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A systematic review of trends in research on seabird behavioral flexibility
Citation
BIAGIOTTI BARCHIESI, M.C., BIONDI, L.M. & GARCÍA, G.O. 2023. A systematic review of trends in research on seabird behavioral flexibility. Marine Ornithology 51: 293 - 300
Received 08 May 2023, accepted 23 June 2023
Date Published: 2023/10/15
Date Online: 2023/10/12
Key words: behavioral ecology, boldness, conservation, environmental issue, neophobia, marine birds, personality
Abstract
There has been an increase in interest in the study of behavioral flexibility for its role in how organisms face disturbances and changes in their environment. However, there is not much research on this topic for seabirds, whose conservation status is affected by multiple issues related to changes in their environment. The goal of this paper was to analyze research on seabird behavioral flexibility and to identify knowledge gaps. A systematic review was conducted using academic search engines and including articles published from 1986 to 2022. In the 143 articles that were analyzed, the following were identified: publication date, family and species being studied, annual cycle period, research context and focus, behavioral flexibility components studied, and related environmental issues. The results show that the study of the issue in seabirds increased between 1986 and 2022, especially for the Spheniscidae, Alcidae, and Laridae families. Most studies were conducted in the field during the reproductive period in a parental-care context, mainly focusing on behavioral diversity and personality. In the studies that focused on behavioral flexibility mechanisms, the most-studied components were neophobia and exploration, whereas in the mixed-approach studies, the study of boldness prevailed. The environmental issue that was examined the most was global climate change. Our review shows that, even if the number of studies on seabird behavioral flexibility has increased in the last decade, few of them focus on the links between specific behavioral flexibility components, conservation status, and the environmental issues pertaining to the places where the species live.
References
AMÉLINEAU, F., GRÉMILLET, D., HARDING, A.M.A., WALKUSZ, W., CHOQUET, R. & FORT, J. 2019. Arctic climate change and pollution impact Little Auk foraging and fitness across a decade. Scientific Reports 9: 1014. doi:10.1038/s41598-018-38042-z
AUDET, J.-N. & LEFEBVRE, L. 2017. What’s flexible in behavioral flexibility? Behavioral Ecology 28: 943–947. doi:10.1093/beheco/arx007
BEEVER, E.A., HALL, L.E., VARNER, J. ET AL. 2017. Behavioral flexibility as a mechanism for coping with climate change. Frontiers in Ecology and the Environment 15: 299–308. doi:10.1002/fee.1502
BUTCHART, S.H.M., STATTERSFIELD, A.J., BENNUN, L.A. ET AL. 2004. Measuring global trends in the status of biodiversity: Red List Indices for birds. PLoS Biology 2: e383. doi:10.1371/journal.pbio.0020383
CARMONA, M., AYMÍ, R. & NAVARRO, J. 2021. Importance of predictable anthropogenic food subsidies for an opportunistic gull inhabiting urban ecosystems. European Journal of Wildlife Research 67: 9. doi:10.1007/s10344-020-01446-2
CARO, T. 2007. Behavior and conservation: A bridge too far? Trends in Ecology & Evolution 22: 394-400. doi:10.1016/j.tree.2007.06.003
CAUCHARD, L., ANGERS, B., BOOGERT, N.J., LENARTH, M., BIZE, P. & DOLIGEZ, B. 2017. An experimental test of a causal link between problem-solving performance and reproductive success in wild Great Tits. Frontiers in Ecology and Evolution 5: 107. doi:10.3389/fevo.2017.00107
CAUCHARD, L., BOOGERT, N.J., LEFEBVRE, L., DUBOIS, F. & DOLIGEZ, B. 2013. Problem-solving performance is correlated with reproductive success in a wild bird population. Animal Behaviour 85: 19–26. doi:10.1016/j.anbehav.2012.10.005
CHOW, P.K.Y., LEA, S.E.G. & LEAVER, L.A. 2016. How practice makes perfect: The role of persistence, flexibility and learning in problem-solving efficiency. Animal Behaviour 112: 273–283. doi:10.1016/j.anbehav.2015.11.014
COCCON, F., VANNI, L., DABALÀ, C. & GIUNCHI, D. 2022. The abundance of Yellow-legged Gulls Larus michahellis breeding in the historic centre of Venice, Italy and the initial effects of the new waste collection policy on the population. Urban Ecosystems 25: 643–656. doi:10.1007/s11252-021-01175-7
COLE, E.F. & QUINN, J.L. 2012. Personality and problem-solving performance explain competitive ability in the wild. Proceedings of the Royal Society B 279: 1168–1175. doi:10.1098/rspb.2011.1539
