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1. Temporary Mate Removal During Incubation Leads to Variable Compensation in a Biparental Shorebird

Author

Martin Bulla, Mihai Valcu, Anne L. Rutten, and Bart Kempenaers

Subjects
biparental incubation, compensation, cooperation, mate removal, nest attendance, nest desertion, Evolution, QH359-425, Ecology, QH540-549.5
Abstract

Theoretical models predict that parents feeding offspring should partially compensate for the reduced care of their partner. However, for incubating birds, the level of compensation may depend on how reduced care changes the risk of entire brood failure, for example due to clutch predation, and on individual variation in the timing of depletion of energy stores. Although biparental incubation dominates in non-passerines, short-term manipulations of care during incubation are scarce. Here, we describe the response of 25 semipalmated sandpipers (Calidris pusilla) to an unexpected ~12-h absence (experimental removal) of their partner in the middle of the 21-day incubation period. During the period when the removed partner would have taken over to start its regular ~12-h incubation bout, parents compensated partially for the absence of their partner's care (mean: 59%, 95%CI: 49–70%). However, individuals varied in their response from no to full compensation, independent of parental sex. In contrast to incubation in undisturbed nests or by uniparental species, nest attendance of compensating parents tended to be higher during the warmer part of the day. Whereas compensation was unrelated to before-experimental share of incubation, parents that left the nest from a further distance upon human approach (more aware of or more “responsive” to their environment) compensated more. The quality of incubation in the after-experimental period, i.e., after return of the partner, was lower than usual, but improved quickly over time. In seven nests where the removed parent never returned, the widowed partner attended the nest for 0–10 days (median: 4), which suggests that widowed semipalmated sandpipers can adjust their incubation behavior to that observed in uniparental incubators. To conclude, our results indicate that biparental incubators are willing to tolerate a missed or irregular incubation bout of their partner. We speculate that all individuals would compensate fully, but that some fail because they deplete their energy stores, while others may be less responsive to or initially unaware of the absence of their partner.

Published
2019
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2. Temporary Mate Removal During Incubation Leads to Variable Compensation in a Biparental Shorebird

Author

Mihai Valcu, Anne L. Rutten, Bart Kempenaers, and Martin Bulla

Subjects
0106 biological sciences, 0301 basic medicine, food.ingredient, Sandpiper, Offspring, mate removal, lcsh:Evolution, cooperation, nest attendance, 010603 evolutionary biology, 01 natural sciences, Predation, Incubation period, compensation, 03 medical and health sciences, food, Nest, nest desertion, lcsh:QH540-549.5, lcsh:QH359-425, Incubation, Ecology, Evolution, Behavior and Systematics, Ecology, biology, Compensation (psychology), biology.organism_classification, biparental incubation, Brood, Calidris, 030104 developmental biology, lcsh:Ecology, Paternal care, Demography
Abstract

Biparental care for offspring requires cooperation, but it is also a potential source of conflict, since one parent may care less at the expense of the other. How, then, do parents respond to the reduction of their partner’s care? Theoretical models predict that parents that feed offspring should partially compensate for the reduced care of their partner. However, for incubating birds partial compensation is unlikely the optimal strategy, because the entire brood can fail with reduced care. Although biparental incubation dominates in non-passerine birds, short-term manipulations of parental care and evaluations of individual differences in the response, both crucial to our understanding of parental cooperation, are scarce. Here, we describe the response of semipalmated sandpiper (Calidris pusilla) parents to a 24-hour removal of their partner during the incubation period, explore factors that can explain individual variation in the response, and describe how incubation rhythms changed after the removed parent returned. On average, the parents compensated partially for the absence of their partner’s care (59%; 95%CI: 49-70%,N= 25 individuals). The level of compensation did not differ between the sexes. However, individual responses varied from no to full compensation (2-101%). In seven nests where the removed parent never returned, the widowed parent attended the nest for 0-10 days (median: 4 days). In contrast to patterns observed in undisturbed nests or in uniparental species, nest attendance during compensation tended to be higher during the warmer part of the day. Although the level of compensation was not related to the before-experimental share of incubation, more responsive parents (that left the nest earlier upon human approach) compensated more. The quality of incubation in the after-experimental period was lower than usual, but improved quickly over time. Our findings suggest that full compensation might be limited by energetic constraints or by variation in responsiveness to the absence of the partner. Nevertheless, semipalmated sandpiper parents are able to adjust their subsequent incubation behaviour to take full responsibility for the nest when widowed. Because (nearly) full compensation was the most common response, we speculate that all individuals attempt full compensation, but that some fail because their energy stores get depleted, or because they are less responsive to the absence of their partner.

