Abstract
Seabirds allocate different amounts of energy to reproduction throughout the breeding season, depending on the trade-off between their own needs and those of their chicks and/or changes in environmental conditions. Provisioning parents therefore modulate their foraging behaviour and diet accordingly. However, for diving seabirds, many studies have extrapolated from individuals monitored over a short period and then assumed the observed patterns were representative of the birds’ foraging activity over the entire breeding stage/season. To address this shortcoming, we monitored continuously the diving performance of ten male little penguins from incubation to chick fledging. Simultaneously, isotopic composition was examined using δ15N and δ13C values from whole blood samples collected every 3 weeks. Birds dived more frequently but performed shallower and shorter dives as the season progressed. The guard period was especially different, with birds spending a consistently smaller proportion of time at the bottom and performing fewer prey pursuits, compared to other periods. Isotopic composition varied less within the season, although there was a slight tendency for δ15N values to decrease through time. Finally, isotopic values were highly repeatable within individuals, suggesting that individuals specialized on different prey and in different areas. Diving was less repeatable within individuals but still explained a small but significant part of the variance in blood isotopic values. Our results suggest that it is important to take into account individual variability over the course of the breeding season, as well as timing of bio-logger deployment within a stage when designing bio-logging studies.
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Data availability
Data are available upon request to Dr Andre Chiaradia achiaradia@penguins.org.au.
References
Alonso H, Granadeiro JP, Paiva VH, Dias AS, Ramos JA, Catry P (2012) Parent–offspring dietary segregation of Cory’s shearwaters breeding in contrasting environments. Mar Biol 159:1197–1207. https://doi.org/10.1007/s00227-012-1900-2
Arnould JP, Dann P, Cullen JM (2004) Determining the sex of little penguins (Eudyptula minor) in northern Bass Strait using morphometric measurements. Emu 104:261–265. https://doi.org/10.1071/MU04035
Ashmole NP (1971) Seabird ecology and the marine environment. Avian Biol 1:223–286
Bannasch R, Wilson RP, Culik B (1994) Hydrodynamic aspects of design and attachment of a back-mounted device in Penguins. J Exp Biol 194:83–96
Bearhop S, Teece MA, Waldron S, Furness RW (2000) Influence of lipid and uric acid on δ13C and δ15N values of avian blood: implications for trophic studies. Auk 117:504–507. https://doi.org/10.1093/auk/117.2.504
Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458. https://doi.org/10.1086/342800
Bell WJ (1991) Searching behaviour: the behavioural ecology of finding resources. Chapman and Hall, London
Bertram DF, Welham CVJ, Ydenberg RC (1996) Flexible effort in breeding seabirds: adjustment of provisioning according to nestling age and mass. Can J Zool 74:1876–1881. https://doi.org/10.1139/z96-211
Bost C-A, Cotté C, Bailleul F, Cherel Y, Charrassin J-B, Guinet C, Ainley DG, Weimerskirch H (2009) The importance of oceanographic fronts to marine birds and mammals of the southern oceans. J Mar Syst 78:363–376. https://doi.org/10.1016/j.jmarsys.2008.11.022
Camprasse ECM, Sutton GJ, Berlincourt M, Arnould JPY (2017) Changing with the times: little penguins exhibit flexibility in foraging behaviour and low behavioural consistency. Mar Biol 164:169. https://doi.org/10.1007/s00227-017-3193-y