COLE, E.F. & QUINN, J.L. 2014. Shy birds play it safe: Personality in captivity predicts risk responsiveness during reproduction in the wild. Biology Letters 10: 20140178. doi:10.1098/rsbl.2014.0178
COPELLO, S., SECO PON, J.P. & FAVERO, M. 2014. Spatial overlap of Black-browed Albatrosses with longline and trawl fisheries in the Patagonian Shelf during the non-breeding season. Journal of Sea Research 89: 44–51. doi:10.1016/j.seares.2014.02.006
COPPENS, C.M., DE BOER, S.F. & KOOLHAAS, J.M. 2010. Coping styles and behavioural flexibility: Towards underlying mechanisms. Philosophical Transactions of the Royal Society B 365: 4021–4028. doi:10.1098/rstb.2010.0217
CROXALL, J.P., BUTCHART, S.H.M., LASCELLES, B. ET AL. 2012. Seabird conservation status, threats and priority actions: A global assessment. Bird Conservation International 22: 1–34. doi:10.1017/S0959270912000020
DIAS, M.P., MARTIN, R., PEARMAIN, E.J. ET AL. 2019. Threats to seabirds: A global assessment. Biological Conservation 237: 525–537. doi:10.1016/j.biocon.2019.06.033
DUCKWORTH, R.A. 2010. Evolution of personality: Developmental constraints on behavioral flexibility. The Auk 127: 752–758. doi:10.1525/auk.2010.127.4.752
FENG, C. & LIANG, W. 2020. Behavioral responses of Black-headed Gulls (Chroicocephalus ridibundus) to artificial provisioning in China. Global Ecology & Conservation 21: 00873. doi:10.1016/j.gecco.2019.e00873
FORT, J., MOE, B., STRØM, H. ET AL. 2013. Multicolony tracking reveals potential threats to Little Auks wintering in the North Atlantic from marine pollution and shrinking sea ice cover. Diversity and Distributions 19: 1322–1332. doi:10.1111/ddi.12105
GARAMSZEGI, L.Z., EENS, M. & TÖRÖK, J. 2008. Birds reveal their personality when singing. PLoS One 3: e2647. doi:10.1371/journal.pone.0002647
GARCÍA-BORBOROGLU, P., POZZI, L.M., PARMA, A.M., DELL'ARCIPRETE, P. & YORIO, P. 2022. Population distribution shifts of Magellanic Penguins in northern Patagonia, Argentina: Implications for conservation and management strategies. Ocean & Coastal Management 226: 106259. doi:10.1016/j.ocecoaman.2022.106259
GÓMEZ-LAICH, A., YODA, K., ZAVALAGA, C. & QUINTANA, F. 2015. Selfies of Imperial Cormorants (Phalacrocorax atriceps): What is happening underwater? PLoS One 10: e0136980. doi:10.1371/journal.pone.0136980
GREEN, J.A., BOYD, I.L., WOAKES, A.J., WARREN, N.L. & BUTLER, P.J. 2005. Behavioural flexibility during year-round foraging in Macaroni Penguins. Marine Ecology Progress Series 296: 183–196. doi:10.3354/meps296183
GREENBERG, R.S. 1990. Ecological plasticity, neophobia, and resource use in birds. Studies in Avian Biology 13: 431–437.
GREENBERG, R. & DROEGE, S. 1999. On the decline of the Rusty Blackbird and the use of ornithological literature to document long‐term population trends. Conservation Biology 13: 553–559.
GREENBERG, R. & METTKE-HOFFMANN, C. 2001. Ecological aspects of neophobia and neophilia in birds. In: NOLAN, V. & THOMPSON, C.F. (Eds.). Current Ornithology. Volume 16. Boston, USA: Springer. doi:10.1007/978-1-4615-1211-0_3
GREGGOR, A.L., CLAYTON, N.S., PHALAN, B. & THORNTON, A. 2014. Comparative cognition for conservationists. Trends in Ecology & Evolution 29: 489-495. doi:10.1016/j.tree.2014.06.004
GRÉMILLET, D., PONCHON, A., PALECZNY, M., PALOMARES, M.-L.D., KARPOUZI, V. & PAULY, D. 2018. Persisting worldwide seabird-fishery competition despite seabird community decline. Current Biology 28: 4009–4013. doi:10.1016/j.cub.2018.10.051
GRIFFIN, A.S. & GUEZ, D. 2014. Innovation and problem solving: A review of common mechanisms. Behavioral Processes 109: 121–134. doi:10.1016/j.beproc.2014.08.027
HARDING, A., PAREDES, R., SURYAN, R. ET AL. 2013. Does location really matter? An inter-colony comparison of seabirds breeding at varying distances from productive oceanographic features in the Bering Sea. Deep-Sea Research Part II 94: 178–191. doi:10.1016/j.dsr2.2013.03.013
HICKCOX, R.P., JARA, M., DEACON, L.A.K., HARVEY, L.P. & PINCHEIRA-DONOSO, D. 2019. Global terrestrial distribution of penguins (Spheniscidae) and their conservation by protected areas. Biodiversity and Conservation 28: 2861–2876. doi:10.1007/s10531-019-01801-z
HODGES, S., ERIKSTAD, K.E. & REIERTSEN, T.K. 2022. Predicting the foraging patterns of wintering auks using a sea surface temperature model for the Barents Sea. Ecological Solutions and Evidence 3: e12181. doi:10.1002/2688-8319.12181
HOLEKAMP, K.E., SWANSON, E.M. & VAN METER, P.E. 2013. Developmental constraints on behavioural flexibility. Philosophical Transactions of the Royal Society B 368: 20120350. doi:10.1098/rstb.2012.0350
HUTCHINSON, G.E. 1957. Concluding remarks. Cold Spring Harbor Symposium on Quantitative Biology 22: 415–427.
