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RESEARCH ARTICLE

Regional variation in trophic ecology of adult female Australian sea lions inferred from stable isotopes in whiskers

A. D. Lowther A B D , R. G. Harcourt C and S. D. Goldsworthy A
+ Author Affiliations
- Author Affiliations

A South Australian Research and Development Institute (Aquatic Sciences), 2 Hamra Avenue, West Beach, SA 5024, Australia.

B Norwegian Polar Institute, Fram Centre, Tromsø 9296, Norway.

C Marine Mammal Research Group, Graduate School of the Environment, Macquarie University, North Ryde, NSW 2019, Australia.

D Corresponding author. Email: Andrew.Lowther@npolar.no

Wildlife Research 40(4) 303-311 https://doi.org/10.1071/WR12181
Submitted: 29 October 2012  Accepted: 20 May 2013   Published: 17 June 2013

Abstract

Context: The primary selective forces responsible for shaping life-history traits come from the physical and biological environment in which a species resides. Consequently, the limits of a species range may provide a useful measure of adaptive potential to environmental change. The proximity of foraging grounds to terrestrial nursing habitat constrains central-place foragers such as otariid seals in selecting breeding locations. The Australian sea lion (Neophoca cinerea) is an endangered otariid endemic to Australia, whose northern-range extent occurs at a temperate–tropical transition zone on the western coast of Western Australia (WA).

Aims: Currently, there is a complete absence of data on the foraging ecology of Australian sea lions in WA. We sought to address this critical knowledge gap and provide data on the foraging ecology of adult female Australian sea lions at three isolated breeding colonies in western WA.

Methods: We used stable-isotope ratios of carbon (δ13C) and nitrogen (δ15N) in the whiskers of pups as proxies to characterise feeding behaviour of 10–28% of all adult female Australian sea lions at each colony. We then compared these geographic data to (1) conspecifics at similar latitude in South Australia (SA) and (2) isotopic data collated from other studies on seabirds that inhabit the region, to place foraging behaviour of adult female Australian sea lions into context.

Key results: At the southernmost colonies in WA, individual animals were members of one of two distinct isotopic clusters that could be described by differences in δ15N and δ13C values. Individuals at the northernmost colony displayed δ15N values similar to those of seabirds in the same region. Across the study, isotope ratios of adult female Australian sea lions in western WA were between 3‰ and 5‰ lower than those observed at a colony at similar latitude in SA.

Conclusions: Gross differences in the physical oceanography between WA and SA may in part explain the differences in isotope ratios of individuals between the regions, with lower δ15N and δ13C values in WA probably reflecting the relatively depauperate conditions of the Leeuwin Current.

Implications: Potential regional differences in trophic structure should be considered when developing appropriate management plans for Australian sea lions and regional variation in the diet of Australian sea lion warrants further investigation.

Additional keywords: diet, foraging, oceanography features, trophic complexity.


References

Aurioles, D., and Trillmich, F. (2008). Zalophus wollebaeki. IUCN 2008. IUCN Red List of Threatened Species. Available at www.iucnredlist.org [verified 29 May 2013.]

Aurioles, D., and Trillmich, F. (2009). Arctocephalus galapagoensis. IUCN 2009. IUCN Red List of Threatened Species. Available at www.iucnredlist.org [verified 29 May 2013.]

Aurioles, D., Fox, C., Sinsel, F., and Tanos, G. (1984). Prey of the California seal lion (Zalophus californianus) in the Bay of La Paz, Baja California Sur, Mexico. Journal of Mammalogy 65, 519–521.
Prey of the California seal lion (Zalophus californianus) in the Bay of La Paz, Baja California Sur, Mexico.Crossref | GoogleScholarGoogle Scholar |

Aurioles, D., Koch, P. L., and Le Boeuf, B. J. (2006). Differences in foraging location of Mexican and California elephant seals: evidence from stable isotopes in pups. Marine Mammal Science 22, 326–338.
Differences in foraging location of Mexican and California elephant seals: evidence from stable isotopes in pups.Crossref | GoogleScholarGoogle Scholar |

