Document [ to be completed by the Secretariat ] WG-EMM-08/43 Date submitted [ to be completed by the Secretariat ] 7 July 2008 Language [ to be completed by the Secretariat ] Original: English Agenda Agenda Item No(s): 7 Title TROPHIC OVERLAP OF WEDDELL SEALS (LEPTONYCHOTES WEDDELLI) AND ANTARCTIC TOOTHFISH (DISSOSTICHUS MAWSONI) IN THE , Author(s) M.H. Pinkerton1, A. Dunn1, S.M. Hanchet2 Affiliation(s) 1 National Institute of Water and Atmospheric Research Ltd (NIWA), Private Bag 14901, Wellington, New Zealand. Email: [email protected] Telephone: +64 4 386 0369 Fax: +64 4 386 2153 2 NIWA, PO Box 893, 217 Akersten Street, Nelson, New Zealand Published or accepted for Yes No 9 publication elsewhere? If published, give details ABSTRACT We present information to investigate the significance of Antarctic toothfish as a prey item for Weddell seals in the Ross Sea. • We summarise the life history of Weddell seals to provide an overview of their use of the Ross Sea. As consumption of prey by Weddell seals (both the amount and type of prey) will vary between different life history stages at different times of the year in different areas, this is relevant to the question of whether seals predate significantly on toothfish. • There is evidence that Antarctic toothfish have lower densities near to seal breeding colonies in McMurdo Sound than further away (Testa et al. 1985). • Direct information on diet of the Weddell seals, including diver observations, -mounted camera information, and observations from field scientists in the McMurdo Sound region suggest that toothfish are a significant prey item for Weddell seals. • In contrast, research using seal stomach contents, vomit and scats provides no evidence that Weddell seals consume toothfish at all. Diver observations suggest that seals may feed selectively on only parts of toothfish so that otoliths and vertebrae may be under-represented in remains. • Indirect information using stable isotopes of carbon and nitrogen, even including recent analyses that have not been previously reported, remains inconclusive. We recommend further research using stable isotope analysis of blood samples from seals not at the breeding colonies, and samples of muscle or other slower-turnover tissue of seals at the breeding colonies. • Information from fatty acids or other biomarkers could potentially be used to investigate the importance of toothfish as a prey item for seals, but no results are available. • We have compared mortality of Antarctic toothfish in McMurdo Sound to consumption by Weddell seals. The estimates, although preliminary and subject to uncertainty, indicate that it is possible that toothfish comprise a substantial proportion of the diet of seals in McMurdo Sound between October and January.

We conclude that while there is strong evidence that toothfish are a prey item for Weddell seals in McMurdo Sound between October and January, it is plausible but unproven that they are an important prey item.

SUMMARY OF FINDINGS AS RELATED TO NOMINATED AGENDA ITEMS Agenda Item Findings We conclude that while there is strong evidence that toothfish are a prey 7 item for Weddell seals in McMurdo Sound between October and January, it is plausible but unproven that they are an important prey item. This paper is presented for consideration by CCAMLR and may contain unpublished data, analyses, and/or conclusions subject to change. Data in this paper shall not be cited or used for purposes other than the work of the CCAMLR Commission, Scientific Committee or their subsidiary bodies without the permission of the originators and/or owners of the data.

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1 INTRODUCTION

Fisheries not only impact the target species, but also other parts of the ecosystem, both directly from by-catches, and indirectly by altering the species composition and inter-specific relationships within the ecosystem. There is presently debate over the degree to which the fishery for Antarctic toothfish (Dissostichus mawsoni) in the Ross Sea may adversely affect the ecological viability of Weddell seals (Leptonychotes weddelli) which breed in the vicinity of McMurdo Sound in the late spring and early summer (e.g. Ainley et al. 2006; Ponganis & Stockard 2007).

The fishery for Antarctic toothfish in the Ross Sea may affect Weddell seals by a number of means, including:

(1) by reducing the availability of Antarctic toothfish for the Weddell seals to eat. This will be addressed by the present study where we consider evidence on the extent to which the fishery may affect Weddell seals through direct trophic overlap. (2) by affecting the ecosystem and/or habitat so that other prey items of Weddell seals are changed in abundance. It is likely that the indirect effects on the availability of other prey of Weddell seals due to the toothfish fishery will be less pronounced than the effect of direct depletion of toothfish itself if toothfish are an important prey item. It is hence important first to determine direct toothfish-seal trophic overlap. Further consideration of second-order ecosystem effects (such as the impact of the fishery on other prey items of Weddell seals) will be considered using approaches similar to the whole-ecosystem trophic model currently under ongoing development at NIWA (Pinkerton et al. 2007). (3) by affecting the ecosystem and/or habitat so that predators of Weddell seals are changed in abundance. Weddell seals have few predators in the Ross Sea so it is unlikely that the toothfish fishery will affect this to any significant extent. (4) by direct disturbance of the seals. The degree to which the fishery may disturb Weddell seals in the Ross Sea (e.g due to noise, human activity, pollution etc) is unlikely to be severe, as most fishing takes place well away from the haul out areas of the seals. No information is available to assess this issue at the present time. (5) by causing death/injury to seals during fishing itself or afterwards due to lost fishing gear. No direct mortality of Weddell seals by the toothfish fishery in the Ross Sea has been reported. As the fishery is entirely based on long-lining, there are no nets for entanglement, and depredation by Weddell seals on on long-lines (which could plausibly lead to death on some occasions) has not been reported over 10 years during which ~40% of all hooks hauled have been directly observed. The impact of lost fishing gear on Weddell seals in the Ross Sea is unknown. Lost fishing gear that remains on the sea-bed is unlikely to affect Weddell seals significantly because fishing takes place in waters >350 m: too deep for Weddell seals to be foraging on the bottom.

