Environmental heterogeneity promotes individual specialisation in habitat selection in a widely distributed seabird.

behavioural consistency foraging behaviour habitat selection kittiwake movement ecology seabird

Journal

The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574

Informations de publication

Date de publication:
12 2021
Historique:
received: 07 12 2020
accepted: 30 08 2021
pubmed: 8 9 2021
medline: 24 12 2021
entrez: 7 9 2021
Statut: ppublish

Résumé

Individual specialisations in behaviour are predicted to arise where divergence benefits fitness. Such specialisations are more likely in heterogeneous environments where there is both greater ecological opportunity and competition-driven frequency dependent selection. Such an effect could explain observed differences in rates of individual specialisation in habitat selection, as it offers individuals an opportunity to select for habitat types that maximise resource gain while minimising competition; however, this mechanism has not been tested before. Here, we use habitat selection functions to quantify individual specialisations while foraging by black-legged kittiwakes Rissa tridactyla, a marine top predator, at 15 colonies around the United Kingdom and Ireland, along a gradient of environmental heterogeneity. We find support for the hypothesis that individual specialisations in habitat selection while foraging are more prevalent in heterogeneous environments. This trend was significant across multiple dynamic habitat variables that change over short time-scales and did not arise through site fidelity, which highlights the importance of environmental processes in facilitating behavioural adaptation by predators. Individual differences may drive evolutionary processes, and therefore these results suggest that there is broad scope for the degree of environmental heterogeneity to determine current and future population, species and community dynamics.

Identifiants

pubmed: 34492121
doi: 10.1111/1365-2656.13588
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2875-2887

Informations de copyright

© 2021 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.