Cannell BL, Cullen JM (1998) The foraging behaviour of little penguins Eudyptula minor at different light levels. Ibis 140:467–471. https://doi.org/10.1111/j.1474-919X.1998.tb04608.x
Carleton SA, Del Rio CM (2005) The effect of cold-induced increased metabolic rate on the rate of 13C and 15N incorporation in house sparrows (Passer domesticus). Oecologia 144:226–232. https://doi.org/10.1007/s00442-005-0066-8
Cavallo C, Chiaradia A, Deagle BE, McInnes JC, Sánchez S, Hays GC, Reina RD (2018) Molecular analysis of predator scats reveals role of salps in temperate inshore food webs. Front Mar Sci 5:381. https://doi.org/10.3389/fmars.2018.00381
Cavallo C, Chiaradia A, Deagle BE, Hays GC, Jarman S, McInnes JC, Ropert-Coudert Y, Sánchez S, Reina RD (2020) Quantifying prey availability using the foraging plasticity of a marine predator, the little penguin. Funct Ecol. https://doi.org/10.1111/1365-2435.13605
Ceia FR, Ramos JA (2015) Individual specialization in the foraging and feeding strategies of seabirds: a review. Mar Biol 162:1923–1938. https://doi.org/10.1007/s00227-015-2735-4
Chaurand T, Weimerskirch H (1994) The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea: a previously undescribed strategy of food provisioning in a pelagic seabird. J Anim Ecol 63:275–282. https://doi.org/10.2307/5546
Chiaradia AF, Kerry KR (1999) Daily nest attendance and breeding performance in the little penguin Eudyptula minor at Phillip Island, Australia. Mar Ornithol 27:13–20
Chiaradia A, Nisbet IC (2006) Plasticity in parental provisioning and chick growth in little penguins Eudyptula minor in years of high and low breeding success. Ardea 94:257–270
Chiaradia A, Ropert-Coudert Y, Kato A, Mattern T, Yorke J (2007) Diving behaviour of little penguins from four colonies across their whole distribution range: bathymetry affecting diving effort and fledging success. Mar Biol 151:1535–1542. https://doi.org/10.1007/s00227-006-0593-9
Chiaradia A, Forero MG, Hobson KA, Cullen JM (2010) Changes in diet and trophic position of a top predator 10 years after a mass mortality of a key prey. ICES J Mar Sci J Cons 67:1710–1720. https://doi.org/10.1093/icesjms/fsq067
Chiaradia A, Forero MG, Hobson KA, Swearer SE, Hume F, Renwick L, Dann P (2012) Diet segregation between two colonies of little penguins Eudyptula minor in southeast Australia. Austral Ecol 37:610–619. https://doi.org/10.1111/j.1442-9993.2011.02323.x
Chiaradia A, Ramírez F, Forero MG, Hobson KA (2016) Stable Isotopes (δ13C, δ15N) combined with conventional dietary approaches reveal plasticity in central-place foraging behavior of little penguins Eudyptula minor. Front Ecol Evol 3:154. https://doi.org/10.3389/fevo.2015.00154
Chilvers BL (2019) Variability of little blue penguin (Eudyptula minor) diving behaviour across New Zealand. N Z J Ecol 43:1–8
Collins M, Cullen JM, Dann P (1999) Seasonal and annual foraging movements of little penguins from Phillip Island, Victoria. Wildl Res 26:705–721. https://doi.org/10.1071/wr98003
Cottin M, Raymond B, Kato A, Amélineau F, Le Maho Y, Raclot T, Galton-Fenzi B, Meijers A, Ropert-Coudert Y (2012) Foraging strategies of male Adélie penguins during their first incubation trip in relation to environmental conditions. Mar Biol 159:1843–1852. https://doi.org/10.1007/s00227-012-1974-x
Davoren GK, Burger AE (1999) Differences in prey selection and behaviour during self-feeding and chick provisioning in rhinoceros auklets. Anim Behav 58:853–863. https://doi.org/10.1006/anbe.1999.1209
Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283. https://doi.org/10.3354/cr033271
Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884. https://doi.org/10.1038/nature02808