It is likely therefore that the main potential impact of the fishery on Weddell seals in the Ross Sea is that toothfish become locally less available as a prey item to seals due to depletion by the fishery. The remainder of this paper addresses the question of whether it is plausible that fishing Antarctic toothfish in the Ross Sea under the current management approach could adversely impact Weddell seals.

We discuss a number of pieces of evidence to quantify the importance of Antarctic toothfish as a prey item for Weddell seals in the Ross Sea. We summarise the life history of Weddell seals with particular reference to the McMurdo Sound region. Because consumption of prey by Weddell seals (both the amount and type of prey) will vary between stages of seals at different times of the year in different areas, the life history of Weddell seals in the Ross Sea is important. Next we consider direct information on diet of the Weddell seals. This includes information from diver observations in the

2 Ross Sea, animal-mounted camera information, stomach contents analysis, and investigation of sea scat remains. We then consider indirect information on diet, including recent information from stable isotope analysis of fish species in the Ross Sea that has not been previously reported. Finally, we compare Antarctic toothfish production near McMurdo Sound with Weddell seals consumption in the same region. This involves estimating toothfish abundance and mortality in the region, and estimating consumption of seals.

Figure 1. Subareas 88.1, 88.2A and 88.2B showing the McMurdo Sound region (red).

2 Weddell seal biology and life history

Weddell seals (Leptonychotes weddelli) are widespread through the Southern Ocean and occur in large numbers on fast ice, right up to the Antarctic continent, and offshore in the pack ice zone north to the Antarctic Convergence (Kooyman 1981). Weddell seals occur throughout the Ross Sea, forming breeding colonies (several hundred ) along the coast of Victoria Land and Ross Island (Ainley 1985; Testa & Siniff 1987).

Weddell seals breeding in the southern Ross Sea have been extensively studied. In McMurdo Sound, they have been studied for over 30 years (e.g. Smith 1965; Stirling 1969; Testa 1987; Schreer & Testa 1992; Burns et al. 1998, 1999; Testa & Siniff 1987; Stewart et al. 2003). An intensive study of a breeding population of Weddell seals in the Erebus Bay region of eastern McMurdo Sound started in 1968 and is ongoing (e.g. Garrott & Rotella 2008; Siniff et al. 2008; Proffitt et al. 2007). Over the 38- years of this study, over 17 000 animals have been tagged, with emphasis on maintaining and enhancing annual demographic data through the use of mark-recapture techniques (Garrott & Rotella 2008).

3 Seals begin to arrive at the breeding colonies from late September, with pups born in October. Non- breeding adults are excluded from the colonies by aggressive territorial behaviour of adult males and females with pups. Pups dive and swim within 2 weeks, and are weaned at 6 weeks. Mating occur around mid-December. During this period (October to December), breeding adults and nursing pups remain inshore (Testa et al 1985; Burns & Kooyman 2001). Nursing finishes around mid-December when pups are weaned. At this time, adults and weaned pups disperse (but not far) from the breeding colonies and mix with immature animals, adult non-breeders, post-breeders and weaned pups from other breeding sites. All pups born in McMurdo Sound have left their natal areas by the end of February, moving north along the Antarctic continent coastline (Burns et al. 1999).

The distribution of Weddell seals between breeding seasons is not clear. Some individuals remain year round in the fast ice at latitudes as high as 78°S in McMurdo Sound, whereas others, particularly newly weaned and subadult animals, spend the winter in the pack ice to the north of the Ross Sea (Stewart et al. 2003). Ice conditions, the availability of prey, and the abundance of predators such as leopard seals and killer whales, appear to determine where adults and young go when they disperse from the breeding colonies (Testa 1994). Tagging experiments show that some pups born in McMurdo Sound return there within a year, while others stay more than 400 km distant for a number of years (Burns et al. 1999). After a number of years, fewer than 25% of pups born in Erebus Bay (in McMurdo Sound) have been observed recruiting into the breeding population there (Testa 1987; Hastings 1996). The low return rate may be because pups suffer higher natural mortality in their first few years of life, because pups tend to recruit into other colonies, or because studies are not long enough to observe pups returning to their natal areas (Burns et al 1999). Satellite tracking of adult females from breeding colonies in McMurdo Sound showed that most remained in the northern part of the Sound during winter, although some travelled as far as 500 km north beyond the Sound (Testa 1994). All adult seals tracked from McMurdo Sound by Stewart et al. (2000) moved north after moulting and then spent the autumn, winter and early spring foraging in open-ocean and pack ice habitats over the broad continental shelf of the western Ross Sea.

