Skip to main content
Log in

From video recordings to whisker stable isotopes: a critical evaluation of timescale in assessing individual foraging specialisation in Australian fur seals

  • Highlighted Student Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Estimating the degree of individual specialisation is likely to be sensitive to the methods used, as they record individuals’ resource use over different time-periods. We combined animal-borne video cameras, GPS/TDR loggers and stable isotope values of plasma, red cells and sub-sampled whiskers to investigate individual foraging specialisation in female Australian fur seals (Arctocephalus pusillus doriferus) over various timescales. Combining these methods enabled us to (1) provide quantitative information on individuals’ diet, allowing the identification of prey, (2) infer the temporal consistency of individual specialisation, and (3) assess how different methods and timescales affect our estimation of the degree of specialisation. Short-term inter-individual variation in diet was observed in the video data (mean pairwise overlap = 0.60), with the sampled population being composed of both generalist and specialist individuals (nested network). However, the brevity of the temporal window is likely to artificially increase the level of specialisation by not recording the entire diet of seals. Indeed, the correlation in isotopic values was tighter between the red cells and whiskers (mid- to long-term foraging ecology) than between plasma and red cells (short- to mid-term) (R 2 = 0.93–0.73 vs. 0.55–0.41). δ13C and δ15N values of whiskers confirmed the temporal consistency of individual specialisation. Variation in isotopic niche was consistent across seasons and years, indicating long-term habitat (WIC/TNW = 0.28) and dietary (WIC/TNW = 0.39) specialisation. The results also highlight time-averaging issues (under-estimation of the degree of specialisation) when calculating individual specialisation indices over long time-periods, so that no single timescale may provide a complete and accurate picture, emphasising the benefits of using complementary methods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Araújo MS, Bolnick DI, Machado G, Giaretta AA, dos Reis SF (2007) Using δ13C stable isotopes to quantify individual-level diet variation. Oecologia 152:643–654

    Article  PubMed  Google Scholar 

  • Araújo MS, Guimarães PR, Svanbäck R, Pinheiro A, Guimarães P, Dos Reis SF, Bolnick DI (2008) Network analysis reveals contrasting effects of intraspecific competition on individual vs. population diets. Ecology 89:1981–1993

    Article  PubMed  Google Scholar 

  • Araújo MS, Martins EG, Cruz LD, Fernandes FR, Linhares AX, Dos Reis SF, Guimarães PR (2010) Nested diets: a novel pattern of individual-level resource use. Oikos 119:81–88

    Article  Google Scholar 

  • Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958

    Article  PubMed  Google Scholar 

  • Arnould JP, Hindell MA (2001) Dive behaviour, foraging locations, and maternal-attendance patterns of Australian fur seals (Arctocephalus pusillus doriferus). Can J Zool 79:35–48

    Article  Google Scholar 

  • Arnould JP, Kirkwood R (2008) Habitat selection by female Australian fur seals (Arctocephalus pusillus doriferus). Aquat Conserv 17:S53–S67

    Article  Google Scholar 

  • Arnould JPY, Cherel Y, Gibbens J, White JG, Littnan CL (2011) Stable isotopes reveal inter-annual and inter-individual variation in the diet of female Australian fur seals. Mar Ecol Prog Ser 422:291–302

    Article  Google Scholar 

  • Bearhop S, Adams CE, Waldron S, Fuller RA, MacLeod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012

    Article  Google Scholar 

  • Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser 311:157–164. doi:10.3354/meps311157

    Article  Google Scholar 

  • Bolnick DI, Yang LH, Fordyce JA, Davis JM, Svanback R (2002) Measuring individual-level resource specialization. Ecology 83:2936–2941. doi:10.2307/3072028

    Article  Google Scholar 

  • Bolnick DI et al (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    Article  PubMed  Google Scholar 

