Role of squid in the Southern Ocean pelagic ecosystem and the possible consequences of climate change

Deep-Sea Research II 95 (2013) 129–138

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Role of squid in the Southern Ocean pelagic ecosystem and the possible consequences of climate change Paul G.K. Rodhouse n British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 0ET, UK

a r t i c l e i n f o

abstract

Available online 13 July 2012

Southern Ocean squid are important predators and prey and are a potential fishery resource. Their future under climate change is analysed from predictions of change by 2100 and assessments of the effects on squid biology. There are  18 Antarctic species of squid. Young feed primarily on crustaceans and switch later to fishes. They are preyed on by odontocetes, seals and seabirds – which together consume  34  106 t yr  1 – and fish. As predators, squid are second to fish as biomass producers but recent evidence suggests predator consumption of squid needs to be reassessed. Fatty acid composition and stable nitrogen isotope ratios indicate some predators consume less squid in their diet than gut contents data suggest. Southern Ocean oceanography is unique in having circumpolar circulation and frontal systems and at high latitudes it is heavily influenced by sea ice. The Antarctic Peninsula is among the fastest warming regions worldwide but elsewhere the Southern Ocean is warming more slowly and the Ross Sea is probably cooling. Sea ice is receding in the Peninsula region and increasing elsewhere. Modelled predictions for 2100 suggest although the Southern Ocean will warm less than other oceans and sea ice will reduce. The Antarctic Circumpolar Current may shift slightly southwards with intensification of westerly winds but resolution of the models is insufficient to predict mesoscale change. Globally, pH of seawater has decreased by 0.1 units since the mid-1900s and is predicted to decrease by another 0.5 units by 2100. Impact on calcifying organisms will be high in the cold Southern Ocean where solubility of calcium carbonate is high. Predicted temperature increases are unlikely to have major effects on squid other than changes in distribution near the limits of their range; acidification may have greater impact. Small changes in large scale circulation are unlikely to affect squid but changes in mesoscale oceanography may have high impact. Change in sea ice extent may not have a direct effect but consequent ecosystem changes could have a major impact. Cephalopods are ecological opportunists adapted to exploit favourable environmental conditions. Given their potential to evolve fast, change in the Southern Ocean pelagic ecosystem might act in their favour. & 2012 Elsevier Ltd. All rights reserved.

Keywords: Squid Pelagic Ecosystem Southern Ocean Oceanography Climate change

1. Introduction This synthesis covers the Southern Ocean pelagic squid fauna, their distribution between the Antarctic continent and the SubAntarctic Front, their role as predators and prey, and their potential as a fishery resource. The future of Antarctic squid populations under global climate change is analysed by taking modelled predictions about changes in the physical environment by the end of this century and making an assessment of the effects of these changes on populations based on knowledge of squid physiology, life cycle biology and ecology. Since the early days of sealing and whaling in the Southern Ocean it has been known from the gut contents that cephalopods,

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and especially squid, form a major part of the diet of elephant seals, sperm whales and albatrosses. Given the pre-exploitation size of the whale and seal populations it has been equally clear that squid must be an important element of the Antarctic marine ecosystem. Nevertheless squid generally remain poorly sampled by nets and other means, especially in the Southern Ocean. However, their role as predators is reasonably well known and much can be inferred about their life style from their gut contents, their functional morphology and distribution as well as from knowledge of related squid species in other oceans. It has been possible to determine the role of squid in the diet of whales, seals, seabirds and fish because squid can be identified from their indigestible beaks which accumulate in the gut contents of their predators (Clarke, 1983). As well as enabling identification of the species of squid eaten by predators, the beaks can also be used to estimate the size of squid allowing estimates to be made of the biomass consumed.

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There are major squid fisheries to the north of the Antarctic on the Patagonian Shelf (Illex argentinus and Loligo gahi), in the Humboldt Current (Dosidicus gigas) and around New Zealand (Nototodarus sloanii and Nototodarus gouldi). No large scale exploitation has taken place in the Southern Ocean but there has been exploratory fishing in the Polar Frontal Zone of the Atlantic sector by squid jiggers fishing with lights for Martialia hyadesi (Rodhouse et al., 2001). The southern hemisphere fisheries for the ommastrephid squids: I. argentinus, D. gigas and the Nototodarus spp. have provided valuable insight into the way squid populations respond rapidly to annual environmental variability (Rodhouse, 2008). These insights in turn may provide an indication of how populations will respond to variability and change over longer time scales. Predictions about the effects of global climate change on the physical conditions in the Southern Ocean by 2100, taken together with what is known about squid ecology and life cycle dynamics, allows an assessment to be made about the effects of change on squid populations. Much of the biological information drawn on here has been reviewed by Boyle and Rodhouse (2005) and Collins and Rodhouse (2006). A major review of Antarctic climate change and the environment prepared by Turner et al. (2009) provides a valuable synthesis of information, including modelled predictions of changes in the physical conditions in the Southern Ocean by the end of the century. The Southern Ocean ecosystem has also been subjected to anthropogenic change driven by overexploitation of living marine resources for over two hundred years. Large scale sealing began, just four years after Cook’s second voyage (1772–1775) when reports of large populations of fur and elephant seals reached Europe and North America. Fur seals were brought to commercial extinction before the middle of the 19th century. Unsustainable exploitation of whales followed until the industry collapsed after the first half of the 20th century. This was followed by intensive fishing, mostly for southern rock cod, Notothenia rossii, Antarctic and Patagonian toothfish, Dissostichus eleginoides and Dissostichus mawsoni, icefish, Champsocephalus gunnari, and, for a limited period before the collapse of the Soviet Union, myctophids (mostly Electrona carlsbergi) were exploited. In some parts of the Southern Ocean fishing was at unsustainable levels leading to the commercial extinction of southern rock cod and some toothfish stocks (Collins et al., 2010; Kock, 1992). The ecosystem has not returned to its preexploitation state as evidenced by the state of stocks of whales, seals and fish. This needs to be borne in mind when trying to assess future climate related change.