3 Information on Weddell seal diet

There is a considerable literature on the feeding of Weddell seals in the Ross Sea, with many studies in McMurdo Sound. Almost all studies of Weddell seal diets throughout Antarctica suggest a dominance of fish in the diet (>90% by mass). Fish species taken in McMurdo Sound are known to include Pleuragramma antarcticum, Antarctic toothfish (Dissostichus mawsoni), cryopelagic fish (including Pagothenia borchgrevinki), and small benthic fish (including Trematomus spp. Small amounts of are also likely to be taken (including Psychroteuthis glacialis, Histioteuthiid sp., Kondakovia longimana, Mastigoteuthiid sp.), and benthic octopods. An unknown but assumed small amount of crustacea (mainly decapods) may also be consumed. Various methods can provide information on Weddell seal diet and are discussed below.

3.1 Habitat overlap

Studies of habitat use by predators can often give useful indications of potential trophic interactions between predator and prey species. There is a considerable literature on where Weddell seals go through the year, and how they forage for food (see above and Ross et al 1982; Burns et al. 1998, 1999; Burns & Kooyman 2001; Hindell et al. 2002; Lake et al. 2005, 2006). Weddell seals forage mainly in shelf waters, usually below ice. When ice cover is continuous, seals often congregate round breathing holes. Adult Weddell seals are reported to dive to depths up to 750 m, but <350 m is more common (e.g. Burns & Kooyman 2001; Hindell et al. 2002). Pups have been measured diving to >400 m, but most dives are less than 80 m deep, with diving patterns indicating they are actively hunting prey which has a diel vertical migration (Burns et al. 1999). There is evidence that yearling Weddell seals in McMurdo Sound are divided into two groups: those that feed close to the bottom in shallower water, and those that dive in the deep-water pelagic zone (Burns et al. 1998). These studies indicate that there could be locally significant overlap between the occurrence of Antarctic toothfish and the

4 foraging of Weddell seals around McMurdo Sound between October and January. Indeed, Ross et al. (1982) suggested that the significant increase in toothfish numbers in the McMurdo Sound region from October to mid-November may be the reason why so many Weddell seal breeding colonies are established there at all, though this is unproven.

Antarctic toothfish eggs and larvae are probably pelagic like those of the closely related (Hanchet et al. 2007). At a length of about 15 cm, the juveniles descend to the bottom and assume a more benthic lifestyle. Adult toothfish are mainly found on the continental slope and are most abundant in depths of 800–1500 m. However, large adult fish have been caught in depths shallower than 500 m at McMurdo and Terra Nova Bay. Although D. mawsoni is caught by bottom longline in the commercial fishery, it can, at times, occupy the entire water column. At McMurdo Sound it was recorded using video at mean depths of 168 m and 93 m (minimum 17 m) during day and night respectively over a bottom depth of 570 m (Fuiman et al. 2002). Movement over deepwater between seamounts to the north of the Ross Sea region (Hanchet et al. 2003, 2007), and presence in sperm whales stomachs caught over deep water (Yukhov 1971) further confirm its pelagic lifestyle. The presence of beaks of pelagic and benthic cephalopods found in the stomachs of toothfish also suggests that toothfish feed both benthically and pelagically within the water column (Thompson et al. 2008).

3.2 Stomach contents analysis

Stomach contents analysis gives an instantaneous indication of diet but has a number of limitations as a method for evaluating long-term diet: (1) diet can vary between years, seasonally, or from day to day depending on factors including prey availability; (2) stomach analysis is known to give results which are biased towards less digestible and/or more readily identified prey items; (3) examination of stomach contents will not show parts of a prey item that are avoided by selective feeding. Plötz et al. (1991) examined stomach contents from 13 Weddell seals from the eastern Weddell Sea coast, and found them to be dominated by fish, with some remains. The fish represented in the remains include Channichthyidae, Nototheniidae (especially Trematomus sp.), Bathdraconidae, and Artedidraconidae. To the author’s knowledge, there are no published studies on stomach contents of Weddell seals from the Ross Sea.

3.3 Scat and vomit remains

Analysis of scats and vomit from Weddell seals has been used to study their diet (e.g. Testa et al. 1985; Green & Burton 1987; Burns et al. 1998, 1999; Casaux et al. 2006). Casaux et al. (2006) reported that, based on scat analysis, the diet of Weddell seals from the Antarctic peninsula was dominated (>90%) by fish (especially Pleuragramma antarcticum, Chaenodraco wilsoni, Chionodraco rastrospinosus, and Gibionotothen gibberifrons). With small amounts of cephalopods. In the South Shetland Islands, Weddell seal diet was dominated by cephalopods (especially benthic octopods), with fish (especially myctophids) important (Casaux et al. 2007). In McMurdo Sound, a number of studies (Testa et al. 1985; Burns et al. 1998) report that seal scats are dominated by fish parts (especially Pleuragramma antarcticum, with some Trematomus sp.), with some cephalopod beaks. In these studies, it is notable that no otoliths from Antarctic toothfish have been found in Weddell seal scats. However, recent diver observations (Kim et al. 2005) suggest that Weddell seals may not consume the head, skin or vertebral column of 85 cm plus Antarctic toothfish. If so, the absence of remains of Antarctic toothfish in the breeding colonies of McMurdo Sound does not preclude toothfish being an important prey item in this region.

