Abstract
A good overlap between offspring energetic requirements and availability of resources is required for successful reproduction. Accordingly, individuals from numerous species fine-tune their timing of breeding by integrating cues that predict environmental conditions during the offspring period. Besides acquiring information from their direct interaction with the environment (personal information), individuals can integrate information by observing the behaviours or performance of others (social information). The use of social information is often beneficial because the accumulated knowledge of conspecifics may represent a source of information more reliable than the intrinsically more limited personal information. However, although social information constitutes the major source of information in a wide range of contexts, studies investigating its use in the context of timing of breeding are scarce. We investigated whether black-legged kittiwakes (Rissa tridactyla) used social information to adjust the timing of egg-laying. We manipulated social information using a food-supplementation experiment, known to advance kittiwakes' reproductive phenology. We expected food-supplemented and unsupplemented pairs to delay and advance, respectively, their timing of laying when surrounded by a majority of neighbours from the opposite food-treatment. However, both unsupplemented and food-supplemented kittiwakes delayed egg-laying when surrounded by a higher proportion of neighbours from the opposite food-treatment. This result shows that kittiwakes use social information to time egg-laying, but that it is not used to match the seasonal peak of food availability. We suggest that when social and personal cues give contradictory environmental information, individuals may benefit from delaying laying to gather more information to make better decisions about investment into eggs. Further, we explored a potential proximate mechanism for the pattern we report. We show that baseline corticosterone, known to mediate reproductive decisions, was lower in unsupplemented females facing a higher proportion of food-supplemented neighbours. Altogether, our results suggest that to fine-tune their timing of laying, kittiwakes use complex decision-making processes in which social and personal information interplay.
Similar content being viewed by others
References
Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defences in animals and plants. Nature 401:60–63
Angelier F, Clément-Chastel C, Welcker J, Gabrielsen GW, Chastel O (2009) How does corticosterone affect parental behaviour and reproductive success? A study of prolactin in black-legged kittiwakes. Funct Ecol 23:784–793
Aplin LM, Farine DR, Morand-Ferron J, Cockburn A, Thornton A, Sheldon BC (2015) Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518:538
Ball GF, Ketterson ED (2008) Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos Trans R Soc Lond B Biol Sci 363:231–246
Beauchamp G (2009) Sleeping gulls monitor the vigilance behaviour of their neighbours. Biol Lett 5:9–11
Benedikt G, Pebesma E, Heuvelink G (2016) Spatio-temporal interpolation using gstat. The R Journal 8:204–218
Boulinier T, McCoy KD, Yoccoz NG, Gasparini J, Tveraa T (2008) Public information affects breeding dispersal in a colonial bird: kittiwakes cue on neighbours. Biol Lett 4:538–540
Bowers EK, Bowden AM, Thompson CF, Sakaluk K (2016) Elevated corticosterone during egg production elicits increased maternal investment and promotes nestling growth in a wild songbird. Horm Behav 83:6–13
Boyd R, Richerson PJ (1988) An evolutionary model of social learning: the effects of spatial and temporal variation. In: Zentall TS, Galef BG Jr (eds) Social learning: psychological and biological perspectives. Psychology Press, pp 29–48
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9:378–400
Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288
Buren AD, Koen-Alonso M, Pepin P, Mowbray F, Nakashima B, Stenson G et al (2014) Bottom-up regulation of capelin, a keystone forage species. PLoS ONE 9:e87589
Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Springer
Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35
Carscadden J, Montevecchi W, Davoren G, Nakashima BS (2002) Trophic relationships among capelin (Mallotus villosus) and seabirds in a changing ecosystem. ICES J Mar Sci 59:1027–1033
Carscadden J, Nakashima BS, Frank K (1997) Effects of fish length and temperature on the timing of peak spawning in capelin (Mallotus villosus). Can J Fish Aquat Sci 54:781–787
Charmantier A, Gienapp P (2014) Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Evol Appl 7:15–28
Cleal JK, Poore KR, Boullin JP, Khan O, Chau R, Hambidge O et al (2007) Mismatched pre-and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood. Proc Natl Acad Sci USA 104:9529–9533
