Central place foraging and feather regrowth rate in bridled terns (Onychoprion anaethetus): an insight from stable isotopes
Aurélie M. T. Labbé A C , James N. Dunlop A B and Neil R. Loneragan AA Centre for Fish, Fisheries and Aquatic Ecosystems Research, School of Veterinary and Life Sciences, Murdoch University, South St, Murdoch, WA 6150, Australia.
B Conservation Council of Western Australia, 2 Delhi Place, West Perth, WA 6005, Australia.
C Corresponding author. Email: aurelie.mt.labbe@gmail.com
Marine and Freshwater Research 64(12) 1184-1191 https://doi.org/10.1071/MF12334
Submitted: 27 November 2012 Accepted: 31 May 2013 Published: 14 October 2013
Abstract
In this study, the stable isotope ratios of δ13C and δ15N of bridled terns’ (Onychoprion anaethetus) tail feathers were used to investigate changes in the food sources assimilated by the birds on Penguin Island, Western Australia, during different phases of the breeding season. Samples were taken immediately after they arrived on the island returning from migration (BM), before egg-laying (BEL), after egg-laying (AEL), after hatching (AH) and from fledglings (F). A one-way MANOVA (excluding the BM phase) and two one-way ANOVAs (including all phases), showed that the δ13C and δ15N values differed significantly between the stages of the breeding season, with the greatest differences between the BM and BEL stages. The mean δ13C values were higher and those for δ15N were lower for BM birds than all other stages, indicating that the food source assimilated by the birds, and their foraging locations, changed during the breeding season. These results support the hypothesis of the Central Place Foraging Theory, i.e. that adult breeding birds adjust their foraging strategies when they are bound to a central place to care for their young. Induced feathers were regenerated over ~70 days and their regrowth rates were similar before and after egg-laying.
Additional keywords: breeding season, convex hull area, optimal foraging, Penguin Island, rectrix, sea birds, south-western Australia, trophic niche parameter.
References
Bearhop, S., Waldron, S., Votier, S. C., and Furness, R. W. (2002). Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiological and Biochemical Zoology 75, 451–458.| Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFygt7w%3D&md5=3523211dd2f1b50ccc745f8453b49d9aCAS | 12529846PubMed |
Bond, A. L., and Jones, I. L. (2009). A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Marine Ornithology 37, 183–188.
Catry, T., Ramos, J. A., Le Corre, M., Kojadinovic, J., and Bustamante, P. (2008). The role of stable isotopes and mercury concentrations to describe seabird foraging ecology in tropical environments. Marine Biology 155, 637–647.
| The role of stable isotopes and mercury concentrations to describe seabird foraging ecology in tropical environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1GrtrjM&md5=fb707e067669c094c223ae5f2e1bef9eCAS |
Cherel, Y., Le Corre, M., Jaquemet, S., Ménard, F., Richard, P., and Weimerskirch, H. (2008). Resource partitioning within a tropical seabird community: new information from stable isotopes. Marine Ecology Progress Series 366, 281–291.
| Resource partitioning within a tropical seabird community: new information from stable isotopes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Klur%2FK&md5=497fb7bd138f0eb04c69690d9047afc8CAS |
Cornwell, W. K., Schwilk, D. W., and Ackerly, D. D. (2006). A trait-based test for habitat filtering: convex-hull volume. Ecology 87, 1465–1471.
| A trait-based test for habitat filtering: convex-hull volume.Crossref | GoogleScholarGoogle Scholar | 16869422PubMed |
Department of Environment and Conservation and Marine Parks & Reserves and Authority (2007). Shoalwater Islands Marine Park Management Plan 2007–2017 – Management Plan Number 58.
Dunlop, J. N. (1997). Foraging range, marine habitat and diet of bridled terns breeding in Western Australia. Corella 21, 77–82.
Dunlop, J. N. (2011). Comparative foraging ecology in the dark tern guild breeding off southwestern Australia – insight from stable isotope analysis. Marine Ornithology 39, 201–206.