2. The squid fauna of the Southern Ocean There are eighteen species of squid known from the Southern Ocean (Table 1) and it is likely that there are others yet to be discovered. Species known from higher latitudes occur in the gut contents of seabirds such as the wandering albatross sampled in Antarctic and Sub-Antarctic locations (Rodhouse et al., 1987). Although these were probably taken from north of the Sub-Antarctic Front (SAF) some may occur further south than those sampled to date. The Antarctic cephalopod fauna remains under sampled, partly because of the remoteness of the Southern Ocean particularly in the Pacific sector, but also because of the inadequacy of most research nets for sampling squid, especially larger specimens, which can escape small, slow moving nets by accelerating rapidly using jet propulsion. More sampling using commercial-scale pelagic nets is needed as these have been most effective at catching squid in the same size range as taken by predators (Rodhouse et al., 1996; Rodhouse and Boyle, 2010). Distribution of the Southern Ocean pelagic squid fauna is determined by latitude and can be classified in relation to the

Table 1 Distribution of the Southern Ocean squid fauna in relation to the latitudinal frontal systems (APF: Antarctic Polar Front; SAF: Sub-Antarctic Front; STF: Sub-Tropical Front). Distribution

Family

Antarctic endemics extending north to the APF

Onychoteuthidae Moroteuthis knipovitchi Neoteuthidae Alluroteuthis antarcticus Mastigoteuthidae Mastigoteuthis psychrophila Cranchiidae Mesonychoteuthis hamiltoni Onychoteuthidae Kondakovia longimana Psychroteuthidae Psychroteuthis glacialis Brachioteuthidae Slocarzykovia circumantarcticus Batoteuthidae Batoteuthis skolops Cranchiidae Galiteuthis glacialis Histioteuthidae Histioteuthis eltaninae Onychoteuthidae Moroteuthis ingens Gonatidae Gonatus antarcticus Ommastrephidae Martialia hyadesi Onychoteuthidae Moroteuthis robsoni Histioteuthidae Histioteuthis atlantica Ommastrephidae Todarodes filippovae Bathyteuthidae Bathyteuthis abyssicola Chiroteuthidae Chiroteuthis veranyi

Antarctic endemics extending north to the SAF

Antarctic endemics extending north to the STF Sub-Antarctic (APF–STF)

Southern hemisphere extending south to the APF

Cosmopolitan extending to south of the APF

Species

Note: The genus Moroteuthis referred to here, and in the literature to date, has recently been determined to be Onykia (Jereb and Roper, 2010).

major latitudinal frontal systems (Table 1). On the basis of current evidence there does not appear to be any species without a circumpolar distribution though there may be gaps between regions of abundance.

3. Squid as predators The foraging behaviour of Antarctic pelagic squid has not been observed in situ and the gut contents of squid are often difficult to identify. The food is finely chopped up by the beak before it enters the narrow oesophagus, which passes through the brain, so even recent meals may contain few identifiable remains. Immunological methods have been used but this was time consuming and limited to testing for specific prey (Kear, 1992). Nevertheless there have been several studies of squid prey in the Southern Ocean and much can be inferred from their functional morphology, distribution in the water column and from submersible and remote camera observations on related species elsewhere. The squid are all predators and are generally opportunistic foragers with the ability to feed on a wide range of prey type and size. Their preferred prey generally shifts as they grow and in the Southern Ocean pelagic realm this generally means early life stages feed on crustaceans and switch to fish later (Rodhouse and Nigmatullin, 1996). Ontogenetic changes in the allometry of the feeding structures (Rodhouse and Piatkowski, 1995) seem to reflect the pelagic biomass spectrum and probably facilitates the shift from one prey size group to another. Functionally the squids can be divided into two main groups which will differ in their foraging behaviour: those which are nonbuoyant, muscular and strong swimmers and others which attain buoyancy by replacing sodium chloride with lighter ammonium salts in vacuoles in their muscle tissue (Clarke et al., 1979). In the case of

P.G.K. Rodhouse / Deep-Sea Research II 95 (2013) 129–138

one family, the Cranchiidae, ammonium salts are stored in a fluid filled coelomic cavity. By evolving an incompressible, bathyscaphlike buoyancy mechanism the ammoniacal squids are able to make vertical migrations without suffering the gas-volume changes experienced by shelled cephalopods or by fishes with swim bladders. The muscular and ammoniacal (buoyant) species of Antarctic squid, their diet and distribution in the water column are identified in Table 2. Some squid families include both muscular and ammoniacal species. Among the most powerful, non-buoyant squid in the Southern Ocean are the ommastrephids, M. hyadesi and Todarodes filippovae and these are the only Southern Ocean species known to form schools. Neither species extends south of the Antarctic Polar Frontal Zone (APFZ) but here, M. hyadesi in particular, can be abundant and together with other squid species: Moroteuthis knipovitchi, Kondakovia longimana, Histioteuthis eltaninae, Gonatus antarcticus, Slocarzykovia circumantarcticus and

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Galiteuthis glacialis (Rodhouse et al., 1996; Rodhouse and Boyle, 2010) it occupies the ecological niche shared with epipelagic fish in other oceanic regions (Rodhouse and White, 1995). There are few epipelagic fish in the Antarctic because of constraints on white and red muscle physiology, the lack of a swim bladder in the Notothenioidea (the predominant sub-order among Antarctic fish) and the highly seasonal food supply that would limit planktovores (Eastman, 1993). The epipelagic squid, especially the ommastrephids, have no internal skeleton, other than a light gladius and possess a large oily digestive gland (Clarke et al., 1994) providing static lift. They also have well developed fins and swimming keels on the third arms which act as hydrovanes enabling ‘climb and glide’ behaviour which reduces the gross cost of swimming (O’Dor, 1988). These adaptations have enabled the squid to occupy the Southern Ocean epipelagic ecosystem despite the constraints on muscle physiology imposed by low water temperature.