3.4 Direct observation by divers and scientists

A number of studies report direct observations of feeding of Weddell seals on Antarctic toothfish in McMurdo Sound (e.g. Calhaem & Christoffel 1969; Ross et al. 1982; Castellini et al. 1992; Kim et al. 2005; Ponganis & Stockard et al. 2007). These include opportunistic observations, as researchers set

5 up camps on the sea ice of McMurdo Sound for various experiments. Experiments between October and January making dive holes through the ice often led to the arrival of Weddell seals that were then observed hunting (e.g. Ponganis & Stockard 2007). In one planned experiment on Weddell seal- toothfish interactions, an Antarctic toothfish released near Weddell seals elicited an immediate hunting reaction in the seals (Ross et al. 1982). Some studies report seals catching toothfish and “caching” them for later consumption (e.g. Kim et al. 2005). High catch rates of toothfish by seals have been reported in the literature: e.g. four toothfish with a combined weight of about 60 kg caught by a single seal in a two days in December (Calhaem & Christoffel 1969); 28 fish caught in a 37-day period in October-November by three Weddell seals (Ponganis & Stockard 2007). 3.5 Animal-mounted cameras

Video cameras have been mounted on Weddell seals in McMurdo Sound to investigate their foraging patterns (Fuiman et al. 2002; Davis et al. 1999, 2003, 2004). Considerable amounts of such video data are available (e.g. >500 hours of recording; Davis et al. 2004). The seals were taken from breeding colonies off Ross Island in McMurdo Sound between October and December 1997–1999, and were observed frequently attacking schools of P. antarcticum, and occasionally taking D. mawsoni. Fuiman et al. (2002) report seals encountering 336 P. antarcticum in 58 dives and always attacking these fish when encountered. The silverfish were 20–25 cm in length and are estimated to weigh approximately 76–160 g each. Seals encountered D. mawsoni rarely, 26 times in 14 dives (Fuiman et al. 2002), sometimes with multiple encounters per dive, and did not always attack. One toothfish was reported as 1 m long which may weigh approximately 12 kg (Dunn et al. 2006). Considering only the 13 encounters between seals and toothfish reported by Fuiman et al. (2002) that are known to be different fish, and assuming that only 10% of these encounters ultimately lead to consumption, these data suggest 1.1 kg/dive D. mawsoni consumed compared to 0.7 kg/dive P. antarcticum consumed. In 500 hours of recording, Davis et al. (2004) report mid-water foraging encounters between seals and 12 large Antarctic toothfish, and between seals and more than 1000 Antarctic silverfish. Data from Davis et al. (2004) agrees with the previous approximate estimate in suggesting that P. antarcticum dominate diet in terms of numbers, but that D. mawsoni and P. antarcticum are of similar importance in terms of biomass taken (118 kg P. antarcticum to 144 kg D. mawsoni).

3.6 Stable isotope analysis

Analysis of carbon and nitrogen stable isotope ratios in muscle tissue can give an integrated, long-term indication of diet (e.g. Fry & Sherr, 1984; Peterson & Fry, 1987). Muscle tissue in fish is replaced relatively slowly so that the C and N isotopic composition gives an indication of diet over a period of 6–12 months (MacNeil et al. 2005). In contrast, blood analysis gives values that probably reflect diet in the previous 10–20 days (Tieszen et al. 1983; Hobson & Clark 1992).

Burns et al. (1998) measured δ13C and δ15N blood from pup (N=16), yearling (N=14), and adult (N=12) Weddell seals at breeding colonies in McMurdo Sound. The blood samples were taken over a number of seasons (1992–1994) but the months of collection are not given by Burns et al. (1998). These values were similar to stable isotope values for Weddell seals taken in the eastern Ross Sea (Zhao et al. 2004). Burns et al. (1998) had values of δ13C and δ15N for 5 Antarctic toothfish, which we replace with a larger dataset recently measured (N=45, Bury et al. 2008). We use a recent set of data for Pleuragramma antarcticum (N=30, Bury et al. 2008) in place of the 4 values used by Burns et al. (1998). Cephalopod remains were found to be present in seal scats, and we have access to recently- acquired data on stable isotope values for Psychroteuthis glacialis (N=20) from the Ross Sea (Thompson et al. 2008; Bury et al. 2008). Results for this species of cephalopod were used because remains of this species are most commonly found in Weddell seal scat samples (e.g. Casaux et al. 2006, 2007). Detailed information on the methods, data and interpretation of these new stable isotope results (with a focus on the diet of toothfish in the Ross Sea) is given in Bury et al. (2008) and will not be repeated here.

6 We used a subset of samples from Bury et al. (2008), selecting those samples closest geographically to McMurdo Sound (figure 2). None of these samples are from McMurdo Sound but are nevertheless considered, at least in terms of the δ15N values, to be applicable to the present study. Bury et al. (2008) and references therein show that δ15N values for toothfish are relatively consistent across the Ross Sea. Also, the differences between the new δ15N values and those in Burns et al. (1998) for Antarctic toothfish and silverfish are not significant. However, differences in sampling locations did affect δ13C values in fish and cephalopods across the Ross Sea and consequently we do not consider δ13C data here.

