University of Groningen Avian adaptation along an aridity gradient Tieleman, Bernadine Irene IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2002 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Tieleman, B. I. (2002). Avian adaptation along an aridity gradient: Physiology, behavior, and life history. s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 04-10-2021 ABSTRACT We investigated interindividual variation and intra- individual phenotypic flexibility in basal metabolic rate (BMR), total evaporative water loss (TEWL), body tem- perature (Tb), the minimum dry heat transfer coefficient (h) and organ and muscle size of five species of larks geographically distributed along an aridity gradient. We exposed all species to constant environments of 15 °C or 35 °C, and examined to what extent interspecific diffe- rences in physiology can be attributed to acclimation. We tested the hypothesis that birds from deserts display larger intra-individual phenotypic flexibility and smaller inter- individual variation than species from mesic areas. Larks from arid areas had lower BMR, TEWL and h, but did not have internal organ sizes different from birds from mesic habitats. BMR of 15 °C-acclimated birds was 18.0%, 29.1%, 12.2%, 25.3% and 4.7% higher than of 35 °C- acclimated Hoopoe Larks, Dunn's Larks, Spike-heeled Larks, Skylarks and Woodlarks, respectively. TEWL of 15 °C-acclimated Hoopoe Larks exceeded values for 35 °C- acclimated individuals by 23%, but did not differ between 15 °C- and 35 °C-acclimated individuals in the other species. The dry heat transfer coefficient was increased in 15 °C-acclimated individuals of Skylarks and Dunn's Larks, but not in the other species. Body temperature was on average 0.4 °C (S.E.M. 0.15 °C) lower in 15 °C- acclimated individuals of all species. Increased food inta- ke in 15 °C-acclimated birds stimulated enlargement of intestine (26.9-38.6%), kidneys (9.8%-24.4%), liver (16.5%-27.2%) and stomach (22.0%-31.6%). The pec- toral muscle increased in 15 °C-acclimated Spike-heeled Larks and Skylarks, remained unchanged in Hoopoe Larks, and decreased in 15 °C-acclimated Woodlarks and Dunn's Larks. We conclude that the degree of intra-indi- vidual flexibility varied between physiological traits and among species, but that acclimation does not account for interspecific differences in BMR, TEWL and h in larks. We found no general support for the hypothesis that spe- cies from desert environments display larger intra-indivi- dual phenotypic flexibility than those from mesic areas. The coefficient of variation of larks acclimated to their natural environment was smaller in species from arid than from mesic areas for mass-corrected BMR and surface-spe- cific h, but not for mass-corrected TEWL. The high re- peatabilities of BMR, TEWL and h in several species indi- cated a within-individual consistency on which natural selection could operate. ABSTRACT CHAPTER 6 Physiological adjustments to arid and mesic environments in larks (Alaudidae) B. Irene Tieleman, Joseph B. Williams, and Michael E. Buschur Physiological and Biochemical Zoology 75: 305-313. 2002. ABSTRACT Because deserts are characterized by low food availability, high ambient temperature extremes and absence of drinking water, one might expect that birds that live in these conditions exhibit a lower basal metabolic rate (BMR), a reduced total evaporative water loss (TEWL) and a greater ability to cope with high air temperatures than their mesic counterparts. To minimize confoun- ding effects of phylogeny, we compared the phys- iological performance of four species of larks at ambient temperatures (Ta) ranging from 0 °C to 50 °C: Hoopoe Larks (Alaemon alaudipes) and Dunn's Larks (Eremalauda dunni) live in hot and dry deserts, whereas Skylarks (Alauda arvensis) and Woodlarks (Lullula arborea) occur in tempe- rate mesic areas. Mass-adjusted BMR and TEWL were indistinguishable between Hoopoe Lark and Dunn's Lark and between Skylark and Woodlark. Combining the two desert birds and the two mesic larks, larks from the desert had levels of BMR 43% lower and values of TEWL 27% lower than the mesic species. Their body temperatures (Tb) were 1.1 °C lower and the minimal dry heat transfer coefficients (h) were 26% below values for the mesic larks. When Ta exceeded Tb, the h of Hoopoe Larks and Dunn's Larks was high and indistinguishable from h at 40 °C, in contrast to the prediction that h should be decreased to min- imize heat gain through conductance, convec- tion or radiation from the environment