Elliott KH, Woo KJ, Gaston AJ (2009) Specialization in Murres: the story of eight specialists. Waterbirds 32:491–506. https://doi.org/10.1675/063.032.0402
Erikstad KE, Asheim M, Fauchald P, Dahlhaug L, Tveraa T, Dahlhaug P (1997) Adjustment of parental effort in the puffin; the roles of adult body condition and chick size. Behav Ecol Sociobiol 40:95–100. https://doi.org/10.1007/s002650050320
Fasola M, Saino N (1995) Sex-biased parental-care allocation in three tern species (Laridae, Aves). Can J Zool 73:1461–1467. https://doi.org/10.1139/z95-172
Fry B (2006) Stable isotope ecology. Springer, New York
González-Solís J, Croxall JP, Wood AG (2000) Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels, Macronectes halli, during incubation. Oikos 90:390–398. https://doi.org/10.1034/j.1600-0706.2000.900220.x
Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2010) Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern, and process on Earth through isotope mapping. Springer, Netherlands, pp 299–318
Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 9–18
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Kato A, Ropert-Coudert Y, Grémillet D, Cannell B (2006) Locomotion and foraging strategy in foot-propelled and wing-propelled shallow-diving seabirds. Mar Ecol Prog Ser 308:293–301. https://doi.org/10.3354/meps308293
Kato A, Ropert-Coudert Y, Chiaradia A (2008) Regulation of trip duration by an inshore forager, the little penguin (Eudyptula minor), during incubation. Auk 125:588–593. https://doi.org/10.1525/auk.2008.06273
Kerry K, Clarke J, Else G (1993) The use of an automated weighing and recording system for the study of the biology of adelie penguins (Pygoscelis adeliae). Proc NIPR Symp Polar Biol 6:62–75
Kowalczyk ND, Reina RD, Preston TJ, Chiaradia A (2015) Environmental variability drives shifts in the foraging behaviour and reproductive success of an inshore seabird. Oecologia 178:967–979. https://doi.org/10.1007/s00442-015-3294-6
Lack DL (1968) Ecological adaptations for breeding in birds. Methuen, North Yorkshire
Le Guen C, Kato A, Raymond B, Barbraud C, Beaulieu M, Bost C-A, Delord K, MacIntosh AJ, Meyer X, Raclot T (2018) Reproductive performance and diving behaviour share a common sea-ice concentration optimum in Adélie penguins (Pygoscelis adeliae). Glob Change Biol 24:5304–5317. https://doi.org/10.1111/gcb.14377
Martin TE (1987) Food as a limit on breeding birds: a life-history perspective. Annu Rev Ecol Syst 18:453–487. https://doi.org/10.1146/annurev.es.18.110187.002321
Masello JF, Wikelski M, Voigt CC, Quillfeldt P (2013) Distribution patterns predict individual specialization in the diet of dolphin gulls. PLoS ONE. https://doi.org/10.1371/journal.pone.0067714
Meyer X, MacIntosh AJJ, Chiaradia A, Kato A, Ramírez F, Sueur C, Ropert-Coudert Y (2020) Oceanic thermal structure mediates dive sequences in a foraging seabird. Ecol Evol 10:6610–6622. https://doi.org/10.1002/ece3.6393
Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956. https://doi.org/10.1111/j.1469-185X.2010.00141.x
Patrick SC, Bearhop S, Grémillet D, Lescroël A, Grecian WJ, Bodey TW, Hamer KC, Wakefield E, Le Nuz M, Votier SC (2014) Individual differences in searching behaviour and spatial foraging consistency in a central place marine predator. Oikos 123:33–40. https://doi.org/10.1111/j.1600-0706.2013.00406.x
Pelletier L, Chiaradia A, Kato A, Ropert-Coudert Y (2014) Fine-scale spatial age segregation in the limited foraging area of an inshore seabird species, the little penguin. Oecologia 176:399–408. https://doi.org/10.1007/s00442-014-3018-3
Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP (2004) Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence? Proc R Soc Lond B Biol Sci 271:1283–1291. https://doi.org/10.1098/rspb.2004.2718
Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233. https://doi.org/10.1016/S0169-5347(03)00036-3
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. https://doi.org/10.1007/s00442-006-0630-x
Potier S, Carpentier A, Grémillet D, Leroy B, Lescroël A (2015) Individual repeatability of foraging behaviour in a marine predator, the great cormorant, Phalacrocorax carbo. Anim Behav 103:83–90. https://doi.org/10.1016/j.anbehav.2015.02.008
Poupart TA, Waugh SM, Bost C, Bost C-A, Dennis T, Lane R, Rogers K, Sugishita J, Taylor GA, Wilson K-J, Zhang J, Arnould JPY (2017) Variability in the foraging range of Eudyptula minor across breeding sites in central New Zealand. N Z J Zool 44:225–244. https://doi.org/10.1080/03014223.2017.1302970
R Core Team (2017) A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2017
Robinson S, Chiaradia A, Hindell MA (2005) The effect of body condition on the timing and success of breeding in little penguins Eudyptula minor. Ibis 147:483–489. https://doi.org/10.1111/j.1474-919x.2005.00431.x
Ropert-Coudert Y, Kato A, Naito Y, Cannell BL (2003) Individual diving strategies in the little penguin. Waterbirds 26:403–408. https://doi.org/10.1675/1524-4695(2003)026[0403:IDSITL]2.0.CO;2
Ropert-Coudert Y, Wilson RP, Daunt F, Kato A (2004) Patterns of energy acquisition by a central place forager: benefits of alternating short and long foraging trips. Behav Ecol 15:824–830. https://doi.org/10.1093/beheco/arh086
Ropert-Coudert Y, Kato A, Wilson RP, Cannell B (2006) Foraging strategies and prey encounter rate of free-ranging little penguins. Mar Biol 149:139–148. https://doi.org/10.1007/s00227-005-0188-x
Ropert-Coudert Y, Knott N, Chiaradia A, Kato A (2007) How do different data logger sizes and attachment positions affect the diving behaviour of little penguins? Deep Sea Res Part II Top Stud Oceanogr 54:415–423. https://doi.org/10.1016/j.dsr2.2006.11.018
Ropert-Coudert Y, Kato A, Grémillet D, Crenner F (2012) Bio-logging: recording the ecophysiology and behaviour of animals moving freely in their environment. In: Le Galliard J-F, Guarini J-M, Gaill F (eds) Sensors for ecology: towards integrated knowledge of ecosystems. CNRS, Paris, pp 17–41
Salamolard M, Weimerskirch H (1993) Relationship between foraging effort and energy requirement throughout the breeding season in the wandering albatross. Funct Ecol. https://doi.org/10.2307/2390184
Sánchez S, Reina R, Kato A, Ropert-Coudert Y, Cavallo C, Hays G, Chiaradia A (2018) Within-colony spatial segregation leads to foraging behaviour variation in a seabird. Mar Ecol Prog Ser 606:215–230. https://doi.org/10.3354/meps12764
Saraux C, Chiaradia A, Le Maho Y, Ropert-Coudert Y (2011a) Everybody needs somebody: unequal parental effort in little penguins. Behav Ecol 22:837–845. https://doi.org/10.1093/beheco/arr049
Saraux C, Robinson-Laverick SM, Le Maho Y, Ropert-Coudert Y, Chiaradia A (2011b) Plasticity in foraging strategies of inshore birds: how little penguins maintain body reserves while feeding offspring. Ecology 92:1909–1916. https://doi.org/10.1890/11-0407.1
Schreiber EA, Burger J (2001) Biology of marine birds. CRC Press, Boca Raton
Shaffer SA, Costa DP, Weimerskirch H (2003) Foraging effort in relation to the constraints of reproduction in free-ranging albatrosses. Funct Ecol 17:66–74. https://doi.org/10.1046/j.1365-2435.2003.00705.x
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Sutherland DR, Dann P (2012) Improving the accuracy of population size estimates for burrow-nesting seabirds. Ibis 154:488–498. https://doi.org/10.1111/j.1474-919X.2012.01234.x