  • Bolnick DI et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradshaw CJ, Hindell MA, Sumner MD, Michael KJ (2004) Loyalty pays: potential life history consequences of fidelity to marine foraging regions by southern elephant seals. Anim Behav 68:1349–1360

    Article  Google Scholar 

  • Bridcut EE, Giller PS (1995) Diet variability and foraging strategies in brown trout (Salmo trutta): an analysis from subpopulations to individuals. Can J Fish Aquat Sci 52:2543–2552

    Article  Google Scholar 

  • Bryan JE, Larkin P (1972) Food specialization by individual trout. J Fish Res Board Can 29:1615–1624

    Article  Google Scholar 

  • Cantor M, Pires MM, Longo GO, Guimarães PR, Setz EZF (2013) Individual variation in resource use by opossums leading to nested fruit consumption. Oikos 122:1085–1093

    Article  Google Scholar 

  • Cazelles B, Chavez M, Berteaux D, Ménard F, Vik JO, Jenouvrier S, Stenseth NC (2008) Wavelet analysis of ecological time series. Oecologia 156:287–304

    Article  PubMed  Google Scholar 

  • Cherel Y, Hobson KA, Weimerskirch H (2005) Using stable isotopes to study resource acquisition and allocation in procellariiform seabirds. Oecologia 145:533–540

    Article  CAS  PubMed  Google Scholar 

  • Cherel Y, Kernaléguen L, Richard P, Guinet C (2009) Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biol Lett 5:830–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connan M, Hofmeyr G, Smale M, Pistorius P (2014) Trophic investigations of cape fur seals at the eastern most extreme of their distribution. Afr J Mar Sci 36:331–344

    Article  Google Scholar 

  • Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968

    Article  CAS  PubMed  Google Scholar 

  • Curtis MA, Bérubé M, Stenzel A (1995) Parasitological evidence for specialized foraging behavior in lake-resident Arctic char (Salvelinus alpinus). Can J Fish Aquat Sci 52:186–194

    Article  Google Scholar 

  • Dalerum F, Angerbjorn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658. doi:10.1007/s00442-005-0118-0

    Article  CAS  PubMed  Google Scholar 

  • Darimont CT, Paquet PC, Reimchen TE (2009) Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. J Anim Ecol 78:126–133

    Article  PubMed  Google Scholar 

  • Davenport SR, Bax NJ (2002) A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. C J Fish Aquat Sci 59:514–530. doi:10.1139/f02-031

    Article  Google Scholar 

  • Deagle BE, Kirkwood R, Jarman SN (2009) Analysis of Australian fur seal diet by pyrosequencing prey DNA in faeces. Mol Ecol 18:2022–2038

    Article  CAS  PubMed  Google Scholar 

  • Del Rio CM, Sabat P, Anderson-Sprecher R, Gonzalez SP (2009) Dietary and isotopic specialization: the isotopic niche of three Cinclodes ovenbirds. Oecologia 161:149–159

    Article  PubMed  Google Scholar 

  • Fish FE, Hurley J, Costa DP (2003) Maneuverability by the sea lion Zalophus californianus: turning performance of an unstable body design. J Exp Biol 206:667–674

    Article  PubMed  Google Scholar 

  • Franco-Trecu V, Aurioles-Gamboa D, Inchausti P (2013) Individual trophic specialisation and niche segregation explain the contrasting population trends of two sympatric otariids. Mar Biol 70:609–618

    Google Scholar 

  • Froese R, Pauly D (2014) FishBase, vol. 2014

  • Fry B, Joern A, Parker P (1978) Grasshopper food web analysis: use of carbon isotope ratios to examine feeding relationships among terrestrial herbivores. Ecology 59:498–506

    Article  Google Scholar 

  • Furlani D, Gales R, Pemberton D (2007) Otoliths of common Australian temperate fish: a photographic guide. CSIRO, Victoria

    Google Scholar 

  • Gales NJ, Mattlin RH (1998) Fast, safe, field-portable gas anesthesia for Otariids. Mar Mamm Sci 14:355–361

