Abstract
Antarctic fur seals Arctocephalus gazella and macaroni penguins Eudyptes chrysolophus are the two main land-based krill Euphausia superba consumers in the northern Scotia Sea. Using a combination of concurrent at-sea (predator observations, net hauls and multi-frequency acoustics), and land-based (animal tracking and diet analysis) techniques, we examined variability in the foraging ecology of these sympatric top predators during the austral summer and autumn of 2004. Krill availability derived from acoustic surveys was low during summer, increasing in autumn. During the breeding season, krill occurred in 80% of fur seal diet samples, with fish remains in 37% of samples. Penguin diets contained the highest proportion of fish in over 20 years of routine monitoring (46% by mass; particularly the myctophid Electrona antarctica), with krill (33%) and amphipods (Themisto gaudichaudii; 21%) also occurring. When constrained by the need to return and feed their offspring both predator species foraged to the northwest of South Georgia, consistent with an area of high macrozooplankton biomass, but fur seals were apparently more successful at exploiting krill. When unconstrained by chick-rearing (during March) penguins foraged close to the Shag Rocks shelf-break, probably exploiting the high daytime biomass of fish in this area. Penguins and seals are able to respond differently to periods of reduced krill abundance (in terms of variability in diet and foraging behaviour), without detriment to the breeding success of either species. This highlights the importance of myctophid fish as an alternative trophic pathway for land-based predators in the Scotia Sea ecosystem.
Similar content being viewed by others
References
Agnew DJ (1997) Review: the CCAMLR ecosystem monitoring programme. Antarct Sci 9:235–242
Atkinson A, Whitehouse MJ, Priddle J, Cripps GC, Ward P, Brandon MA (2001) South Georgia, Antarctica: a productive, cold water, pelagic ecosystem. Mar Ecol Prog Ser 216:279–308
Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103
Austin D, McMillan JI, Bowen WD (2003) A three-stage algorithm for filtering erroneous Argos satellite locations. Mar Mamm Sci 19:371–383
Barlow KE, Croxall JP (2002) Seasonal and interannual variation in foraging range and habitat of macaroni penguins Eudyptes chrysolophus at South Georgia. Mar Ecol Prog Ser 232:291–304
Barlow KE, Boyd IL, Croxall JP, Reid K, Staniland IJ, Brierley AS (2002) Are penguins and seals in competition for Antarctic krill at South Georgia? Mar Biol 140:205–213
Biuw M, Krafft BA, Hofmeyr GJG, Lydersen C, Kovacs KM (2009) Time budgets and at-sea behaviour of lactating female Antarctic fur seals Arctocephalus gazella at Bouvetøya. Mar Ecol Prog Ser 385:271–284
Bost CA, Georges JY, Guinet C, Cherel Y, Pütz K, Charrassin JB, Handrich Y, Zorn T, Lage J, Le Maho Y (1997) Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozet Archipelago. Mar Ecol Prog Ser 150:21–33
Boyd IL (1993) Pup production and distribution of breeding Antarctic fur seals (Arctocephalus gazella) at South Georgia. Antarct Sci 5:17–24
Boyd IL (1999) Foraging and provisioning in Antarctic fur seals: inter-annual variability in time-energy budgets. Behav Ecol 10:198–208
Boyd IL (2002) Estimating food consumption of marine predators: Antarctic fur seals and macaroni penguins. J Appl Ecol 39:103–119
Boyd IL, Croxall JP (1992) Diving behaviour of lactating Antarctic fur seals. Can J Zool 70:919–928
Boyd IL, Arnould JPY, Barton T, Croxall JP (1994) Foraging behaviour of Antarctic fur seals during periods of contrasting prey abundance. J Anim Ecol 63:703–713
Boyd IL, McCafferty DJ, Reid K, Taylor R, Walker TR (1998) Dispersal of male and female Antarctic fur seals (Arctocephalus gazella). Can J Fish Aquat Sci 55:845–852
Boyd IL, Staniland IJ, Martin AR (2002) Distribution of foraging by female Antarctic fur seals. Mar Ecol Prog Ser 242:285–294
Brierley AS, Watkins JL, Murray AWA (1997) Interannual variability in krill abundance at South Georgia. Mar Ecol Prog Ser 150:87–98
Brierley AS, Watkins JL, Goss C, Wilkinson MT, Everson I (1999) Acoustic estimates of krill density at South Georgia, 1981 to 1998. CCAMLR Sci 6:47–57