Table 2 Buoyancy (from sources cited by Voight et al., 1994 and Jereb and Roper, 2010), diet (from sources cited by Collins and Rodhouse, 2006), vertical distribution (from Nesis, 1987) and inferred foraging behaviour of the Southern Ocean squid (from sources shown below). Family

Species

Buoyancy

Diet

Vertical distribution

Inferred foraging behaviour

Ommastrephidae

Martialia hyadesi

None

Mesopelagic fish; Antarctic krill; squid

Todarodes filippovae

None

Epi/mesopelagic/near seabed on continental slope Epi/mesopelagic/near bottom: continental shelves to near-bathyl

Diel vertical migrators feeding in epipelagic at night in open oceana Diel vertical migrators feeding in epipelagic at night in open oceanb

Moroteuthis knipovitchi

Ammoniacal

Mesopelagic/near bottom

Moroteuthis robsoni

None

Mesopelagic fish and Antarctic krill Antarctic krill

Moroteuthis ingens

Ammoniacal

Kondakovia longimana

Ammoniacal

Deep living/midwater feeder approaches surface at nightc,d Deep living, migrates into water column at night, does not approach surfacec Extensive vertical range, approaches surface at nightc Extensive vertical range, approaches surface at nightc

Psychroteuthidae

Psychroteuthis glacialis

None

Gonatidae

Gonatus antarcticus

None

No data

Brachioteuthidae

Slocarzykovia circumantarcticus Alluroteuthis antarcticus

None

No data

Ammoniacal

Epipelagic/mesopelagic/ bathypelagic Antarctic krill, fish, squid Mesopelagic

Batoteuthidae Bathyteuthidae Histioteuthidae

Batoteuthis skolops Bathyteuthis abyssicola Histioteuthis eltaninae Histioteuthis atlantica

Ammoniacal Ammoniacal Ammoniacal

No data No data No data

Meso/bathypelagic Meso/bathypelagic Meso/bathypelagic Meso/bathy/abyssopelagic

Chiroteuthidae Mastigoteuthidae

Chiroteuthis veranyi Mastigoteuthis psychrophila Galiteuthis glacialis

Ammoniacal Ammoniacal

No data No data

Bathyl/bathy/mesopelagic Meso/bathypelagic

Ammoniacal

Mesonychoteuthis hamiltoni

Ammoniacal

Bathy/mesopelagic//lower Antarctic krill, other epipelagic euphausids, chaetognaths, copepods, pelagic amphipods Large fish as adults Bathypelagic/near bottom (based on morphology)

Onychoteuthidae

Neoteuthidae

Cranchiidae

1

Rodhouse and Clarke (1985). Wormuth (1998). Dunning and Wormuth (1998). c Kubodera et al. (1998). d Rodhouse et al. (1996). e Rodhouse (1988). f Young and Roper (1968). g Roper (1969). h Voss et al. (1998). i Rodhouse and Lu (1998). j Lu and Williams (1994). k Rodhouse and Clarke (1986). a

b

Pelagic/near bottom

Mesopelagic fish, squid Near seabed/shelf to bathyl and Antarctic krill Epi/meso/bathypelagic/ Antarctic krill, pelagic amphipods, chaetognaths, fish, squid near bottom Antarctic krill, Antarctic Meso/bathypelagic/near silverfish, Chionodraco bottom Meso/bathypelagic

Deep living, may make vertical migrations at night but not near surfacee Deep living/midwater feeder approaches surface at nightd,e Feeds near surface but extends to deep waterd Feeds in midwater, small specimens approach surfacee Feeds in deep waterf Feeds in deep layers below 500 mg Deep feeder, juveniles near surfaced,h Deep feeder, juveniles within 100 m of surfaceh Deep feeder but data limitedi Deep feeder but data limitedj Feeds over wide vertical range, juveniles approach surfacek

Adults feed in deep water, juveniles approach surface1

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Other large, muscular, non-buoyant squid in the Southern Ocean include the Moroteuthis species and the high Antarctic endemic, Psychroteuthis glacialis. These generally live close to the seabed but do extend upwards into the mesopelagic. The ammoniacal squids are mostly deepwater species though is it clear from the evidence of near surface feeding predators that they must approach the sea surface sometimes, if not regularly. Given their musculature and the morphology of the brachial crown, some including the Histioteuthis spp. are active predators but others like Chiroteuthis, Mastigoteuthis and Galiteuthis live a relatively passive lifestyle, hanging vertically, head down in the water column with arms and tentacles spread below them to capture passing prey. One exception is almost certainly Mesonychoteuthis hamiltoni, the so-called colossal squid which grows to a mantle length of at least 2 m. This is an ammoniacal cranchiid, but it is very powerfully built. It is taken as an occasional by-catch in toothfish fisheries in the Southern Ocean, and it probably preys actively on these large fish to depths 4 1000 m in the high Antarctic where the Antarctic toothfish, D. mawsoni occurs and in the Sub-Antarctic habitat of D. eleginoides occurs. Cherel et al. (2009) have demonstrated, using stable nitrogen isotope ratios, that M. hamiltoni in slope waters of the Sub-Antarctic Kerguelen Islands occupy a distinct, higher trophic level than other cephalopods in the same habitat confirming its role as a top predator.

