly
below the Antarctic surface water (Rodhouse and Clarke, 1985). In Prydz
Bay, juveniles of P. glacialis (5–17 mm ML) were found close to the surface,
with adults generally deeper (Filippova and Pakhomov, 1994).
3.6. Mass strandings
Mass strandings of M. hyadesi have been reported in the Falkland Islands
(Nolan et al., 1998) and at Macquarie Island (O’Sullivan et al., 1983). The
cause of these strandings is not known, but other migratory oceanic squid
are known to strand occasionally and Nolan et al. (1998) speculated that this
was due to localised changes in oceanographic circulation trapping the squid
close to land.
4. GROWTH
4.1. Methods of measuring growth
The main methods of assessing growth in cephalopods are by counting
growth rings in statolith microstructure (squid only) (see Rodhouse
and Hatfield, 1990a; Jereb et al., 1991), analysis of length-frequency data
SOUTHERN OCEAN CEPHALOPODS 217
(e.g., Collins et al. ,1999) an d laborat ory-reari ng studi es (e.g., Forsythe and
Hanlon, 1989 ). How ever, all these methods are prob lematic and can be
subject to biases. Statol ith growth rings are now routin ely us ed to age sq uid,
but resul ts must be treated with cauti on unless the da ily pe riodicity of deposi-
tion has been valid ated, which is not the case for an y South ern Ocean specie s.
Furtherm ore, vali dation can only really be achieve d by maintaini ng squid in
laborato ry tanks, which is noto riously di Y cult. Octopo did specie s, which
cannot be aged using stato liths, can be kept in experi mental tank s, but it is
not know n whet her na tural rates of grow th a re reprodu ced in a c aptive
environm ent. Length-f requency an alysis has be en app lied to many tempe rate
and tropi cal specie s. In putative short- lived specie s, it require s regula r sam-
pling ov er the co urse of a year, which is not normal ly possibl e in the sh ort
Antarcti c field season and is sub ject to a num ber of pot ential biases, particu -
larly in migrator y specie s (Caddy, 1991; Hatfie ld an d Rodhouse, 1994 ).
4.2. Rate s of growth
Low tempe rature is a major fact or aVectin g metab olism and grow th in pola r
organis ms ( Clarke, 1998; Somero, 1998 ), with, in general , Anta rctic
ectoth erms showi ng consider ably lower grow th rates than warmer water
counterpar ts an d attaining larger final sizes. Most tropi cal and tempe rate
specie s of cephalopo d have short life cycles , with rapid grow th and longevi -
ty, typic ally 1 yr, but this is unlikel y to be the case in Southern Ocean
specie s, wi th low tempe ratur es and high ly season al primary an d secondary
producti on. In the only study to ha ve directly measur ed grow th in an
Antarcti c cephalopo d, Daly and Pec k (2000) determined the capti ve growth
of the octopod P. charcoti at 0 C. Growth rates were extremely slow (0.1%
body weight d
1
), although growth eYciency was high. Similar results have
been obtained for growth of Arctic octopodids such as Bathypolypus arcticus
(O’Dor and Macalaster, 1983).
Whilst statolith growth increments have been used in many temperate and
tropical species of squid (Rodhouse and Hatfield, 1990a), they have not been
applied to any of the high Antarctic species, and of the sub-Antarctic species,
only M. hyadesi and M. ingens have been studied in detail, and the growth of
these species is likely to be faster than the high Antarctic squid. Ageing studies,
based on the putative daily deposition of growth rings on M. hyadesi statoliths,
suggest a 2-yr life cycle (including egg stage) for animals caught at South
Georgia (Rodhouse et al., 1994; Gonzalez et al., 1997; Gonzalez andRodhouse,
1998) compared with estimates of 1 yr for Falklands-caught squid (Rodhouse
et al., 1994; Arkhipkin and Silvanovich, 1997). Growth rates at the APF were
1.10 and 1.06 mm ML d
1
for males and females, respectively, compared with
rates of 1.38 and 1.46 mm ML d
1
for Patagonian shelf animals. This may
218 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
support the hypothesis that growth is slower in cold Antarctic waters, but given
that M. hyadesi is migratory, they may have sampled the same population.
Growth of M. ingens, investigated in New Zealand waters, showed
that females (2.11 mm ML d
1
) grew at twice the rate of males (1.13 mm
ML d
1
), with mature females (maximum 5 Kg) reaching weights five times
those of males (Jackson, 1997). This study indicated a life cycle of 1yrin
New Zealand waters, assuming daily deposition of growth rings, but growth
may be slower in cold Southern Ocean water. Jackson and Lu (1994) exam-
ined the statolith microstructure of seven species of squid from Prydz Bay and
found clear increments, similar in appearance to daily increments in temper-
ate and tropical species, in K. longimana (445 mm ML), P. glacialis (95–142
mm ML), Brachioteuthis sp. (242 mm ML), M. psychrophila (116–129 mm
ML) and G. glacialis (185–355 mm ML). The number of specimens was small,
but in all cases, the increment count was <300. However, the deposition may
not be daily, particularly in the seasonal absence of diel light cues.
The presence of two to three size classes of P. glacialis in Prydz Bay (Lu
and Williams, 1994a), the Weddell Sea (Piatkowski et al., 1990)andin
stomach contents from predators (e.g., OVredo et al., 1985; Lake et al.,
2003) is indicative of an extended life cycle of 2 or perhaps 3 yr, with
considerably slower growth than temperate and sub-Antarctic species. How-
ever, based on evidence from predators (emperor and adelie penguins),
OVredo et al. (1985) suggested that the two size classes of beaks could be
explained as spent animals and new recruits, with a life cycle of 1 yr.
Multiple size classes could also be explained by multiple spawning events
within a year, but this appears less plausible in a highly seasonal system and
with putative planktonic paralarvae. Two size classes are also frequently
found in G. glacialis (Lu and Williams, 1994a; Rodhouse and Clarke, 1986).
Two species of Southern Ocean squid, K. longimana and M. hamiltoni,
reach extremely large size (Lynnes and Rodhouse, 2002; Young, 2003) and
are likely to live much longer than the 1 yr typical of temperate and tropical
squid species. Gigantism is common among polar (and deepsea) animals and
is typically associated with slow growth in cold oxygen-rich waters
(Atkinson and Sibly, 1997; Chapelle and Peck, 1999).
5. REPRODUCTION
5.1. Life-cycle strategies
With the exception of Nautilus, all extant cephalopods are semelparous, with
a single cycle of egg production, albeit with diVerent strategies for releasing
the eggs (Mangold, 1987). There has been considerable debate in recent
SOUTHERN OCEAN CEPHALOPODS 219
cephalopod literature regarding spawning strategies of species (Villanueva,
1992; Boyle et al., 1995; Rocha et al., 2001), with attempts made to categorise
the strategies of diVerent species; however, this pigeonhole approach is
probably not appropriate, with species occupying a continuum from a single
burst of spawning to a continuous release of individual eggs (cirrates). There
are limited data on reproduction in the high-latitude Antarctic cephalopods
and only slightly more in the sub-Antarctic species such as M. hyadesi and
M. ingens, but a certain amount of information can be inferred from closely
related species about which more is known.