Published
2019

3. Unexpected diversity in socially synchronized rhythms of shorebirds

Author

Laura McKinnon, David B. Lank, Joël Bêty, Caleb S. Spiegel, Joanna Burger, Pavel S. Tomkovich, James A. Johnson, Paul A. Smith, Tomás Montalvo, Klaus Michael Exo, Clemens Küpper, Egor Y. Loktionov, Jos C.E.W. Hooijmeijer, Bruno J. Ens, Laura Koloski, Marcel Klaassen, Jean-François Lamarre, Orsolya Vincze, Vanessa Loverti, Marie-Andrée Giroux, Mihai Valcu, Stephen Brown, Hanna Prüter, Jennie Rausch, Stephen Yezerinac, Richard B. Lanctot, Chris J. Hassell, David C. Payer, Lawrence J. Niles, Bruce Casler, Jordi Figuerola, Ron Porter, Martin Sládeček, Megan L. Boldenow, Jonathan T. Coleman, Clive Minton, Brett K. Sandercock, Kari Koivula, Bart Kempenaers, Oscar W. Johnson, Adriaan M. Dokter, András Kosztolányi, Paul F. Woodard, Sarah T. Saalfeld, Jeroen Reneerkens, Joseph A. M. Smith, Olivier Gilg, Erica Nol, Martin Bulla, Libor Praus, Barbara Helm, Alexei A. Dondua, Eunbi Kwon, Theunis Piersma, Rebecca Bentzen, Nicolas Lecomte, Nelli Rönkä, Anne L. Rutten, Phil F. Battley, James J. H. St Clair, Wim Tijsen, Tamás Székely, Michael I. Goldstein, Miroslav Šálek, José A. Alves, Nathan R. Senner, H. River Gates, F M Smith, Jesse R. Conklin, Joe Liebezeit, Hana Vitnerová, Karel Weidinger, Scott Freeman, Ken Gosbell, Veli-Matti Pakanen, Daniel Burgas, Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Max-Planck-Gesellschaft-Max-Planck-Gesellschaft, Computational Geo-Ecology, University of Amsterdam [Amsterdam] (UvA)-Institute for Biodiversity and Ecosystem Dynamics (IBED), Department of Ecology, University of Veterinary Medicine Budapest, MTA-DE ‘Lendület’ Behavioural Ecology Research Group, University of Debrecen, Apiloa GmbH, Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Division of Biology, Kansas State University, Coastal Ecology Team, Sovon Dutch Centre for Field Ornithology, Division of Migratory Birds - Northeast Region, US Fish and Wildlife Service, Global Flyway Network, Institute of Zoology, Graz University of Technology [Graz] (TU Graz), Australasian Wader Studies Group, Department of Forest Sciences [Helsinki], Faculty of Agriculture and Forestry [Helsinki], University of Helsinki-University of Helsinki, Department of Biological and Environmental Science [Jyväskylä Univ] (JYU), University of Jyväskylä (JYU), Department of Biological Sciences [Burnaby], Simon Fraser University (SFU.ca), National Park Service, State Lab for Photon Energetics, Bauman Moscow State Technical University, Biology Department, Trent University, Department of Fish and Wildlife Conservation, Virginia Polytechnic Institute and State University [Blacksburg], Center for Conservation Biology, College of William and Mary [Williamsburg] (WM), Pacifica Ecological Services, Migratory Bird Management, Shorebird Recovery Program, Manomet Center for Conservation Sciences, Faculty of Science, Charles University [Prague] (CU), Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Department of Biology and Biochemistry, University of Bath [Bath], Centre for Evolutionary Biology, The University of Western Australia (UWA), Departement de Biologie, Chimie et Géographie, Université du Québec à Rimouski (UQAR), Canadian Wildlife Service, Environment and Climate Change Canada, Chair in Global Flyway Ecology - Conservation Ecology Group, University of Groningen [Groningen]-Groningen Institute for Evolutionary Life Sciences (GELIFES), Division of Life Sciences, Rutgers, The State University of New Jersey [New Brunswick] (RU), Rutgers University System (Rutgers)-Rutgers University System (Rutgers), Audubon Society of Portland, Queensland Wader Study Group, Estación Biológica de Doñana (EBD), Consejo Superior de Investigaciones Científicas [Madrid] (CSIC), South Iceland Research Centre, University of Iceland [Reykjavik], CESAM, Universidade de Aveiro, LJ Niles Associates, Department of Zoology and Laboratory of Ornithology, Faculty of Science, Palacky University Olomouc, University of Oulu, Institute of Avian Research, Vogelwarte Helgoland, Environmental and Life Sciences, Bilingual Biology Program, York University [Toronto], Centre for Integrative Ecology, Deakin University [Burwood], Canada Research in Northern Biodiversity, Centre d'Etudes Nordiques (CEN), Université Laval [Québec] (ULaval), Canada Research in Polar and Boreal Ecology, Université de Moncton, Faculty of Environmental Sciences, Czech University of Life Sciences Prague (CZU), Department of Biology and Wildlife, University of Alaska [Fairbanks] (UAF), Alaska Coastal Rainforest Center, University of Alaska [Southeast] (UAS), Cornell University [New York], Biogéosciences [UMR 6282] [Dijon] (BGS), Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Centre National de la Recherche Scientifique (CNRS), Evolutionary Ecology Group, Babes-Bolyai University [Cluj-Napoca] (UBB), Montana State University (MSU), Wildlife Research Division, Zoological Museum, Lomonosov Moscow State University (MSU), Ecology Group, Institute of Agriculture and Environment, Arctic Beringia Program, Wildlife Conservation Society, Delaware Bay Shorebird Project, Arctic National Wildlife Refuge, Fieldday Consulting, Milner Centre for Evolution, Servei de Vigilància i Control de Plagues Urbanes, Agència de salut pública de barcelona, Royal Netherlands Institute for Sea Research (NIOZ), Migratory Bird and Habitat Program, Study supported by the Max Planck Society., Max Planck Society, University of Amsterdam [Amsterdam] ( UvA ) -Institute for Biodiversity and Ecosystem Dynamics ( IBED ), Graz University of Technology [Graz] ( TU Graz ), University of Helsinki [Helsinki], Department of Biological and Environmental Sciences, University of Jyväskylä, Department of Biological Sciences, Simon Fraser University ( SFU.ca ), US National Park Service - Alaska Region, College of William & Mary and Virginia Commonwealth University, Charles University in Prague, The University of Western Australia ( UWA ), Université du Québec A Rimouski ( UQAR ), University of Groningen [Groningen]-Groningen Institute for Evolutionary Life Sciences ( GELIFES ), Rutgers, The State University of New Jersey [New Brunswick] ( RUTGERS ), Department of Wetland Ecology, Consejo Superior de Investigaciones Científicas [Spain] ( CSIC ), Palacky University, Centre d'Etudes Nordiques ( CEN ), Université Laval, Czech University of Life Sciences Prague, University of Alaska Fairbanks ( UAF ), University of Alaska Southeast, Cornell Laboratory of Ornithology, Biogéosciences [Dijon] ( BGS ), AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université de Bourgogne ( UB ) -Centre National de la Recherche Scientifique ( CNRS ), Babeș-Bolyai University ( UBB ), Montana State University ( MSU ), Lomonosov Moscow State University ( MSU ), Massey University-Institute of Agriculture and Environment, Royal Netherlands Institute for Sea Research ( NIOZ ), Theoretical and Computational Ecology (IBED, FNWI), Piersma group, Palsbøll lab, and Conservation Ecology Group