Takahashi A, Watanuki Y, Sato K, Kato A, Arai N, Nishikawa J, Naito Y (2003) Parental foraging effort and offspring growth in Adélie penguins: does working hard improve reproductive success? Funct Ecol 17:590–597. https://doi.org/10.1046/j.1365-2435.2003.00772.x
Wakefield ED, Bodey TW, Bearhop S, Blackburn J, Colhoun K, Davies R, Dwyer RG, Green J, Grémillet D, Jackson AL, Jessopp MJ, Kane A, Langston RHW, Lescroël A, Murray S, Nuz ML, Patrick SC, Péron C, Soanes L, Wanless S, Votier SC, Hamer KC (2013) Space partitioning without territoriality in Gannets. Science. https://doi.org/10.1126/science.1236077
Weimerskirch H, Cherel Y, Cuenot-Chaillet F, Ridoux V (1997) Alternative foraging strategies and resource allocation by male and female wandering albatrosses. Ecology 78:2051–2063. https://doi.org/10.1890/0012-9658(1997)078[2051:AFSARA]2.0.CO;2
Wilson R (1995) Foraging ecology. The penguins Spheniscidae. Oxford University Press, Oxford, pp 81–106
Wilson RP (2003) Penguins predict their performance. Mar Ecol Prog Ser 249:305–310. https://doi.org/10.3354/meps249305
Wilson RP, Wilson M-PT (1990) Foraging ecology of breeding Spheniscus penguins. In: Davis LS, Darby J (eds) Penguin biology. Academic Press, San Diego, pp 181–206
Wilson RP, Pütz K, Peters G, Culik B, Scolaro JA, Charrassin J-B, Ropert-Coudert Y (1997) Long-term attachment of transmitting and recording devices to penguins and other seabirds. Wildl Soc Bull 25:101–106
Wilson LJ, Daunt F, Wanless S (2004) Self-feeding and chick provisioning diet differ in the common guillemot Uria aalge. Ardea 92:197–207
Woo KJ, Elliott KH, Davidson M, Gaston AJ, Davoren GK (2008) Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. J Anim Ecol 77:1082–1091. https://doi.org/10.1111/j.1365-2656.2008.01429.x
Ydenberg RC, Clark CW (1989) Aerobiosis and anaerobiosis during diving by western grebes: an optimal foraging approach. J Theor Biol 139:437–447. https://doi.org/10.1016/S0022-5193(89)80064-5
Zimmer I, Wilson RP, Beaulieu M, Ropert-Coudert Y, Kato A, Ancel A, Plötz J (2010) Dive efficiency versus depth in foraging emperor penguins. Aquat Biol 8:269–277. https://doi.org/10.3354/ab00213
Zuur A, Ieno EN, Smith GM (2007) Analyzing ecological data. Springer, New York
Acknowledgements
We would like to thank the research staff and rangers at the Phillip Island Nature Park for their help. Finally, we thank three anonymous reviewers for their valuable comments.
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The study was financially supported by the Japan Science Society, the Australian Academy of Science, the University of Strasbourg, the Penguin Foundation and the Japan Society for the Promotion of Science.
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YRC, AK, AC designed the study, IZ, AC performed the field work, KH performed the isotope analyses, AK and YRC ran logger data analyses, FA, CS analysed the data, FA, CS, AC wrote the manuscript. All authors read and commented on the final manuscript.
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The study was conducted with research permits issued by the Department of Environment, Land, Water and Planning, Victorian State Government, Australia, and ethics approvals from the Animal Ethics Committee of Phillip Island Nature Parks.
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Amélineau, F., Saraux, C., Ropert-Coudert, Y. et al. Intra- and inter-individual changes in little penguin diving and isotopic composition over the breeding season. Mar Biol 168, 62 (2021). https://doi.org/10.1007/s00227-021-03867-2
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DOI: https://doi.org/10.1007/s00227-021-03867-2