4. Squid as prey Use of indigestible squid beaks from the gut contents of Antarctic predators to identify squid prey and estimate consumption was pioneered by Clarke (1962) who went on to make a comprehensive study of the cephalopod prey of sperm whales in the Southern Ocean (Clarke, 1980). Since then at least 140 papers have been published by numerous authors documenting the squid prey of other Southern Ocean toothed whales, seals, seabirds, fish and cephalopods (Collins and Rodhouse, 2006). The proportion (in terms of mass) of cephalopods and, or, percent occurrence in the diet of some of the most important Southern Ocean squid predators is given in Table 3. Clarke (1980) reports that cephalopods comprise most of the diet of sperm whales in all regions of the world’s oceans apart from Icelandic waters. There is little evidence in their stomach contents that elephant seals consume prey other than cephalopods and they have been found in up to 100% of all seals sampled. Up to 94% of Ross seals sampled have been found to contain cephalopod remains. Cephalopods are a major prey of southern bottlenose whales and, although there are no data on their relative importance, they are also consumed by long finned pilot whales and false killer whales. Several large fish species consume cephalopods: Patagonian toothfish (up to 35% occurrence); Antarctic toothfish (14% occurrence); lantern shark (86% occurrence); porbeagle shark (92% occurrence) and sleeper shark (100% occurrence). Cephalopods occur in the diet of the squid M. hyadesi (54% occurrence) but this includes cannibalism. In spite of the shortcomings associated with analysis of gut contents more is known about the Southern Ocean cephalopod fauna from dietary studies than from material caught with nets. The predators of squid range over large areas of the ocean, covering regions that have been little sampled by nets and some, especially sperm whales, elephant seals, and emperor and king penguins dive to substantial depths so the spatial coverage provided the by predators is substantial. Satellite tracking of squid predators has been used to extend knowledge of squid distribution (Xavier et al., 2006) and there is further scope for research using instrumented predators fitted with cameras as has been done with Antarctic krill predators (Takahashi et al., 2004).

Table 3 Summary of percentage mass and occurrence of cephalopods in the diet of Southern Ocean predators (sources cited in Collins and Rodhouse, 2006). Predator category

Predator

Percentage mass

Percentage occurrence

Flying birds

Wandering albatross Royal albatross Black-browed albatross Grey-headed albatross Yellow-nosed albatross Light-mantled sooty albatross Sooty albatross Northern giant petrel Southern giant petrel White-chinned petrel Antarctic petrel Blue petrel Cape petrel Antarctic prion Grey petrel Mottled petrel Snow petrel Great-winged petrel Soft-plumaged petrel Kerguelen petrel Antarctic fulmar South polar skua Blue-eyed shag King Emperor Gentoo Adelie Rockhopper Royal Macaroni Elephant Fur seal Crabeater Weddell Leopard Ross Southern bottlenose

32–59 Major 7–49 49–75 Present Major

100

42 1 74 17–25 22–86 1–2 1–97 1–3 70 98 35 64–90 16–89 6–70 53–94 72 o1 3–65 1–69 1–13 3 2–5 3 1–13

100

Sperm Pilot False killer

100 Present Present but no % data

Penguins

Seals

Toothed whales

Fishes

Patagonian toothfish Antarctic toothfish Lantern shark Porbeagle shark Sleeper shark

70–100

90–97 19

35–100 Up to 49 2 2–82 Up to 40 Present

94 Present 100 Present Present but no % data 1-35 14 86 92 100

On the basis of data from beaks the total annual consumption of cephalopod biomass (mostly squid) by higher predators in the Southern Ocean was estimated by Clarke (1983) to be 34  106 t yr  1. Croxall et al. (1985) estimated consumption in the Scotia Sea alone to be 3.7  106 t yr  1. Using these data and published data on other major groups of producers Harvey Marchant and Simon Wright (Pers. com) have determined that squid are second only to fish in terms of total annual biomass production by higher predators in the Southern Ocean (Table 4). Although there are sometimes large numbers of squid beaks in the gut contents of Antarctic higher predators there is an on-going debate about the relative importance of squid in the diet of one predator in particular, the southern elephant seal. Rodhouse et al. (1992) examined squid beaks collected by stomach lavaging anaesthetised seals and suggested, on the basis of experiments on other seal species by Bigg and Fawcett (1985), that the data collected might overestimate the importance of squid in the diet

P.G.K. Rodhouse / Deep-Sea Research II 95 (2013) 129–138

Table 4 Annual production of major producers in the Southern Ocean. Trophic level

Group

Annual production 106 t

Primary producers Secondary producers (protozoan) Secondary producers (prokaryote) Secondary producers (metazoans—invertebrates)