Brierley AS, Goss C, Grant SA, Watkins JL, Reid K, Belchier M, Everson I, Jessopp MJ, Afanasyev V, Robst J (2002) Significant intra-annual variability in krill distribution and abundance at South Georgia revealed by multiple acoustic surveys during 2000/01. CCAMLR Sci 9:71–82
Brooke MdL (2004) The food consumption of the world’s seabirds. Proc R Soc Lond B 271:S246–S248
Charrassin JB, Bost CA (2001) Utilisation of the oceanic habitat by king penguins over the annual cycle. Mar Ecol Prog Ser 221:285–298
Collins MA, Shreeve RS, Fielding S, Thurston MH (2008a) Distribution, growth, diet and foraging behaviour of the yellow-fin notothen Patagonotothen guntheri (Norman) on the Shag Rocks shelf (Southern Ocean). J Fish Biol 72:271–286
Collins MA, Xavier JCC, Johnston NM, North AW, Enderlein P, Tarling GA, Waluda CM, Hawker EJ, Cunningham NJ (2008b) Patterns in the distribution of myctophid fish in the northern Scotia Sea ecosystem. Polar Biol 31:837–851
Croxall JP, Everson I, Kooyman GL, Ricketts C, Davis RW (1985) Fur seal diving behaviour in relation to vertical distribution of krill. J Anim Ecol 54:1–8
Croxall JP, Davis RW, O’Connell MJ (1988a) Diving patterns in relation to diet of gentoo and macaroni penguins at South Georgia. Condor 90:157–167
Croxall JP, McCann TS, Prince PA, Rothery P (1988b) Reproductive performance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976–1987: implications for Southern Ocean monitoring studies. In: Sahrhage D (ed) Antarctic Ocean and resources variability. Springer, Berlin, pp 261–285
Croxall JP, Briggs DR, Kato A, Naito Y, Watanuki Y, Williams TD (1993) Diving pattern and performance in the macaroni penguin Eudyptes chrysolophus. J Zool, Lond 230:31–47
Croxall JP, Prince PA, Reid K (1997) Dietary segregation of krill-eating South Georgia seabirds. J Zool Lond 242:531–556
Croxall JP, Reid K, Prince PA (1999) Diet, provisioning and productivity responses of marine predators to differences in availability of Antarctic krill. Mar Ecol Prog Ser 177:115–131
Demer DA, Conti SG (2005) New target-strength model indicates more krill in the Southern Ocean. ICES J Mar Sci 62:25–32
Doidge DW, Croxall JP (1989) Factors affecting weaning weight in Antarctic fur seals Arctocephalus gazella at South Georgia. Polar Biol 9:155–160
Foote KG, Knudsen HP, Vestnes G, MacLennan DN, Simmonds EJ (1987) Calibration of acoustic instruments for fish density estimation: a practical guide. ICES, Copenhagen
Fraser WR, Hoffman EE (2003) A predator’s perspective on causal links between climate change, physical forcing and ecosystem response. Mar Ecol Prog Ser 265:1–15
Gon O, Heemstra PC (1990) Fishes of the Southern Ocean. JLB Smith Institute of Icthyology, Grahamstown
Green JA, Boyd IL, Woakes AJ, Warren NL, Butler PJ (2005) Behavioural flexibility during year-round foraging in macaroni penguins. Mar Ecol Prog Ser 296:183–196
Guinet C, Dubroca L, Lea MA, Goldsworthy S, Cherel Y, Duhamel G, Bonadonna F, Donnay J-P (2001) Spatial distribution of foraging in female Antarctic fur seals Arctocephalus gazella in relation to oceanographic variables: a scale-dependent approach using geographical information systems. Mar Ecol Prog Ser 219:251–264
Hewitt RP, Watkins JL, Naganobu M, Sushin V, Brierley AS, Demer DA, Kasatkina S, Takao Y, Goss C, Malyshko A, Brandon MA, Kawaguchi S, Siegel V, Trathan PN, Emery J, Everson I, Miller DGM (2004) Biomass of Antarctic krill in the Scotia Sea in January/February 2000 and its use in revising an estimate of precautionary yield. Deep Sea Res II 51:1215–1236
Hill HJ, Trathan PN, Croxall JP, Watkins JL (1996) A comparison of Antarctic krill Euphausia superba caught by nets and taken by macaroni penguins Eudyptes chrysolophus: evidence for selection? Mar Ecol Prog Ser 140:1–11
Hull CL, Hindell MA, Michael K (1997) Foraging zones of royal penguins during the breeding season, and their association with oceanographic features. Mar Ecol Prog Ser 153:217–228
Hulley PA (1981) Results of the research cruises of FRV ‘Walther Herwig’ to South America. 58. Family Myctophidae (Osteichthyes, Myctophiformes). Archiv für Fischereiwissenschaft 31(Suppl 1):300