    Article  Google Scholar 

  • Gales R, Pemberton D, Lu C, Clarke M (1993) Cephalopod diet of the Australian fur seal: variation due to location, season and sample type. Mar Freshw Res 44:657–671

    Article  Google Scholar 

  • Gibbs C (1992) Oceanography of bass strait: implications for the food supply of little penguins Eudyptula minor. Emu 91:395–401

    Article  Google Scholar 

  • Harris G, Griffiths F, Clementson L, Lyne V, Van der Doe H (1991) Seasonal and interannual variability in physical processes, nutrient cycling and the structure of the food chain in Tasmanian shelf waters. J Plankton Res 13:109–131

    Google Scholar 

  • Heaslip SG, Hooker SK (2008) Effect of animal-borne camera and flash on the diving behaviour of the female Antarctic fur seal Arctocephalus gazella. Deep Sea Res Pt I 55:1179–1192

    Article  Google Scholar 

  • Heaslip SG, Iverson SJ, Bowen WD, James MC (2012) Jellyfish support high energy intake of leatherback sea turtles (Dermochelys coriacea): video evidence from animal-borne cameras. PLoS ONE 7:e33259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hilderbrand GV, Farley SD, Robbins CT, Hanley TA, Titus K, Servheen C (1996) Use of stable isotopes to determine diets of living and extinct bears. Can J Zool 74:2080–2088. doi:10.1139/z96-236

    Article  Google Scholar 

  • Hirons AC, Schell DM, St Aubin DJ (2001) Growth rates of vibrissae of harbor seals (Phoca vitulina) and Steller sea lions (Eumetopias jubatus). Can J Zool 79:1053–1061

    Article  Google Scholar 

  • Hoskins AJ, Arnould JP (2014) Relationship between long-term environmental fluctuations and diving effort of female Australian fur seals. Mar Ecol Prog Ser 511:285–295

    Article  Google Scholar 

  • Hoskins AJ, Costa DP, Arnould JPY (2015) Utilisation of intensive foraging zones by female Australian Fur seals. PLoS ONE 10:e0117997

    Article  PubMed  PubMed Central  Google Scholar 

  • Hughes AR, Inouye BD, Johnson MT, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623

    Article  PubMed  Google Scholar 

  • Hume F, Hindell M, Pemberton D, Gales R (2004) Spatial and temporal variation in the diet of a high trophic level predator, the Australian fur seal (Arctocephalus pusillus doriferus). Mar Biol 144:407–415

    Article  Google Scholar 

  • Kernaléguen L, Cazelles B, Arnould JPY, Richard P, Guinet C, Cherel Y (2012) Long-term species, sexual and individual variations in foraging strategies of Fur seals revealed by stable isotopes in Whiskers. PLoS ONE 7:e32916

    Article  PubMed  PubMed Central  Google Scholar 

  • Kernaléguen L, Arnould J, Guinet C, Cherel Y (2015) Determinants of individual foraging specialisation in large marine vertebrates, the Antarctic and Subantarctic fur seals. J Anim Ecol 84:1081–1092

    Article  PubMed  Google Scholar 

  • Kirkwood R, Arnould JP (2011) Foraging trip strategies and habitat use during late pup rearing by lactating Australian fur seals. Aust J Zool 59:216–226

    Article  Google Scholar 

  • Kirkwood R, Hume F, Hindell M (2008) Sea temperature variations mediate annual changes in the diet of Australian fur seals in Bass Strait. Mar Ecol Prog Ser 369:297–309

    Article  Google Scholar 

  • Kirkwood R et al (2010) Continued population recovery by Australian fur seals. Mar Freshw Res 61:695–701

    Article  CAS  Google Scholar 

  • Kleiber M (1961) The fire of life: an introduction to animal energetics. Wiley, New York