Unfortunately, there are no new values of stable isotope composition for rock cod (Tremotomus loennbergii, T. bernacchii) available, and so we use the small (N=2, 1 respectively) data set from Burns et al. (1998). There were substantial differences in isotope values between the two samples of T. loennbergii in their study and here we use the sample with a δ15N value similar to the sample of T. bernacchii.

Isotope values are shown in figure 3.

Figure 2. Location of stable isotope data for Dissostichus mawsoni (top left), Pleuragramma antarcticum (top right), and Psychroteuthis glacialis (bottom) from the Ross Sea.

7 15 Leptonychotes weddelli (adults) 14 Leptonychotes weddelli (deep diving yearlings) 13 Leptonychotes weddelli (NDR yearlings)

12 Leptonychotes weddelli (shallow diving yearlings)

11 Leptonychotes weddelli (pups) N 15 δ 10 Dissostichus mawsoni Pleuragramma antarcticum 9 Trematomus loennbergii 8 Trematomus bernacchii 7 Psychroteuthis glacialis 6 -28 -27 -26 -25 -24 -23 -22 δ 13C

Figure 3. Stable isotope values for Weddell seals (Leptonychotes weddelli), fish, and (Psychroteuthis glacialis) in the Ross Sea. NDR=“No dive record”.

We employ a mixing model (IsoSource: Phillips & Gregg 2003) to determine the range of diets of Weddell seals that is consistent with these data. We exclude pups from the analysis because they were nursing when blood samples were taken so their isotopic signature will not indicate prey (Hobson et al. 1997). In the model, we only use the nitrogen isotope and assume changes in δ15N between trophic levels of a typical +3.4 ‰ per trophic level (Post 2002). We do not use the δ13C data because we consider the carbon isotope data from Burns et al. (1998) to be questionable because of lipid extraction issues (see Bury et al. 2008). The carbon isotope data from Bury et al. (2008) is not applicable because of sampling location issues discussed above. We set the diet resolution to 5% and the tolerance to 0.1 ‰ (Phillips & Gregg 2003). We further constrain IsoSource by requiring that Pleuragramma antarcticum should not be less than 30% of the diet, and that Psychroteuthis glacialis, Trematomus loennbergii and Trematomus bernachchii should each not be more than 50% of the diet. These are termed “secondary constraints”. The primary constraints come from the nitrogen isotope information itself.

Table 1. Maximum proportions of prey species in the diet of Weddell seals based on applying a mixing model (IsoSource) to δ15N values as explained in the text. The values in grey indicate that the secondary constraint has been reached (diet items not to be greater than 50% of diet). Dissostichus Pleuragramma Psychroteuthis Trematomus Trematomus mawsoni antarcticum glacialis loennbergii bernachchii Leptonychotes max max max max max weddelli proportion proportion proportion proportion proportion Adults 0.15 0.7 0.5 0.45 0.4 Deep diving yearlings 0 0.5 0.5 0.25 0.2 NDR1 yearlings 0.1 0.6 0.5 0.35 0.35 Shallow diving yearlings 0.2 0.8 0.5 0.5 0.5 1 “No Dive Record” information (Burns et al. 1998).

Assuming that these secondary constraints are reasonable, the δ15N stable isotope data here are consistent with all Weddell seal groups except deep diving yearlings feeding on maximum proportions of Antarctic toothfish of between 10% and 20% according to seal group. However, it can be seen that

8 at least one secondary constraint (diet items not to be greater than 50% of diet for Psychroteuthis glacialis, T. loennbergii, T. bernachchii) was reached in all runs of the IsoSource model. This means that the method used here has low power for constraining the plausible diet fractions of the predators based on the δ15N isotope data alone. Carbon (or other) isotope information are needed to allow the isotope data, rather than the secondary constraints, to estimate feasible diet fractions.

Stable isotope data are hence inconclusive in terms of answering the question of whether toothfish are a significant fraction of the diet of Weddell seals in McMurdo Sound. Also, as stable isotope values for seals were based on blood samples of breeders, the data only give an indication of very recent feeding – the last day or two – of one part of the population. Muscle biopsy samples from breeding Weddell seals, and samples of blood and/or muscle from non-breeders over the breeding season would be useful.

3.7 Biomarkers

There are other indirect methods of measuring trophic overlap, and one method which has obvious applicability to the current question is the use of fatty acid biomarkers (e.g. Lee et al. 1971; Budge et al. 2006). In contrast to stable isotope analysis which gives an amalgamated signal from all prey species, fatty acid biomarker analysis can provide evidence of consumption of a specific prey item in a predator. Different prey items often have characteristic fatty acid signatures so that the relative abundance of prey-specific biomarkers in the lipids of a predator can be used to indicate the degree of feeding on a particular prey species (Lee et al. 1971; Budge et al. 2006). It is believed that research using biomarkers applied to Weddell seals in the Ross Sea is underway in New Zealand (Lenky & Metcalf 2008), and possibly by researchers in the USA.

