Phenotypic and genotypic sources of variation in the thermal physiology of a passerine bird

Abstract

There is considerable variation in avian thermal physiology, with traits such as metabolic rates correlated with climate at both inter- and intraspecific levels. However, it is often unclear whether these correlations result from genotypic adaptation, developmental plasticity or phenotypic flexibility. Seasonal acclimatization is a frequently cited example of phenotypic flexibility, with small, temperate-zone birds typically increasing metabolic rates in response to low winter air temperatures (Ta). Recent studies suggest considerable variation in patterns of seasonal acclimatization in birds inhabiting lower latitudes with milder winters, with variation also reported among populations of subtropical species such as the white-browed sparrow-weaver (Plocepasser mahali). To gain insights into the sources of intraspecific variation, I investigated phenotypic flexibility in the thermal physiology of Afrotropical passerine birds, using sparrow-weavers as a model species. I measured seasonal variation in basal metabolic rate (BMR) and summit metabolism (Msum) over a four-year period in arid-zone populations of sparrow-weavers and scaly-feathered weavers (Sporopipes squamifrons; chapter 1). Patterns of acclimatization varied substantially among years in both species, for example, sparrow-weaver BMR ranged from ~ 20 % lower to 68 % higher during winter compared to summer. In contrast to higher-latitude species, interannual metabolic variation was never related to minimum Ta or enhanced cold tolerance, but metabolic rates were significantly lower in seasons with lower food abundance. I also investigated seasonal changes in the body composition of sparrow-weavers, focusing on traits commonly correlated with BMR and Msum in temperate-zone birds (chapter 2). As expected, a lack of seasonal variation in BMR during the study period was associated with no significant variation in the dry mass of digestive and excretory organs. However, despite significant winter increases in pectoral muscle (~ 9 % higher; primary muscle for avian shivering thermogenesis) and heart mass (~ 18 % higher), there was a winter decrease in Msum. These findings support the idea that factors other than enhanced cold tolerance drive patterns of metabolic variation in subtropical birds. I used short-term (~ 30 days) thermal acclimation experiments to investigate whether phenotypic flexibility in thermoregulatory responses of sparrow-weaver varies among populations across a climatic gradient (~ 8 °C and 11 °C in mean daily winter minimum and summer maximum Ta respectively). I measured BMR and Msum after acclimating individuals to one of three acclimation Ta (Taccl) treatments (5 °C, 15 °C or 35 °C; chapter 3). There was ~ 12 % lower BMR and 25 % lower evaporative water loss in birds at the hottest Taccl compared to cooler treatments, with no interpopulation variation after acclimation (i.e., similar reaction norms). In contrast to the findings of most studies on temperate-zone birds, Msum did not vary with Taccl regardless of population. I also investigated flexibility in heat tolerance and evaporative cooling capacity of sparrow-weavers, measuring their ability to handle high Ta (~ 38 °C to 54 °C) after acclimation to one of three treatments (day-time Taccl = 30 °C, 36 °C or 42 °C; chapter 4). Birds at the hottest Taccl coped better with high Ta than those at milder Taccl, maintaining lower body temperatures and reaching Ta ≈ 2 °C higher before the onset of severe hyperthermia. There was no variation among populations after acclimation, suggesting similar reaction norms for heat tolerance and evaporative cooling capacity. These findings suggest previously documented interpopulation differences in sparrow-weaver thermal physiology is largely the result of phenotypic flexibility rather than local adaptation. In conclusion, I found considerable flexibility in the thermal physiology of an Afrotropical passerine bird, both within and among populations. My data support the idea that enhancing winter cold tolerance is less important in subtropical birds compared to higher-latitude species. Moreover, similar thermoregulatory reaction norms among populations highlights the importance of phenotypic flexibility as a source of variation in avian physiology.