    Google Scholar 

  • Knox TC, Stuart-Williams H, Warneke RM, Hoskins AJ, Arnould JP (2014) Analysis of growth and stable isotopes in teeth of male Australian fur seals reveals interannual variability in prey resources. Mar Mamm Sci 30:763–781

    Article  CAS  Google Scholar 

  • Kuiter RH, Kuiter RH (1996) Guide to sea fishes of Australia. New Holland, Sydney

    Google Scholar 

  • Levenson DH, Ponganis PJ, Crognale MA, Deegan JF II, Dizon A, Jacobs GH (2006) Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter. J Comp Physiol A 192:833–843

    Article  CAS  Google Scholar 

  • Littnan C, Arnould J, Harcourt R (2007) Effect of proximity to the shelf edge on the diet of female Australian fur seals. Mar Ecol Prog Ser 338:257–267

    Article  Google Scholar 

  • Lomnicki A (1978) Individual differences between animals and the natural regulation of their numbers. J Anim Ecol 47:461–475

    Article  Google Scholar 

  • Lorrain A et al (2011) Sequential isotopic signature along gladius highlights contrasted individual foraging strategies of jumbo squid (Dosidicus gigas). PLoS ONE 6:e22194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lythgoe J, Partridge J (1989) Visual pigments and the acquisition of visual information. J Exp Biol 146:1–20

    CAS  PubMed  Google Scholar 

  • MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609

    Article  Google Scholar 

  • Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305

    Article  PubMed  Google Scholar 

  • Matthews B, Mazumder A (2004) A critical evaluation of intrapopulation variation of delta C-13 and isotopic evidence of individual specialization. Oecologia 140:361–371

    Article  PubMed  Google Scholar 

  • McConnell B, Chambers C, Fedak M (1992) Foraging ecology of southern elephant seals in relation to the bathymetry and productivity of the southern Ocean. Antarct Sci 4:393–398

    Article  Google Scholar 

  • Meynier L, Morel PC, Chilvers BL, Mackenzie DD, Duignan PJ, MacLatchey D (2014) Foraging diversity in lactating New Zealand sea lions: insights from qualitative and quantitative fatty acid analysis. Can J Fish Aquat Sci 71:984–991

    Article  CAS  Google Scholar 

  • Novak M, Tinker MT (2015) Timescales alter the inferred strength and temporal consistency of intraspecific diet specialization. Oecologia 1(178):61–74

    Article  Google Scholar 

  • Passlow V, O’Hara T, Daniell J, Beaman R (2004) Sediments and benthic biota of Bass Strait: an approach to benthic habitat mapping. Geoscience. Australia Record 23

  • Pires M, Guimarães P, Araújo M, Giaretta A, Costa J, Dos Reis S (2011) The nested assembly of individual-resource networks. J Anim Ecol 80:896–903

    Article  CAS  PubMed  Google Scholar 

  • Pruitt JN, Ferrari MC (2011) Intraspecific trait variants determine the nature of interspecific interactions in a habitat-forming species. Ecology 92:1902–1908

    Article  PubMed  Google Scholar 

  • Quevedo M, Svanbäck R, Eklöv P (2009) Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology 90:2263–2274

    Article  PubMed  Google Scholar 

  • Rea LD et al (2015) Age-specific vibrissae growth rates: A tool for determining the timing of ecologically important events in Steller sea lions. Mar Mamm Sci 31:1213–1233

    Article  Google Scholar 

  • Ridgway K (2007) Long-term trend and decadal variability of the southward penetration of the East Australian current. Geophys Res Lett 34:L13613

    Google Scholar 

  • Robertson A, McDonald RA, Delahay RJ, Kelly SD, Bearhop S (2014) Individual foraging specialisation in a social mammal: the European badger (Meles meles). Oecologia 176:409–421

    Article  PubMed  Google Scholar 

  • Robinson BW, Wilson DS, Margosian AS, Lotito PT (1993) Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish. Evol Ecol 7:451–464