Phytoplankton Protozoa Bacteria Copepods Salps Antarctic krill Squid

6000 1500 800 4300 100 100–200 40

Fish Seals Whales Penguins

100 10 5 0.8

Higher predators (metazoans—invertebrates) Higher predators (metazoans—chordates)

because it is likely that the indigestible beaks are preferentially retained in the stomach and so accumulate, while fish bones being more digestible disappear from the gut faster. Subsequent analysis of fatty acids in the milk and blubber of Mirounga leonina by Brown et al. (1999) and Bradshaw et al. (2003) seemed to confirm that these seals eats more fish than analysis of gut contents would suggest—particularly in winter when the seals are foraging close to the Antarctic continent. However, most of the lipid in squid is found in the digestive gland and is of dietary origin so the total fatty acid signature of squid will reflect their prey (Phillips et al., 2002). The diet of larger, pelagic squid in the Southern Ocean often includes mesopelagic fish (Table 2) so it is likely that the milk or blubber of M. leonina which had been feeding on squid would have a fatty acid signature erroneously consistent with a mesopelagic fish diet. Cherel et al. (2008) have recently estimated the trophic position of elephant seals from the Kerguelen archipelago by analysis of stable nitrogen isotope ratios in blood samples and also found there is evidence that M. leonina feeds primarily on mesoplegaic fish. This analytical approach may be less biased than fatty acid signatures. But the fact remains that large numbers of squid beaks have regularly been found in M. leonina gut contents so they undoubtedly consume large numbers of squid. These conflicting observations remain to be fully reconciled. The seals probably feed on both prey types and new data are needed to determine the relative proportions and how they change with season, foraging area, age of seal, etc. The wider question is whether other squid predators take a more varied diet than the evidence of their gut contents suggests. King penguins were classified as squid predators on the basis of beaks in the gut contents (Croxall and Prince, 1980) but later evidence demonstrated that they prey primarily on mesopelagic fish (Raclot et al., 1998; Cherel et al., 2002). Sperm whales killed in the Southern Ocean generally had mostly squid remains in the gut contents (Clarke, 1980). However, some Russian data (Filippova, 2002) have revealed that they also feed on toothfish, though there is no indication of the relative importance of this fish in the diet. Researchers have generally recognised the potential for bias inherent in using analysis of gut contents to construct marine food webs. This potential is highlighted by the more recent data on fatty acids and stable nitrogen isotopes but these also have their limitations. The emerging field of molecular scatology (sequencing bar code genes in faeces and gut contents) holds some promise though it has its own limitations, for instance it can only provide semi-quantitative data on diet composition (Deagle et al., 2005). In the meantime the relative importance of the prey of some Southern Ocean squid predators is uncertain.

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5. Squid fisheries There is no substantial fishery for squid in the Southern Ocean but two species of ommastrephid, M. hyadesi and T. filippovae are caught to the north of the SAF and are of some fishery interest further south, at least to the APFZ (Rodhouse et al., 2001). Exploratory fishing in the Atlantic sector has taken small catches of M. hyadesi which have thrown light on the ecology of pelagic squid in the APFZ that could not have been obtained by scientific sampling (Dickson et al., 2004; Gonza´lez et al., 1997; Gonza´lez and Rodhouse, 1998;Rodhouse, 1991) but no large-scale fishery has developed. T. filippovae may have some fishery potential in the northern part of the Southern Ocean (Rodhouse, 1988) but to date there has been no targeted fishing. Intensive exploitation of M. hyadesi at unsustainable levels would have potentially damaging consequences for dependent predators and precautionary measures were established for CCMLR (Commission for the Conservation of Antarctic Marine Living Resources) by Rodhouse (1997) in anticipation of a fishery starting up. These measures were based on estimates of biomass consumed by predators from gut contents data. If the lower estimates of biomass consumed by predators obtained by more recent analytical methods (fatty acid composition and stable nitrogen isotope ratios) prove to be correct then the calculations based on gut contents will have overestimated consumption. If this is the case, the precautionary ‘total allowable catch’ will need to be revised downwards. In the meantime an experimental fishery, pursued and monitored under a precautionary approach and taking the predators needs into account (Rodhouse, 1997), would provide valuable information independent of data from predators.

6. Physical oceanography of the Southern Ocean The Southern Ocean surrounds the Antarctic continent and is continuous with the southern parts of the Atlantic, Indian and Pacific Oceans (Fig. 1). Its narrowest part is the Drake Passage between South America and the Antarctic Peninsula. Three deep sea basins are separated by three systems of ridges: the Scotia ridge, the Kerguelen Plateau and the Macquarie Ridge. The periAntarctic islands are located on these ridges. The dominant geostrophic flow of the Antarctic Circumpolar Current, is west to east, driven by the prevailing westerly winds. Close to the Antarctic continent easterly winds drive the flow from east to west. At the surface, water masses are defined by a series of circumpolar fronts—from north to south these are the: Sub-Antarctic Front (SAF, which is considered here to mark the northern limit of the Southern Ocean), the Antarctic Polar Front (APF), formerly known as the Antarctic Convergence and the northern limit of Antarctic waters), the Southern Antarctic Circumpolar Current Front (SACCF) and the Southern Antarctic Circumpolar Current Boundary (SACCB) (Fig. 1). There are clockwise gyres in the two major embayments of the Antarctic continent, the Weddell and Ross Seas. The vertical structure and dynamics of the Southern Ocean are unique in the world’s oceans and the overturning circulation is an important component of the thermohaline circulation of the global ocean, particularly in the Atlantic sector. Relatively warm circumpolar deep water (CDW) flows at intermediate depths south towards Antarctica and rises towards the surface south the APF. The upper layer of the UCDW starts to flow northwards as it approaches the surface. The lower layer of the LCDW, which extends further towards Antarctica, sinks in the vicinity of the continent and forms Antarctic Bottom Water (AABW) which then flows northwards into the North Atlantic (Fig. 2). The high latitude Southern Ocean is dominated by the annual sea ice cycle. The ice extends over approximately 3  106 km2 in

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summer increasing to some 19  106 km2 in winter (Turner et al., 2009). At its maximum sea ice extends over an area greater than that of the Antarctic continent (  14  106 km2).