5.2. Fecundity, egg size and development
Fecundity and egg size are essentially inversely related, with large egg size
necessitating reduced fecundity. Thorson (1950) suggested that, in general,
lecithotrophic and direct developing eggs would be expected at the poles,
with large eggs and extended development times, and this appears to be the
case in the Southern Ocean cephalopod fauna (Table 3). Within the Southern
Ocean octopods, the eggs are amongst the largest in the cephalopods and
consequently fecundity is low (Kuehl, 1988; Lu and Stranks, 1994; Collins
and Henriques, 2000). In the squids, eggs tend to be larger than confamilial
species from lower latitudes, with, for instance, M. hyadesi (1.9 mm) having
larger eggs than other ommastrephids. Eggs of M. ingens are 2.1 mm. Little
is known about egg size in the cranchiids, but Nesis et al. (1998a) found single
mature eggs in the ovaries of two spent G. glacialis with lengths of 3.2 mm,
rather large for an oegopsid squid. Laptikhovsky and Arkhipkin (2003)
caught a mature G. glacialis in deep water near the Falkland Islands, with
similarly sized mature eggs and relatively few (3600) oocytes in the ovary,
indicating relatively low fecundity. Nesis et al. (1998a) suggested that poten-
tial fecundity may be higher (40,000–80,000), but that a large portion of
the oocytes may not develop. In the north Atlantic, Gonatus fabricii has
large eggs (5 mm) (Bjrke et al., 1997), and egg size is probably similar in
G. antarcticus.
The inverse relationship between environmental temperature and duration
of embryonic development in marine poikilotherms is well established (Naef,
1928; Clarke, A., 1982). In cephalopods, the duration of the embryonic
phase is related to both egg size and incubation temperature (Boletzky,
1994, 2003; Nesis, 1999b), with smaller eggs having shorter embryonic
phases. The large size of Antarctic incirrate octopod eggs (8–19 mm)
(Table 3) indicates an extremely long developmental time, probably in excess
of a year if the data of Boletzky (1994:Figure 1) are extrapolated to
tempe ratures of <2 C. Based on egg size an d tempe rature, and Nesis
220 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
(1999b) suggested incubat ion times of 30 a nd 41 mo for C. glacia lis and
Megaleledone setebos, respectively. All cirrate octopods (e.g., Stauroteuthis
gilchristi and Cirroctopus spp.) have large eggs (9–16 mm), which are
laid individually and protected in a tough chitinous coat, again indicating
extremely long development. The squid generally have smaller eggs, although
Table 3 Egg size, fecundity and seasonality of reproduction in Southern Ocean
cephalopods
Egg size
(mm) Fecundity Seasonality Source
Martialia
hyadesi
1.9 115,000–560,000 Winter Laptikhovsky and
Nigmatullin,
1999
Todarodes
filippovae
1–1.5 million Laptikhovsky and
Nigmatullin,
1999
Moroteuthis
ingens
2.1 84,000–287,000 Winter Jackson and
Mladenov,
1994; Jackson
2001
Galiteuthis
glacialis
3.3 12,700–24,000
a
Nesis et al., 1998a
Pareledone
turqueti
19 37
b
Autumn? Kuehl, 1988
Adelieledone
polymorpha
14 34–65
b
Autumn? Kuehl, 1988
Adelieledone
adelieana
8–9 Lu and Stranks,
1994
Pareledone
sp.
c
18 21–58
b
Autumn? Kuehl, 1988
Pareledone
sp.
c
11–14 Lu and Stranks,
1994
Pareledone
harissoni
12–15 Not known Lu and Stranks,
1994
Megaleledone
setebos
18–19 Not known Lu and Stranks,
1994
Stauroteuthis
gilchristi
9.5 750 Not known Collins and
Henriques,
2000
Cirroctopus
glacialis
10 16 Not known Vecchione et al.,
1998
a
Minimum estimate.
b
Kuehl (1988) only included maturing and mature ova.
c
Recorded as Pareledone charcoti.
SOUTHERN OCEAN CEPHALOPODS 221
those of Southern Ocean squid tend to be larger than temperate counterparts,
again suggesting a relatively extended development.
5.3. Maturation and spawning
In a strongly seasonal environment, such as the Antarctic, it might be
expected that maturation and spawning would be highly seasonal, with
hatching timed to coincide with the productive summer period, although
this is not always the case in temperate species (e.g., Illex argentinus a winter
spawner) (Rodhouse and Hatfield, 1990b). However, the extended develop-
ment times at low temperatures, particularly in species with large eggs, will
make it diYcult to coordinate the timing of spawning with the brief summer
season and many species of octopod appear to have extended spawning
seasons or even spawn throughout the year (Kuehl, 1988; Allcock et al.,
2001; Yau et al., 2002).
In the squids, with smaller eggs, spawning may be more seasonal, and the
distinct size classes present in populations of Psychroteuthis and Galiteuthis
(Rodhouse and Clarke, 1986; Piatkowski et al., 1990; Lu and Williams,
1994a) are indicative of discrete spawning periods, as is the size frequency
of eggs in the ovary of mature G. glacialis (Laptikhovsky and Arkhipkin,
2003). Back-calculation of hatching dates from statoliths of M. hyadesi
suggests that spawning occurs in the winter in this species (Gonzalez et al.,
1997), although this would depend on the time taken to hatch.
In cephalopods, the females are generally larger than males, the main
exception being the loliginid squids that are not present in the Southern
Ocean. The larger size is probably achieved by faster growth rather than
greater longevity (e.g., M. ingens)(Jackson, 1997). In many cephalopods,
mating happens well ahead of spawning, with sperm transferred by a mod-
ified male arm (hectocotylus) and females using a range of methods to store
either spermatophores or sperm. Among the Antarctic squids, G. glacialis
females store spermatophores in the mantle wall (Nesis et al., 1998a). The
cirrate octopods lack a hectocotylus but transfer sperm packets, presumably
through the funnel, to the female, which are believed to be stored in the
oviducal gland (Aldred et al., 1983).
In some squid species, the adults migrate deep and it is possible that
spawning occurs in deep water, with either the egg masses rising to the surface
or females migrating to the surface with them, perhaps brooding them until
hatching. Female squid of the families Gonatidae (Seibel et al., 2000), Ony-
choteuthidae (Bello, 1998) and Cranchidae (Nesis et al., 1998a) are known to
undergo muscle degeneration and become gelatinous following spawning.
This gelatinous degeneration may be associated with an increase in buoyancy,
222 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
particularly once the eggs are released, making spent stages available to
surface (nondiving) seabird predators such as albatross (see Section 6.2).
6. TROPHIC ECOLOGY
Cephalopods clearly play an important role in the ecology of the Southern
Ocean, having been identified as key species in the diets of many higher
predators, including penguins, seals, albatross and cetaceans. Whilst Antarctic
krill are considered a key species in Southern Ocean food webs (particularly in
the Scotia Sea), linking phytoplankton to higher predators in short eYcient food
chains (Atkinson et al., 2001), a food web involving planktivorous mesopelagic
fish, cephalopods and higher predators provides an alternative and poten-
tially highly significant pathway in the Antarctic Polar Frontal Zone (APF)
(Rodhouse and White, 1995). Studies of predator diets and foraging have been a
major source of information on cephalopods in the Southern Ocean; however,
knowledge of the diets of squid and octopods in the Southern Ocean remains
rather limited.
6.1. Role as predators
The conventional method of studying the diet of squid is from stomach
contents analysis. However, because the prey of cephalopods is macerated
before swallowing, the identification of prey is not always straightforward
and is even more problematic in some octopus species where some digestion
occurs before ingestion. In many cases, squid reject the head of fish prey,
precluding identification from otoliths, and any soft-bodied prey are likely to
be underestimated. Alternative methods of investigating the diets of cepha-
lopods include serological methods (Grisley and Boyle, 1985; Kear, 1992)
and the use of biomarkers (e.g., Phillips et al., 2001, 2002, 2003a; Cherel and
Hobson, 2005). Serological methods are labour intensive, requiring antisera
to be developed for each putative prey species. The use of biomarkers, such
as fatty acids and stable isotopes, may prove a useful tool in determining
cephalopod diets. In a recent innovation, Cherel and Hobson (2005) have
demonstrated that stable isotope signatures in cephalopod beaks can be used
to investigate trophic ecology. Beaks of the same species show an increase in
D
15
N values with increased size, which agrees with a dietary shift from lower
to higher trophic levels with growth. DiVerences in D
15
N between species
indicated that the cephalopod fauna of Kerguelen operates over three
SOUTHERN OCEAN CEPHALOPODS 223
trophic levels, with large M. hamiltoni operating at a higher trophic level
than all other species investigated. DiVerences in D
13
C indicated that
Kerguelen cephalopods grow in three marine ecosystems, with most species
studied living in Kerguelen waters but with species migrating from both
Antarctic and subtropical regions. The ability to gain insights in cephalopod
trophic ecology from beaks represents a major advance, particularly with the
diYculty in capturing squid in nets and the availability of beaks from a range
of predators.
Data on Antarctic cephalopod diets are limited (Table 4), but in general
the squid are pelagic feeders, whilst the octopods, with the probable excep-
tion of Stauroteuthis gilchristi, are benthic feeders (see also Rodhouse and
Nigmatullin, 1996). In general, the squids are catholic opportunistic preda-
tors, feeding on a variety of fish, cephalopods and crustacea, with a general
shift from crustacea to fish with increased size (Rodhouse and Nigmatullin,
1996).