    Article  Google Scholar 

  • Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt AE et al (2015) Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator. Oecologia 1(178):5–16

    Article  Google Scholar 

  • Roughgarden J (1972) Evolution of niche width. Am Nat 106:683–718

    Article  Google Scholar 

  • Roughgarden J (1974) Niche width: biogeographic patterns among Anolis lizard populations. Am Nat 108:429–442

    Article  Google Scholar 

  • Svanbäck R, Bolnick DI (2005) Intraspecific competition affects the strength of individual specialization: an optimal diet theory method. Evol Ecol Res 7:993–1012

    Google Scholar 

  • Takahashi A, Kokubun N, Mori Y, Shin HC (2008) Krill-feeding behaviour of gentoo penguins as shown by animal-borne camera loggers. Polar Biol 31:1291–1294

    Article  Google Scholar 

  • Tieszen LL, Boutton TW, Tesdahl K, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37

    Article  Google Scholar 

  • Tinker MT, Bentall G, Estes JA (2008) Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proc Natl Acad Sci USA 105:560–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tinker MT et al (2012) Structure and mechanism of diet specialisation: testing models of individual variation in resource use with sea otters. Ecol Lett 15:475–483

    Article  Google Scholar 

  • Tollit D et al (1998) Variations in harbour seal Phoca vitulina diet and dive-depths in relation to foraging habitat. J Zool 244:209–222

    Article  Google Scholar 

  • Tranquilla LAM et al (2014) Individual winter movement strategies in two species of Murre (Uria spp.) in the Northwest Atlantic. PLoS ONE 9:e90583

    Article  Google Scholar 

  • Young J, Jordan A, Bobbi C, Johannes R, Haskard K, Pullen G (1993) Seasonal and interannual variability in krill (Nyctiphanes australis) stocks and their relationship to the fishery for jack mackerel (Trachurus declivis) off eastern Tasmania, Australia. Mar Biol 116:9–18

    Article  Google Scholar 

  • Zaccarelli N, Bolnick DI, Mancinelli G (2013) RInSp: an r package for the analysis of individual specialization in resource use. Methods Ecol Evol 4:1018–1023

    Article  Google Scholar 

Download references

Acknowledgments

The assistance of the many field workers involved in this study is gratefully acknowledged. The authors thank Bernard Cazelles for his precious contribution in the wavelet analysis, Gaël Guillou for running the isotopic analyses and Gaël Caro for his help in the analyses. The logistical support of Parks Victoria, in particular the Rangers from the Foster and Tidal River offices was crucial for the success of the study as was the skill and experience of the boat charter operator (Geoff Boyd). The research was financially supported by the Australian Research Council (DP110102065), Holsworth Wildlife Research Endowment and the Office of Naval Research (Marine Mammals and Biological Oceanography Program Award N00014-10-1-0385). All procedures were conducted under Deakin University Animal Ethics Committee Approval (A16/2008) and Department of Sustainability and Environment (Victoria) Wildlife Research Permits (10005362, 10005848) and all applicable institutional and/or national guidelines for the care and use of animals were followed.

Author contribution statements

LK and JPYA conceived the study design with meaningful input from YC. KA and GJM designed, developed and programmed for deployment the animal-borne video cameras and MAH and JS provided essential logistic support. JPYA and AJH collected the field data and samples. ND, DI and AB processed the video recordings and LK completed the laboratory work and performed the statistical analyses of the video and isotopic data. LK wrote the manuscript with significant editorial inputs from JPYA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laëtitia Kernaléguen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Aaron J Wirsing.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kernaléguen, L., Dorville, N., Ierodiaconou, D. et al. From video recordings to whisker stable isotopes: a critical evaluation of timescale in assessing individual foraging specialisation in Australian fur seals. Oecologia 180, 657–670 (2016). https://doi.org/10.1007/s00442-015-3407-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3407-2

Keywords

Navigation