when Ta exceeds Tb. ABSTRACT Introduction Animals that live in deserts might be expected to possess behavioral and physio- logical adaptations that would enable them to cope with high ambient tempera- tures (Ta), low food resources and lack of drinking water, the main characteris- tics of these environments (Bartholomew & Cade 1963; Dawson & Schmidt- Nielsen 1964; Williams & Tieleman 2001). Unlike small mammals, that are generally nocturnal and as a result do not experience the temperature extremes of the desert environment, desert birds are exposed to Tas that are among the highest on earth. Shade Ta can exceed 50 °C in some deserts and anecdotical evidence suggests that extreme heat can be a major source of mortality in some bird populations (Serventy 1971). Avian physiological mechanisms that favor survival during extended periods of high Tas are poorly understood. Exposure to high Ta not only requires mechanisms of heat tolerance, but also puts additional strain on the water and energy balance that may already be compromised by lack of drinking water and low food availability. Early investigators hypothesized that low primary productivity, high Ta and absence of drinking water in deserts would select for low levels of basal metabo- lic rate (BMR) and total evaporative water loss (TEWL) in desert birds, but found no general support for this idea (Bartholomew & Cade 1963; Bartholomew 1964; Dawson & Schmidt-Nielsen 1964; Serventy 1971; Dawson 1984). Subsequent studies reported levels of BMR and TEWL below allometric predictions, but because these investigations were often based on a single species, conclusions were tentative (Dawson & Bennett 1973; Weathers 1979; Arad & Marder 1982; Withers & Williams 1990). Across species comparisons between desert and non-desert species support the hypothesis that arid-zone birds have on average a lower BMR (Tieleman & Williams 2000) and a lower TEWL (Williams 1996). Broad-scale interspecific comparisons of BMR and TEWL have the inherent interpretational problem that species not only differ in habitat but also in phy- logenetic background, diet and behavior. In addition, knowledge of minimum ENVIRONMENTS levels of metabolism and TEWL provides limited understanding of the physiolo- MESIC gical responses to varying environmental circumstances, including Ta. AND Restricting comparative analyses to a small group of closely related species occu- ARID ring in different environments provides the opportunity for a more detailed exa- TO mination of physiological adjustment while potentially limiting complications due to markedly different evolutionary history or current dissimilar life styles. At high Ta, birds increase TEWL to maintain body temperature (Tb) below lethal ADJUSTMENTS limits (Calder & King 1974), even when water is in short supply. To minimize evaporative water loss at high Ta, birds could reduce heat production from met- abolism. Another strategy to reduce water requirements for evaporative cooling PHYSIOLOGICAL at high Ta entails minimizing dry heat gain from the environment, quantified by 133 the equation Heat gain = h (Tb - Ta), where Tb - Ta is the gradient between the bird’s Tb and the environment and h is the dry heat transfer coefficient (Dawson & Schmidt-Nielsen 1966; Hinds & Calder 1973; Weathers & Caccamise 1975; Tieleman & Williams 1999). Influenced by feather insulation, skin vasodilation, surface to volume ratios and subcutaneous fat reserves, h is a complex variable that combines heat transfer coefficients for conduction, convection and radia- tion (Calder & King 1974). The optimal response of h to Ta presumably inclu- des adjustments to minimal levels below the thermoneutral zone, an increase to maximum values when Ta approaches Tb, and a decrease to minimal values again when Ta exceeds Tb (Dawson & Schmidt-Nielsen 1966; Hinds & Calder 1973; Tieleman & Williams 1999). We hypothesized that increasing aridity selects for gradually decreasing levels of BMR and TEWL in birds, and for improved physiological performance under exposure to extreme heat. To test these ideas, we studied the temperature regu- lation of four closely related birds, Dunn's Larks and Hoopoe Larks from the hyperarid and arid deserts in Arabia and northern Africa, and Skylarks and Woodlarks that live in the mesic temperate zones of Europe and Asia. We deter- mined metabolism, total evaporative water loss, dry heat transfer coefficient and body temperature at Tas ranging from 0-40 °C in the mesic birds and from 0-50 °C in the arid-zone species.