Largely on the basis of work undertaken by the former Soviet Union,
Filippova and Yukhov (1979) divided the squid into two trophic groups. The
first group, including brachioteuthids, live near the surface and feed almost
exclusively on crustaceans (krill, hyperiid amphipods and mysids). The second
group includes the larger species such as adults of Mesonychoteuthis and
Kondakovia, which are thought to inhabit the mesopelagic and bathypelagic
zones and feed mostly on vertically migrating fish, such as myctophids and
gonostomatids. These larger squid will feed on crustaceans during early life
and changes in the allometry of the brachial crown during ontogenesis are
associated with a shift in prey (Rodhouse and Piatkowski, 1995).
The only squids that have been the subject of detailed dietary studies are
the sub-Antarctic squids M. hyadesi and M. ingens (Table 4) and the adults
of both species feed on mesopelagic fish and invertebrates. The diet of
M. hyadesi is dominated by the hyperiid amphipod Themisto gaudichaudii
and myctophid fish (particularly Protomyctophum choriodon, Electrona
carlsbergi and KreVtichthys anderssoni)(Rodhouse et al., 1992a; Gonzalez
et al., 1997; Gonzalez and Rodhouse, 1998; Dickson et al., 2004), although
significant consumption of other cephalopods, including cannibalism, has
been reported (Gonzalez and Rodhouse, 1998).
The diet of M. ingens has been studied at various locations in the Southern
Ocean, to the north and south of the APF, and the diet is dominated by
mesopelagic (particularly myctophid) fish (Jackson et al., 1998b; Phillips
et al., 2001, 2003a,b,c; Cherel and Duhamel, 2003). In studies south of
the APF, the main prey species are myctophids of the genera Electrona,
Gymnoscopelus and KreVtichthys and the paralepid Acrtozenus risso (Cherel
and Duhamel, 2003; Phillips et al., 2003c). In common with many squid
species, there is evidence of a gradual switch from crustacea to fish and
squid with increasing size (Phillips et al., 2003b).
224 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Table 4 Diets of Southern Ocean squids
Species/location Size range (mm) Prey types Main prey species Source
Martialia hyadesi
South Georgia 278–370 Myctophids, crustacea
and cephalopods
KreVtichthys anderssoni,
Protomyctophum
choriodon, P. bolini,
Gymnoscopelus
nicholsi, Euphausia
superba, Gonatus
antarcticus
Gonzalez and
Rodhouse, 1998
South Georgia 190–310 (n ¼61) Myctophids,
euphausids,
amphipods
K. andersoni, Electrona
carlsbergi E. superba
Rodhouse et al., 1992a
Falkland Islands 190–350 (n ¼336) Myctophids,
euphausids,
amphipods and
cephalopods
K. anderssoni, G.
nicholsi, Themisto
gaudichaudii,
Martialia hyadesi
Gonzalez et al., 1997
Patagonian Shelf 220–370 Myctophids,
euphausids,
amphipods and
cephalopods
Protomyctophum
tenisoni, G. nicholsi,
M. hyadesi
Ivanovic et al., 1998
Scotia Sea 216–260 (n ¼25) Fish and cephalopods K. anderssoni, G.
nicholsi, Electrona
antarctica
Kear, 1992
South Georgia 225–312 (n ¼40) Amphipods,
myctophids and
cephalopods
T. gaudichaudii, K.
anderssoni, P.
choriodon
Dickson et al., 2004
Moroteuthis ingens
(Continued)
SOUTHERN OCEAN CEPHALOPODS 225
New Zealand 264–445 (n ¼37) Principally fish >90%;
9% squid
Stomias boa/Chauliodus
sloani,
Lampanyctodes
hectoris
Jackson et al., 1998b
Macquarie and Heard 150–432 (n ¼54) 96% Myctophids
Bathylagus
Electrona spp.,
Gymnoscopelus spp.,
P. bolini, K. andersoni
Phillips et al., 2001
New Zealand,
Macquarie,
Falklands
200–500 (n ¼316) Primarily myctophid
fish
L. hectoris, E. carlsbergi Phillips et al., 2003a
Falklands 75–375 (n ¼100) Crustacea, myctophids
and cephalopods
G. nicholsi, Loligo gahi,
Moroteuthis ingens
Phillips et al., 2003b
South Shetlands (n ¼1) Krill E. superba Nemoto et al., 1988
Kerguelen 112–286 (n ¼72) Principally fish, with
squid & crustacea
Arctozenus risso,
Paradiplospinosus
gracilis, M. ingens
Cherel and Duhamel,
2003
Kondakovia longimana
South Shetlands 60–360 (n ¼121) Macroplankton E. superba, T.
gaudichaudii, T.
macrura, amphipods,
chaetognaths, fish,
squid
Nemoto et al., 1985,
1988
Moroteuthis knipovitchi
South Shetlands 140–360 (n ¼23) Krill, fish Myctophids, E. superba Nemoto et al., 1985,
1988
South Georgia 212–321 (n ¼8) Krill, fish E. superba, G. nicholsi Collins et al., 2004
Moroteuthis robsoni
South Shetlands 60–100 (n ¼5) Euphausids E. superba Nemoto et al., 1988
Table 4 (Continued)
Species/location Size range (mm) Prey types Main prey species Source
226 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Alluroteuthis antarcticus
South Shetlands 40–140 (n ¼7) Macroplankton E. superba, T.
gaudichaudii, fish,
squid
Nemoto et al., 1985,
1988
Scotia Sea 221 (n ¼1) Euphausids, fish E. superba Kear, 1992
Prydz Bay (n ¼2) Squid, fish Psychrateuthis glacialis,
Pleurogramma
Lu and Willliams,
1994a
Galiteuthis glacialis
South Shetlands 100–240 (n ¼19) Macroplankton E. superba, T.
gaudichaudii,
chaetognaths
Nemoto et al., 1985,
1988
Macroplankton Eupausids, amphipods,
copepods and
chaetognaths
McSweeney, 1978
Prydz Bay 74–493 (n ¼3) Crustacea, fish E. superba Lu and Williams, 1994a
Slosarczykovia
circumantarctica
South Shetlands 40–160 (n ¼75) Krill E. superba Nemoto et al., 1985,
1988
Scotia Sea 67–113 (n ¼3) Crustacea Kear, 1992
Gonatus antarcticus
South Shetlands 40–160 (n ¼48) Krill E. superba Nemoto et al., 1988
Scotia Sea 57–375 (n ¼2) Unidentified fish Kear, 1992
Psychroteuthis glacialis
Scotia Sea 114–360 (n ¼13) Euphausids, fish E. superba,
Chionodraco,
Chaenodraco
Kear, 1992
Prydz Bay 121–201 (n ¼53) Krill & fish Pleuragramma,
E. superba.
Lu and Williams, 1994a
South Georgia (n ¼4) Krill E. superba Collins et al., 2004
SOUTHERN OCEAN CEPHALOPODS 227
Trophic links between Antarctic krill and squid are not well established. Krill
are not a major component of the diet of sub-Antarctic species such as M.
ingens or Martialia, but there are too few data on other species to consider the
role of squid in a krill-independent food chain that was proposed by Rodhouse
and White (1995) in the APF . M yctophi d fish are abu ndant in the Southern
Ocean, and like the squid, their role in the ecology of the ocean is poorly
known. Nemoto et al. (1985, 1988) found krill to be a major component in the
diet of a range of Antarctic squid species taken as by-catch in the Japanese krill
fishery to the north of the South Shetland Islands (Table 4). However, the
sample sizes were small, and most of the squid were small (so might be
expected to be feeding on crustaceans; see Rodhouse and Nigmatullin,
1996) and the association with krill aggregations may give a biased view.