Austin, M. (2007). Species distribution models and ecological theory: a critical assessment and some possible new approaches. Ecological Modelling 200, 1–19.
Species distribution models and ecological theory: a critical assessment and some possible new approaches.Crossref | GoogleScholarGoogle Scholar |

Barve, N., Barve, V., Jiménez-Valverde, A., Lira-Noriega, A., Maher, S. P., Peterson, A. T., Soberón, J., and Villalobos, F. (2011). The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling 222, 1810–1819.
The crucial role of the accessible area in ecological niche modeling and species distribution modeling.Crossref | GoogleScholarGoogle Scholar |

Baylis, A. M. M., Page, B., and Goldsworthy, S. D. (2008). Effect of seasonal changes in upwelling activity on the foraging locations of a wide-ranging central-place forager, the New Zealand fur seal. Canadian Journal of Zoology 86, 774–789.
Effect of seasonal changes in upwelling activity on the foraging locations of a wide-ranging central-place forager, the New Zealand fur seal.Crossref | GoogleScholarGoogle Scholar |

Baylis, A. M. M., Hamer, D. J., and Nichols, P. D. (2009). Assessing the use of milk fatty acids to infer the diet of the Australian sea lion (Neophoca cinerea). Wildlife Research 36, 169–176.
Assessing the use of milk fatty acids to infer the diet of the Australian sea lion (Neophoca cinerea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVyhtLY%3D&md5=db20e60038d521bd81b28476146b5f26CAS |

Campbell, R. A., Gales, N. J., Lento, G. M., and Baker, C. S. (2008). Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea. Biology Letters 4, 139–142.
Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2FhsVGnug%3D%3D&md5=d97cc1f3d2b85c410ed2a916aff2667cCAS | 18042512PubMed |

Caputi, N., Fletcher, W. J., Pearce, A., and Chubb, C. F. (1996). Effect of the Leeuwin Current on the recruitment of fish and invertebrates along the Western Australian coast. Marine and Freshwater Research 47, 147–155.
Effect of the Leeuwin Current on the recruitment of fish and invertebrates along the Western Australian coast.Crossref | GoogleScholarGoogle Scholar |

Caputi, N., Chubb, C., and Pearce, A. (2001). Environmental effects on recruitment of the western rock lobster, Panulirus cygnus. Marine and Freshwater Research 52, 1167–1174.
Environmental effects on recruitment of the western rock lobster, Panulirus cygnus.Crossref | GoogleScholarGoogle Scholar |

Cherel, Y., Kernaleguen, L., Richard, P., and Guinet, C. (2009). Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biology Letters 5, 830–832.
Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MjltFOgtw%3D%3D&md5=f5f41d55c84851dd826f6c5558327f2cCAS | 19793740PubMed |

Collins, M., An, S. I., Cai, W., Ganachaud, A., Guilyardi, E., Jin, F.-F., Jochum, M., Lengaigne, M., Power, S., and Timmermann, A. (2010). The impact of global warming on the tropical Pacific Ocean and El Niño. Nature Geoscience 3, 391–397.
The impact of global warming on the tropical Pacific Ocean and El Niño.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslSrtrc%3D&md5=afe20841580264a86a6c5f1aa35ce0c4CAS |

Costa, D. P., and Gales, N. J. (2003). Energetics of a benthic diver: seasonal foraging ecology of the Australian sea lion, Neophoca cinerea. Ecological Monographs 73, 27–43.
Energetics of a benthic diver: seasonal foraging ecology of the Australian sea lion, Neophoca cinerea.Crossref | GoogleScholarGoogle Scholar |

Crawford, K., McDonald, R. A., and Bearhop, S. (2008). Applications of stable isotope techniques to the ecology of mammals. Mammal Review 38, 87–107.
Applications of stable isotope techniques to the ecology of mammals.Crossref | GoogleScholarGoogle Scholar |

Ducklow, H. W., Doney, S. C., and Steinberg, D. K. (2009). Contributions of long-term research and time-series observations to marine ecology and biogeochemistry. Annual Review of Marine Science 1, 279–302.
Contributions of long-term research and time-series observations to marine ecology and biogeochemistry.Crossref | GoogleScholarGoogle Scholar | 21141038PubMed |

Dunlop, J. N. (2011). Comparative foraging ecology in the dark tern build breeding of southwestern Australia – insights from stable isotope analysis. Marine Ornithology 39, 201–206.