4 Toothfish production vs seal consumption

Progress towards developing a balanced trophic ecosystem model of the Ross Sea shelf and slope (to 3000 m) has been ongoing for a number of years (Pinkerton et al. 2007). Such mass balance approaches, where we estimate and compare predator consumption and prey mortality, can help to investigate trophic overlap.

The trophic model of the Ross Sea suggested that D. mawsoni were likely to comprise less than 2% of the diet of Weddell seals on an annual basic across the whole Ross Sea (Pinkerton et al. 2007). At this scale, we suggested that D. mawsoni were unlikely to be a significant prey item for Weddell seals. However, we noted that there may be significant localised predation which was not considered by this version of the trophic model. We noted that the consumption of D. mawsoni in particular locations, at particular times of the year, or by particular parts of the seal population may be especially important to predators. Here, we revisit the modeling, focusing only on the Weddell seal-Antarctic toothfish interactions in the McMurdo Sound region. Two factors are required: (1) an estimate of the consumption of seals in the McMurdo Sound region; (2) an estimate of the biomass of toothfish being predated on in the McMurdo Sound region. For the latter, we assume that toothfish natural mortality is a proxy for predation by seals.

4.1 Weddell seal consumption in McMurdo Sound region

4.1.1 Weddell seal biomass

At-sea censusing of marine mammals has estimated substantial numbers of Weddell seals in the Ross Sea sector, of the order of 32 000–50 000 individuals (Stirling 1969; Ainley 1985; Stewart et al. 2003). While this may or may not be an accurate estimate of Weddell seals in the Ross Sea sector, the number of seals in McMurdo Sound is known to be much smaller. On the eastern side of McMurdo Sound region there appears to be ~1500 breeders, and about 2700 animals in total (Testa & Siniff 1987), implying that non-breeders are about 44% of the population. On the western side of McMurdo Sound,

9 there are about 1520 seals associated with breeding colonies near the Strand Moraines and Blue Glacier (Ross et al. 1982). The proportion of breeders in the western breeding population is not known, but if non-breeders are again 44% of the population, this implies about 850 breeders on the western side and 670 non-breeders. This suggests 2350 breeder and 1860 non-breeding Weddell seals are in McMurdo Sound (4210 adults) at the time when the counts were made: November–January. The “non-breeders” include adult non-breeders, subadults, and weaners. The populations on both sides of McMurdo Sound are thought to be relatively stable in number (Testa & Siniff 1987; Ross et al. 1982).

4.1.2 Seal consumption rate

Food consumption requirements for Weddell seals were estimated by two methods. First, Nagy (1987, 1994, 2005) estimated daily dry weight food consumption for eutherian mammals (with placenta) 0.822 according to body weight as Qd=0.235W , where Qd is the daily consumption in g dry weight; W is the animal weight (g). Adult seals reach 2.6–3.0 m (males) and 2.6–3.3 m (females) in length, with a maximum weight of c. 300 kg (Harcourt 2001; Shirihai 2002). Average Weddell seal weight in a stable population is much less than the maximum weight, and was estimated to be 160 kg by Trites & Pauly (1998) which we will use here. This method gave an annual consumption rate as a proportion of individual weight (Q/B) of 40.7 y-1.

In the second method, consumption of seals was estimated based on the amount of food they require to supply sufficient energy to satisfy their standard metabolic rate (SMR: Lasiewski & Dawson 1967). Here, we used the relation: SMR (kcal/d)=71.3·W0.892, where W is the animal weight in kg which was developed for marine mammals in polar areas (Irving 1970). The average daily energy requirement of seals was taken as 2.8 times the standard metabolic rate (Lasiewski & Dawson 1967). An assimilation efficiency of 0.75, energy/carbon ratio of 10 kcal/gC and carbon proportion of 0.108 gC/gWW were used to give prey requirements (Croxall 1987; Lasiewski & Dawson 1967; Schneider & Hunt 1982). This method gave an annual average value of Q/B=25.7 y-1. Other work reports daily food intake for captive seals as 10% of body weight (Laws 1984), implying Q/B of 36.5 y-1.

The range of consumptions is hence likely to be 26–41 y-1. Weddell seals are likely to remain in the McMurdo Sound region for about 4 months of the year (October–January). The degree of annual consumption occurring during the breeding season is not well known, but we assume that seals feed at the average annual rate for the time they are in McMurdo Sound. If there are 2350 breeding and 1860 non-breeding Weddell seals in the region and all feed, we would estimate consumption in the region of 3200–5000 t (breeders), 2500–4000 t (non-breeders), and 5700–9000 t (all). Given the good information on seal numbers in McMurdo Sound and relatively consistent estimates of consumption rates for Antarctic seals, these figures are likely to have acceptable accuracy for the present study.

4.2 Antarctic toothfish mortality in McMurdo Sound region

In order to estimate mortality of toothfish in the McMurdo Sound region between October and January it is necessary to estimate numbers and sizes of toothfish in the region, take into account movements into and out of the region, estimate growth of fish in the region, and estimate mortality rates. We note the development of a spatially-explicit model of toothfish in subarea 88.1 (Dunn & Rasmussen 2008). It is possible that this model may provide better indications of local toothfish biomass and mortality that may assist in developing these spatially-explicit estimates. As an interim approach for this study we present the following method.