Références

Ainley, D. G., Ford, R. G., Brown, E. D., Suryan, R. M., & Irons, D. B. (2003). Prey resources, competition, and geographic structure of Kittiwake colonies in Prince William Sound. Ecology, 84(3), 709-723. https://doi.org/10.1890/0012-9658(2003)084[0709:PRCAGS]2.0.CO;2
Anderson, M. J., Ellingsen, K. E., & McArdle, B. H. (2006). Multivariate dispersion as a measure of beta diversity. Ecology Letters, 9(6), 683-693. https://doi.org/10.1111/j.1461-0248.2006.00926.x
Araújo, M. S., Bolnick, D. I., & Layman, C. A. (2011). The ecological causes of individual specialisation. Ecology Letters, 14(9), 948-958. https://doi.org/10.1111/j.1461-0248.2011.01662.x
Bastos, R., Martins, B., Cabral, J. A., Ceia, F. R., Ramos, J. A., Paiva, V. H., Luís, A., & Santos, M. (2020). Oceans of stimuli: An individual-based model to assess the role of olfactory cues and local enhancement in seabirds’ foraging behaviour. Animal Cognition, 23(4), 629-642. https://doi.org/10.1007/s10071-020-01368-1
Bates, D., Mächler, M., Bolker, B. M., & Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01
Beaugrand, G., Reid, P. C., Ibañez, F., Lindley, J. A., & Edwards, M. (2002). Reorganization of North Atlantic marine copepod biodiversity and climate. Science, 296(5573), 1692-1694. https://doi.org/10.1126/science.1071329
Beerens, J. M., Gawlik, D. E., Herring, G., & Cook, M. I. (2011). Dynamic habitat selection by two wading bird species with divergent foraging strategies in a seasonally fluctuating wetland. The Auk, 128(4), 651-662. https://doi.org/10.1525/auk.2011.10165
Behrenfeld, M. J., & Boss, E. S. (2014). Resurrecting the ecological underpinnings of ocean plankton blooms. Annual Review of Marine Science, 6(1), 167-194. https://doi.org/10.1146/annurev-marine-052913-021325
Bell, A. M., Hankison, S. J., & Laskowski, K. L. (2009). The repeatability of behaviour: A meta-analysis. Animal Behaviour, 77(4), 771-783. https://doi.org/10.1016/j.anbehav.2008.12.022
Benazzouz, A., Mordane, S., Orbi, A., Chagdali, M., Hilmi, K., Atillah, A., Lluís Pelegrí, J., & Hervé, D. (2014). An improved coastal upwelling index from sea surface temperature using satellite-based approach - The case of the Canary Current upwelling system. Continental Shelf Research, 81, 38-54. https://doi.org/10.1016/J.CSR.2014.03.012
Bolnick, D. I., & Ballare, K. M. (2020). Resource diversity promotes among-individual diet variation, but not genomic diversity, in lake stickleback. Ecology Letters, 23(3), 495-505. https://doi.org/10.1111/ele.13448
Bolnick, D. I., Svanbäck, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D., & Forister, M. L. (2003). The ecology of individuals: Incidence and implications of individual specialization. The American Naturalist, 161(1), 1-28. https://doi.org/10.1086/343878
Bonnet-Lebrun, A.-S., Phillips, R. A., Manica, A., & Rodrigues, A. S. L. (2018). Quantifying individual specialization using tracking data: A case study on two species of albatrosses. Marine Biology, 165(10), 152. https://doi.org/10.1007/s00227-018-3408-x
Bradshaw, C. J. A., Hindell, M. A., Sumner, M. D., & Michael, K. J. (2004). Loyalty pays: Potential life history consequences of fidelity to marine foraging regions by southern elephant seals. Animal Behaviour, 68(6), 1349-1360. https://doi.org/10.1016/j.anbehav.2003.12.013
Carroll, M. J., Bolton, M., Owen, E., Anderson, G. Q. A., Mackley, E. K., Dunn, E. K., & Furness, R. W. (2017). Kittiwake breeding success in the southern North Sea correlates with prior sandeel fishing mortality. Aquatic Conservation: Marine and Freshwater Ecosystems, 27(6), 1164-1175. https://doi.org/10.1002/aqc.2780
Carroll, M. J., Butler, A., Owen, E., Ewing, S. R., Cole, T., Green, J. A., Soanes, L. M., Arnould, J. P. Y., Newton, S. F., Baer, J., Daunt, F., Wanless, S., Newell, M. A., Robertson, G. S., Mavor, R. A., & Bolton, M. (2015). Effects of sea temperature and stratification changes on seabird breeding success. Climate Research, 66(1), 75-89. https://doi.org/10.3354/cr01332
Ceia, F. R., & Ramos, J. A. (2015). Individual specialization in the foraging and feeding strategies of seabirds: A review. Marine Biology, 162(10), 1923-1938. https://doi.org/10.1007/s00227-015-2735-4
Chivers, L. S., Lundy, M. G., Colhoun, K., Newton, S. F., & Reid, N. (2012). Diet of Black-legged Kittiwakes (Rissa tridactyla) feeding chicks at two Irish colonies highlights the importance of clupeids. Bird Study, 59(3), 363-367. https://doi.org/10.1080/00063657.2012.707638
Courbin, N., Besnard, A., Péron, C., Saraux, C., Fort, J., Perret, S., Tornos, J., & Grémillet, D. (2018). Short-term prey field lability constrains individual specialisation in resource selection and foraging site fidelity in a marine predator. Ecology Letters, 21(7), 1043-1054. https://doi.org/10.1111/ele.12970
Cox, S. L., Miller, P. I., Embling, C. B., Scales, K. L., Bicknell, A. W., Hosegood, P. J., Morgan, G., Ingram, S. N., & Votier, S. C. (2016). Seabird diving behaviour reveals the functional significance of shelf-sea fronts as foraging hotspots. Royal Society Open Science, 3(9), 160317. https://doi.org/10.1098/rsos.160317
Dall, S. R. X., Bell, A. M., Bolnick, D. I., & Ratnieks, F. L. W. (2012). An evolutionary ecology of individual differences. Ecology Letters, 15(10), 1189-1198. https://doi.org/10.1111/j.1461-0248.2012.01846.x
Davoren, G. K., & Montevecchi, W. A. (2003). Consequences of foraging trip duration on provisioning behaviour and fledging condition of common murres Uria aalgae. Journal of Avian Biology, 34(1), 44-53. https://doi.org/10.1034/j.1600-048X.2003.03008.x