Fedak, M. (2004). Marine animals as platforms for oceanographic sampling: a ‘win/win’ situation for biology and operational oceanography. Memoires of National Institute of Polar Research 58, 133–147.

Feldkamp, S. D., DeLong, R. L., and Antonelis, G. A. (1991). Effects of El Niño 1983 on the foraging patterns of California sea lions (Zalophus californianus) near San Miguel Island, California. In ‘Pinnipeds and El Niño: Responses to Environmental Stress. Vol. 88’. (Eds F. Trillmich and K. A. Ono.) pp. 146–155. (Springer-Verlag: Berlin.)

Ferguson, S. H., and Higdon, J. W. (2006). How seals divide up the world: environment, life history, and conservation. Oecologia 150, 318–329.
How seals divide up the world: environment, life history, and conservation.Crossref | GoogleScholarGoogle Scholar | 16865408PubMed |

Ferguson, A., Taggart, J. B., Prodohl, P. A., McMeel, O., Thompson, C., Stone, C., McGinnity, P., and Hynes, R. A. (1995). The application of molecular markers to the study and conservation of fish populations, with special reference to Salmo. Journal of Fish Biology 47, 103–126.
The application of molecular markers to the study and conservation of fish populations, with special reference to Salmo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xht12jurw%3D&md5=f8fb199c1dc8cefafe2ef2c132d53585CAS |

Fraley, C., and Raftery, A. (2002). Model-based clustering, discriminant analysis, and density estimation. Journal of the American Statistical Association 97, 611–631.
Model-based clustering, discriminant analysis, and density estimation.Crossref | GoogleScholarGoogle Scholar |

Gales, N., and Cheal, A. (1992). Estimating diet composition of the Australian sea lion (Neophoa cinerea) from scat analysis: an unrliable technique. Wildlife Research 19, 447–455.
Estimating diet composition of the Australian sea lion (Neophoa cinerea) from scat analysis: an unrliable technique.Crossref | GoogleScholarGoogle Scholar |

Gales, N. J., and Costa, D. P. (1997). The Australian sea lion: a review of an unusual life history. In ‘Marine Mammal Research in the Southern Hemisphere. Vol. 1. Status, Ecology and Medicine’. (Eds M. A. Hindell and C. Kemper.) pp. 78–87. (Surrey Beatty: Sydney.)

Gentry, R. L., Costa, D. P., Croxall, J. P., David, J. H. M., Davis, R. W., Kooyman, G. L., Majluf, P., McCann, T. S., and Trillmich, F. (1986). Synthesis and conclusions. In ‘Fur Seals: Maternal Strategies on Land and at Sea’. (Eds R. L. Gentry and G. L. Kooyman.) pp. 220–278. (Princeton University Press: Princeton, NJ.)

Gill, P. C., Morrice, M. G., Page, B., Pirzl, R., Levings, A. H., and Coyne, M. (2011). Blue whale habitat selection and within-season distribution in a regional upwelling system off southern Australia. Marine Ecology Progress Series 421, 243–263.
Blue whale habitat selection and within-season distribution in a regional upwelling system off southern Australia.Crossref | GoogleScholarGoogle Scholar |

Goldsworthy, S. D., McKenzie, J., Shaughnessy, P. D., McIntosh, R. R., Page, B., and Campbell, R. A. (2009). An update of the report: understanding the impediments to the growth of Australian sea lion populations. Department of the Environment Water Heritage and The Arts., No. SARDI Research Report Series No. 356., Adelaide.