4.2.1 Toothfish biomass

We estimated the biomass of Antarctic toothfish in the McMurdo Sound region based on CCAMLR C2 data as follows. CPUE from a given set (biomass of catch of Antarctic toothfish per baited hook) is assumed to be an indication of the density of toothfish in an area 0.1° x 0.1° surrounding the nominal fishing location (midway between set and haul positions) at the time of fishing. This is equivalent to

10 an area 11 km x 3.5 km (at 72°S). CPUE from all sets within each 0.1° x 0.1° area since the start of the fishery were averaged. This is taken to give an indication of the spatial distribution of toothfish vulnerable to the fishery in the Ross Sea sector (comprising 88.1, 88.2A and 88.2B). The densities were normalized to area by dividing by cos(θ) where θ is the latitude. The densities were made to sum to unity by dividing by the total of all densities across the whole of subareas 88.1, 88.2A and 88.2B.

The normalized density for cell i is denoted ρi. We assume that all the biomass vulnerable to fishing in the Ross Sea region (Bvul) is represented by the distribution of densities. In this case, the vulnerable i biomass in cell i, Bvul is given by: i Bvul = ρi ⋅ Bvul [1]

The toothfish biomass in the Ross Sea vulnerable to fishing in a given cell will be less than the total i (vulnerable plus non-vulnerable) biomass in the same cell ( Btotal ). The vulnerability in a given cell (i) is denoted as αi such that 0 < αi ≤ 1 and:

i i Bvul = αi ⋅ Btotal [2]

Using a stock model, the total unfished (virgin) biomass of toothfish in the Ross Sea was estimated to be Btotal = 86500 t (Dunn & Hanchet 2007). This stock model is designed to be precautionary, with details and sensitivity analyses of the method given in Dunn & Hanchet (2007). Using the stock model output and our assumptions about the distribution of vulnerable biomass and the vulnerability within a given cell, we estimate the total toothfish biomass in cell i as:

i ρi /αi Btotal = Btotal [3] ∑ ρi /αi all _ i

The foraging region of Weddell seals around McMurdo Sound were obtained from ARGOS-satellite tracking of females and weaned pups (3–12 months old) (see Ainley et al. 2006, figure 5). These data suggest that the majority of the seal foraging in the vicinity of McMurdo Sound is contained in the region bounded to the north by 76°S and to the east by 175°E.

The approach given above assumes that the catchability coefficient for toothfish is constant across all habitats and depths within each cell, and that variations in fishable seabed area within each cell are relatively small. We assume net biomass import in the McMurdo Sound region between October and January is small compared to the size of the resident population.

Applying this method, with all vulnerabilities set to unity, we estimate that the biomass of toothfish overlapping with the Weddell seal foraging range is 4400 t. The vulnerability of toothfish to the fishery (α) is likely to be highest in the south eastern part of the Ross Sea as it is thought that smaller fish here are not taken effectively by the fishery (Dunn & Hanchet 2007). This value hence represents our lower plausible limit on the biomass of toothfish in the region.

To obtain an approximate plausible upper bound on toothfish in the greater McMurdo Sound region, we take the vulnerability to be low (α=0.5) in the south-eastern part of the Ross Sea (south of 74°S and west of 180°), and unity elsewhere. This allows us to estimate an approximate plausible upper bound on toothfish biomass in the region of 7770 t. Note that these values are based on the stock model estimate of virgin biomass (before fishing began) and may now be different. 4.2.2 Toothfish mortality

Mortality of toothfish is likely to be age-dependent, with higher mortality for young and old fish than for mid-age fish. Most toothfish in McMurdo Sound are too young to be affected by senescent mortality (younger than the median of the population) and may be too old to be subject to increased

11 juvenile mortality. We consider it reasonable therefore in this interim approach to set mortality equal to the value for the population as a whole as in the stock model (Dunn et al. 2006; Dunn & Hanchet 2007).

Natural mortality for toothfish in the shelf region was estimated to be 0.11–0.15 y-1, with a typical value of M=0.13 y-1 (Dunn et al. 2006). This implies that 12.2% of the population dies each year. If mortality rate is constant with age in the population then annual mortality scales with biomass, that is, the contribution of each age class to the total population biomass is the same as its contribution to the annual mortality in terms of weight. The majority of this mass of fish are assumed to be consumed by predators. The most likely predators in the McMurdo Sound region are Weddell seals, though killer whales may also take toothfish in the region. It is possible that most of the annual predation on toothfish in this region occurs between October and January when the largest number of Weddell seals are present due to breeding congregation. During the other months, few predators of toothfish are likely to be present in this region due to high ice cover and consequently mortality rates of toothfish may be much smaller. We hence assume that all toothfish mortality in the McMurdo Sound region happens between October and January when Weddell seal numbers there are highest. This implies that, as a plausible but preliminary estimate, 540–950 t of toothfish are consumed by Weddell seals in the McMurdo Sounds region each year.

4.3 Mortality-consumption comparison

Given the consumption rates for seals above, if only the non-breeding seals are preying heavily on toothfish and the annual mortality of toothfish in the region occurs between October and January, the feasible proportions of toothfish in their diet are 13–38% during this period. If the whole breeding and non-breeding seal populations are predating on toothfish, the average proportion of toothfish in their diet in McMurdo Sound between October and January is likely to be 6–17%. Note that these are the feasible proportions of toothfish in the diet of seals for the 4 month period October–January and do not represent annual diet proportions. If the Weddell seals do not feed on toothfish except at this time of year and in this location, the annual proportion of the toothfish in the seal diet will be reduced by a factor of three from these values. It is possible however that Weddell seals take toothfish during their dispersion to the north and east of the Ross Sea. If toothfish mortality is spread out evenly over the year rather than all occurring between October and January, the contribution of toothfish to seal diet will also be lower than the values given above by a factor of three.

As discussed above, our estimates for seal consumption and toothfish mortality rely on a number of assumptions and, although they represent the only estimates currently available, they include considerable uncertainty. Nevertheless, the preliminary result from the trophic modeling presented here supports the hypothesis that toothfish could be an important prey item for Weddell seals in McMurdo Sound between October and January.

5 DISCUSSION AND CONCLUSIONS

We have discussed a number of pieces of evidence to investigate the significance of Antarctic toothfish as a prey item for Weddell seals in the McMurdo Sound region.

• We have summarised the life history of Weddell seals which provides an overview of their use of the Ross Sea. As consumption of prey by Weddell seals (both the amount and type of prey) will vary between stages of seals at different times of the year in different regions, this is relevant to the question of whether seals predate significantly on toothfish. • Based on limited sampling, Antarctic toothfish are reported as having lower densities around seal breeding colonies than further away in summer (Testa et al. 1985). • Direct information on the feeding behaviour of the Weddell seals, including diver observations, animal-mounted camera information, and observations from field scientists in the region indicate that Antarctic toothfish are predated by seals in McMurdo Sound in late

12 spring and early summer (Calhaem & Christoffel 1969; Ross et al. 1982; Castellini et al. 1992; Davis et al. 1999; Fuiman et al. 2002; Davis et al. 1999, 2003, 2004; Kim et al. 2005; Ponganis & Stockard et al. 2007). There is evidence that some seals are effective hunters of even large toothfish, and can consume a greater weight of toothfish as Antarctic silverfish at some times (Fuiman et al. 2002; Davis et al. 2004). • Research using seal stomach contents, vomit and scats provides no evidence that Weddell seals consume toothfish. Diver observations (Kim et al. 2005) suggest that seals may feed selectively on only parts of toothfish so that otoliths and vertebrae may be under-represented in remains. • Information from isoSource modelling of nitrogen stable isotope analysis of fish muscle and seal blood (Burns et al. 1998), including new data for fish that have not been previously reported (Bury et al. 2008), remains inconclusive. No information using biomarkers was available. We recommend further urgent research using stable isotope and fatty acid biomarkers to investigate the degree to which toothfish are preyed on by seals. Tissue samples from non-breeding seals, and/or samples of muscle, hair or other slower-turnover tissue of seals at the breeding colonies would be valuable. • We have compared natural mortality of Antarctic toothfish in McMurdo Sound to consumption by Weddell seals. The resident population in the McMurdo Sound region was estimated by assuming average CPUE (catch-per-unit-effort) over all years of fishing is indicative of toothfish density in a given region, with a correction for the proportion of toothfish vulnerable to fishing in different parts of the Ross Sea. The estimates are interim and subject to substantial uncertainty, but suggest that it is possible that toothfish comprise an important proportion of the diet of seals in McMurdo Sound between October and January.

We conclude that while there is strong evidence that toothfish are a prey item for Weddell seals in McMurdo Sound between October and January, it is plausible but unproven that they are an important significant prey item.

It is hence possible that the fishery for Antarctic toothfish in the Ross Sea will have a detrimental effect on Weddell seal populations in the McMurdo Sound region. This would require that: (1) the commercial fishery reduces the abundance of toothfish in the McMurdo Sound region; (2) the magnitude of the change in toothfish abundance is enough to change the behaviour and/or foraging success of seals there; and, (3) the change of behaviour and/or foraging has an adverse effect on the seal population.

The impact of commercial fishing in Subarea 88.1 on the abundance of toothfish in the McMurdo Sound region is not known. More reliable spatially-explicit estimates of the abundance, growth, movement and mortality of toothfish are required to better address this question.

How much depletion of toothfish is required to adversely affect seal populations is not known. Weddell seals probably consume more Antarctic silverfish than toothfish while in McMurdo Sound, but the degree to which these prey items are interchangeable in the diet of Weddell seals is not understood. The importance of foraging during lactation by Weddell seals is also not clear. However, if we assume that seals are making optimal use of the environment at unfished toothfish abundances, it is reasonable to assume that any change of diet, foraging success or other behaviour in seals caused by depletion of toothfish is likely to be detrimental.

6 ACKNOWLEDGEMENTS

Funding for this work was provided by Foundation for Research, Science and Technology, New Zealand, under project C01X0505. We would also like to thank the members of the New Zealand Antarctic Fisheries Stock Assessment Working Group for helpful discussions and input into this paper.

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