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Egalitarian mixed-species bird groups enhance winter survival of subordinate group members but only in high-quality forests

  • 1.

    Krause, J. & Ruxton, G. D. Living in groups (Oxford University Press, 2002).

  • 2.

    Goodale, E. et al. The structure of mixed-species bird flocks, and their response to anthropogenic disturbance, with special reference to East Asia. Avian. Res. 6, 14 (2015).

    • Article
    • Google Scholar
  • 3.

    Goodale, E., Beuchamp, G. & Ruxton, G. D. Mixed-Species Groups of Animals: Behavior, Community Structure, and Conservation. (Academic Press, 2017).

  • 4.

    Eguchi, K., Yamagishi, S. & Randrianasolo, V. The composition and foraging behaviour of mixed-species flocks of forest-living birds in Madagascar. Ibis 135, 91–96 (1993).

    • Article
    • Google Scholar
  • 5.

    Goodale, E. et al. Regional variation in the composition and structure of mixed-species bird flocks in the Western Ghats and Sri Lanka. Curr. Sci. India 97, 648–663 (2009).

    • Google Scholar
  • 6.

    Sridhar, H. et al. Positive relationships between association strength and phenotypic similarity characterize the assembly of mixed-species bird flocks worldwide. Am. Nat. 180, 777–790 (2012).

  • 7.

    Hermann, H. R. Dominance and Aggression in Humans and Other Animals: The Great Game of Life (Academic Press, 2017).

  • 8.

    Pulliam, H. R. On the advantages of flocking. J. Theor. Biol. 38, 419–422 (1973).

  • 9.

    Elgar, M. A. Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol. Rev. 64, 13–33 (1989).

  • 10.

    Lima, S. Back to the basics of anti-predatory vigilance: the group-size effect. Anim. Behav. 49, 11–20 (1995).

    • Article
    • Google Scholar
  • 11.

    Olson, R. S., Haley, P. B., Dyer, F. C. & Adami, C. Exploring the evolution of a trade-off between vigilance and foraging in group-living organisms. Roy. Soc. Open Sci. 2, https://doi.org/10.1098/rsos.150135 (2015).

  • 12.

    Ekman, J. Ecology of non-breeding social systems of Parus. Wilson Bull. 101, 263–288 (1989).

    • Google Scholar
  • 13.

    Matthysen, E. Nonbreeding social organization in Parus. Curr Ornithol. 7, 209–249 (1990).

    • Google Scholar
  • 14.

    Beauchamp, G. Social predation: How group living benefits predators and prey (Academic Press, 2014).

  • 15.

    MacArthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377–385 (1967).

    • Google Scholar
  • 16.

    Dhondt, A. A. Interspecific Competition in Birds (Oxford University Press, 2011).

  • 17.

    Gil, M. A., Emberts, Z., Jones, H. & St Mary, C. M. Social information on fear and food drives animal grouping and fitness. Am. Nat. 189, 227–241 (2017).

  • 18.

    Sridhar, H. & Guttal, V. Friendship across species borders: factors that facilitate and constrain heterospecific sociality. Phil. Trans. Roy. Soc. 373, 20170014 (2018).

    • Article
    • Google Scholar
  • 19.

    Krams, I., Krama, T., Freeberg, T. M., Kullberg, C. & Lucas, J. R. Linking social complexity and vocal complexity: a parid perspective. Phil. Trans. Roy. Soc. B 367, 1879–1891 (2012).

    • Article
    • Google Scholar
  • 20.

    Suhonen, J. Risk of predation and foraging sites of individuals in mixed-species tit flocks. Anim. Behav. 45, 1193–1198 (1993).

    • Article
    • Google Scholar
  • 21.

    Suhonen, J. Predation risk influences the use of foraging sites by tits. Ecology 74, 1197–1203 (1993).

    • Article
    • Google Scholar
  • 22.

    Hogstad, O. The influence of energy stress on social organization and behaviour of willow tits Parus montanus. Fauna Norv. Ser. C. 11, 89–94 (1988).