7. Climate change and the Southern Ocean The Antarctic Peninsula region is one of the three places on the planet, and the only one of the three in the Southern Hemisphere,

Fig. 1. Bathymetry and four circumpolar frontal systems (from the north: SubAntarctic Front; Antarctic Polar Front; Southern Antarctic Circumpolar Current Front; Southern Antarctic Circumpolar Current Boundary) of the Southern Ocean. Currents flow west to east (clockwise in this figure) except close to the coast where the direction is east to west (from Orsi et al., 1995).

where surface air temperatures are warming the fastest (http://data. giss.nasa.gov/gistemp/). Increases measured at the Argentine Islands have been þ0.53 1C per decade between 1951 and 2006. Warming of the air on the eastern side of the Peninsula has been linked to stronger westerly winds associated with changes in the Southern Annular Mode (SAM) and has been attributed to anthropogenic activity (Marshall et al., 2006). Sea temperatures in the region are also warming—most quickly at the surface but the effects can be measured to a depth of 100 m (Meredith and King, 2005). Elsewhere, in the Antarctic surface air temperature increases have been less in West Antarctica (þ0.1 1C per decade) and have cooled on the Plateau (Turner et al., 2009). Modelled predictions for increase in overall temperature by 2100 are 0.5–0.75 1C in the Southern Ocean. This is less than for other parts of the world ocean (Turner et al., 2009) and it will not be uniform; the Antarctic Peninsula region is likely to continue to warm faster than elsewhere. Nevertheless if temperatures in eastern Antarctica are being held down by recent trends in the polar vortex of the lower stratosphere, due to thinning of the ozone layer (Thompson et al., 2011), then as ozone concentrations recover this trend may reverse in due course and drive ecological change here as well. Between 1979 and 2008 total sea ice extent around Antarctica has increased by a mean of 0.9% per decade. However, trends differ markedly in different sectors. In the Bellingshausen/Amundsen Sea sector ice extent has decreased by 6.8% per decade whereas in the Ross Sea sector there has been an increase of 4.3% per decade. These areas are adjacent and the changes seem to be due to advection of ice from the former sector into the latter driven by deepening of the Amundsen Sea Low, which in turn has been caused by reduction of stratospheric ozone (Turner et al., 2009). Overall sea ice extent is predicted to reduce over this century. Model predictions for physical conditions in the Southern Ocean, summarised by Turner et al. (2009), indicate that present warming of surface water and mid-depth layers will continue and extend deeper so that by 2100 bottom waters may be warmer by 0.25 1C. Generally surface temperatures are predicted to increase less than in other oceanic regions but the models indicate that the area of sea ice will decrease by some 33%, especially in winter and spring, decreasing the amplitude of the seasonal cycle. These model predictions contain uncertainties and the quantifications must be treated with caution.

Fig. 2. Meridional section through the overturning circulation in the Southern Ocean (PF: Antarctic Polar Front; SAF: Sub-Antarctic Front; STF Subtropical Front; AABW: Antarctic Bottom Water; LCDW: Lower Circumpolar Deep Water; UCDW: Upper Circumpolar Deep Water; NADW: North Atlantic Deep Water, AAIW: Antarctic Intermediate Water; SAMW: Sub-Antarctic Mode Water. Currents are also moving west to east (out of the page) except close to the coast where the direction is east to west (from Speer et al., 2000).

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Circulation models are limited in their ability to predict change in the Southern Ocean. They typically have a resolution of 100 km which is larger than typical ocean eddies which play a key role in north/south heat transport in the Southern Ocean. A southward shift and intensification of westerly winds is predicted to intensify the Antarctic Circumpolar Current and shift it slightly southwards possibly by o11 of latitude. It should be noted however, that interactions between ocean flows and topography are complex and such predictions are uncertain. Increased uptake of CO2 in the oceans has lowered the pH of seawater by 0.1 units since the start of the industrial revolution which is equivalent to a 30% increase in hydrogen ion concentration (Raven et al., 2005). If the current trend continues pH will fall by 0.5 units—equivalent to a tripling of hydrogen ion concentration by 2100. This is lower than the pH of the oceans have been for hundreds of millennia and the rate of change is much higher than has occurred in the same time scale. Increased acidity has potentially damaging consequences for those marine organisms that possess calcareous structures – and probably for other species as well, especially the larval stages. The impact on marine life will be especially high in the Southern Ocean where low temperatures increase the solubility of calcium carbonate and where the compensation depth is relatively shallow (Andersson et al., 2008). Models predict that in the Southern Ocean there will be significant calcium carbonate undersaturation in surface water by 2050 (Orr et al., 2005).