Dunlop, J. N., and Jenkins, J. (1992). Known-age birds at a subtropical breeding colony of the bridled tern (Sterna anaethetus): a comparison with the sooty tern. Colonial Waterbirds 15, 75–82.
| Known-age birds at a subtropical breeding colony of the bridled tern (Sterna anaethetus): a comparison with the sooty tern.Crossref | GoogleScholarGoogle Scholar |
Dunlop, J. N., and Rippey, E. (1998). ‘The Natural History of the Bridled Tern on Penguin Island, Western Australia.’ (Penguin Books: Perth, Australia.)
Feng, M., Meyers, G., Pearce, A., and Wijffels, S. (2003). Annual and interannual variations of the Leeuwin Current at 32þS. Journal of Geophysical Research 108, 3355–3375.
| Annual and interannual variations of the Leeuwin Current at 32þS.Crossref | GoogleScholarGoogle Scholar |
Field, A. (2009). ‘Discovering Statistics Using SPSS.’ (SAGE Publications: London.)
France, R. L. (1995). Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series 124, 307–312.
| Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications.Crossref | GoogleScholarGoogle Scholar |
Garavanta, C. A. M., and Wooller, R. D. (2000). Courtship behaviour and breeding biology of bridled terns Sterna anaethetus on Penguin Island, Western Australia. Emu 100, 169–174.
| Courtship behaviour and breeding biology of bridled terns Sterna anaethetus on Penguin Island, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Grubb, T. C., Jr. (2006). ‘Ptilochronology: Feather Time and the Biology of Birds.’ (Oxford University Press, New York.)
Haig, D. W. (2002). Guidebook for mid-conference excursion: Penguin Island–Lake Clifton. In ‘International Symposium on Foraminifera, February 2002’. (University of Western Australia: Perth, Australia.)
Haney, J. C. (1986). Seabird patchiness in tropical oceanic waters: the influence of Sargassum “reefs”. The Auk 103, 141–151.
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 |
Hulsman, K., and Langham, N. P. E. (1985). Breeding biology of the bridled tern Sterna anaethetus. Emu 85, 240–249.
| Breeding biology of the bridled tern Sterna anaethetus.Crossref | GoogleScholarGoogle Scholar |
Hunt, G. L. (1990). The pelagic distribution of marine birds in a heterogeneous environment. Polar Research 8, 43–54.
| The pelagic distribution of marine birds in a heterogeneous environment.Crossref | GoogleScholarGoogle Scholar |
Hyndes, G. A., and Lavery, P. S. (2005). Does transported seagrass provide an important trophic link in unvegetated, nearshore areas? Estuarine, Coastal and Shelf Science 63, 633–643.
| Does transported seagrass provide an important trophic link in unvegetated, nearshore areas?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkslSks7k%3D&md5=752db97dcc8e741a8a1b10d87e244317CAS |
Hyslop, E. J. (1980). Stomach contents analysis – a review of methods and their application. Journal of Fish Biology 17, 411–429.
| Stomach contents analysis – a review of methods and their application.Crossref | GoogleScholarGoogle Scholar |
Ince, R., Hyndes, G. A., Lavery, P. S., and Vanderklift, M. A. (2007). Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuarine, Coastal and Shelf Science 74, 77–86.
| Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat.Crossref | GoogleScholarGoogle Scholar |
Inger, R., and Bearhop, S. (2008). Applications of stable isotope analyses to avian ecology. The Ibis 150, 447–461.
| Applications of stable isotope analyses to avian ecology.Crossref | GoogleScholarGoogle Scholar |
Janssen, M. H., Arcese, P., Kyser, T. K., Bertram, D. F., and Norris, D. R. (2011). Stable isotopes reveal strategic allocation of resources during juvenile development in a cryptic and threatened seabird, the marbled murrelet (Brachyramphus marmoratus). Revue Canadienne de Zoologie 89, 859–868.
| Stable isotopes reveal strategic allocation of resources during juvenile development in a cryptic and threatened seabird, the marbled murrelet (Brachyramphus marmoratus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Gmur3L&md5=0768ddda8ac695d508ad2c0d3b106d60CAS |
Jaquemet, S. (2010). Postfledging parental care and unexpected foraging behaviour of juvenile sooty terns Onychoprion fuscata in the southern Mozambique Channel. Ostrich: Journal of African Ornithology 81, 271–272.