Hunt GL, Heinemann D, Everson I (1992) Distributions and predator–prey interactions of macaroni penguins, Antarctic fur seals, and Antarctic krill near Bird Island, South Georgia. Mar Ecol Prog Ser 86:15–30
Jouventin P, Capdeville D, Cuenot-Chaillet R, Boiteau C (1994) Exploitation of pelagic resources by a non-flying seabird: satellite tracking of the king penguin throughout the breeding cycle. Mar Ecol Prog Ser 106:11–19
Kock K-H, Purves MG, Duhamel G (2006) Interactions between cetacean and fisheries in the Southern Ocean. Polar Biol 29:379–388
Lea MA, Cherel Y, Guinet C, Nichols PD (2002) Antarctic fur seals foraging in the Polar Frontal Zone: inter-annual shifts in diet as shown from fecal and fatty acid analyses. Mar Ecol Prog Ser 245:281–297
Madureira LSP, Ward P, Atkinson A (1993) Differences in backscattering strength determined at 120 and 38 kHz for three species of Antarctic macroplankton. Mar Ecol Prog Ser 93:17–24
Main CE, Collins MA, Mitchell R, Belchier M (2009) Identifying patterns in the diet of mackerel icefish (Champsocephalus gunnari) at South Georgia using bootstrapped confidence intervals of a dietary index. Polar Biol 32:569–581
McCafferty DJ, Boyd IL, Walker TR, Taylor RI (1998) Foraging responses of Antarctic fur seals to changes in the marine environment. Mar Ecol Prog Ser 166:285–299
McKenna JE (1991) Trophic relationships within the Antarctic demersal fish community of South Georgia Island. Fish Bull 89:643–654
Murphy EJ, Watkins JL, Trathan PN, Reid K, Meredith MP, Thorpe SE, Johnston NM, Clarke A, Tarling GA, Collins MA, Forcada J, Shreeve RS, Atkinson A, Korb R, Whitehouse MJ, Ward P, Rodhouse PG, Enderlein P, Hirst AG, Martin AR, Hill SL, Staniland IJ, Pond DW, Briggs DR, Cunningham NJ, Fleming AH (2007) Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web. Phil Trans R Soc Lond B 362:113–148
North AW (1996) Fish in the diet of Antarctic fur seals (Arctocephalus gazella) at South Georgia during winter and spring. Antarct Sci 8:155–160
North AW, Croxall JP, Doidge DW (1983) Fish prey of the Antarctic fur seal Arctocephalus gazella at South Georgia. Br Antarct Surv Bull 61:27–37
Orsi AH, Whitworth T, Nowlin WD (1995) On the meridional extent and fronts of the Antarctic circumpolar current. Deep Sea Res I 42:641–673
Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP (2004) Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence? Proc R Soc Lond B 271:1283–1291
Phillips RA, Silk JRD, Croxall JP, Afanasyev V (2006) Year-round distribution of white-chinned petrels from South Georgia: Relationships with oceanography and fisheries. Biol Conserv 129:336–347
Piatkowski U, Rodhouse PG, White MG, Bone DG, Symon C (1994) Nekton community of the Scotia Sea as sampled by the RMT 25 during austral summer. Mar Ecol Prog Ser 112:13–28
Reid K (1995) The diet of Antarctic fur seals (Arctocephalus gazella Peters 1875) during winter at South Georgia. Antarct Sci 7:241–249
Reid K, Arnould JPY (1996) The diet of Antarctic fur seals Arctocephalus gazella during the breeding season at South Georgia. Polar Biol 16:105–114
Reid K, Croxall JP (2001) Environmental response of upper trophic-level predators reveals a system change in an Antarctic marine ecosystem. Proc R Soc Lond B 268:377–384
Reid K, Jessopp MJ, Barrett MS, Kawaguchi S, Siegel V, Goebel ME (2004) Widening the net: spatio-temporal variability in the krill population structure across the Scotia Sea. Deep-Sea Res II 51:1275–1287
Reid K, Davis D, Staniland IJ (2006) Spatial and temporal variability in the fish diet of Antarctic fur seal (Arctocephalus gazella) in the Atlantic sector of the Southern Ocean. Can J Zool 84:1025–1037
Reiss CS, Cossio AM, Loeb V, Demer DA (2008) Variations in the biomass of Antarctic krill (Euphausia superba) around the South Shetland Islands, 1996–2006. ICES J Mar Sci 65:497–508
Rodhouse PG, Prince PA, Trathan PN, Hatfield EMC, Watkins JL, Bone DG, Murphy EJ, White MG (1996) Cephalopods and mesoscale oceanography at the Antarctic Polar Front: satellite tracked predators locate pelagic trophic interactions. Mar Ecol Prog Ser 136:37–50