8. Climate change and pelagic squid ecology in the Southern Ocean Given our knowledge of the physiology, life cycle biology and ecology of cephalopods a tentative assessment can be made about how squid populations in the Southern Ocean might respond to modelled predictions of the effects of global climate change on the environment between now and the end of the 21st century. The response of inshore squid to increased temperature under global warming has been assessed by Pecl and Jackson (2007) and the effects on octopus population dynamics has been modelled by Andre´ et al. (2010). In the Southern Ocean we can envisage responses of squid to: (1) temperature per se; (2) physical changes such as in ocean circulation, sea ice extent, and ocean acidification and (3) complex ecological changes. All members of the high latitude endemic squid fauna extend at least as far north as the APF with some reaching the SAF and the STF (Table 1) so they are eurythermic up to temperatures of at least 4 1C. It is therefore unlikely that temperature increase per se will have a major effect on the endemic high latitude species, other than by reducing the northern limit of their range. Conversely the lower latitude species may extend their range southwards as temperatures increase. The short life span and generation time of squid coupled with high mobility means that regional changes in water temperature will have less effect on squid than on long lived, slow reproducing, benthic invertebrate species. Transport of squid eggs and paralarvae by ocean currents enables a proportion of each new generation to be carried into suitable thermal habitat and the adults can actively avoid localised warming events. There has been little experimental work on the potential impact of global climate change on squid physiology. One study has shown that the combined effects of warming, low oxygen tension, and acidification are likely to reduce the size of habitat available to the Humboldt squid, Dosidicus giagas, in the Eastern Tropical Pacific (Rosa and Seibel, 2008). This is a region where temperature is near the upper, and oxygen near the lower, extreme anywhere in the world’s oceans. It is unlikely that even

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the most active squid in the cold, generally well oxygenated, waters of the Southern Ocean will be limited by temperature and oxygen levels predicted for 2100. The effect of ocean acidification on marine organisms has mostly focused on the calcifying species Hofmann et al. (2010). The squid have lost completely the ancestral calcified shell but they still possess small, paired, calcified statoliths within fluid filled spaces (the statocycts) in the skull. These are part of the squid’s mechanism for detecting angular acceleration and disruption of their development following hatching has severe consequences. For instance in culture conditions Hanlon et al. (1989a) found, in a squid hatchery, that use of artificial seawater with insufficient strontium for normal statolith development resulted in abnormal hatchlings with defective statoliths and uncontrolled swimming behaviour. Acidity of the statocyst fluid is critical to precipitation of calcium carbonate for statolith growth (Morris, 1991) so the process could be disrupted under reduced ambient pH if this influences the statocyst fluid. Any disruption of statolith development caused by ocean acidification might also result in abnormal statolith development and behaviour. Circulation models suggest that by 2100 changes in large scale circulation patterns in the Southern Ocean will be driven by intensification of westerly winds causing the Antarctic Circumpolar Current to shift slightly to the south. This small amount of change seems unlikely to have any major effect on squid populations. Changes in mesoscale oceanographic processes, however, might have more substantial impact. Surface mesoscale structures such as eddies and core rings support enhanced primary productivity (Mann and Lazier, 1991) and oceanic squid and their predators aggregate to feed in their vicinity (Wadley and Lu, 1983; Sugimoto and Tameishi, 1992; Waring et al., 1993; Rodhouse et al., 1996). Core rings in western boundary current systems are also implicated in the transport of squid paralarvae, which is critical to completion of the early phase of the life cycle (Bakun and Csirke, 1998; Dawe et al., 2000). Change in mesoscale activity therefore has the potential to affect oceanic squid ecology fundamentally. Low resolution (4100 km) in the present generation of ocean circulation models means that changes in mesoscale oceanographic features cannot be predicted with any certainty but increase in the velocity of the ACC is likely to intensify the mesoscale eddy field (Hogg et al., 2008; Meredith and Hogg, 2006). This could be at a level which would have large scale affects on squid populations in the Southern Ocean. There is no evidence that Antarctic squid have any direct dependence on sea ice so there is no obvious reason why changes in ice extent would have any direct affect on squid populations. The wider ecosystem changes, driven by sea ice change, seem more likely to affect squid populations. These changes are likely to include reduction in species dependent on sea ice such as Antarctic krill and change in the flux of Antarctic Bottom Water which might affect deep living forms. Predicted ecosystem changes in the Southern Ocean pelagic by the end of the 21st century include: reduced production of sea ice algae, reduced krill biomass and possible replacement by salps (Clarke et al., 2007), reduction in specialist krill predators, reduction in the extent of sea ice covered ecosystems, increase in open water phytoplankton production and changes in phytoplankton community structure, and reduction in calcifying organisms such as pteropods caused by ocean acidification. The likely effects of climate change on the Antarctic krill population at South Georgia in the Atlantic sector have been examined in detail by Murphy et al. (2007) and modelled by Hill et al. 2012. Squid would probably be negatively affected by reduction in krill unless they are replaced by other larger crustacean zooplankters because the squid rely on crustaceans in this size range, at least during early life. Squid do not prey on salps and other gelatinous forms so an ecosystem where these replaced suspension feeding crustaceans to