Cornelius JM, Breuner CW, Hahn TP (2010) Under a neighbour’s influence: public information affects stress hormones and behaviour of a songbird. Proc R Soc B 277:2399–2404
Cornelius JM, Perreau G, Bishop VR, Krause JS, Smith R, Hahn TP et al (2018) Social information changes stress hormone receptor expression in the songbird brain. Horm Behav 97:31–38
Coulson JC (1966) The influence of the pair-bond and age on the breeding biology of the kittiwake gull Rissa tridactyla. J Anim Ecol 35:269–279
Daan S, Dijkstra C, Drent R, Meijer T (1988) Food supply and the annual timing of avian reproduction. In: Proceedings of the international ornithological congress, 1988, vol 19. University of Ottawa Press Ottawa, pp 392–407
Dall SRX, Giraldeau L-A, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193
Danchin E, Boulinier T, Massot M (1998) Conspecific reproductive success and breeding habitat selection: Implications for the study of coloniality. Ecology 79:2415–2428
Danchin E, Giraldeau L-A, Valone TJ, Wagner RH (2004) Public information: from nosy neighbors to cultural evolution. Science 305:487–491
Darling FF (1938) Bird flocks and the breeding cycle; a contribution to the study of avian sociality
Davoren GK, Penton P, Burke C, Montevecchi WA (2012) Water temperature and timing of capelin spawning determine seabird diets. ICES J Mar Sci 69:1234–1241
Doligez B, Danchin E, Clobert J (2002) Public information and breeding habitat selection in a wild bird population. Science 297:1168–1170
Dunn PO, Winkler DW (2010) Effects of climate change on timing of breeding and reproductive success in birds. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, pp 113–128
Emlen ST, Demong NJ (1975) Adaptive significance of synchronized breeding in a colonial bird: a new hypothesis. Science 188:1029–1031
Farnan JM, Johnson JK, Meltzer DO, Humphrey HJ, Arora VM (2008) Resident uncertainty in clinical decision making and impact on patient care: a qualitative study. BMJ Qual Saf 17:122–126
Fernández-Juricic E, Kacelnik A (2004) Information transfer and gain in flocks: the effects of quality and quantity of social information at different neighbour distances. Behav Ecol Sociobiol 55:502–511
Forsman JT, Hjernquist MB, Taipale J, Gustafsson L (2008) Competitor density cues for habitat quality facilitating habitat selection and investment decisions. Behav Ecol 19:539–545
Forsman JT, Seppänen J-T, Nykänen IL (2011) Observed heterospecific clutch size can affect offspring investment decisions. Biol Lett 8:341–343
Galef BG (2009) Strategies for social learning: testing predictions from formal theory. Adv Study Behav 39:117–151
Gasparini J, Boulinier T, Gill VA, Gil D, Hatch SA, Roulin A (2007) Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird. J Evol Biol 20:874–880
Gelman A, Su Y-S, Yajima M, Hill J, Pittau MG, Kerman J et al (2016) Package ‘arm’
Gill VA, Hatch SA (2002) Components of productivity in black-legged kittiwakes Rissa tridactyla: response to supplemental feeding. J Avian Biol 33:113–126
Gill VA, Hatch SA, Lanctot RB (2002) Sensitivity of breeding parameters to food supply in black-legged kittiwakes Rissa tridactyla. Ibis 144:268–283
Giraldeau LA, Valone TJ, Templeton JJ (2002) Potential disadvantages of using socially acquired information. Philos Trans R Soc Lond B Biol Sci 357:1559–1566
Goutte A, Angelier F, Bech C, Clément-Chastel C, Dell’Omo G, Gabrielsen GW et al (2014) Annual variation in the timing of breeding, pre-breeding foraging areas and corticosterone levels in an Arctic population of black-legged kittiwakes. Mar Ecol Prog Ser 496:233–247
Goutte A, Angelier F, Chastel CC, Trouvé C, Moe B, Bech C et al (2010) Stress and the timing of breeding: Glucocorticoid-luteinizing hormones relationships in an arctic seabird. Gen Comp Endocrinol 169:108–116
Goutte A, Clément-Chastel C, Moe B, Bech C, Gabrielsen GW, Chastel O (2011) Experimentally reduced corticosterone release promotes early breeding in black-legged kittiwakes. J Exp Biol 214:2005–2013
Grueber C, Nakagawa S, Laws R, Jamieson I (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711
Harvey S, Klandorf H, Pinchasov Y (1983) Visual and metabolic stimuli cause adrenocortical suppression in fasted chickens during refeeding. Neuroendocrinology 37:59–63
Hatch SA (2013) Kittiwake diets and chick production signal a 2008 regime shift in the Northeast Pacific. Mar Ecol Prog Ser 477:271–284
Heinen V, Stephens D (2016) Blue jays, Cyanocitta cristata, devalue social information in uncertain environments. Anim Behav 112:53–62
Hennin HL, Legagneux P, Bêty J, Williams TD, Gilchrist HG, Baker TM et al (2015) Pre-breeding energetic management in a mixed-strategy breeder. Oecologia 177:235–243
Hipfner JM (2008) Matches and mismatches: ocean climate, prey phenology and breeding success in a zooplanktivorous seabird. Mar Ecol Prog Ser 368:295–304
Jones S, Czaczkes TJ, Gallager AJ, Oberhauser FB, Gourlay E, Bacon JP (2019) Copy when uncertain: lower light levels increase trail pheromone depositing and reliance on pheromone trails in ants. Anim Behav 156:87–95
Juster R-P, McEwen BS, Lupien SJ (2010) Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev 35:2–16
Kendal RL, Coolen I, Laland KN (2004) The role of conformity in foraging when personal and social information conflict. Behav Ecol 15:269–277
Kendal RL, Coolen I, van Bergen Y, Laland KN (2005) Trade-offs in the adaptive use of social and asocial learning. Adv Study Behav 35:333–379
Kovach RP, Ellison SC, Pyare S, Tallmon DA (2015) Temporal patterns in adult salmon migration timing across southeast Alaska. Glob Chang Biol 21:1821–1833
Laland KN (2004) Social learning strategies. Anim Learn Behav 32:4–14
Lanctot RB, Hatch SA, Gill VA, Eens M (2003) Are corticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? Horm Behav 43:489–502
Lattin CR, Breuner CW, Michael Romero L (2016) Does corticosterone regulate the onset of breeding in free-living birds?: The CORT-Flexibility Hypothesis and six potential mechanisms for priming corticosteroid function. Horm Behav 78:107–120
Leclaire S, Bourret V, Pineaux M, Blanchard P, Danchin E, Hatch SA (2019) Red coloration varies with dietary carotenoid access and nutritional condition in kittiwakes. J Exp Biol 222:jeb210237
Lormée H, Jouventin P, Trouvé C, Chastel O (2003) Sex-specific patterns in baseline corticosterone and body condition changes in breeding red-footed boobies Sula sula. Ibis 145:212–219
Love OP, Gilchrist HG, Descamps S, Semeniuk CAD, Bêty J (2010) Pre-laying climatic cues can time reproduction to optimally match offspring hatching and ice conditions in an Arctic marine bird. Oecologia 164:277–286
Massaro M, Chardine JW, Jones IL, Robertson GJ (2000) Delayed capelin (Mallotus villosus) availability influences predatory behaviour of large gulls on black-legged kittiwakes (Rissa tridactyla), causing a reduction in kittiwake breeding success. Can J Zool 78:1588–1596
McLinn CM, Stephens DW (2010) An experimental analysis of receiver economics: cost, reliability and uncertainty interact to determine a signal’s value. Oikos 119:254–263
Meijer T, Langer U (1995) Food availability and egg-laying of captive European starlings. The Condor 97:718–728
Merkling T, Agdere L, Albert E, Durieux R, Hatch SA, Danchin E et al (2014) Is natural hatching asynchrony optimal? An experimental investigation of sibling competition patterns in a facultatively siblicidal seabird. Behav Ecol Sociobiol 68:309–319
Merkling T, Blanchard P, Chastel O, Glauser G, Vallat-Michel A, Hatch SA et al (2017) Reproductive effort and oxidative stress: effects of offspring sex and number on the physiological state of a long-lived bird. Funct Ecol 31:1201–1209
Merkling T, Hatch SA, Leclaire S, Danchin E, Blanchard P (2019) Offspring sex-ratio and environmental conditions in a seabird with sex-specific rearing costs: a long-term experimental approach. Evol Ecol 33:417–433
Merkling T, Immer A, Chastel O, Hatch SA, Danchin E, Blanchard P et al (2020) Materials for the study “Spying on your neighbours? Social information affects timing of breeding and stress hormone levels in a colonial seabird". Open Science Framework. https://osf.io/ejduq/
Merkling T, Leclaire S, Danchin E, Lhuillier E, Wagner RH, White J et al (2012) Food availability and offspring sex in a monogamous seabird: insights from an experimental approach. Behav Ecol 23:751–758
Merkling T, Perrot C, Helfenstein F, Ferdy JB, Gaillard L, Lefol E et al (2016) Maternal effects as drivers of sibling competition in a parent–offspring conflict context? An experimental test. Ecol Evol 6:3699–3710
Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B Biol Sci 363:1635–1645
Moore IT, Jessop TS (2003) Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm Behav 43:39–47
Morgan TJH, Laland KN (2012) The biological bases of conformity. Front Neurosci 6:87
Nager RG, Ruegger C, Van Noordwijk AJ (1997) Nutrient or energy limitation on egg formation: a feeding experiment in great tits. J Anim Ecol 66:495–507
Nakahashi W (2007) The evolution of conformist transmission in social learning when the environment changes periodically. Theor Popul Biol 72:52–66
Ouyang JQ, Muturi M, Quetting M, Hau M (2013) Small increases in corticosterone before the breeding season increase parental investment but not fitness in a wild passerine bird. Horm Behav 63:776–781
Perrins CM (1996) Eggs, egg formation and the timing of breeding. Ibis 138:2–15
Pike TW, Laland KN (2010) Conformist learning in nine-spined sticklebacks’ foraging decisions. Biol Lett 6:466–468
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing
Reed TE, Warzybok P, Wilson AJ, Bradley RW, Wanless S, Sydeman WJ (2009) Timing is everything: flexible phenology and shifting selection in a colonial seabird. J Anim Ecol 78:376–387
Regehr HM, Montevecchi WA (1997) Interactive effects of food shortage and predation on breeding failure of black-legged kittiwakes: indirect effects of fisheries activities and implications for indicator species. Mar Ecol Prog Ser 155:249–260
Regular P, Shuhood F, Power T, Montevecchi W, Robertson G, Ballam D et al (2009) Murres, capelin and ocean climate: inter-annual associations across a decadal shift. Environ Monit Assess 156:293
Rendell L, Boyd R, Cownden D, Enquist M, Eriksson K, Feldman MW et al (2010) Why copy others? Insights from the social learning strategies tournament. Science 328:208–213
Rieucau G, Giraldeau L-A (2011) Exploring the costs and benefits of social information use: an appraisal of current experimental evidence. Philos Trans R Soc Lond B Biol Sci 366:949–957
Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Phys A 140:73–79
Ruffino L, Salo P, Koivisto E, Banks PB, Korpimäki E (2014) Reproductive responses of birds to experimental food supplementation: a meta-analysis. Front Zool 11:80
Shultz MT, Piatt JF, Harding AM, Kettle AB, Van Pelt TI (2009) Timing of breeding and reproductive performance in murres and kittiwakes reflect mismatched seasonal prey dynamics. Mar Ecol Prog Ser 393:247–258
Sirot E (2006) Social information, antipredatory vigilance and flight in bird flocks. Anim Behav 72:373–382
Symonds MR, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21
Tversky A, Shafir E (1992) Choice under conflict: the dynamics of deferred decision. Psychol Sci 3:358–361
Urbany JE, Dickson PR, Wilkie WL (1989) Buyer uncertainty and information search. J Consum Res 16:208–215
Valone TJ (1989) Group foraging, public information, and patch estimation. Oikos 56:357–363
Valone TJ, Templeton JJ (2002) Public information for the assessment of quality: a widespread social phenomenon. Philos Trans R Soc Lond B Biol Sci 357:1549–1557
van Bergen Y, Coolen I, Laland KN (2004) Nine-spined sticklebacks exploit the most reliable source when public and private information conflict. Proc R Soc B 271:957–962
Verhulst S, Nilsson J-Å (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos Trans R Soc Lond B Biol Sci 363:399–410
Visser ME, Holleman LJ, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147:164–172
Visser ME, Holleman LJM, Caro SP (2009) Temperature has a causal effect on avian timing of reproduction. Proc R Soc B 276:2323–2331
Wagner RH, Danchin E (2010) A taxonomy of biological information. Oikos 119:203–209
Webster M, Laland K (2008) Social learning strategies and predation risk: minnows copy only when using private information would be costly. Proc R Soc B 275:2869–2876
Weimerskirch H, Bertrand S, Silva J, Marques JC, Goya E (2010) Use of social information in seabirds: Compass rafts indicate the heading of food patches. PLoS ONE 5:e9928
Williams TD (2005) Mechanisms underlying the costs of egg production. Bioscience 55:39–48
Wingfield J, Sapolsky R (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724
Wittenberger JF (1985) The adaptive significance of coloniality in birds. Avian Biol 8:1–78
Acknowledgements
We thank Lena Agdere, Elise Albert, Romain Durieux, Laurent Gaillard, Emilie Lefol and Emmanuelle Voisin for their help in the field. At the CEBC we thank Colette Trouvé and Charline Parenteau for corticosterone assay. We thank Jean-Baptiste Ferdy, François Rousset and Thierry Onkelinx for their help in statistical analyses.
Funding
The study was financed by a 4-year grant from the French Polar Institute Paul-Emile Victor (IPEV ‘Programme 1162 SexCoMonArc’), and is part of the ‘Laboratoire d'Excellence’ (LABEX) entitled TULIP (ANR-10-LABX-41).
Author information
Authors and Affiliations
Author notes
Anika Immer and Thomas Merkling have contributed equally to this work.
Pierrick Blanchard and Sarah Leclaire are co-last authors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This experiment was conducted under the approval of the USGS Alaska Science Center Animal Care and Use Committee, in accordance with US law and under permits from the US Fish and Wildlife Service (No. MB210495) and the State of Alaska (No. 11–108 and No. 12–115-A1). All data, code and models that were used to generate results, figures and tables presented in the main text and supplementary information are available to download from dedicated repositories on the Open Science Framework (Merkling et al. 2020).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Immer, A., Merkling, T., Chastel, O. et al. Spying on your neighbours? Social information affects timing of breeding and stress hormone levels in a colonial seabird. Evol Ecol 35, 463–481 (2021). https://doi.org/10.1007/s10682-021-10112-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-021-10112-1