Kear (1992) applied serological methods to determine the presence of krill in
the diet of 12 species of Antarctic squid and obtained positive results for six
(P. glacialis, M. psychrophila, M. knipovitchi, M. robsoni, Slosarczykovia
circumantarctica and M. hyadesi). Collins et al. (2004) also found krill to be
the major item in a small number of P. glacialis and M. knipovitchi stomachs
from specimens caught at South Georgia. The significance of krill in squid
diets is still not clear, but around South Georgia the availability of krill varies
both seasonally and interannually (Murphy et al. 1998; Brierley et al., 2002),
and with squid generally being catholic opportunistic predators, krill are
likely to be taken when abundantly available. Furthermore, at South Geor-
gia, myctophids of the genus Gymnoscopelus feed extensively on krill (Collins,
unpublished), so a food web involving squid and myctophids is unlikely to be
entirely independent of krill south of the APF.
Cannibalism is well documented in squids, either with larger members of
the cohort preying on smaller ones or with a larger cohort consuming
animals from a smaller cohort (see Johnston, 2002). Cannibalism appears
to be particularly important in the shoaling, muscular, migratory species
such as the ommastrephids (O’Dor, 1983; Lipinski and Linkowski, 1988)
where cannibalism may serve to fuel the migration during periods of poor
food availability (O’Dor, 1992). Among the Southern Ocean squids, canni-
balism has been recorded in M. hyadesi (Rodhouse et al., 1992a; Gonzalez
and Rodhouse, 1998; Dickson et al., 2004), M. ingens (Phillips et al., 2003a)
and P. glacialis (Lu and Williams, 1994a).
The diet of Antarctic octopods is also poorly known, although the incir-
rate octopods are all benthic feeders (Table 5). In a preliminary study,
Piatkowski et al. (2003) examined the diet of five incirrate species from the
Antarctic Peninsula and found amphipods, polychaetes and ophiuroids to
be the most common prey items. DiVerences in beak morphology between
species such as P. turqueti and Adelieledone polymorpha (Figure 9) suggest
diVerences in foraging and diet (Daly and Rodhouse, 1994), and Daly (1996)
228 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
examined the stomach and crop contents of these species at South Georgia
and found the diet of both species dominated by crustacea and polychaetes,
with bivalve and gastropod molluscs also taken by P. turqueti. Because of
the macerated nature of the contents and limited knowledge of the benthic
fauna, specific identifications were not possible, which is a common problem
in octopod diet studies. Vecchione et al. (1998) examined the stomach
contents of a small number of the cirrate octopod C. glacialis but only
found unidentifiable crustacean fragments. Given the diYculty in identifying
the prey of octopods, the use of biomarkers, such as fatty acids, may be
useful in determining broad patterns in diet and possible niche separation.
6.2. Role as prey
Cephalopods play an important role in the diets of Southern Ocean higher
predators, which have been estimated to consume in the region of 34 million
tonnes of cephalopods per annum (Clarke, 1983). In the Scotia Sea alone,
Croxall et al. (1985) estimated that predators take 3.7 million tonnes of
Table 5 Diets of Southern Ocean Octopods
Species/location Size range (mm) Prey types Source
Adelieledone
polymorpha
n¼41 Crustacea and
polychaetes
Daly, 1996
n¼3 Amphipods,
polychaetes
Piatkowski
et al., 2003
Pareledone
turqueti
n¼84 Crustacea,
gastropods,
bivalves &
polychaetes
Daly, 1996
Amphipods,
polychaetes, fish,
octopod
Piatkowski
et al., 2003
Megaleledone
setebos
n¼15 Ophiuroids,
amphipods, fish
Piatkowski
et al., 2003
Pareledone
charcoti
n¼33 Amphipods Piatkowski
et al., 2003
Benthoctopus cf
levis
n¼7 Amphipods, fish,
ophiuroids,
crustacea
Piatkowski
et al., 2003
Cirroctopus
glacialis
Unidentifiable
crustacean
fragments
Vecchione
et al., 1998
SOUTHERN OCEAN CEPHALOPODS 229
squid per annum. Four main methods have been used to determine
the cephalopod component of the diet of Antarctic higher predators:
stomach contents from dead animals; stomach flushing; regurgitations; and
faeces (scats). All these methods are highly dependent on the identification
of beaks, which was pioneered by Clarke ( 1962a, b, 1977, 1986 ). Beaks
are the major indigestible parts of cephalopods and their identification
to genus and in some cases species level (see Figure 9) has led to major
Figure 9 Lower beaks of some Southern Ocean cephalopod species (a) Pareledone
turqueti, (b) Thaumeledone gunteri, (c) Adelieledone polymorpha, (d) Stauroteuthis
gilchristi, (e) Chiroteuthis veranyi, (f) Martialia hyadesi, (g) Alluroteuthis antarcticus,
(h) Psychroteuthis glacialis, (i) Slosarczykovia circumantarctica, (j) Kondakovia
longimana, (k) Moroteuthis knipovitchi, (l) Mastigoteuthis psychrophila and (m)
Mesonychoteuthis hamiltoni.
230 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
advances in understanding the trophic ecology of cephalopods but is subject
to certain biases. In particular, beaks are frequently retained in predator
stomachs for considerable periods, potentially leading to an overestimation
of the importance of cephalopod prey (Piatkowski and Pu
¨tz, 1994), and
diVerent sized beaks may be diVerentially retained. Piatkowski and Pu
¨tz
(1994) showed that using only relatively undigested beaks, rather than all
beaks, had a major impact on the assessment of the importance of cephalo-
pods in emperor penguin diet. Furthermore, there has been considerable
confusion in the literature regarding the correct identification of beaks,
making comparisons between studies diYcult (see Imber, 1992). Part of
the problem is the lack of good reference collections of beaks from captured
squid, particularly large squid. For instance, two types of Psychroteuthis
beak have been described from predators, but the genus is considered
monotypic (Imber, 1992). However, the two types of beak are diVerent
sizes and may simply represent diVerent sizes of a single Psychroteuthis
species (Rodhouse, 1989b). Despite these diYculties, the use of beaks has
added greatly to our knowledge of Southern Ocean cephalopods and many
Antarctic cephalopods are better known from dietary studies of predators
than from captures in nets.
Biomarkers, such as fatty acids and stable isotopes, have been used to
indicate diet and trophic level of many predators (e.g., Lea et al., 2002).
However, the majority of the lipid in cephalopods is found in the digestive
gland, which is likely to be of dietary origin, and thus, the fatty acid signature
of a cephalopod may simply reflect that of its prey, which could lead to an
underestimate of the contribution of cephalopods (Phillips et al., 2002).
Cephalopod predators can be divided into four main groups: seabirds,
marine mammals, fish and other cephalopods. DiVerent predators forage at
diVerent depths (Figure 10) and over diVerent scales, taking a diVerent range of
species and sizes of cephalopods (Figure 11), not all of which will be Southern
Ocean species. Tables 6–10 include data from studies that have identified
cephalopods as prey, but for many species there are other studies that have
not found a cephalopod component in the diet. The method of reporting the
cephalopod contribution also varies between studies. Where percent mass is
used, it is often based on the reconstructed mass, estimated from the size of all
beaks, and may overestimate the relative amount of cephalopods taken.
6.2.1. Seabirds
Cephalopods are important in the diet of many seabird species and squid are
the major prey of grey-headed, wandering and light-mantled sooty albatross
(Table 6). In particular, M. hyadesi is the main prey of grey-headed albatross
(Clarke and Prince, 1981; Rodhouse et al., 1990; Xavier et al., 2003a,b,c),
SOUTHERN OCEAN CEPHALOPODS 231
whilst K. longimana is the main prey of wandering albatross and light-mantled
sooty albatross (Clarke et al., 1981; Rodhouse et al., 1987; Cooper et al., 1992a;
HoV, 2001; Xavier et al., 2003b). The foraging range of most albatross species
extends outside of the Southern Ocean (e.g., wandering albatross; Xavi er et al.,
2004), so some of the prey will be non–Southern Ocean species (Xavier et al.,
2003c); however, much of the diet work is undertaken during the chick-rearing
period when foraging trips are shorter (Weimerskirch et al., 1986).
Satellite tracking studies indicate that albatross frequently rest on the
surface at night, and this may well be the time that they feed, but the
question of when and how albatross feed remains largely unanswered
(see Croxall and Prince, 1994). The size of beaks found in wandering
albatross regurgitates (Figure 11) indicates that they are frequently taking
very large squid, particularly K. longimana, M. hamiltoni and M. knipovitchi.