Subjects
0301 basic medicine, Male, 0106 biological sciences, Periodicity, Time Factors, Zygote, Behavioural ecology, Captivity, Biológiai tudományok, Evolutionary ecology, 01 natural sciences, SEXUAL SELECTION, Nesting Behavior, Predation, Charadriiformes, Természettudományok, Nest, PHYLOGENIES, Incubation, Social evolution, 0303 health sciences, Multidisciplinary, ROLES, Ecology, Reproduction, Animal behaviour, Biological Evolution, Circadian Rhythm, INCUBATION PATTERNS, Sexual selection, GEOLOCATOR DATA, Crypsis, Female, CIRCADIAN-RHYTHMS, Cues, Photoperiod, Foraging, NEST PREDATION, Zoology, shorebirds, Context (language use), [SDV.BID]Life Sciences [q-bio]/Biodiversity, Environment, Biology, 010603 evolutionary biology, CLOCKS, 03 medical and health sciences, Rhythm, Species Specificity, Animals, 14. Life underwater, Sensory cue, 030304 developmental biology, [ SDV.BID ] Life Sciences [q-bio]/Biodiversity, [ SDE.BE ] Environmental Sciences/Biodiversity and Ecology, BIRDS, Feeding Behavior, EVOLUTION, 030104 developmental biology, Starvation, Predatory Behavior, socially synchronized rhythms, ta1181, [SDE.BE]Environmental Sciences/Biodiversity and Ecology
Abstract

