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Diet and Trophic Niche of Antarctic Silverfish Pleuragramma

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Diet and Trophic Niche of Antarctic Silverfish Pleuragramma Journal of Fish Biology (2013) 82, 141–164 doi:10.1111/j.1095-8649.2012.03476.x, available online at wileyonlinelibrary.com Diet and trophic niche of Antarctic silverfish Pleuragramma antarcticum in the Ross Sea, Antarctica M. H. Pinkerton*, J. Forman, S. J. Bury, J. Brown, P. Horn and R. L. O’Driscoll National Institute of Water and Atmospheric Research Ltd, Private Bag 14901, Wellington 6241, New Zealand (Received 16 April 2012, Accepted 18 September 2012) The diet of Antarctic silverfish Pleuragramma antarcticum was evaluated by examining stomach ◦ ◦ ◦ ◦ contents of specimens collected in the Ross Sea (71 –77 S; 165 –180 E) in January to March 2008. Pleuragramma antarcticum (50–236 mm standard length, LS) and prey items were analysed for stable-isotopic composition of carbon and nitrogen. According to index of relative importance (IRI), which incorporates frequency of occurrence, mass and number of prey items, the most impor- tant prey items were copepods (81%IRI over all specimens), predominantly Metridia gerlachei and Paraeuchaeta sp., with krill and fishes having low IRI (2·2and5·6%IRI overall). According to mass of prey (M) in stomachs, however, fishes (P. antarcticum and myctophids) and krill domi- nated overall diet (48 and 22%M, respectively), with copepods being a relatively minor constituent of overall diet by mass (9·9%M). Piscivory by P. antarcticum occurred mainly in the extreme south- west of the region and near the continental slope. Krill identified to species level in P. antarcticum stomachs were predominantly Euphausia superba (14·1%M) with some Euphausia crystallopho- rias (4·8%M). Both DistLM modelling (PRIMER-permanova+) on stomach contents (by IRI) and stepwise generalized linear modelling on stable isotopes showed that LS and location were sig- nificant predictors of P. antarcticum diet. Postlarval P. antarcticum (50–89 mm LS) consumed exclusively copepods. Juvenile P. antarcticum (90–151 mm LS) consumed predominantly krill and copepods by mass (46 and 30%M, respectively). Small adult P. antarcticum (152–178 mm LS) consumed krill, fishes and copepods (37, 36 and 15%M, respectively). Large adult P. antarcticum (179–236 mm LS) consumed predominantly fishes and krill (55 and 17%M, respectively), espe- cially in the north (near the Ross Sea slope) and in the SW Ross Sea. Amphipods were occasionally important prey items for P. antarcticum (western Ross Sea, 39%M). General concordance between stomach contents and trophic level of P. antarcticum and prey based on δ15N was demonstrated. Pleuragramma antarcticum trophic level was estimated as 3·7 (postlarval fish) and 4·1(fishaged 3+ years). © 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles Key words: Southern Ocean; stable isotope; stomach content analysis; trophic level. INTRODUCTION New Zealand’s International Polar Year Census of Antarctic Marine Life project included a 50 day voyage on the R.V. Tangaroa to the Ross Sea region in February to March 2008. One key aim of the study was to investigate trophic connections in the Ross Sea with a focus on particularly abundant and ecologically important species. *Author to whom correspondence should be addressed. Tel.: +64 4 386 0300; email: m.pinkerton@ niwa.co.nz 141 © 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles 142 M. H. PINKERTON Antarctic silverfish Pleuragramma antarcticum Boulenger 1902 are the most abun- dant pelagic fish over the high-Antarctic shelf. This species is especially abundant in the Ross Sea where it accounts for >90% of the total ichthyoplankton and pelagic fish biomass (DeWitt, 1970; Guglielmo et al., 1998). Pleuragramma antarcticum are a key prey item for fishes, marine mammals and birds in high-Antarctic shelf ecosys- tems (Takahashi & Nemoto, 1984; Eastman, 1985) including the Ross Sea (Smith et al., 2007). Elucidating the long-term diet and trophic position of P. antarcticum is hence important for understanding the trophic structure and function of the Ross Sea (Pinkerton et al., 2010). Pleuragramma antarcticum can be described as a discriminate zooplanktivore (Eastman & McCune, 2000), with main prey variously reported as copepods (Gorelova & Gerasimchuk, 1981; Pakhomov & Pankratov, 1992; Hubold & Hagen, 1997), Euphausia crystallorophias (DeWitt & Hopkins, 1977; Takahashi & Nemoto, 1984; Hubold, 1985) and Euphausia superba (Daniels, 1982; Takahashi, 1983; Pakhomov, 1997). Moreno et al. (1986) concluded that P. antarcticum ‘has invaded the pelagic environment looking for copepods’ and Williams (1985) wrote that euphausiids are only consumed as ‘alternative copepods’. La Mesa & Eastman (2011), however, stated that ‘Antarctic krill [were] the major item in fish collected in the northern sector of the Ross Sea, ice krill [were] the major prey inside the Ross Sea’. It is clear from these and other studies of P. antarcticum stomach contents that this species has a high plasticity of diet where the main prey items vary depending