Descamps, S., Anker-Nilssen, T., Barrett, R. T., Irons, D. B., Merkel, F., Robertson, G. J., Yoccoz, N. G., Mallory, M. L., Montevecchi, W. A., Boertmann, D., Artukhin, Y., Christensen-Dalsgaard, S., Erikstad, K.-E., Gilchrist, H. G., Labansen, A. L., Lorentsen, S.-H., Mosbech, A., Olsen, B., Petersen, A., … Zelenskaya, L. (2017). Circumpolar dynamics of a marine top-predator track ocean warming rates. Global Change Biology, 23(9), 3770-3780. https://doi.org/10.1111/gcb.13715
Edelaar, P., & Bolnick, D. I. (2019). Appreciating the multiple processes increasing individual or population fitness. Trends in Ecology & Evolution, 34(5), 435-446. https://doi.org/10.1016/j.tree.2019.02.001
Edelaar, P., Jovani, R., & Gomez-Mestre, I. (2017). Should I change or should I go? Phenotypic plasticity and matching habitat choice in the adaptation to environmental heterogeneity. The American Naturalist, 190(4), 506-520. https://doi.org/10.1086/693345
Fieberg, J., Matthiopoulos, J., Hebblewhite, M., Boyce, M. S., & Frair, J. L. (2010). Correlation and studies of habitat selection: Problem, red herring or opportunity? Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1550), 2233-2244. https://doi.org/10.1098/rstb.2010.0079
Frederiksen, M., Wanless, S., Harris, M. P., Rothery, P., & Wilson, L. J. (2004). The role of industrial fisheries and oceanographic change in the decline of North Sea black-legged kittiwakes. Journal of Applied Ecology, 41(6), 1129-1139. https://doi.org/10.1111/j.0021-8901.2004.00966.x
Grecian, J. W., Lane, J. V., Michelot, T., Wade, H. M., & Hamer, K. C. (2018). Understanding the ontogeny of foraging behaviour: Insights from combining marine predator bio-logging with satellite-derived oceanography in hidden Markov models. Journal of the Royal Society Interface, 15(143), 20180084. https://doi.org/10.1098/rsif.2018.0084
Greenstreet, S. P. R., Armstrong, E., Mosegaard, H., Jensen, H., Gibb, I. M., Fraser, H. M., Scott, B. E., Holland, G. J., & Sharples, J. (2006). Variation in the abundance of sandeels Ammodytes marinus off southeast Scotland: An evaluation of area-closure fisheries management and stock abundance assessment methods. ICES Journal of Marine Science, 63(8), 1530-1550. https://doi.org/10.1016/j.icesjms.2006.05.009
Harris, S. M., Descamps, S., Sneddon, L. U., Bertrand, P., Chastel, O., & Patrick, S. C. (2020). Personality predicts foraging site fidelity and trip repeatability in a marine predator. Journal of Animal Ecology, 89(1), 68-79. https://doi.org/10.1111/1365-2656.13106
Jensen, H., Wright, P. J., & Munk, P. (2003). Vertical distribution of pre-settled sandeel (Ammodytes marinus) in the North Sea in relation to size and environmental variables. ICES Journal of Marine Science, 60(6), 1342-1351. https://doi.org/10.1016/S1054-3139(03)00150-4
Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7(12), 1225-1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x
Leclerc, M., Vander Wal, E., Zedrosser, A., Swenson, J. E., Kindberg, J., & Pelletier, F. (2016). Quantifying consistent individual differences in habitat selection. Oecologia, 180(3), 697-705. https://doi.org/10.1007/s00442-015-3500-6
Lesmerises, R., & St-Laurent, M.-H. H. (2017). Not accounting for interindividual variability can mask habitat selection patterns: A case study on black bears. Oecologia, 185(3), 415-425. https://doi.org/10.1007/s00442-017-3939-8
Lewis, S., Sherratt, T. N., Hamer, K. C., & Wanless, S. (2001). Evidence of intra-specific competition for food in a pelagic seabird. Nature, 412(6849), 816-819. https://doi.org/10.1038/35090566
López-Bao, J. V., Palomares, F., Rodríguez, A., & Ferreras, P. (2011). Intraspecific interference influences the use of prey hotspots. Oikos, 120(10), 1489-1496. https://doi.org/10.1111/j.1600-0706.2011.19194.x
Manly, B. F. J., McDonald, L. L., Thomas, D. L., McDonald, T. L., & Erickson, W. P. (2002). Resource selection by animals: Statistical design and analysis for field studies. Technology, 221. https://doi.org/10.1007/0-306-48151-0
McCoy, K. D., Boulinier, T., & Tirard, C. (2005). Comparative host-parasite population structures: Disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla. Molecular Ecology, 14(9), 2825-2838. https://doi.org/10.1111/j.1365-294X.2005.02631.x
Merkel, B., Descamps, S., Yoccoz, N. G., Grémillet, D., Daunt, F., Erikstad, K. E., Ezhov, A. V., Harris, M. P., Gavrilo, M., Lorentsen, S. H., Reiertsen, T. K., Steen, H., Systad, G. H., Þórarinsson, Þ. L., Wanless, S., & Strøm, H. (2020). Individual migration strategy fidelity but no habitat specialization in two congeneric seabirds. Journal of Biogeography, 48(2), 263-275. https://doi.org/10.1111/jbi.13883
Michelot, T., Langrock, R., & Patterson, T. A. (2016). moveHMM: An R package for the statistical modelling of animal movement data using hidden Markov models. Methods in Ecology and Evolution, 7(11), 1308-1315. https://doi.org/10.1111/2041-210X.12578
Mitchell, P. I., Newton, S. F., Ratcliffe, N., Eds, T. E. D., Dunn, T. E., Poyser, A. D., & May, L. (2004). Seabird populations of Britain and Ireland: Results of the Seabird 2000 census. In JNCC, Poyser, London. (Issue August). T. & A.D. Poyser.
Muff, S., Signer, J., & Fieberg, J. (2020). Accounting for individual-specific variation in habitat-selection studies: Efficient estimation of mixed-effects models using Bayesian or frequentist computation. Journal of Animal Ecology, 89(1), 80-92. https://doi.org/10.1111/1365-2656.13087