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a significant extent would not support the squid during the subadult phase of the life cycle. Antarctic squid are not known to prey on pteropods and it is unlikely that loss or reduction of these from the ecosystem would have a direct effect on squid populations. Little is known about how disease will affect marine populations under climate change but as in terrestrial ecosystems it is likely that rapid climate change will be accompanied by disease epidemics. Cephalopods are known to become infected by viruses which cause tumours and they host a number of protistan and metazoan parasites but, to date, no pathogenic bacteria have been isolated from cephalopods in the wild (Hanlon et al., 1989b). Cephalopods are probably as susceptible to disease as other marine animals but the effect of epidemics on populations cannot be predicted with the current state of knowledge. It seems most likely that the effects of climate change on Southern Ocean pelagic squid will be via ecosystem changes that will be complex and dynamic and driven by multiple stresses. It may however be simplistic to conclude that environmentally driven changes at positions low in the food chain will simply be propagated upwards and have a negative impact on the pelagic squid. The cephalopods in general are ecological opportunists. They are fast growing, iteroparous and have short generation times. They are also voracious predators and all have a broad spectrum diet. These are characteristics which provide the capability to rapidly fill ecological niches that have been vacated by other groups. This seems to have occurred in regions where overfishing on groundfish has severely depleted stocks and which has been followed by increased catches of cephalopods (Caddy and Rodhouse, 1998). There are also a number of instances of rapid growth of cephalopod populations giving rise to rapid increases in fishery yield, plagues and range expansions (Croker, 1937; Field et al., 2007; Garstang, 1900; Rees and Lumby, 1954). The most likely explanation for these phenomena is that environmental conditions were unusually favourable, probably at some crucial point in the life cycle. Data from southern hemisphere squid fisheries illustrate the rapid response of squid populations to annual environmental variability (Waluda et al., 1999, 2001, 2004, 2006; Waluda and Rodhouse, 2006). Change in Southern Ocean pelagic ecosystems could provide opportunities for some ecologically opportunistic squid species to increase the size of their populations as they expand into ecological niches vacated for instance by fish populations or as they benefit from changed environmental conditions at the expense of other species. In an unstable environment short-lived semelparous forms are adapted to increase rapidly when conditions are suitable and so out compete slow growing, slow reproducing forms (Genner et al., 2010; Perry et al., 2005). Climate change related extreme events in the physical and biological environments (such as collapse of ice shelves and disease epidemics) are difficult to incorporate into ecological models. Nevertheless they have the potential to create conditions in which some ecologically opportunistic forms could change the shape of the ecosystem in unpredictable ways.

9. Discussion This synthesis largely covers three decades of Antarctic squid ecology since the publication of Clarke’s (1980) Discovery Report on cephalopods in the diet of sperm whales in the southern hemisphere. A considerable body of literature has since been published on Antarctic squid biology and ecology which was reviewed by Collins and Rodhouse (2006). Some Southern Ocean squid species had been discovered in the 19th century and since 1980 only one new species, S. circumantarcticus, has been described and named. It seems unlikely that no new Antarctic species remain to be discovered and new sampling methods,

deployed in the more remote regions of the Southern Ocean, may well reveal new forms. Much of the literature on Southern Ocean squid has been concerned with their consumption by higher predators and despite the evidence of squid beaks in predator gut contents, the more recent data from research on stable isotope ratios and fatty acid composition of predators has cast some doubt on the relative importance of squid in their diet. The implication is that fish may be more important for some species than has been recognised. These apparent contradictions remain to be reconciled. Understanding of the role of Antarctic squid as predators is still incomplete because squid are only rarely found with easily identifiable gut contents and the new scatological methods employing genetic bar coding (http://www.caml.aq/barcoding/ index.html) may hold promise for the future. Improved insight into the role of squid as predators would enable better predictions to be made about the way squid populations will respond to ecological change. Following exploratory squid fishing in the Antarctic no large scale fishery has started up so the impetus for research provided by commercial exploitation has not developed. Antarctic teuthology is therefore in an unsettled state and is likely to remain an active field of research into the future. In much of current ecological science the ecosystems being studied are changing both with the climate and in response to increasing exploitation, and this is the case in the Southern Ocean. Predictions about how ecosystems will change in the future are difficult and well information speculation risks becoming ‘‘accepted as fact’’ if cited as such by careless authors. Data on the effects of single variables such as temperature and pH on physiology give no insight into the effects of change in multiple variables on the physiology of individuals, let alone on population and community ecology. The ecological processes that will take place in response to climate change, combined with the on-going effects of unsustainable exploitation of marine living resources are complex and require sophisticated modelling to predict future ecosystem structure. The likelihood of extreme events increases the difficulty as these may tip ecosystems into a new state. Following such events ecological opportunists are likely to benefit initially so squid and other cephalopods should be included with other higher predators in future models. Their response will differ from that of other Southern Ocean predators which are generally large, long lived and slow to reproduce. The cephalopods have been around for a long time; they probably arose in the Cambrian from a chambered monoplacophoran (Yochelson et al., 1973) and were certainly present by the late Cambrian. They have survived two major extinction events at the Permian-Triassic (P-Tr) and Cretaceous/Palaeogene (K-Pg) boundaries. They have also thrived despite competition from the fishes which evolved after the cephalopods and are more energetically efficient (O’Dor and Webber, 1986). Nevertheless the ammonites, which were once a dominant group in the oceans, disappeared completely at the K-Pg boundary and the global cephalopod fauna today is quite distinct from that in earlier geological eras. Radiation of the coleoid cephalopods – including the squid – took place in the Tertiary following the K-Pg extinction event and they are a group that might continue to evolve in response to future rapid change. Modelling studies on the short term effects of fisheries selection on squid show that, given their short generation time – for a large metazoan – and the general absence of mating between generations, the squids have the ability to evolve rapidly under high selection pressure (Murphy et al., 1994; Murphy and Rodhouse, 1999). In some instances their ability to evolve rapidly, even under rapid anthropogenic climate change, might enable them to outpace extinction and ultimately give rise to a new radiation.

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Acknowledgments I thank Bob Olson and Jock Young for inviting me to contribute to this thematic issue of Deep-Sea Research II. Mike Meredith made several helpful suggestions about the physical oceanographic and climate change sections and three reviewers took pains to point out my ‘‘sins of commission and omission’’. I could not have written this paper without countless stimulating discussions with fellow scientists from various disciplines at the British Antarctic Survey and other polar institutes worldwide, or with my international group of friends and colleagues in the field of cephalopod ecology and fisheries. This paper is a contribution to a CLIOTOP initiative to develop understanding of squid in pelagic ecosystems.

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