| Postfledging parental care and unexpected foraging behaviour of juvenile sooty terns Onychoprion fuscata in the southern Mozambique Channel.Crossref | GoogleScholarGoogle Scholar |
Layman, C. A., Arrington, D. A., Montaña, C. G., and Post, D. M. (2007a). Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48.
| Can stable isotope ratios provide for community-wide measures of trophic structure?Crossref | GoogleScholarGoogle Scholar | 17489452PubMed |
Layman, C. A., Quattrochi, J. P., Peyer, C. M., and Allgeier, J. E. (2007b). Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecology Letters 10, 937–944.
| Niche width collapse in a resilient top predator following ecosystem fragmentation.Crossref | GoogleScholarGoogle Scholar | 17845294PubMed |
Lenanton, R. C. J., Valesini, F., Bastow, T. P., Nowara, G. B., Edmonds, J. S., and Connard, M. N. (2003). The use of stable isotope ratios in whitebait otolith carbonate to identify the source of prey for Western Australian penguins. Journal of Experimental Marine Biology and Ecology 291, 17–27.
| The use of stable isotope ratios in whitebait otolith carbonate to identify the source of prey for Western Australian penguins.Crossref | GoogleScholarGoogle Scholar |
Logan, J. M., and Lutcavage, M. E. (2008). A comparison of carbon and nitrogen stable isotope ratios of fish tissues following lipid extractions with non-polar and traditional chloroform/methanol solvent systems. Rapid Communications in Mass Spectrometry 22, 1081–1086.
| A comparison of carbon and nitrogen stable isotope ratios of fish tissues following lipid extractions with non-polar and traditional chloroform/methanol solvent systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWrsr0%3D&md5=e02225e38f3c94a59bf3b5bf96e56846CAS | 18327856PubMed |
Orians, G. H., and Pearson, N. E. (1979). On the theory of central place foraging. In ‘Analysis of Ecological Systems’. (Eds D. J, Horn, G. R. Stairs and R. D. Mitchell.) pp. 155–177. (Ohio State University Press: Columbia, OH.)
Perry, G., and Pianka, E. R. (1997). Animal foraging: past, present and future. Trends in Ecology & Evolution 12, 360–364.
| Animal foraging: past, present and future.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFOgsQ%3D%3D&md5=26a3235cc6c31a2b221475b779103645CAS |
Ramos, R., Militão, T., González-Solís, S., and Ruiz, X. (2009). Moulting strategies of a long-distance migratory seabird, the Mediterranean Cory's Shearwater Calonectris diomedea diomedea. The Ibis 151, 151–159.
| Moulting strategies of a long-distance migratory seabird, the Mediterranean Cory's Shearwater Calonectris diomedea diomedea.Crossref | GoogleScholarGoogle Scholar |
Schreiber, E. A., and Burger, J. (2002). Seabirds in the marine environment. In ‘Biology of Marine Birds’. (Eds E. A. Schreiber and J. Burger.) pp. 115–135. (CRC Press: Boca Raton, FL.)
Smit, A. J., Brearley, A., Hyndes, G. A., Lavery, P. S., and Walker, D. I. (2005). Carbon and nitrogen stable isotope analysis of an Amphibolis griffithii seagrass bed. Estuarine, Coastal and Shelf Science 65, 545–556.
| Carbon and nitrogen stable isotope analysis of an Amphibolis griffithii seagrass bed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2mtr7P&md5=58b779f8c38e5ca715eaaf511e8fc6b1CAS |
Thompson, D. R., Phillips, R. A., Stewart, F. M., and Waldron, S. (2000). Low δ13C signatures in pelagic seabirds: lipid ingestion as a potential source of 13C-depleted carbon in the Procellariiformes. Marine Ecology Progress Series 208, 265–271.
| Low δ13C signatures in pelagic seabirds: lipid ingestion as a potential source of 13C-depleted carbon in the Procellariiformes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFCku7g%3D&md5=b53241c64e0a54d960a7f79ae566225aCAS |
Wanless, S., Harris, M. P., Redman, P., and Speakman, J. R. (2005). Low energy values of fish as a probable cause of a major seabird breeding failure in the North Sea. Marine Ecology Progress Series 294, 1–8.
| Low energy values of fish as a probable cause of a major seabird breeding failure in the North Sea.Crossref | GoogleScholarGoogle Scholar |