Nakagawa, S., & Schielzeth, H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4(2), 133-142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., & Wagner, H. (2018). vegan: Community Ecology Package (R Package version 2.5-1; p. 295). CRAN.
Patrick, S. C., & Weimerskirch, H. (2014). Consistency pays: Sex differences and fitness consequences of behavioural specialization in a wide-ranging seabird. Biology Letters, 10(10), 20140630. https://doi.org/10.1098/rsbl.2014.0630
Patrick, S. C., & Weimerskirch, H. (2017). Reproductive success is driven by local site fidelity despite stronger specialisation by individuals for large-scale habitat preference. Journal of Animal Ecology, 86(3), 674-682. https://doi.org/10.1111/1365-2656.12636
Phillips, R., Lewis, S., González-Solís, J., & Daunt, F. (2017). Causes and consequences of individual variability and specialization in foraging and migration strategies of seabirds. Marine Ecology Progress Series, 578, 117-150. https://doi.org/10.3354/meps12217
Polis, G. A. (1984). Age structure component of niche width and intra-specific resource partitioning: Can age groups function as ecological species? The American Naturalist, 123(4), 541-564. https://doi.org/10.1086/284221
Riotte-Lambert, L., Benhamou, S., & Chamaillé-Jammes, S. (2015). How memory-based movement leads to nonterritorial spatial segregation. The American Naturalist, 185(4), E103-E116. https://doi.org/10.1086/680009
Rosenzweig, M. L. (1981). A theory of habitat selection. Ecology, 62(2), 327-335. https://doi.org/10.2307/1936707
Scales, K. L., Miller, P. I., Embling, C. B., Ingram, S. N., Pirotta, E., & Votier, S. C. (2014). Mesoscale fronts as foraging habitats: Composite front mapping reveals oceanographic drivers of habitat use for a pelagic seabird. Journal of the Royal Society, Interface / the Royal Society, 11(100), 20140679. https://doi.org/10.1098/rsif.2014.0679
Scott, B. E., Webb, A., Palmer, M. R., Embling, C. B., & Sharples, J. (2013). Fine scale bio-physical oceanographic characteristics predict the foraging occurrence of contrasting seabird species; Gannet (Morus bassanus) and storm petrel (Hydrobates pelagicus). Progress in Oceanography, 117, 118-129. https://doi.org/10.1016/j.pocean.2013.06.011
Sih, A., Bell, A., & Johnson, J. C. (2004). Behavioral syndromes: An ecological and evolutionary overview. Trends in Ecology & Evolution, 19(7), 372-378. https://doi.org/10.1016/j.tree.2004.04.009
Sparrow, A. D. (1999). A heterogeneity of heterogeneities. Trends in Ecology & Evolution, 14(11), 422-423. https://doi.org/10.1016/S0169-5347(99)01735-8
Svanbäck, R., & Bolnick, D. I. (2007). Intraspecific competition drives increased resource use diversity within a natural population. Proceedings of the Royal Society B: Biological Sciences, 274(1611), 839-844. https://doi.org/10.1098/rspb.2006.0198
Trevail, A. M., Green, J. A., Bolton, M., Daunt, F., Harris, S. M., Miller, P. I., Newton, S., Owen, E., Polton, J. A., Robertson, G., Sharples, & J., Patrick, S. (2021). Data from: Environmental heterogeneity promotes individual specialisation in habitat selection in a widely distributed seabird. Figshare, https://doi.org/10.6084/m9.figshare.12871634.v2
Trevail, A. M., Green, J. A., Sharples, J., Polton, J. A., Arnould, J. P. Y., & Patrick, S. C. (2019). Environmental heterogeneity amplifies behavioural response to a temporal cycle. Oikos, 128(4), 517-528. https://doi.org/10.1111/oik.05579
Trevail, A. M., Green, J. A., Sharples, J., Polton, J. A., Miller, P. I., Daunt, F., Owen, E., Bolton, M., Colhoun, K., Newton, S., Robertson, G., & Patrick, S. C. (2019). Environmental heterogeneity decreases reproductive success via effects on foraging behaviour. Proceedings of the Royal Society B: Biological Sciences, 286(1904), 20190795. https://doi.org/10.1098/rspb.2019.0795
Waggitt, J. J., Cazenave, P. W., Howarth, L. M., Evans, P. G. H., van der Kooij, J., & Hiddink, J. G. (2018). Combined measurements of prey availability explain habitat selection in foraging seabirds. Biology Letters, 14(8), 20180348. https://doi.org/10.1098/rsbl.2018.0348
Wakefield, E. D., Owen, E., Baer, J., Carroll, M. J., Daunt, F., Dodd, S. G., Green, J. A., Guilford, T., Mavor, R. A., Miller, P. I., Newell, M. A., Newton, S. F., Robertson, G. S., Shoji, A., Soanes, L. M., Votier, S. C., Wanless, S., & Bolton, M. (2017). Breeding density, fine-scale tracking, and large-scale modeling reveal the regional distribution of four seabird species. Ecological Applications, 27(7), 2074-2091. https://doi.org/10.1002/eap.1591
Webster, S. E., Galindo, J., Grahame, J. W., & Butlin, R. K. (2012). Habitat choice and speciation. International Journal of Ecology, 2012, 1-12. https://doi.org/10.1155/2012/154686
Weimerskirch, H. (2007). Are seabirds foraging for unpredictable resources? Deep Sea Research Part II: Topical Studies in Oceanography, 54(3-4), 211-223. https://doi.org/10.1016/j.dsr2.2006.11.013
Zamon, J. E. (2003). Mixed species aggregations feeding upon herring and sandlance schools in a nearshore archipelago depend on flooding tidal currents. Marine Ecology Progress Series, 261(1), 243-255. https://doi.org/10.3354/meps261243
Zweig, M. H., & Campbell, G. (1993). Receiver-operating characteristic (ROC) plots: A fundamental evaluation tool in clinical medicine. Clinical Chemistry, 39(4), 561-577. https://doi.org/10.1093/clinchem/39.4.561