Given that larger squid are generally found deeper and are capable of
rapid movement, it seems unlikely that albatrosses are taking these
large squid alive either by dip feeding or by diving in the surface layer
(Croxall and Prince, 1994). Instead, the wandering albatross probably
Figure 10 Foraging depths of Southern Ocean cephalopod predators. MP: maca-
roni penguin, GP: gentoo penguin, Ap: adelie penguin, GH: grey-headed albatross,
BB: black-browed albatross, WA: wandering albatross, FS: fur seal, KP: king pen-
guin, EP: emperor penguin, ES: elephant seal, SW: sperm whale. Depth in metres.
232 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Table 6 Cephalopod prey of Southern Ocean albatross
Predator Location % cephalopods in diet Main cephalopod prey Source
Wandering albatross
(Diomedea exulans)
South Georgia Not recorded Kol, Mor, Hi, Tap,
Tnd
Clarke et al., 1981
Circum-Antarctic Major Kol, Hia, Gag, Hie Imber, 1992
Marion Island 59% (mass) Kol, Mok, Moi, Ala Cooper et al., 1992a
Macquarie Island 100% (occurrence) Moi, Msp, Aa, Pb HoV, 2001
South Georgia 32% (mass) Kol Xavier et al., 2003b
South Georgia
1989–1989
Not available Kol, Tap, Hi Xavier et al., 2003c
Royal albatross
(Diomedea
epomophora)
New Zealand Major Moi, Hia Imber, 1999
Black-browed
albatross
(Thalassarche
melanophrys)
South Georgia 21% (mass) Mah*
1
, Meh,
Ancistrocheirus
Prince, 1980
South Georgia Not recorded Mah*
1
, Gag Clarke and Prince,
1981
South Georgia
(Feb)
31% (mass) Mah, Gag Rodhouse and Prince,
1993
South Georgia 23% (mass) Mah, Gag Croxall et al., 1999
South Georgia
(1996–2000)
7–49% (mass) Mah, Kol, Gag, Mok Xavier et al., 2003b
Grey-headed albatross
(Thalassarche
chrysostoma)
South Georgia 49% (mass) Mah*
1
, Meh Prince, 1980
South Georgia Not recorded Mah*
1
, Gag Clarke and Prince,
1981
Marion Island Not recorded Mok, Mor, Kol Brooke and Klages,
1986
South Georgia Not recorded Mah, Psg, Kol, Gag Rodhouse et al., 1990
South Georgia 37% (mass) Mah, Kol, Gag Croxall et al., 1999
South Georgia
(1996–2000)
17–75% (mass) Mah, Kol, Gag, Psg Xavier et al., 2003a
South Georgia
(2003)
40% (mass) Mah, Gag, Goa Catry et al., 2004
234 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Yellow-nosed
albatross
(Thalassarche
chlororynchos)
Prince Edward
Island
Not recorded Mok, Mor, Kol Brooke and Klages,
1986
Light-mantled sooty
albatross
(Phoebetria
palpebrata)
Marion Island Major Kol, Mok, Hie Berruti and Harcus,
1978
Marion Island Not recorded Gag, Mok, Kol, Psg,
Hie
Berruti, 1979
Prince Edward
Islands
Not recorded Kol, Ala Imber and Berruti,
1981
South Georgia 46% (mass) Mah, Gag , Psg, Goa Thomas, 1982
Macquarie Island Not recorded Kol, Psg, Mah, Ala,
Gag
Imber, 1991
Marion Island 34% mass (94%
occurrence)
Kol, Mok, Mor, Ala Cooper and Klages,
1995
Macquarie Island Kol, Ala, Gag, Mah Green et al., 1998
Heard Island 70–100% occurrence Kol, Gag Green et al., 1998
Not recorded
Sooty albatross
(Phoebetria fusca)
Marion Island Major Kol, Mok, Hie, Berruti and Harcus,
1978
Marion Island 42% mass (100% occ) Kol, Mor, Ch, Gag Cooper and Klages,
1995
Key: Ala ¼Alluroteuthis antarcticus;Bas¼Batoteuthis skolops;Ch¼Chiroteuthis sp.; Gag ¼Galiteuthis glacialis;Goa¼Gonatus antarcticus;Hi
¼Histioteuthis sp.; Hia ¼Histioteuthis atlantica; Hie ¼Histioteuthis eltaninae; Kol ¼Kondakovia longimana;Mah¼Martialia hyadesi;Meh¼
Mesonychoteuthis hamiltoni;Msp¼Mastigoteuthis psychrophila;Mo¼Moroteuthis spp.; Mok ¼Moroteuthis knipovitchi;Moi¼Moroteuthis
ingens;Mor¼Moroteuthis robsoni; Psg ¼Psychroteuthis glacialis;Pa¼Pareledone sp.; Pac ¼Pareledone charcoti; Pat ¼Pareledone turqueti; Slc ¼
Slosarczykovia circumantarctica; Tap ¼Taonius pavo; Tnd ¼Taningia danae;To¼Todarodes sp.; Tof ¼Todarodes filippovae.
*
1
Recorded as Todarodes.
*
2
Recorded as Brachioteuthis picta.
*
3
Recorded as Discoteuthis sp.
*
4
Recorded as Brachioteuthis ?riisei.
SOUTHERN OCEAN CEPHALOPODS 235
scavenge much of their food, and although some prey may be obtained from
discards from fishing vessels, this is unlikely to account for all prey. A more
plausible scenario is that the birds feed on post-spawning animals that lose
neutral buoyancy and rise to the surface (Lipinski and Jackson, 1989). In the
gonatids, onychoteuthids and G. glacialis, the mature females become highly
gelatinous after spawning, with the mantle muscle losing its structure
(Lipinski and Jackson, 1989; Nesis et al., 1998a). Spawning may occur in
the upper part of the water column, and as the female squid releases the last
of the egg mass, neutral buoyancy may be lost, causing it to float to the
surface. These post-spawning females may occur in a seasonal and geo-
graphically predictable manner, allowing albatross to take advantage.
Clarke et al. (1981) also suggested that some seabirds, particularly wander-
ing albatross, scavenge from squid remains vomited by sperm whales. Sperm
whales are reported to vomit during whaling activities, but also to periodi-
cally empty their stomachs of cephalopod beaks. This may be another
method by which seabirds ingest beaks from large squid and would lead to
an overestimation of the importance of cephalopods. Imber and Russ (1975)
suggested that bioluminescent squid are preferentially preyed upon, but as
Clarke et al. (1981) pointed out, most Southern Ocean squid lack biolumi-
nescence, and when present, it is on the ventral surface, which is unlikely to
increase their visibility from above.
Xavier et al. (2003b) combined satellite tracking of wandering and grey-
headed albatross with diet studies to determine the distribution of some of
the prey species. Such analyses may be valuable in tracing the distribution of
species that cannot be caught in nets but will be subject to the biases outlined
earlier in this chapter. However, by using only fresh material, indicative of
recent feeding, Xavier et al. (2003b) provided important data on interannual
variability of prey species such as M. hyadesi.
King, emperor, royal, gentoo, adelie, macaroni and rockhopper penguins
all take cephalopods (Table 7), but it is only the deeper diving king and
emperor penguins (Williams, 1995)(Figure 10) that take significant quanti-
ties in any location. The other penguins tend to forage closer to shore and
dive less deep, typically favouring krill and inshore fish. Cherel et al. (1996)
found that 65% of king penguin diet at Crozet was squid (mostly M. ingens),
whilst Piatkowski and Pu
¨tz (1994) found 54% of the diet of emperors in the
Weddell Sea area was squid (predominantly K. longimana, P. glacialis and
A. antarcticus). At South Georgia, the king penguins’ diet is dominated by
mesopelagic fish, with only small amounts of squid recorded (Olsson and
North, 1997; Rodhouse et al.,1998). In general, penguins take smaller sized
cephalopod prey than albatross (Figure 11).