KLOPFER, P.H. & MACARTHUR, R.H. 1960. Niche size and faunal diversity. The American Naturalist 94: 293–300. doi:10.1086/282130
KOOLHAAS, J.M., DE BOER, S.F., COPPENS, C.M. & BUWALDA, B. 2010. Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Frontiers in Neuroendocrinology 31: 307–321. doi:10.1016/j.yfrne.2010.04.001
LOPES, C.S., RAMOS, J.A. & PAIVA, V.H. 2015. Changes in vegetation cover explain shifts of colony sites by Little Terns (Sternula albifrons) in coastal Portugal. Waterbirds 38: 260–268. doi:10.1675/063.038.0306
MOHER, D., LIBERATI, A., TETZLAFF, J. & ALTMAN, D.G. 2010. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. International Journal of Surgery 8: 336–341. doi:10.1016/j.ijsu.2010.02.007
NICOLAKAKIS, N., SOL, D. & LEFEBVRE, L. 2003. Behavioural flexibility predicts species richness in birds, but not extinction risk. Animal Behaviour 65: 445–452. doi:10.1006/anbe.2003.2085
OVERINGTON, S.E., GRIFFIN, A.S., SOL, D. & LEFEBVRE, L. 2011. Are innovative species ecological generalists? A test in North American birds. Behavioral Ecology 22: 1286–1293. doi:10.1093/beheco/arr130
PAIS DE FARIA, J., PAIVA, V.H., VERÍSSIMO, S., GONÇALVES, A.M.M. & RAMOS, J.A. 2021. Seasonal variation in habitat use, daily routines and interactions with humans by urban–dwelling gulls. Urban Ecosystems 24: 1101–1115. doi:10.1007/s11252-021-01101-x
PALECZNY, M., HAMMILL, E., KARPOUZI, V. & PAULY, D. 2015. Population trend of the world’s monitored seabirds, 1950–2010. PLoS One 10: e0129342. doi:10.1371/journal.pone.0129342
PAZ, J.A., SECO PON, J.P., FAVERO, M., BLANCO, G. & COPELLO, S. 2018. Seabird interactions and by‐catch in the anchovy pelagic trawl fishery operating in northern Argentina. Aquatic Conservation 28: 850–860. doi:10.1002/aqc.2907
PHILLIPS, R.A., GALES, R., BAKER, G.B. ET AL. 2016. The conservation status and priorities for albatrosses and large petrels. Biological Conservation 201: 169–183. doi:10.1016/j.biocon.2016.06.017
PIATT, J.F., SYDEMAN, W.J. & WIESE, F. 2007. Introduction: A modern role for seabirds as indicators. Marine Ecology Progress Series 352: 199–204. doi:10.3354/meps07070
READER, S.M. & LALAND, K.N. 2003. Animal Innovation. Oxford, UK: Oxford University Press.
RECABARREN-VILLALÓN, T., RONDA, A.C., LA SALA, L. ET AL. 2023. First assessment of debris pollution in the gastrointestinal content of juvenile Magellanic Penguins (Spheniscus magellanicus) stranded on the west south Atlantic coasts. Marine Pollution Bulletin 188: 114628. doi:10.1016/j.marpolbul.2023.114628
RICKLEFS, R.E. 2004. The cognitive face of avian life histories. The Wilson Bulletin 116: 119–133.