Hanson, C. E., Pattiaratchi, C. B., and Waite, A. M. (2005). Seasonal production regimes off south-western Australia: influence of the Capes and Leeuwin Currents on phytoplankton dynamics. Marine and Freshwater Research 56, 1011–1026.
Seasonal production regimes off south-western Australia: influence of the Capes and Leeuwin Currents on phytoplankton dynamics.Crossref | GoogleScholarGoogle Scholar |

Harley, C. D. G. (2011). Climate change, keystone predation, and biodiversity loss. Science 334, 1124–1127.
Climate change, keystone predation, and biodiversity loss.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsV2mu7vK&md5=b463fbf622e064ba522f25c08fddcd7eCAS |

Harley, C. D. G., Randall Hughes, A., Hultgren, K. M., Miner, B. G., Sorte, C. J. B., Thornber, C. S., Rodriguez, L. F., Tomanek, L., and Williams, S. L. (2006). The impacts of climate change in coastal marine systems. Ecology Letters 9, 228–241.
The impacts of climate change in coastal marine systems.Crossref | GoogleScholarGoogle Scholar |

Higgins, L. V., and Gass, L. (1993). Birth to weaning: partuition, duration of lactation, and attendance cycles of Australian sea lions (Neophoca cinerea). Canadian Journal of Zoology 71, 2047–2055.
Birth to weaning: partuition, duration of lactation, and attendance cycles of Australian sea lions (Neophoca cinerea).Crossref | GoogleScholarGoogle Scholar |

Hobson, K. A., Schell, D. M., Renouf, D., and Noseworthy, E. (1996). Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences 53, 528–533.
Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals.Crossref | GoogleScholarGoogle Scholar |

Kämpf, J., Doubell, M., Griffin, D., Matthews, R. L., and Ward, T. M. (2004). Evidence of a large seasonal coastal upwelling system along the southern shelf of Australia. Geophysical Research Letters 31, L09310.
Evidence of a large seasonal coastal upwelling system along the southern shelf of Australia.Crossref | GoogleScholarGoogle Scholar |

Kretzmann, M. B., Costa, D. P., and Higgins, L. V. (1991). Milk composition of Australian sea lions, Neophoca cinerea: variability in lipid content. Canadian Journal of Zoology 69, 2556–2561.
Milk composition of Australian sea lions, Neophoca cinerea: variability in lipid content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhvFWmsLw%3D&md5=8fcae0483207a115c46f0ab62f9c6d6fCAS |

Liou, L. W., Price, T., Boyce, M. S., and Perrins, C. M. (1993). Fluctuating and clutch size evolution in great tits. American Naturalist 141, 507–516.
Fluctuating and clutch size evolution in great tits.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mzjt1Gqtw%3D%3D&md5=6763c8bdc278bb61c10cf5b4faaa91d5CAS | 19426019PubMed |

Lowther, A. D., and Goldsworthy, S. D. (2011a). Detecting alternate foraging ecotypes in Australian sea lion (Neophoca cinerea) breeding colonies using stable isotope analysis. Marine Mammal Science 27, 567–586.
Detecting alternate foraging ecotypes in Australian sea lion (Neophoca cinerea) breeding colonies using stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

Lowther, A. D., and Goldsworthy, S. D. (2011b). Maternal strategies of the Australian sea lion (Neophoca cinerea) at Dangerous Reef, South Australia. Australian Journal of Zoology 59, 54–62.
Maternal strategies of the Australian sea lion (Neophoca cinerea) at Dangerous Reef, South Australia.Crossref | GoogleScholarGoogle Scholar |

Lowther, A. D., and Goldsworthy, S. D. (2012). Head start: Australian sea lion pups gain experience of adult foraging grounds before weaning. Marine Biology 159, 2687–2696.
Head start: Australian sea lion pups gain experience of adult foraging grounds before weaning.Crossref | GoogleScholarGoogle Scholar |

Lowther, A. D., Hamer, D., Harcourt, R. G., and Goldsworthy, S. D. (2011). Creatures of habit: foraging habitat fildelity of adult female Australian sea lions. Marine Ecology Progress Series 443, 249–263.
Creatures of habit: foraging habitat fildelity of adult female Australian sea lions.Crossref | GoogleScholarGoogle Scholar |