Among the other flying seabirds, white-chinned petrel diet includes up to
25% squid at South Georgia (Croxall et al., 1995; Berrow and Croxall, 1999),
Marion Island (Cooper et al., 1992b) and Crozet Island (Ridoux, 1994), with
236 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Table 7 Cephalopod prey of Southern Ocean penguins (Key: see Table 6)
Predator Location % cephalopods in diet Main cephalopod prey Source
King penguin
(Aptenodytes
patagonicus)
Marion Island 17 % (mass) Kol Adams and Klages,
1987
Crozet 65% (mass) Moi, Mok, Mah Cherel et al., 1996
South Georgia
(summer)
3% (mass) Not identified Olsson and North,
1997
South Georgia
(summer)
3% (mass) Mah, Mok, Kol, Psg,
Ala
Rodhouse Olsson and
North, 1997, 1998
Falklands not recorded Mah, Moi, Mok Piatkowski et al., 1998
Emperor penguin
(Aptenodytes
forsteri)
Adelie Land Minor Psg, Goa, Kol OVredo et al., 1985
Adelie Land 1% (mass) Psg, Goa, Kol OVredo and Ridoux,
1986
Weddell 90–97% (occurrence) Kol, Psg, Ala Piatkowski and Pu
¨tz,
1994
Mawson Coast:
Auster Colony
45% (mass) Ala, Psg Robertson et al., 1994
Taylor Colony 69% (mass) Ala, Psg Robertson et al., 1994
Ross Sea 3% (mass) Psg Cherel and Kooyman,
1998
(Continued)
SOUTHERN OCEAN CEPHALOPODS 237
Gentoo penguin
(Pygoscelis papua)
South Georgia 1.2% (mass) Slc*
2
Croxall et al., 1999
Laurie Island 5% (mass) Psg Coria et al., 2000
Kerguelen up to 13% (mass) Kol, Goa, octopods Lescroe
¨let al., 2004
Adelie penguin
(Pygoscelis adeliae)
Adelie Land 3% (mass) Psg OVredo et al., 1985
Rockhopper penguin
(Eudyptes
chrysocome)
Marion Island 5% (mass) Kol, octopods Brown and Klages,
1987
Macquarie Island 2% (mass) Mah, Mo Hindell, 1988a
Marion Island 19% (occurrence) Kol, octopods Adams and Klages,
1989
Royal penguin
(Eudyptes schlegeli)
Macquarie Island 3% (mass) Mo, Mah Hindell, 1988b
Macaroni penguin
(Eudyptes
chrysolophus)
Marion Island 8–13% (mass) Kol Brown and Klages,
1987
South Georgia 1% (mass) Mah Croxall et al., 1999
Table 7 (Continued)
Predator Location % cephalopods in diet Main cephalopod prey Source
238 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
the main species taken being Gonatus antarcticus, G. glacialis and M. hyadesi.
Squid constitute the bulk of the diet of petrels of the genus Pterodroma at the
Prince Edward Islands (Schramm, 1986) and have been reported in small
quantities in the diets of blue petrels, giant petrels, Cape petrels, Antarctic
fulmars and blue-eyed shags (Table 8).
6.2.2. Seals
Of the seals, the southern elephant seal (Mirounga leonina)isprobablythe
most significant predator of squid, with many dietary studies indicating
that cephalopods are normally the preferred prey (Table 9); however, this is
based on a small number of studies and may be biased by the retention of beaks
in the stomach. Elephant seals typically forage at depths of between 200 and
700 m (Boyd and Arnbom, 1991) but are capable of diving to depths inexcess of
1,000 m (Slip et al.,1994). They take a range of cephalopod species and sizes
(Table 9;Figure 11), particularly K. longimana, M. hyadesi, M. knipovitchi and
A. antarcticus. Elephant seals also take benthic octopods, which indicates that
they forage on the sea floor and on pelagic squid prey, and this is supported by
studies of foraging ecology (e.g., McConnell et al., 1992)(Table 10).
Antarctic fur seals take a small amount of squid, but krill and fish usually
dominate the diet of this species (Reid, 1995; Reid and Arnould, 1996). In
some areas, cephalopods form a major part of the diet of Weddell seals with
M. knipovitchi, P. glacialis and P. charcoti the main prey species at the South
Shetlands and South Orkney Islands (Clarke and MacLeod, 1982b; Casaux
et al., 1997) and P. glacialis and Pareledone spp. the main cephalopod prey
at four sites in east Antarctica (Lake et al., 2003). P. glacialis was the main
prey item during spring on the Mawson Coast, with two distinct size classes
taken (Lake et al., 2003). From a small number of studies, cephalopods
appear to be the main prey of Ross seals (Oritsland, 1977; Skinner and
Klages, 1994), with Psychroteuthis, Galiteuthis and Alluroteuthis the main
species taken. However, Skinner and Klages (1994) noticed diVerences in the
prey spectrum between full stomachs and those containing just hard parts,
with fish comprising a greater part of the diet in animals with full stomachs.
Cephalopods have also been reported in the diets of crabeater and leopard
seals but are usually a minor component of the diet (Table 9).
6.2.3. Cetaceans
Since the cessation of commercial whaling, dietary data on cetaceans have
been limited to stranded specimens, but many toothed whales are thought to
be major consumers of cephalopods (Clarke, 1996). Sperm whales, which are
SOUTHERN OCEAN CEPHALOPODS 239
Table 8 Cephalopod prey of Southern Ocean petrels, fulmars and shags (key: see Table 6)
Predator Location % cephalopods in diet Main cephalopod prey Source
Northern giant petrel
(Macronectes halli)
South Georgia Not recorded Mah, Gag, Kol Hunter, 1983
Crozet 1% (mass) Kol Ridoux, 1994
Southern giant petrel
(Macronectes giganteus)
South Georgia Not recorded Mah, Gag, Kol Hunter, 1983
Ross Sea 74% (mass) Goa, Psg, Gag Ainley et al., 1984
White-chinned petrel
(Procellaria aequinoctialis)
Marion 17% (mass) Mah, Hi Cooper et al., 1992b
Crozet 25% (mass) Goa, Gag Ridoux, 1994
South Georgia 19% (mass) Mah, Goa Croxall et al., 1995
South Georgia 19–25% (mass) Gag, Goa, Kol Berrow and Croxall, 1999
South Georgia 20% (mass) Gag, Slc*
2
Berrow et al., 2000
Crozet 12% (mass) Slc*
4
Catard et al., 2000
Antarctic petrel
(Thalassoica antarctica)
AAT 75% (mass) Psg Norman and Ward, 1992
Weddell Sea 22% (mass) Goa, Psg Ainley et al., 1992
Ross Sea 86% (mass) Goa Ainley et al., 1984
Blue petrel
(Halobaena caerulea)
South Georgia 0.7 (weight)
6.4 (occasional)
Psg Prince, 1980
Kerguelen 2.1% (mass) Kol Cherel et al., 2002c
Cape petrel (Daption
capense)
Ross Sea 97% (mass) Not identified Ainley et al., 1984
Weddell Sea 19% (mass) Goa, Gag Ainley et al., 1992
King George Island <1% (mass) Not identified Creet et al., 1994
Antarctic prion (Pachyptila
desolata)
South Georgia 0.6 (mass)
8.9 (occasional)
Ala Prince, 1980
Kerguelen 3% (mass) Slc Cherel et al., 2002d
240 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Grey petrel (Procellaria
cinerea)
Crozet 70% (mass) Moi, Goa Ridoux, 1994
Mottled petrel (Pterodroma
inexpectata)
Ross Sea 98% (mass) Goa, Psg, Gag Ainley et al., 1984
Snow petrel
(Pagodroma nivea)
Ross Sea 35% (mass) Goa, Psg, Gag Ainley et al., 1984
Great-winged petrel
(Pterodroma macroptera)
Prince Edward Islands 90% (mass) Goa, Hi, Psg*
3
Schramm, 1986
Crozet 64% (mass) Ta, Goa, Hi Ridoux, 1994
Soft-plumaged petrel
(Pterodroma mollis)
Prince Edward Islands 89% (mass) Goa, Ch, Psg*
3
Schramm, 1986
Crozet 16% (mass) Hie, Tap Ridoux, 1994
Kerguelen petrel
(Pterodroma brevirostris)
Prince Edward Islands 70% (mass) Goa Schramm, 1986
Weddell Sea 24% (mass) Gag Ainley et al., 1992
Crozet 6% (mass) Kol Ridoux, 1994
Antarctic fulmar
(Fulmarus glacialoides)
Weddell Sea 53% (mass) Psg, Goa Ainley et al., 1992