on the size of P. antarcticum and on location and season, probably in response to prey availability (Kellermann & Kock, 1984; Hubold & Hagen, 1997; Granata et al., 2009). The first aim of the study was to determine the main prey of P. antarcticum in the Ross Sea at the time of the survey. Especially because of the high variability in P. antarcticum diet, stomach contents analysis has limited utility for elucidating long-term diet and trophic position (Hys- lop, 1980; Cortes,´ 1997). Stable-isotope analysis (DeNiro & Epstein, 1981; Van der Zanden & Rasmussen, 2001; Post, 2002) can complement stomach contents data by providing information on longer term feeding (Cherel et al., 2011). Stable-isotope analysis has recently been applied to P. antarcticum in the Weddell and Dumont d’Urville Seas (Mintenbeck, 2008; Giraldo et al., 2011), and elsewhere (Scotia Sea; Stowasser et al., 2012: Kerguelen waters; Cherel et al., 2010). The second aim of the study was to test whether stomach contents of P. antarcticum during the survey were consistent with stable-isotope values of P. antarcticum and prey items. Estimates of the trophic level of P. antarcticum have increased as new data are available. DeWitt & Hopkins (1977) stated that P. antarcticum are ‘at a relatively low trophic level’. Later, trophic levels of 3·0–3·3 were reported (Linkowski et al., 1983; Pakhomov & Pankratov, 1992; Pakhomov, 1997). More recently, trophic levels of adult and juvenile P. antarcticum in Prydz Bay were given as 3·9–4·3 (Hodum & Hobson, 2000) and 3·2 for juveniles in east Antarctica (Giraldo et al., 2011). The final aim of the study was to determine the trophic level of P. antarcticum in the Ross Sea. MATERIALS AND METHODS SAMPLING A total of 417 specimens of P. antarcticum was obtained from 21 stations representing 16 different sites over the Ross Sea shelf and slope (Fig. 1). Pleuragramma antarcticum © 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2013, 82, 141–164 PLEURAGRAMMA ANTARCTICUM DIET IN THE ROSS SEA 143 180° ° 170 170° ° 160° 160 ° 70 North 149,151 115 ° 72 17,19 4000 m West 39,41 26 ° 103 East 74 49 3000 m 66 54 92,94 2000 m SW 79,81,84 1000 m ° 68 75,77 76 70 ° 78 ° 80 Fig. 1. Sample locations of Pleuragramma antarcticum, showing station numbers and four strata used for description of diet: North, East, West and south-west (SW). Depth contours plotted at 1000, 2000, 3000 and 4000 m. See Table SI, Supporting information, for more information of sampling by station number. were collected by three types of trawling: rough-bottom orange roughy trawl, oblique mid- water trawl and targeted midwater trawl (sampling details by station are given in Table SI, Supporting Information). On the voyage, a random sub-set of P. antarcticum from each catch was measured for standard length (L ) to the nearest mm and weighed. Pleuragramma antarcticum were then ◦ S frozen at −20 C until analysis. In the laboratory, whole P. antarcticum were thawed, mea- sured and weighed (to correct for length and mass shrinkage due to freezing preservation), sexed (where possible) and sagittal otoliths were extracted. A total of 304 otoliths were thin- sectioned and read to provide ages (Sutton & Horn, 2011). To aid comparison with other work, diet is discussed in terms of P. antarcticum stage (postlarval, juvenile and adult), but these were inferred from LS following La Mesa & Eastman (2011): 50–89 mm LS implied postlarval fish (aged 1–2 years), 90–151 mm LS implied juveniles (3–6 years) and adults were taken as fish with >151 mm LS corresponding to ages >7 years. STOMACH CONTENTS Stomachs were removed from thawed P. antarcticum, rinsed with water on a 500 μm steel sieve and a qualitative assessment was made of stomach fullness [empty, trace, part full (one-fourth to three-fourth) and full] and prey digestive state. Prey items were identified under a stereoscopic microscope to the lowest taxon possible. Fishes digested beyond visual recognition were identified, if possible, from their otoliths. Each prey taxon was counted and its wet mass (MW) recorded to the nearest 0·01 g after removal of surface water by blotting paper. A nominal mass of 0·005 g was assigned to prey items that were too small to be weighed. A fragmented prey count was based on the number of eyes, heads, mouthparts, © 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2013, 82, 141–164 144 M. H. PINKERTON Table I. Number of stomach samples by stratum (see Fig. 1) and Pleuragramma antarcticum standard length (LS): number of non-empty stomachs/number of stomachs sampled (per cent stomachs sampled which were non-empty) Postlarvae Juvenile Small adult Large adult (50–89 mm (90–151 mm (152–178 mm (179–236 mm Stratum LS) LS) LS) LS) All fish North 0 5/21 (24%) 6/18 (33%) 8/12 (67%) 19/51 (37%) East 0/2 (0%) 40/61 (66%) 35/60 (58%) 14/29 (48%) 89/152 (59%) West 1/1 (100%) 16/21 (76%) 14/29 (48%) 15/26 (58%) 46/77 (60%) South-west 12/21 (57%) 7/7 (100%) 17/27 (63%) 27/35 (77%) 63/90 (70%) All strata 13/24 (54%) 68/110 (62%) 72/134 (54%) 64/102 (63%) 217/370 (59%) tails, otoliths or other anatomical parts traceable to a single specimen.
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