ROPERT-COUDERT, Y., CHIARADIA, A., AINLEY, D. ET AL. 2019. Happy feet in a hostile world? The future of penguins depends on proactive management of current and expected threats. Frontiers in Marine Science 6: 248. doi:10.3389/fmars.2019.00248
SIH, A. 2013. Understanding variation in behavioural responses to human-induced rapid environmental change: A conceptual overview. Animal Behaviour 85: 1077–1088. doi:10.1016/j.anbehav.2013.02.017
SIH, A., FERRARI, M.C.O. & HARRIS, D.J. 2011. Evolution and behavioural responses to human-induced rapid environmental change. Evolutionary Applications 4: 367–387. doi:10.1111/j.1752-4571.2010.00166.x
SMITH, B.R. & BLUMSTEIN, D.T. 2008. Fitness consequences of personality: A meta-analysis. Behavioral Ecology 19: 448–455. doi:10.1093/beheco/arm144
SOL, D., DUNCAN, R.P., BLACKBURN, T.M., CASSEY, P. & LEFEBVRE, L. 2005a. Big brains, enhanced cognition, and response of birds to novel environments. Proceedings of the National Academy of Sciences 102: 5460–5465. doi:10.1073/pnas.0408145102
SOL, D., LEFEBVRE, L. & RODRÍGUEZ–TEIJEIRO, J.D. 2005b. Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds. Proceedings of the Royal Society B 272: 1433–1441. doi:10.1098/rspb.2005.3099
SOL, D., TIMMERMANS, S. & LEFEBVRE, L. 2002. Behavioural flexibility and invasion success in birds. Animal Behaviour 63: 495–502. doi:10.1006/anbe.2001.1953
SOL, D., TRISOS, C., MÚRRIA, C. ET AL. 2020. The worldwide impact of urbanisation on avian functional diversity. Ecology Letters 23: 962–972. doi:10.1111/ele.13495
STAMPS, J.A. 2016. Individual differences in behavioural plasticities. Biological Reviews 91: 534–567. doi:10.1111/brv.12186
STEWART, L.G., LAVERS, J.L., GRANT, M.L., PUSKIC, P.S. & BOND, A.L. 2020. Seasonal ingestion of anthropogenic debris in an urban population of gulls. Marine Pollution Bulletin 160: 111549. doi:10.1016/j.marpolbul.2020.111549
SYDEMAN, W.J., SCHOEMAN, D.S., THOMPSON, S.A. ET AL. 2021. Hemispheric asymmetry in ocean change and the productivity of ecosystem sentinels. Science 372: 980–983. doi:10.1126/science.abf1772
SYDEMAN, W.J., THOMPSON, S.A. & KITAYSKY, A. 2012. Seabirds and climate change: Roadmap for the future. Marine Ecology Progress Series 454: 107–117. doi:10.3354/meps09806
TEBBICH, S., GRIFFIN, A.S., PESCHL, M.F. & STERELNY, K. 2016. From mechanisms to function: An integrated framework of animal innovation. Philosophical Transactions of the Royal Society B 371: 20150195. doi:10.1098/rstb.2015.0195
VARDI, R. & BERGER-TAL, O. 2022. Environmental variability as a predictor of behavioral flexibility in urban environments. Behavioral Ecology 33: 573-581. doi:10.1093/beheco/arac002
WILCOX, C., VAN SEBILLE, E. & HARDESTY, B.D. 2015. Threat of plastic pollution to seabirds is global, pervasive, and increasing. Proceedings of the National Academy of Sciences 112: 11899–11904. doi:10.1073/pnas.1502108112
WILLIAMS, H.J., TAYLOR, L.A., BENHAMOU, S. ET AL. 2020. Optimizing the use of biologgers for movement ecology research. Journal of Animal Ecology 89: 186–206. doi:10.1111/1365-2656.13094
WONG, B.B.M. & CANDOLIN, U. 2015. Behavioral responses to changing environments. Behavioral Ecology 26: 665–673. doi:10.1093/beheco/aru183
YDENBERG, R.C. & PRINS, H.H.T. 2012. Foraging. In: CANDOLIN, U. & WONG B.B.M. (Eds.). Behavioural Responses to a Changing World. Oxford, UK: Oxford University Press.
YORIO, P., BRANCO, J.O., LENZI, J., LUNA-JORQUERA, G. & ZAVALAGA, C. 2016. Distribution and trends in Kelp Gull (Larus dominicanus) coastal breeding populations in South America. Waterbirds 39: 114–135. doi:10.1675/063.039.sp103
YORIO, P., FRERE, E., GANDINI, P. & SCHIAVINI, A. 2001. Tourism and recreation at seabird breeding sites in Patagonia, Argentina: Current concerns and future prospects. Bird Conservation International 11: 231–245. doi:10.1017/S0959270901000314