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      Heat Loss May Explain Bill Size Differences between Birds Occupying Different Habitats

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          Abstract

          Background

          Research on variation in bill morphology has focused on the role of diet. Bills have other functions, however, including a role in heat and water balance. The role of the bill in heat loss may be particularly important in birds where water is limiting. Song sparrows localized in coastal dunes and salt marsh edge ( Melospiza melodia atlantica) are similar in size to, but have bills with a 17% greater surface area than, those that live in mesic habitats ( M. m. melodia), a pattern shared with other coastal sparrows. We tested the hypotheses that sparrows can use their bills to dissipate “dry” heat, and that heat loss from the bill is higher in M. m. atlantica than M. m. melodia, which would indicate a role of heat loss and water conservation in selection for bill size.

          Methodology/Principal Findings

          Bill, tarsus, and body surface temperatures were measured using thermal imaging of sparrows exposed to temperatures from 15–37°C and combined with surface area and physical modeling to estimate the contribution of each body part to total heat loss. Song sparrow bills averaged 5–10°C hotter than ambient. The bill of M. m atlantica dissipated up to 33% more heat and 38% greater proportion of total heat than that of M. m. melodia. This could potentially reduce water loss requirements by approximately 7.7%.

          Conclusions/Significance

          This >30% higher heat loss in the bill of M. m. atlantica is independent of evaporative water loss and thus could play an important role in the water balance of sparrows occupying the hot and exposed dune/salt marsh environments during the summer. Heat loss capacity and water conservation could play an important role in the selection for bill size differences between bird populations and should be considered along with trophic adaptations when studying variation in bill size.

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          Most cited references37

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          Intense Natural Selection in a Population of Darwin's Finches (Geospizinae) in the Galapagos.

          Survival of Darwin's finches through a drought on Daphne Major Island was nonrandom. Large birds, especially males with large beaks, survived best because they were able to crack the large and hard seeds that predominated in the drought. Selection intensities, calculated by O'Donald's method, are the highest yet recorded for a vertebrate population.
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            Heat exchange from the toucan bill reveals a controllable vascular thermal radiator.

            The toco toucan (Ramphastos toco), the largest member of the toucan family, possesses the largest beak relative to body size of all birds. This exaggerated feature has received various interpretations, from serving as a sexual ornament to being a refined adaptation for feeding. However, it is also a significant surface area for heat exchange. Here we show the remarkable capacity of the toco toucan to regulate heat distribution by modifying blood flow, using the bill as a transient thermal radiator. Our results indicate that the toucan's bill is, relative to its size, one of the largest thermal windows in the animal kingdom, rivaling elephants' ears in its ability to radiate body heat.
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              Geographical variation in bill size across bird species provides evidence for Allen's rule.

              Allen's rule proposes that the appendages of endotherms are smaller, relative to body size, in colder climates, in order to reduce heat loss. Empirical support for Allen's rule is mainly derived from occasional reports of geographical clines in extremity size of individual species. Interspecific evidence is restricted to two studies of leg proportions in seabirds and shorebirds. We used phylogenetic comparative analyses of 214 bird species to examine whether bird bills, significant sites of heat exchange, conform to Allen's rule. The species comprised eight diverse taxonomic groups-toucans, African barbets, Australian parrots, estrildid finches, Canadian galliforms, penguins, gulls, and terns. Across all species, there were strongly significant relationships between bill length and both latitude and environmental temperature, with species in colder climates having significantly shorter bills. Patterns supporting Allen's rule in relation to latitudinal or altitudinal distribution held within all groups except the finches. Evidence for a direct association with temperature was found within four groups (parrots, galliforms, penguins, and gulls). Support for Allen's rule in leg elements was weaker, suggesting that bird bills may be more susceptible to thermoregulatory constraints generally. Our results provide the strongest comparative support yet published for Allen's rule and demonstrate that thermoregulation has been an important factor in shaping the evolution of bird bills.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                25 July 2012
                : 7
                : 7
                : e40933
                Affiliations
                [1 ]Smithsonian Migratory Bird Center, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, United States of America
                [2 ]Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada
                [3 ]Avian Ecology Group, Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia, United States of America
                University of Lethbridge, Canada
                Author notes

                Conceived and designed the experiments: RG RMD VC GT. Performed the experiments: VC RMD RG. Analyzed the data: RG RMD VC GT. Contributed reagents/materials/analysis tools: RG VC. Wrote the paper: RG RMD VC GT.

                Article
                PONE-D-12-01895
                10.1371/journal.pone.0040933
                3405045
                22848413
                ead539db-bc10-47eb-92a2-e0264838a44d
                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
                History
                : 20 January 2012
                : 15 June 2012
                Page count
                Pages: 9
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Ecology
                Coastal Ecology
                Physiological Ecology
                Evolutionary Biology
                Organismal Evolution
                Animal Evolution
                Evolutionary Ecology
                Zoology
                Animal Physiology
                Ornithology

                Uncategorized
                Uncategorized

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