Shreeve RS, Collins MA, Tarling GA, Main CE, Ward P, Johnston NM (2009) Feeding ecology of myctophid fish in the northern Scotia Sea. Mar Ecol Prog Ser 386:221–236
Sirovic A, Hildebrand JA, Thiele D (2006) Baleen whale spatial patterns in the Scotia Sea during January and February 2003. J Cetacean Res Manag 8:161–171
Staniland IJ, Boyd IL (2003) Variation in the foraging location of Antarctic fur seals (Arctocephalus gazella) and the effects on diving behavior. Mar Mamm Sci 19:331–343
Staniland IJ, Robinson SL (2008) Segregation between the sexes: Antarctic fur seals, Arctocephalus gazella, foraging at South Georgia. Anim Behav 75:1581–1590
Staniland IJ, Taylor RI, Boyd IL (2003) An enema method for obtaining fecal material from known individual seals on land. Mar Mamm Sci 19:363–370
Staniland IJ, Boyd IL, Reid K (2007) An energy-distance trade-off in a central-place forager, the Antarctic fur seal (Arctocephalus gazella). Mar Biol 152:233–241
Tasker ML, Jones PH, Dixon T, Blake BF (1984) Counting seabirds at sea from ships: a review of methods employed and a suggestion for a standardized approach. Auk 101:567–577
Trathan PN, Brandon MA, Murphy EJ (1997) Characterisation of the Antarctic Polar frontal zone to the north of South Georgia in summer 1994. J Geophys Res 102:10483–10497
Trathan PN, Murphy EJ, Croxall JP, Everson I (1998) Use of at-sea distribution data to derive potential foraging ranges of macaroni penguins during the breeding season. Mar Ecol Prog Ser 169:263–275
Trathan PN, Brierley AS, Brandon MA, Bone DG, Goss C, Grant SA, Murphy EJ, Watkins JL (2003) Oceanographic variability and changes in Antarctic krill (Euphausia superba) abundance at South Georgia. Fish Oceanogr 12:569–583
Trathan PN, Green C, Tanton JL, Peat H, Poncet J, Morton A (2006) Foraging dynamics of macaroni penguins Eudyptes chrysolophus at South Georgia during brood-guard. Mar Ecol Prog Ser 323:239–251
Trathan PN, Bishop C, Maclean G, Brown P, Fleming A, Collins MA (2008) Linear tracks and restricted temperature ranges characterise penguin foraging pathways. Mar Ecol Prog Ser 370:285–294
Veit RR, Silverman ED, Everson I (1993) Aggregation patterns of pelagic predators and their principal prey, Antarctic krill, near South Georgia. J Anim Ecol 62:551–564
Waluda CM, Gregory S, Dunn MJ (2009) Long-term variability in the abundance of Antarctic fur seals Arctocephalus gazella at Signy Island, South Orkneys. Polar Biol. doi http://doi.org/10.1007/s00300-009-0706-2
Watkins JL, Brierley AS (2002) Verification of the acoustic techniques used to identify Antarctic krill. ICES J Mar Sci 59:1326–1336
Webb A, Durinck J (1992) Counting birds from ship. In: Komdeur K, Bertelsen J, Cracknell G (eds) Manual for aeroplane and ship surveys of waterfowl and seabirds. IWRB Special Publication 19, Slimbridge, UK, pp 24–37
Weimerskirch H (2007) Are seabirds foraging for unpredictable resources? Deep Sea Res II 54:211–223
Williams TD (1991) Foraging ecology and diet of gentoo penguins Pygoscelis papua at South Georgia during winter and an assessment of their winter prey consumption. Ibis 133:3–13
Williams TD (1995) The penguins. Oxford University Press, Oxford
Wilson RP (1984) An improved stomach pump for penguins and other seabirds. J Field Ornithol 55:109–112
Acknowledgments
Thanks to the scientists and crew on board RRS James Clark Ross during cruise JR100, and to all members of the Bird Island science team for their assistance with instrument deployments. Thanks also to Keith Reid for advice and guidance during the early part of the study and to Sophie Fielding and three referees for useful comments on an earlier draft. This is a contribution to the Ecosystems Programme at the British Antarctic Survey.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Lewison.
Rights and permissions
About this article
Cite this article
Waluda, C.M., Collins, M.A., Black, A.D. et al. Linking predator and prey behaviour: contrasts between Antarctic fur seals and macaroni penguins at South Georgia. Mar Biol 157, 99–112 (2010). https://doi.org/10.1007/s00227-009-1299-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-009-1299-6