    • Google Scholar
  • 23.

    Hogstad, O. Advantages of social foraging of willow tits Parus montanus. Ibis 130, 275–283 (1988).

    • Article
    • Google Scholar
  • 24.

    Krams, I. A. Predation risk and shifts of foraging sites in mixed willow and crested tit flocks. J. Avian Biol. 27, 153–156 (1996).

    • Article
    • Google Scholar
  • 25.

    Ekman, J., Cederholm, G. & Askenmo, C. Spacing and survival in winter groups of willow tit Parus montanus Conrad and crested tit Parus cristatus L. – a removal study. J Anim Ecol 50, 1–9 (1981).

    • Article
    • Google Scholar
  • 26.

    Koivula, K. & Orell, M. Social rank and winter survival in the willow tit Parus montanus. Ornis Fenn 65, 114–120 (1988).

    • Google Scholar
  • 27.

    Koivula, K., Orell, M. & Rytkönen, S. Winter survival and breeding success of dominant and subordinate willow tits Parus montanus. Ibis 138, 624–629 (1996).

    • Article
    • Google Scholar
  • 28.

    Ekman, J. Tree use and predator vulnerability of wintering passerines. Ornis Scand. 17, 261–267 (1986).

    • Article
    • Google Scholar
  • 29.

    Hogstad, O. Subordination in mixed-age bird flocks-a removal study. Ibis 131, 128–134 (1989).

    • Article
    • Google Scholar
  • 30.

    Lahti, K. Social dominance and survival in flocking passerine birds: a review with an emphasis on the willow tit Parus montanus. Ornis Fenn. 75, 1–17 (1998).

    • Google Scholar
  • 31.

    Rodríguez, A., Jansson, G. & Andrén, H. Composition of an avian guild in spatially structured habitats supports a competition–colonization trade-off. Proc. Roy. Soc. B. 274, 1403–1411 (2007).

    • Article
    • Google Scholar
  • 32.

    Speakman, J. R. The evolution of body fatness: trading off disease and predation risk. J. Exp. Biol. 221, jeb167254 (2018).

  • 33.

    Ekman, J. B. & Hake, M. K. Monitoring starvation risk: adjustments of body reserves in greenfinches (Carduelis chloris L.) during periods of unpredictable foraging success. Behav. Ecol. 1, 62–67 (1990).

    • Article
    • Google Scholar
  • 34.

    Krams, I. Rank-dependent fattening strategies of willow tit Parus montanus and crested tit P. cristatus mixed flock members. Ornis Fenn. 75, 19–26 (1998).

    • Google Scholar
  • 35.

    Witter, M. S., Cuthill, I. C. & Bonser, R. H. C. Experimental investigations of mass-dependent predation risk in the European starling, Sturnus vulgaris. Anim Behav 48, 201–222 (1994).

    • Article
    • Google Scholar
  • 36.

    Krams, I. Mass-dependent take-off ability in wintering great tits (Parus major): comparison of top-ranked adult males and subordinate juvenile females. Behav. Ecol. Sociobiol. 51, 345–349 (2002).

    • Article
    • Google Scholar
  • 37.

    Hogstad, O. Social rank in winter flocks of willow tits Parus montanus. Ibis 129, 1–9 (1987).

    • Article
    • Google Scholar
  • 38.

    Freeberg, T. M. Social complexity can drive vocal complexity: group size influences vocal information in Carolina chickadees. Psychol. Sci. 17, 557–561 (2006).

  • 39.

    Grabowska-Zhang, A. M., Sheldon, B. C. & Hinde, C. A. Long-term familiarity promotes joining in neighbour nest defence. Biol. Lett. 8, 544–546 (2012).

  • 40.

    Goodale, E., Beauchamp, G., Magrath, R., Nieh, J. C. & Ruxton, G. D. Interspecific information transfer influences animal community structure. Trends Ecol. Evol. 25, 354–361 (2010).

  • 41.

    Firth, J. & Sheldon, B. C. Social carry-over effects underpin trans-seasonally linked structure in a wild bird population. Ecol. Lett. 19, 1324–1332 (2016).

  • 42.

    Freeberg, T. M., Dunbar, R. I. M. & Ord, T. J. Social complexity as a proximate and ultimate factor in communicative complexity. Phil. Trans. Roy. Soc. B. 367, 1785–1801 (2012).

    • Article
    • Google Scholar
  • 43.

    Chazdon, R. L. et al. The potential for species conservation in tropical secondary forests. Conserv. Biol. 23, 1406–1417, https://doi.org/10.1111/j.1523-1739.2009.01338.x (2009).

  • 44.

    Griesser, M. & Nystrand, M. Vigilance and predation of a forest-living bird species depend on large-scale habitat structure. Behav. Ecol. 20, 709–715 (2009).

    • Article
    • Google Scholar
  • 45.

    Barlow, J. et al. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proc. Natl. Acad. Sci. USA 104, 18555–18560 (2007).

  • 46.

    Dolby, A. S. & Grubb, T. C. Jr. Benefits to satellite members in mixed-species foraging groups: an experimental analysis. Anim. Behav. 56, 501–509 (1998).

  • 47.

    Jullien, M. & Clobert, J. The survival value of flocking in neotropical birds: reality or fiction? Ecology 81, 3416–3430 (2000).

    • Article
    • Google Scholar
  • 48.

    Farine, D. R., Garroway, C. J. & Sheldon, B. C. Social network analysis of mixed-species flocks: Exploring the structure and evolution of interspecific social behaviour. Anim. Behav. 84, 1271–1277 (2012).

    • Article
    • Google Scholar
  • 49.

    Farine, D. R. & Milburn, P. J. Social organisation of thornbill-dominated mixed-species flocks using social network analysis. Behav. Ecol. Sociobiol. 67, 321–330 (2013).

    • Article
    • Google Scholar
  • 50.

    Hino, T. Intraspecific differences in benefits from feeding in mixed-species flocks. J. Avian Biol. 31, 441–446 (2000).

    • Article
    • Google Scholar
  • 51.

    Marra, P. P., Sherry, T. W. & Holmes, R. T. Territorial exclusion by a long-distance migrant warbler in Jamaica: a removal experiment with American redstarts (Setophaga ruticilla). Auk 110, 565–572 (1993).

    • Article
    • Google Scholar
  • 52.

    Gibson, R. M., Aspbury, A. S. & McDaniel, L. L. Active formation of mixed-species grouse leks: a role for predation in lek evolution? Proc. Roy. Soc. B. 269, 2503–2507 (2002).

    • Article
    • Google Scholar
  • 53.

    Weise, C. M. & Meyer, J. R. Juvenile dispersal and development of site-fidelity in the black-capped chickadee. Auk 96, 40–55 (1979).

    • Google Scholar
  • 54.

    Strier, K. B. Primate Behavioral Ecology (Routledge, 2016).

  • 55.

    Jansson, C. & von Brömssen, A. Winter decline of spiders and insects in spruce Picea abies and its relation to predation by birds. Holarct Ecol. 4, 82–93 (1981).

    • Google Scholar
  • 56.

    Suhonen, J., Alatalo, R. V., Carlson, A. & Höglund, J. Food resource distribution and the organization of the Parus guild in a spruce forest. Ornis Scand 23, 467–474 (1992).

    • Article
    • Google Scholar
  • 57.

    Pravosudov, V. V. Individual differences in foraging and storing behaviour in Siberian tit Parus cinctus Bodd. and willow tit Parus montanus Bald. Soviet. J. Ecol. 4, 60–64 (1986).

    • Google Scholar
  • 58.

    Sherry, D., Avery, D. M. & Stevens, A. The spacing of stored food by marsh tits. Z Tierpsychol 8, 153–162 (1982).

    • Google Scholar
  • 59.

    Stevens, T. A. & Krebs, J. R. Retrieval of stored see& by marsh its (Parus palustris) in the field. Ibis 128, 513–525 (1986).

    • Article
    • Google Scholar
  • 60.

    Inki, K. & Suhonen, J. Characteristics of cache sites most likely to be robbed by willow tits (Parus montanus). Condor 95, 742–744 (1993).

    • Article
    • Google Scholar
  • 61.

    Smith, S. M. The Black-capped Chickadee: Behavioral Ecology and Natural History (Cornell University Press, 1991).

  • 62.

    Krams, I. Long-range call use in dominance-structured crested tit Parus cristatus winter groups. J. Avian Biol. 31, 15–19 (2000).

    • Article
    • Google Scholar
  • 63.

    Ward, A. & Webster, M. Sociality: The Behaviour of Group-Living Animals (Springer, 2016).

  • 64.

    Nilsson, J. A. & Smith, H. Effects of dispersal date on winter flock establishment and social dominance in marsh tits Parus palustris. J. Anim. Ecol. 57, 917–928 (1988).

    • Article
    • Google Scholar
  • 65.

    Tóth, Z., Tuliozi, B., Baldan, D., Hoi, H. & Griggio, M. The effect of social connections on the discovery of multiple hidden food patches in a bird species. Sci. Rep. 7, 816, https://doi.org/10.1038/s41598-017-00929-8 (2017).

  • 66.

    Loukola, O. J., Seppänen, J.-T., Krams, I., Torvinen, S. S. & Forsman, J. T. Observed fitness may affect niche overlap in competing species via selective social information use. Am. Nat. 182, 474–483, https://doi.org/10.1086/671815 (2014).

    • Article
    • Google Scholar
  • 67.

    Mineka, S., Gunnar, M. & Champoux, M. Control and early socioemotional development: Infant rhesus monkeys reared in controllable versus uncontrollable environments. Child Developm. 57, 1241–1256 (1986).

    • Article
    • Google Scholar
  • 68.

    Vellucci, S.V. Primate social behavior: anxiety or depression in Psychopharmacology of Allxiolylics and Anlidepressants (ed. File, S. E.) 83–105, (Pergamon Press, 1991).

  • 69.

    Carlson, B. A. Early life experiences have complex and long-lasting effects on behaviour. Proc. Natl. Acad. Sci. USA 31, 11571–11573 (2017).

  • 70.

    Dugatkin, L. A. Winner and loser effects and the structure of dominance hierarchies. Behav. Ecol. 8, 583–587 (1997).

    • Article
    • Google Scholar
  • 71.

    Drummond, H. & Osorno, J. L. Training siblings to be submissive losers: dominance between booby nestlings. Anim. Behav. 44, 881–893 (1992).

    • Article
    • Google Scholar
  • 72.

    Mönkkönen, M., Forsman, J. T. & Helle, P. Mixed species foraging aggregations and heterospecific attraction in boreal bird communities. Oikos 77, 127–136 (1996).

    • Article
    • Google Scholar
  • 73.

    Fuxjager, M. J. et al. Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc. Natl. Acad. Sci. USA 107, 12393–12398 (2010).

  • 74.

    Colléter, M. & Brown, C. Personality traits predict hierarchy rank in male rainbowfish. Anim Behav 81, 1231–1237 (2011).

    • Article
    • Google Scholar
  • 75.

    Kurvers, R. H. J. M. et al. Personality differences explain leadership in barnacle geese. Anim. Behav. 78, 447–453 (2009).

    • Article
    • Google Scholar
  • 76.

    Gavrilets, S. On the evolutionary origins of the egalitarian syndrome. Proc. Natl. Acad. Sci. USA 109, 14069–14074 (2012).

  • 77.

    Rendenieks, Z., Nikodemus, O. & Brūmelis, G. Dynamics in forest patterns during times of forest policy changes in Latvia. European. J. Forest. Res. 134, 819–832 (2015).

    • Google Scholar
  • 78.

    Rytkönen, S. & Krams, I. Does foraging behaviour explain the poor breeding success of great tits Parus major in northern Europe? J. Avian Biol. 34, 288–297 (2003).

    • Article
    • Google Scholar
  • 79.

    Smith, S. M. Flock switching in chickadees: why be a winter floater? Am. Nat. 123, 81–98 (1984).

    • Article
    • Google Scholar
  • 80.

    Hogstad, O. Social behaviour in the non-breeding season in great tits Parus major and willow tits Poecile montanus: differences in juvenile birds’ route to territorial ownership, and pair-bond stability and mate protection in adults Ornis Norvegica 38, 1–8 (2015).

    • Article
    • Google Scholar
  • 81.

    Laaksonen, M. & Lehikoinen, E. Age determinations of willow and crested tit Parus montanus and P. cristatus. Ornis Fenn. 53, 9–14 (1976).

    • Google Scholar
  • 82.

    Svensson, L. Identification Guide to European Passerines (BTO, 2016).

  • 83.

    Lens, L. & Dhondt, A. A. Variation in coherence of crested tit winter flocks: an example of multivariative optimization. Acta Oecol. 13, 553–567 (1992).

    • Google Scholar
  • 84.

    Vinogradova, N. V., Dolnik, V. R., Efremov, V. D., Paevskij, V. A. Identification of Sex and Age of Passerine Birds of the USSR Fauna (Nauka, 1976).

  • 85.

    Adam, I., Scharff, C. & Honarmand, M. Who is who? Non-invasive methods to individually sex and mark altricial chicks. J. Visual Exp. 87, 51429 (2014).

    • Google Scholar
  • 86.

    Russell, W. M. S. & Burch, R. L. The Principles of Humane Experimental Technique. Special edition published by Universities Federation for Animal Welfare (UFAW), 1992 (Methuen & Co, 1959).

  • 87.

    Summers, R. W. The use of linear measurements when comparing masses. Bird Study 36, 77–79 (1988).

    • Article
    • Google Scholar
  • 88.

    McNamara, J. M. & Houston, A. I. The value of fat reserves and the trade-off between starvation and predation. Acta Biotheor. 38, 37–61 (1990).

  • 89.

    Pravosudov, V. V. et al. Social dominance and energy reserves in wintering woodland birds. Condor 101, 880–884 (1999).

    • Article
    • Google Scholar
  • 90.

    Kullberg, C. Strategy of pygmy owl while hunting avian and mammalian prey. Ornis Fenn. 72, 72–78 (1995).

    • Google Scholar
  • 91.

    Krams, I. Length of feeding day and body weight of great tits in a single-and a two-predator environment. Behav. Ecol. Sociobiol. 48, 147–153 (2000).

    • Article
    • Google Scholar
  • 92.

    Krams, I. A., Krams, T. & Černihovičs, J. Selection of foraging sites in mixed willow and crested tit flocks: rank-dependent strategies. Ornis Fenn. 78, 1–11 (2001).

    • Google Scholar
  • 93.

    Krama, T. et al. Intensity of haemosporidian infection of parids positively correlates with proximity to water-bodies, but negatively with host survival. J. Ornithol. 156, 1075–1084 (2015).

    • Article
    • Google Scholar
  • 94.

    Cīrule, D. et al. Habitat quality affects stress responses and survival in a bird wintering under extremely low ambient temperatures. Science of Nature 104, 99 (2017).

  • 95.

    Kullberg, C. & Ekman, J. Does predation maintain tit community diversity? Oikos 89, 41–45 (2000).

    • Article
    • Google Scholar
  • 96.

    Agresti, A. & Coull, B. A. Approximate is better than “exact” for interval estimation of binomial proportions. Am. Statistic 52, 119–126 (1998).

    • MathSciNet
    • Google Scholar
  • 97.

    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. nlme: linear and nonlinear mixed effects models. R package version 3.1–137, https://CRAN.R-project.org/package=nlme (2018).

  • 98.

    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/ (2016).


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