AAT Not recorded Goa Norman and Ward, 1992
Ross Sea 94% (mass) Goa Ainley et al., 1984
South polar skua
(Catharacta maccormicki)
Ross Sea 72% (mass) Psg, Goa, Gag Ainley et al., 1992
Blue-eyed shag
(Phalacrocorax atriceps)
Bransfield Strait 0.1% (mass) Pa Casaux and Barreraoro,
1993
SOUTHERN OCEAN CEPHALOPODS 241
Table 9 Cephalopod prey of Southern Ocean marine mammals (key: see Table 6)
Predator Location Cephalopods in diet Main cephalopod prey Source
Elephant seal
(Mirounga leonina)
Signy Island 81% (occurrence) Mok, Goa, Pa, Clarke and MacLeod,
1982a
South Georgia 90% (occurrence) Mok, Kol, Psg,
Mah, Ala, Goa,
Rodhouse et al., 1992c
Heard 86% (occurrence) Slc*
2
Ala, Mok,
Moi
Green and Burton, 1993
Macquarie 100% (occurrence) Ala, Kol, Moi,
Mok,
Green and Burton, 1993
Heard Major Psg, Ala, Mok,
Kol, Goa, Pac
Slip, 1995
South Shetlands 72% (occurrence) Psg, Ala, Kol, Moi,
Mok, Tof
Daneri et al., 2000
King George Island Major Psg, Ala, Gag, Slc,
Kol, Goa
Piatkowski et al., 2002
Vincennes Bay, East
Antarctica
35% (occurrence) Psg, Ala HoVet al., 2003
Fur seal (Artocephalus
gazella)
Heard (Sep–Feb) <5% (occurrence) Not identified Green et al., 1989
Heard (winter) 49% (occurrence) Msp Green et al., 1991
Laurie Island
(South Orkneys)
34% (occurrence) Not identified Daneri and Coria, 1992
South Georgia
(winter)
1.3% (occurrence) Slc*
2
, Pat Reid, 1995
South Georgia
(Jan–Mar)
5% (occurrence) Mok, Slc*
2
, Ala, Pat Reid and Arnould, 1996
South Georgia <1% (occurrence) Mah North, 1996
South Orkney 34% (occurrence) Psg, Slc*
2
Daneri et al., 1999
South Shetlands 15% (occurrence) Psg, Slc*
2
Daneri et al., 1999
242 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Crabeater seals (Lobodon
carcinophagus)
Scotia/Weddell
Sea Pack Ice
2% (occurrence) Goa Oritsland, 1977
Weddell seal (Leptonychotes
weddellii)
McMurdo 17% (occurrence) Pa Dearborn, 1965
Scotia/Weddell
Sea Pack Ice
11% (occurrence) Not identified Oritsland, 1977
Deception 88% (occurrence) Mok, Psg, Pa Clarke and MacLeod,
1982b
Weddell Sea 28% (occurrence) Not identified Plo
¨tz, 1986
Davis 2% (mass) Not identified Green and Burton, 1987
Mawson 21% (mass) Not identified Green and Burton, 1987
McMurdo 0.7% (mass) Not identified Green and Burton, 1987
Weddell Sea 8.5% (mass) Psg, Pac Plo
¨tz et al., 1991
South Shetlands
(Jan–Feb)
66% (mass) Pac, Psg Casaux et al., 1997
Commonwealth
Bay
36% (mass) Pa Lake et al., 2003
Laresemann Hills 14% (mass) Pa, Psg Lake et al., 2003
Mawson 82% (mass) Psg, Pa Lake et al., 2003
Vestfold Hills 18% (mass) Pa, Psg Lake et al., 2003
Leopard seal
(Hydrurga leptonyx)
Scotia/Weddell
Sea Pack Ice
8% (occurrence) Not identified Oritsland, 1977
Antarctic
Peninsula
Up to 40% Not identified SiniVand Stone, 1985
Ross seal
(Omatophoca rossii)
Scotia/Weddell
Sea Pack Ice
79% Not identified Oritsland, 1977
Pack ice zone 94% (occurrence) Psg, Gag, Ala,
Kol, Ch
Skinner and Klages,
1994
Southern bottlenose
whale (Hyperoodon
planifrons)
Tierra del Fuego Not recorded Mah, Kol, Goa,
Hie, Tap
Clarke and Goodall,
1994
Heard Island Major Kol, Psg, Goa,
Gag, Mok, Ala,
Slip et al., 1995
(Continued)
SOUTHERN OCEAN CEPHALOPODS 243
Sperm whales
(Physeter macrocephalus)
Antarctica Major Mor, Mok, Kol,
Meh, Goa, Hi
Clarke, 1980
New Zealand Not recorded Not identified Clarke and Roeleveld,
1998
Pilot whale
(Globiocephala malaena)
Tierra del Fuego Not recorded Hie, Moi Clarke and Goodall,
1994
False killer whales
(Pseudorca crassidens)
Tierra del Fuego Not recorded Mah, Moi Alonso et al., 1999
Table 9 (Continued)
Predator Location Cephalopods in diet Main cephalopod prey Source
244 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
Table 10 Cephalopod prey of Southern Ocean fish and cephalopods (key: see Table 6)
Predator Location % cephalopods in diet Main cephalopod prey Source
Patagonian toothfish
(Dissostichus eleginoides)
Kerguelen 1% (occurrence) Unidentified Duhamel, 1981
Crozet 8% (occurrence) Unidentified Duhamel and Pletikosic,
1983
South Georgia
<300 m
1% (occurrence) Octopods Garcia de la Rosa et al.,
1997
South Georgia
1000–1500 m
15% (occurrence) Kol Garcia de la Rosa et al.,
1997
Macquarie
Island
35% (occurrence) Goa, Msp, cirrates Goldsworthy et al., 2002
South Georgia 7% (occurrence) Kol, Mok, Goa, Pat, Ala, Chv Xavier et al., 2002b
Kerguelen Not stated Kol, Chv, Goa, To Cherel et al., 2004
Crozet Not stated Kol, Moi, Goa Cherel et al., 2004
Antarctic toothfish
(Dissostichus mawsoni)
Ross Sea 14% (occurrence) Not identified Fenaughty et al., 2003
Lanternshark
(Etmopterus cf.
granulosus)
Kerguelen 86% (occurrence) Msp, Slc, Hia, Bas Cherel and Duhamel,
2004
Porbeagle shark
(Lamna nasus)
Kerguelen 92% (occurrence) Hia, To, Kol Cherel and Duhamel,
2004
Sleeper shark (Somniosus
cf. microcephalus)
Kerguelen 100% (occurrence) Meh, Kol, Tad Cherel and Duhamel,
2004
Squid (Martialia hyadesi) South Georgia 54% (occurrence) Goa, Mah Gonzalez and Rodhouse,
1998
SOUTHERN OCEAN CEPHALOPODS 245
capable of diving to depths in excess of 2000 m (Clarke, 1980), feed predom-
inantly on cephalopods. Clarke (1980) identified the squid beaks obtained
from 46 whales processed at South Georgia and a further 35 taken by the
pelagic whaling fleet in the Antarctic and found the most important species
to be M. hamiltoni (76% by weight) and K. longimana (17% by weight), both
of which grow to large size. Beaked whales are also considered to be major
cephalopod predators, but the diet of this group is poorly known (Goodall
and Galeazzi, 1985). Cephalopods formed the main part of the stomach
contents of a southern bottlenose whale stranded at Heard Island (Slip
et al., 1995). Other whales that are reported to take Antarctic cephalopods
are the long-finned pilot whale (Clarke and Goodall, 1994) and the false
killer whale (Alonso et al., 1999), but the cephalopod component of the diet
is relatively small.
6.2.4. Fish and other cephalopods
The shallow water Antarctic fish fauna is dominated by the notothenioids, the
diets of which have been studied in reasonable detail around Kerguelen and the
South Georgia/Scotia Sea area, but these rarely take cephalopod prey (see
Kock, 1987, 1992). Deeper-living fish such as toothfish (Dissostichus spp.)
and larger sharks such as the sleeper shark do take a significant quantity of
cephalopods. Adult toothfish live at depths of 200–2000 m and take a range of
cephalopod prey. At South Georgia, Xavier et al. (2002b) found that the diet
of long-line and pot-caught adult Patagonian toothfish (Dissostichus elegi-
noides) included around 7% cephalopods (frequency). Octopods were the most
frequently taken prey, but the squids K. longimana, M. knipovitchi and G.
antarcticus contributed the bulk of the biomass consumed. Garcia de la Rosa
et al. (1997) only found cephalopods in the larger (deeper) toothfish, with K.
longimana the only species identified. At Macquarie Island, where cephalopods
made up 32% (by mass) of the diet (Goldsworthy et al.,2002), the main species
taken was G. antarcticus. In the Ross Sea, Antarctic toothfish (Dissostichus
mawsoni) also take cephalopods, but the cephalopod component has not been
studied in detail (Fenaughty et al., 2003).