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment1,2,3,4. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions1,5, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators6,7,8,9,10. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring)6,7,8,9,11. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood5,6,7,9. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization12 where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parent’s incubation bout varied from 1–19 h, whereas period length—the time in which a parent’s probability to incubate cycles once between its highest and lowest value—varied from 6–43 h. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or who actively protect their nest against predators. Rhythms entrainable to the 24-h light–dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity5,6,7,9. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms., The study was supported by the Max Planck Society (to B.K.). M.B. is a PhD student in the International Max Planck Research School for Organismal Biology.

Published
2016

4. Biparental incubation-scheduling : no experimental evidence for major energetic constraints

Author

Martin Bulla, Anne L. Rutten, Mihai Valcu, Will Cresswell, Bart Kempenaers, University of St Andrews. School of Biology, University of St Andrews. Scottish Oceans Institute, University of St Andrews. Institute of Behavioural and Neural Sciences, University of St Andrews. St Andrews Sustainability Institute, and University of St Andrews. Centre for Biological Diversity

Subjects
replication, Semipalmated sandpiper, Sandpiper, Artic, QH301 Biology, Constancy, Replication, statistical power, energetic demands, QH301, Animal science, Arctic, Nest, constancy, Baparental incubation, Calidris pusilla, scheduling, Cross-over design, Energetic constraints, energetic constraints, Incubation, Ecology, Evolution, Behavior and Systematics, Energetic demands, biology, Ecology, Scheduling, semipalmated sandpiper, DAS, Incubation bout length, Shorebird, biology.organism_classification, biparental incubation, incubation bout length, shorebird, Animal Science and Zoology, Original Article, Statistical power, cross-over design
Abstract

Lay Summary It is believed that a bird’s energetic reserves determine when and for how long it incubates its eggs. We challenge this view for species where both parents incubate. We experimentally reduced the energetic demands of incubation by heating and insulating the nest. These treatments had no major effect on the length of incubation bouts., Incubation is energetically demanding, but it is debated whether these demands constrain incubation-scheduling (i.e., the length, constancy, and timing of incubation bouts) in cases where both parents incubate. Using 2 methods, we experimentally reduced the energetic demands of incubation in the semipalmated sandpiper, a biparental shorebird breeding in the harsh conditions of the high Arctic. First, we decreased the demands of incubation for 1 parent only by exchanging 1 of the 4 eggs for an artificial egg that heated up when the focal bird incubated. Second, we reanalyzed the data from the only published experimental study that has explicitly tested energetic constraints on incubation-scheduling in a biparentally incubating species (Cresswell et al. 2003). In this experiment, the energetic demands of incubation were decreased for both parents by insulating the nest cup. We expected that the treated birds, in both experiments, would change the length of their incubation bouts, if biparental incubation-scheduling is energetically constrained. However, we found no evidence that heating or insulation of the nest affected the length of incubation bouts: the combined effect of both experiments was an increase in bout length of 3.6min (95% CI: −33 to 40), which is equivalent to a 0.5% increase in the length of the average incubation bout. These results demonstrate that the observed biparental incubation-scheduling in semipalmated sandpipers is not primarily driven by energetic constraints and therefore by the state of the incubating bird, implying that we still do not understand the factors driving biparental incubation-scheduling.

Published
2015

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