Auteurs

Alice M Trevail (AM)

School of Environmental Sciences, University of Liverpool, Liverpool, UK.
Environment and Sustainability Institute, University of Exeter, Penryn, UK.

Jonathan A Green (JA)

School of Environmental Sciences, University of Liverpool, Liverpool, UK.

Mark Bolton (M)

RSPB Centre for Conservation Science, Royal Society for the Protection of Birds, Sandy, UK.

Francis Daunt (F)

Centre for Ecology & Hydrology Edinburgh, Penicuik, UK.

Stephanie M Harris (SM)

Cornell Lab of Ornithology, Cornell University, Ithaca, New York, USA.

Peter I Miller (PI)

Remote Sensing Group, Plymouth Marine Laboratory, Plymouth, UK.

Stephen Newton (S)

BirdWatch Ireland, Kilcoole, Ireland.

Ellie Owen (E)

RSPB Centre for Conservation Science, Royal Society for the Protection of Birds, Sandy, UK.

Jeff A Polton (JA)

National Oceanography Centre, Liverpool, UK.

Gail Robertson (G)

School of Mathematics, University of Edinburgh, Edinburgh, UK.

Jonathan Sharples (J)

School of Environmental Sciences, University of Liverpool, Liverpool, UK.

Samantha C Patrick (SC)

School of Environmental Sciences, University of Liverpool, Liverpool, UK.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH