in

Thermal adaptation best explains Bergmann’s and Allen’s Rules across ecologically diverse shorebirds

  • Delhey, K. A review of Gloger’s rule, an ecogeographical rule of colour: definitions, interpretations and evidence. Biol. Rev. 94, 1294–1316 (2019).

    PubMed 

    Google Scholar 

  • Tian, L. & Benton, M. J. Predicting biotic responses to future climate warming with classic ecogeographic rules. Curr. Biol. 30, R744–R749 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Ryding, S., Klaassen, M., Tattersall, G. J., Gardner, J. L. & Symonds, M. R. E. Shape-shifting: changing animal morphologies as a response to climatic warming. Trends Ecol. Evol. 36, 1036–1048 (2021).

  • Salewski, V. & Watt, C. Bergmann’s rule: a biophysiological rule examined in birds. Oikos 126, 161–172 (2017).

    Google Scholar 

  • Allen, J. A. The influence of physical conditions in the genesis of species. Radic. Rev. 1, 108–140 (1877).

    Google Scholar 

  • Ashton, K. G., Tracy, M. C. & De Queiroz, A. Is Bergmann’s rule valid for mammals? Am. Nat. 156, 390–415 (2000).

    PubMed 

    Google Scholar 

  • Ashton, K. G. Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Glob. Ecol. Biogeogr. 11, 505–523 (2002).

    Google Scholar 

  • Nudds, R. L. & Oswald, S. A. An interspecific test of Allen’s rule: evolutionary implications for endothermic species. Evolution (N. Y) 61, 2839–2848 (2007).

    CAS 

    Google Scholar 

  • Symonds, M. R. E. & Tattersall, G. J. Geographical variation in bill size across bird species provides evidence for Allen’s rule. Am. Nat. 176, 188–197 (2010).

    PubMed 

    Google Scholar 

  • Cardilini, A. P. A., Buchanan, K. L., Sherman, C. D. H., Cassey, P. & Symonds, M. R. E. Tests of ecogeographical relationships in a non-native species: what rules avian morphology? Oecologia 181, 783–793 (2016).

    ADS 
    PubMed 

    Google Scholar 

  • Alhajeri, B. H., Fourcade, Y., Upham, N. S. & Alhaddad, H. A global test of Allen’s rule in rodents. Glob. Ecol. Biogeogr. 29, 2248–2260 (2020).

    Google Scholar 

  • McNab, B. K. On the ecological significance of Bergmann’s rule. Ecology 52, 845–854 (1971).

    Google Scholar 

  • Meiri, S., Dayan, T. & Simberloff, D. Carnivores, biases and Bergmann’s rule. Biol. J. Linn. Soc. 81, 579–588 (2004).

    Google Scholar 

  • Gohli, J. & Voje, K. L. An interspecific assessment of Bergmann’s rule in 22 mammalian families. BMC Evol. Biol. 16, 1–12 (2016).

    Google Scholar 

  • Freeman, B. G. Little evidence for Bergmann’s rule body size clines in passerines along tropical elevational gradients. J. Biogeogr. 44, 502–510 (2017).

    Google Scholar 

  • Riemer, K., Guralnick, R. P. & White, E. No general relationship between mass and temperature in endothermic species. Elife 7, e27166 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Blackburn, T. M., Gaston, K. J. & Loder, N. Geographic gradients in body size: a clarification of Bergmann’s rule. Divers. Distrib. 5, 165–174 (1999).

    Google Scholar 

  • Watt, C., Mitchell, S. & Salewski, V. Bergmann’s rule; a concept cluster? Oikos 119, 89–100 (2010).

    Google Scholar 

  • James, F. C. Geographic size variation in birds and its relationship to climate. Ecology 51, 365–390 (1970).

    Google Scholar 

  • Cartar, R. V. & Morrison, R. I. G. Metabolic correlates of leg length in breeding arctic shorebirds: the cost of getting high. J. Biogeogr. 32, 377–382 (2005).

    Google Scholar 

  • Friedman, N. R., Harmáčková, L., Economo, E. P. & Remeš, V. Smaller beaks for colder winters: thermoregulation drives beak size evolution in Australasian songbirds. Evolution (N. Y). 71, 2120–2129 (2017).

  • Fan, L., Cai, T., Xiong, Y., Song, G. & Lei, F. Bergmann’s rule and Allen’s rule in two passerine birds in China. Avian. Res. 10, 1–11 (2019).

    Google Scholar 

  • Romano, A., Séchaud, R. & Roulin, A. Geographical variation in bill size provides evidence for Allen’s rule in a cosmopolitan raptor. Glob. Ecol. Biogeogr. 29, 65–75 (2020).

    Google Scholar 

  • Romano, A., Séchaud, R. & Roulin, A. Generalized evidence for Bergmann’s rule: body size variation in a cosmopolitan owl genus. J. Biogeogr. 48, 51–63 (2021).

    Google Scholar 

  • Gardner, J. L. et al. Spatial variation in avian bill size is associated with humidity in summer among Australian passerines. Clim. Chang. Responses 3, 1–11 (2016).

    Google Scholar 

  • Greenberg, R. & Danner, R. M. The influence of the california marine layer on bill size in a generalist songbird. Evolution (N. Y) 66, 3825–3835 (2012).

    Google Scholar 

  • Greenberg, R., Danner, R., Olsen, B. & Luther, D. High summer temperature explains bill size variation in salt marsh sparrows. Ecography (Cop.) 35, 146–152 (2012).

    Google Scholar 

  • Klir, J. J. & Heath, J. E. An infrared thermographic study of surface temperature in relation to external thermal stress in three species of foxes: the red fox (Vulpes vulpes), Arctic fox, and kit fox (Vulpes macrotis). Physiol. Zool. 65, 1011–1021 (1992).

    Google Scholar 

  • Ballentine, B. & Greenberg, R. Common garden experiment reveals genetic control of phenotypic divergence between swamp sparrow subspecies that lack divergence in neutral genotypes. PLoS One 5, 1–6 (2010).

    Google Scholar 

  • Nord, A. & Giroud, S. Lifelong effects of thermal challenges during development in birds and mammals. Front. Physiol. 11, 1–9 (2020).

    Google Scholar 

  • Riek, A. & Geiser, F. Developmental phenotypic plasticity in a marsupial. J. Exp. Biol. 215, 1552–1558 (2012).

    PubMed 

    Google Scholar 

  • Cunningham, S. J., Martin, R. O., Hojem, C. L. & Hockey, P. A. R. Temperatures in excess of critical thresholds threaten nestling growth and survival in a rapidly-warming arid savanna: a study of common fiscals. PLoS One 8, e74613 (2013).

  • Mariette, M. M. & Buchanan, K. L. Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird. Science 353, 812–814 (2016).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Nord, A. & Nilsson, J. Å. Incubation temperature affects growth and energy metabolism in blue tit nestlings. Am. Nat. 178, 639–651 (2011).

    PubMed 

    Google Scholar 

  • Serrat, M. A. Allen’s rule revisited: temperature influences bone elongation during a critical period of postnatal development. Anat. Rec. 296, 1534–1545 (2013).

    Google Scholar 

  • Larson, E. R. et al. Nest microclimate predicts bill growth in the Adelaide rosella (Aves: Psittaculidae). Biol. J. Linn. Soc. 124, 339–349 (2018).

    Google Scholar 

  • Burness, G., Huard, J. R., Malcolm, E. & Tattersall, G. J. Post-hatch heat warms adult beaks: irreversible physiological plasticity in Japanese quail. Proc. R. Soc. B Biol. Sci. 280, 20131436 (2013).

  • Husby, A., Hille, S. M. & Visser, M. E. Testing mechanisms of bergmann’s rule: phenotypic decline but no genetic change in body size in three passerine bird populations. Am. Nat. 178, 202–213 (2011).

    PubMed 

    Google Scholar 

  • Cresswell, W., Clark, J. A. & Macleod, R. How climate change might influence the starvation-predation risk trade-off response. Proc. R. Soc. B Biol. Sci. 276, 3553–3560 (2009).

    CAS 

    Google Scholar 

  • McNamara, J. M., Higginson, A. D. & Verhulst, S. The influence of the starvation-predation trade-off on the relationship between ambient temperature and body size among endotherms. J. Biogeogr. 43, 809–819 (2016).

    PubMed 

    Google Scholar 

  • Dickman, C. R. Body size, prey size, and community structure in insectivorous mammals. Ecology 69, 569–580 (1988).

    Google Scholar 

  • Carbone, C., Mace, G. M., Roberts, S. C. & Macdonald, D. W. Energetic constraints on the diet of terrestrial carnivores. Nature 402, 286–288 (1999).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Cohen, J. E., Pimm, S. L., Yodzis, P., & Saldaña, J. Body sizes of animal predators and animal prey in food webs. J. Anim. Ecol. 62, 67–78 (1993).

    Google Scholar 

  • McKinnon, L. et al. Lower predation risk for migratory birds at high latitudes. Science 327, 326–327 (2010).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Díaz, M. et al. The geography of fear: a latitudinal gradient in anti-predator escape distances of birds across Europe. PLoS One 8, e64634 (2013).

  • Gosler, A. G., Greenwood, J. J. D. & Perrins, C. Predation risk and the cost of being fat. Nature 377, 621–623 (1995).

    ADS 
    CAS 

    Google Scholar 

  • Anderson, A. M. et al. Consistent declines in wing lengths of Calidridine sandpipers suggest a rapid morphometric response to environmental change. PLoS One 14, 1–21 (2019).

    CAS 

    Google Scholar 

  • Milá, B., Wayne, R. K. & Smith, T. B. Ecomorphology of migratory and sedentary populations of the yellow-rumped warbler (Dendroica Coronata). Condor 110, 335–344 (2008).

    Google Scholar 

  • O’Hara, P. D., Fernández, G., Haase, B., de la Cueva, H. & Lank, D. B. Differential migration in western sandpipers with respect to body size and wing length. Condor 108, 225–232 (2006).

    Google Scholar 

  • Ketterson, E. D. & Nolan, V. Geographic variation and its climatic correlates in the sex ratio of eastern-wintering dark-eyed juncos (Junco hyemalis hyemalis). Ecology 57, 679–693 (1976).

    Google Scholar 

  • Nebel, S. Differential migration of shorebirds in the East Asian-Australasian Flyway. Emu 107, 14–18 (2007).

    Google Scholar 

  • Elner, R. W. & Seaman, D. A. Calidrid conservation: unrequited needs. Wader Study Gr. Bull. 100, 30–34 (2003).

    Google Scholar 

  • Greenberg, R. Dissimilar bill shapes in new world tropical versus temperate forest foliage-gleaning birds. Oecologia 49, 143–147 (1981).

    ADS 
    PubMed 

    Google Scholar 

  • Nebel, S. Latitudinal clines in bill length and sex ratio in a migratory shorebird: a case of resource partitioning? Acta Oecologica 28, 33–38 (2005).

    ADS 

    Google Scholar 

  • Mathot, K. J., Smith, B. D. & Elner, R. W. Latitudinal clines in food distribution correlate with differential migration in the Western Sandpiper. Ecology 88, 781–791 (2007).

    PubMed 

    Google Scholar 

  • Duijns, S. et al. Sex-specific winter distribution in a sexually dimorphic shorebird is explained by resource partitioning. Ecol. Evol. 4, 4009–4018 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Wilson, J. R., Nebel, S. & Minton, C. D. T. Migration ecology and morphometrics of two Bar-tailed Godwit populations in Australia. Emu 107, 262–274 (2007).

    Google Scholar 

  • Nebel, S., Rogers, K. G., Minton, C. D. T. & Rogers, D. I. Is geographical variation in the size of Australian shorebirds consistent with hypotheses on differential migration? Emu 113, 99–111 (2013).

    Google Scholar 

  • Beltran, R. S., Burns, J. M. & Breed, G. A. Convergence of biannual moulting strategies across birds and mammals. Proc. R. Soc. B Biol. Sci. 285, 20180318 (2018).

  • Tattersall, G. J., Arnaout, B. & Symonds, M. R. E. The evolution of the avian bill as a thermoregulatory organ. Biol. Rev. 92, 1630–1656 (2017).

    PubMed 

    Google Scholar 

  • Battley, P. F., Rogers, D. I., Piersma, T. & Koolhaas, A. Behavioural evidence for heat-load problems in Great Knots in tropical Australia fuelling for long-distance flight. Emu 103, 97–103 (2003).

    Google Scholar 

  • Rogers, D. I., Piersma, T. & Hassell, C. J. Roost availability may constrain shorebird distribution: Exploring the energetic costs of roosting and disturbance around a tropical bay. Biol. Conserv. 133, 225–235 (2006).

    Google Scholar 

  • Danner, R. M. & Greenberg, R. A critical season approach to Allen’s rule: Bill size declines with winter temperature in a cold temperate environment. J. Biogeogr. 42, 114–120 (2015).

    Google Scholar 

  • Buchholz, R. Thermoregulatory role of the unfeathered head and neck in male wild turkeys. Auk 113, 310–318 (1996).

    Google Scholar 

  • Marchant, S. & Higgins, P. J. (eds.) Handbook of Australian, New Zealand and Antarctic Birds. Volume 2: Raptors to Lapwings (Oxford University Press, 1993).

  • Higgins, P. J. & Davies, S. J. J. F. (eds.) Handbook of Australian, New Zealand and Antarctic Birds. Volume 3: Snipe to Pigeons (Oxford University Press, 1996).

  • Andrew, S. C., Hurley, L. L., Mariette, M. M. & Griffith, S. C. Higher temperatures during development reduce body size in the zebra finch in the laboratory and in the wild. J. Evol. Biol. 30, 2156–2164 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Morrick, Z. N. et al. Differential population trends align with migratory connectivity in an endangered shorebird. Conserv. Sci. Pract. 4, 1–13 (2022).

    Google Scholar 

  • Hassell, C., Southey, I., Boyle, A. & Yang, H.-Y. Red knot Calidris canutus: subspecies and migration in the East Asian-Australasian flyway – where do all the red knot go? BirdingASIA 16, 89–93 (2011).

    Google Scholar 

  • Battley, P. F. et al. Contrasting extreme long-distance migration patterns in bar-tailed godwits Limosa lapponica. J. Avian Biol. 43, 21–32 (2012).

    Google Scholar 

  • Aharon-Rotman, Y., Buchanan, K. L., Clark, N. J., Klaassen, M. & Buttemer, W. A. Why fly the extra mile? Using stress biomarkers to assess wintering habitat quality in migratory shorebirds. Oecologia 182, 385–395 (2016).

    ADS 
    PubMed 

    Google Scholar 

  • Aharon-Rotman, Y., Gosbell, K., Minton, C. & Klaassen, M. Why fly the extra mile? Latitudinal trend in migratory fuel deposition rate as driver of trans-equatorial long-distance migration. Ecol. Evol. 6, 6616–6624 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hollands, D. & Minton, C. Waders: The Shorebirds of Australia (Bloomings Books, 2012).

  • Siepielski, A. M. et al. No evidence that warmer temperatures are associated with selection for smaller body sizes. Proc. R. Soc. B Biol. Sci. 286, 20191332 (2019).

  • Ho, C. K., Pennings, S. C. & Carefoot, T. H. Is diet quality an overlooked mechanism for Bergmann’s rule? Am. Nat. 175, 269–276 (2010).

    PubMed 

    Google Scholar 

  • Piersma, T. et al. Fuel storage rates in Red Knots worldwide: facing the severest ecological constraint in tropical intertidal environments? In Birds of Two Worlds: Ecology and Evolution of Migration (eds Greenburg, R. & Marra, P. P.) (Smithsonian Institution Press, 2005).

  • Hedenström, A. & Rosén, M. Predator versus prey: on aerial hunting and escape strategies in birds. Behav. Ecol. 12, 150–156 (2001).

    Google Scholar 

  • Van Den Hout, P. J., Mathot, K. J., Maas, L. R. M. & Piersma, T. Predator escape tactics in birds: linking ecology and aerodynamics. Behav. Ecol. 21, 16–25 (2010).

    Google Scholar 

  • Schemske, D. W., Mittelbach, G. G., Cornell, H. V., Sobel, J. M. & Roy, K. Is there a latitudinal gradient in the importance of biotic interactions? Annu. Rev. Ecol. Evol. Syst. 40, 245–269 (2009).

    Google Scholar 

  • Cain, K. E. et al. Conspicuous plumage does not increase predation risk: a continent-wide test using model songbirds. Am. Nat. 193, 359–372 (2019).

    PubMed 

    Google Scholar 

  • Cohen, J. E., Pimm, S. L., Yodzis, P. & Saldana, J. Body sizes of animal predators and animal prey in food webs. J. Anim. Ecol. 62, 67–78 (1993).

    Google Scholar 

  • Gotmark, F. & Post, P. Prey selection by sparrowhawks, Accipiter nisus: relative predation risk for breeding passerine birds in relation to their size, ecology and behaviour. Philos. Trans. R. Soc. B Biol. Sci. 351, 1559–1577 (1996).

    ADS 

    Google Scholar 

  • McQueen, A. et al. Evolutionary drivers of seasonal plumage colours: colour change by moult correlates with sexual selection, predation risk and seasonality across passerines. Ecol. Lett. 22, 1838–1849 (2019).

    PubMed 

    Google Scholar 

  • Martínez, A. E. & Zenil, R. T. Foraging guild influences dependence on heterospecific alarm calls in Amazonian bird flocks. Behav. Ecol. 23, 544–550 (2012).

    Google Scholar 

  • Gauthreaux, S. A. The ecological significance of behavioral dominance. In Social Behavior. Perspectives in Ethology, vol 3 (eds Bateson, P. P. G. & Klopfer, P. H.) (Springer, 1978).

  • Friedman, N. R. et al. Evolution of a multifunctional trait: Shared effects of foraging ecology and thermoregulation on beak morphology, with consequences for song evolution. Proc. R. Soc. B Biol. Sci. 286, 20192474 (2019).

  • Campbell-Tennant, D. J. E., Gardner, J. L., Kearney, M. R. & Symonds, M. R. E. Climate-related spatial and temporal variation in bill morphology over the past century in Australian parrots. J. Biogeogr. 42, 1163–1175 (2015).

    Google Scholar 

  • Sullivan, T. N., Meyers, M. A. & Arzt, E. Scaling of bird wings and feathers for efficient flight. Sci. Adv. 5, 1–9 (2019).

    Google Scholar 

  • Gosler, A. G., Greenwood, J. J. D., Baker, J. K. & Davidson, N. C. The field determination of body size and condition in passerines: a report to the British Ringing Committee. Bird. Study 45, 92–103 (1998).

    Google Scholar 

  • Tattersall, G. J., Chaves, J. A. & Danner, R. M. Thermoregulatory windows in Darwin’s finches. Funct. Ecol. 32, 358–368 (2018).

    Google Scholar 

  • Weeks, B. C. et al. Shared morphological consequences of global warming in North American migratory birds. Ecol. Lett. 23, 316–325 (2020).

    PubMed 

    Google Scholar 

  • Minton, C. The history and achievements of the Victorian Wader Study Group. Stilt 50, 285–294 (2006).

    Google Scholar 

  • Minton, C. The history of wader studies in north-west Australia. Stilt 50, 224–234 (2006).

    Google Scholar 

  • Lowe, K. W. The Australian Bird Bander’s Manual (Australian Bird and Bat Banding Scemes, Australian National Parks and Wildlife Services, 1989).

  • Aarif, K. M. Some aspects of feeding ecology of the lesser sand plover Charadrius mongolus in three different zones in the Kadalundy Estuary, Kerala, South India. Podoces 4, 100–1007 (2009).

    Google Scholar 

  • Bates, D., Maechler, M. & Bolker, B. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Google Scholar 

  • Rue, H. et al. Bayesian computing with INLA: a review. Annu. Rev. Stat. Its Appl. 4, 395–421 (2017).

    ADS 

    Google Scholar 

  • Li, D., Dinnage, R., Nell, L. A., Helmus, M. R. & Ives, A. R. phyr: an r package for phylogenetic species-distribution modelling in ecological communities. Methods Ecol. Evol. 11, 1455–1463 (2020).

    Google Scholar 

  • Simpson, D., Rue, H., Riebler, A., Martins, T. G. & Sørbye, S. H. Penalising model component complexity: a principled, practical approach to constructing priors. Stat. Sci. 32, 1–28 (2017).

    MathSciNet 
    MATH 

    Google Scholar 

  • Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Schliep, K. Phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • McQueen, A et al. Data from: thermal adaptation best explains Bergmann’s and Allen’s rule across ecologically diverse shorebirds. Dryad Dataset. https://doi.org/10.5061/dryad.xsj3tx9j5.

  • Tattersall, G. J., Andrade, D. V. & Abe, A. S. Heat exchange from the toucan bill reveals a controllable vascular thermal radiator. Science 325, 468–470 (2009).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Greenberg, R., Cadena, V., Danner, R. M. & Tattersall, G. Heat loss may explain bill size differences between birds occupying different habitats. PLoS One 7, 1–9 (2012).

    Google Scholar 

  • Ryeland, J., Weston, M. A. & Symonds, M. R. E. Bill size mediates behavioural thermoregulation in birds. Funct. Ecol. 31, 885–893 (2017).

    Google Scholar 

  • Pavlovic, G., Weston, M. A. & Symonds, M. R. E. Morphology and geography predict the use of heat conservation behaviours across birds. Funct. Ecol. 33, 286–296 (2019).

    Google Scholar 

  • Long-term study on survival and development of successive generations of Mytilus galloprovincialis cryopreserved larvae

    Distribution and genetic diversity of Anisakis spp. in cetaceans from the Northeast Atlantic Ocean and the Mediterranean Sea