Cherel and Duhamel (2004) investigated the cephalopod component of
three shark species, taken as by-catch in commercial fishing operations at
Kerguelen. All sleeper sharks (Somniosus sp.) examined (36) had cephalopod
remains in the stomachs, with 18 species identified, the most important being
M. hamiltoni, Taningia danae, Kondakovia longimana and Architeuthis dux.In
porbeagle sharks (Lamna nasus) 20 out of 26 stomachs included cephalopod
remains, with 15 species identified, the most important being K. longimana
and Todarodes cf angolensis. Finally cephalopod remains were found in 12 out
246 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
of 32 lantern shark (Etmopterus sp.) stomachs, with M. psychrophila the
dominant species.
Squid frequently consume squid of their own (see earlier discussion)
and other species. Graneledone antarcticus is a common component of the
diet of M. hyadesi (Gonzalez and Rodhouse, 1998), with P. glacialis also taken.
7. PHYSIOLOGY
While the physiology of Antarctic fishes and other invertebrates has been
studied in detail, the Antarctic cephalopods have received little attention,
which probably reflects their low abundance, the diYculty of maintaining
captive animals and poor capture rates. The only detailed physiological
studies that have been conducted are on octopods of the genus Pareledone
(Por tner a nd Zielinsk i, 1998; Daly and Pec k, 2000 ). Portner and Zielin ski
(1998) showed that the uppe r letha l tempe rature for P. charcot i is 10 C,
which is considerably higher than the ambient temperature.
Daly and Peck (2000) maintained P. charcoti in captivity, developed
an energy budget and undertook comparative physiological studies with
the northern octopus Eledone cirrhosa. The captive respiration rate of
P. charcoti at 0 C was low, but consistent with predictions based on E.
cirrhosa respiration at 4.5 and 11 C, and with no evidence of metabolic
compensation for low temperature.
Bustamante et al. (1998) investigated the concentration of trace elements
in Benthoctopus thielei and Graneledone sp. from Kerguelen and found
elevated levels of cadmium, but low levels of zinc and copper. The source
of the high levels of cadmium is not clear but appears to be derived from diet
and the cadmium is likely to be transferred to higher predators, which also
show elevated cadmium.
8. COMMERCIAL EXPLOITATION
As yet no Antarctic cephalopods have been subject to significant com-
mercial exploitation. Squid fisheries usually target muscular species such
as the ommastrephids (e.g., Illex argentinus) and loliginids (e.g., Loligo
gahi), which support major fisheries on the Patagonian Shelf (Hatfield
and Rodhouse, 1991; Waluda et al., 2002). There are no loliginid squid in
the Southern Ocean, but the two ommastrephid species, M. hyadesi and
Todarodes filippovae, have been the subject of commercial interest.
SOUTHERN OCEAN CEPHALOPODS 247
Evidence from predators, particularly grey-headed albatross, suggests that
M. hyadesi is abundant in the South Georgia and Scotia Sea area, but a
series of short exploratory fisheries in the vicinity of South Georgia have
produced mixed results. In February 1989 two Japanese jigging vessels
undertook exploratory fishing near South Georgia, catching around 8 tonnes
of M. hyadesi close to the APF, northwest of South Georgia (Rodhouse,
1991). Further fishing to the north and south of South Georgia and at Shag
Rocks failed to catch any Martialia. In June 1996, 52 tonnes were taken
along the shelf break north of South Georgia and Shag Rocks by the Korean
jigger Ihn Sung 101 (Gonzalez and Rodhouse, 1998), but the same vessel
failed to catch any in January of the following year. In June 1997, 81 tonnes
were taken, again on the shelf break north of South Georgia, whilst the most
recent attempt in June 2001 caught just 2 tonnes (Dickson et al., 2004),
mostly in the area of the APF, but with some caught near Shag Rocks.
Outside Antarctic waters, Martialia is taken in some years in the Falkland
Islands jig fishery that targets Illex argentinus (Rodhouse, 1991). The ap-
pearance of M. hyadesi to the northeast of the Falklands appears to be
related to the extent of the cold-water Falkland Current spreading over the
shelf (Anderson and Rodhouse, 2001).
Given the abundance in predator stomachs, M. hyadesi is clearly season-
ally abundant in the Southern Ocean, but to date the fishers have been less
successful than the albatross at catching it. Should a fishery develop for
Martialia, it would be overseen by CCAMLR and require careful manage-
ment to avoid competition with the dependent predators (Rodhouse, 2005).
Rodhouse (1997) estimated that higher predators take 245,000 tonnes of
M. hyadesi in the Scotia Sea and proposed that any future fishery should
have a limited season avoiding the sensitive chick-rearing period of the main
predator, the grey-headed albatross.
Todarodes fillipovae is another muscular squid that may have fishery
potential but that to date has not been subject to any directed fishing.
Rodhouse (1998) appraised the potential for exploitation and considered
the management implications. As with M. hyadesi, it would need to be
carefully managed with full consideration of the impacts of dependent
species.
9. DISCUSSION
The evidence from higher predators suggests that cephalopods play a
significant role in the ecology of the Southern Ocean, linking macro-
zooplankton and fish with higher predators such as toothed whales, alba-
tross and elephant seals. However, this review highlights the paucity of basic
248 MARTIN A. COLLINS AND PAUL G. K. RODHOUSE
(distribution, ecology) data available for many species, and much of our
knowledge of the cephalopods has come from predator studies. Pelagic cepha-
lopods are notoriously diYcult to catch, and as much of the sampling in the
Southern Ocean has been undertaken with small scientific nets, catches have
been small. The use of commercial-sized nets and jigs has been more successful
in capturing mobile squid species, particularly the large adult forms.
The Southern Ocean cephalopod fauna is distinctive, with high levels of
endemism, particularly in the octopods and with some of the main groups
found in temperate and tropical areas absent. The squid typically occupy
broad often circumpolar ranges, whilst the octopods show greater diversity,
much of which is only now becoming apparent.
Problems still remain with the taxonomy of many of the groups, which
require detailed systematic studies, most notably in the Brachioteuthidae. It
has also been suggested that there is more than one Psychroteuthis species
and that Todarodes filippovae may include more than one species. Consider-
able taxonomic confusion remains in the benthic octopods, although work
(Allcock et al., 2003a,b, 2004; Allcock, 2005) has started to resolve some
important issues in the southwest Atlantic sector. As research extends into
deeper water, it is likely that more new species will be captured.
The cephalopods are usually considered to have a ‘‘live fast and die
young’’ semelparous life cycle, and while the Southern Ocean cephalopods
conform to the basic semelparous pattern, the rather sparse data indicate
that growth is considerably slower than equivalent temperate species. Even
within the same species (M. hyadesi), there is some evidence of slower
growth to the south of the APF than on the Patagonian Shelf. This slower
growth, presumably accompanied by greater longevity, is a consequence of
the low temperatures and the limited food supply outside of the produc-
tive but brief summer period. Despite the greater longevity, there is no
evidence to suggest that Southern Ocean cephalopods are anything other
than semelparous.
ACKNOWLEDGEMENTS
Thanks to Ian Rendal l and Liz White for the illu strations in Figures 3, 4, 8 and
10; Peter Fretwell for pr oducing Figure 1 and Jose Xavier for allowi ng
the modification of his maps for Figures 5–8. Richard Phillips helped
source information for the seabird predator section. Jose Xavier, Jon
Watkins, Louise Allcock and an anonymous referee provided constructive
comments on the manuscript. The photographs (Figure 2) were taken by
Louise Allcock, Amanda Lynnes, Inigo Everson, Chris Gilbert and Paul
Rodhouse.
SOUTHERN OCEAN CEPHALOPODS 249
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