Lowther, A. D., Harcourt, R. G., Goldsworthy, S. D., and Stow, A. J. (2012). Population structure of adult female Australian sea lions is driven by fine-scale foraging site fidelity. Animal Behaviour 83, 691–701.
Population structure of adult female Australian sea lions is driven by fine-scale foraging site fidelity.Crossref | GoogleScholarGoogle Scholar |

Newsome, S. D., Clementz, M. T., and Koch, P. L. (2010). Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26, 509–572.
| 1:CAS:528:DC%2BC3cXhtVaksrzJ&md5=4ea2bd0f1e4eeaee069ddd3febb54538CAS |

O’Connell, T. C., and Hedges, R. E. M. (1999). Isotopic comparison of hair and bone: archaelogical analyses. Journal of Archaeological Science 26, 661–665.
Isotopic comparison of hair and bone: archaelogical analyses.Crossref | GoogleScholarGoogle Scholar |

Ono, K. A., Boness, D. J., and Oftedal, O. T. (1987). The effect of a natural environmental disturbance on maternal investment and pup behaviour in the Californian sea lion. Behavioral Ecology and Sociobiology 21, 109–118.
The effect of a natural environmental disturbance on maternal investment and pup behaviour in the Californian sea lion.Crossref | GoogleScholarGoogle Scholar |

Pearce, A., and Pattiaratchi, C. (1999). The Capes Current: a summer countercurrent flowing past Cape Leeuwin and Cape Naturaliste, Western Australia. Continental Shelf Research 19, 401–420.
The Capes Current: a summer countercurrent flowing past Cape Leeuwin and Cape Naturaliste, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Post, E., Forchhammer, M. C., Bret-Harte, M. S., Callaghan, T. V., Christensen, T. R., Elberling, B., Fox, A. D., Gilg, O., Hik, D. S., and Høye, T. T. (2009). Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355–1358.
Ecological dynamics across the Arctic associated with recent climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2ltbnK&md5=c5644389ddfd0dc3c1cc14a6bd749dd1CAS | 19745143PubMed |

Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science 323, 737–741.
Evidence for ecological speciation and its alternative.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlert78%3D&md5=df18351b60752986dfb67dbf1850d4b0CAS | 19197053PubMed |

Shaughnessy, P. D., Goldsworthy, S. D., Hamer, D., Page, B., and McIntosh, R. R. (2011). Australian sea lions Neophoca cinerea at colonies in South Australia: distribution and abundance, 2004 to 2008. Endangered Species Research 13, 87–98.
Australian sea lions Neophoca cinerea at colonies in South Australia: distribution and abundance, 2004 to 2008.Crossref | GoogleScholarGoogle Scholar |

Thomas, A., O’Hara, B., Ligges, U., and Sturtz, S. (2006). Making BUGS open. R News 6, 12–17.

Trillmich, F., and Lechner, E. (1986). Milk of the Galapagos fur seal and sea lion, with comparison of the milk of eared seals (Otariidae). Journal of Zoology 209, 271–277.
Milk of the Galapagos fur seal and sea lion, with comparison of the milk of eared seals (Otariidae).Crossref | GoogleScholarGoogle Scholar |

Trillmich, F., and Limberger, D. (1985). Drastic effects of El Niño on Galapagos pinnipeds. Oecologia 67, 19–22.
Drastic effects of El Niño on Galapagos pinnipeds.Crossref | GoogleScholarGoogle Scholar |

Trillmich, F., and Wolf, J. B. W. (2008). Parent offspring and sibling conflict in Galapagos fur seals and sea lions. Behavioral Ecology and Sociobiology 62, 363–375.
Parent offspring and sibling conflict in Galapagos fur seals and sea lions.Crossref | GoogleScholarGoogle Scholar |

Waite, A., Thompson, P., Pesant, S., Feng, M., Beckley, L., Domingues, C., Gaughan, D., Hanson, C., Holl, C., and Koslow, T. (2007). The Leeuwin Current and its eddies: an introductory overview. Deep-sea Research. Part II, Topical Studies in Oceanography 54, 789–796.
The Leeuwin Current and its eddies: an introductory overview.Crossref | GoogleScholarGoogle Scholar |