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). 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: 27-09-2021 CHAPTER 8 Energy and water budgets of larks in a life history perspective: is parental effort related to environmental aridity? B. Irene Tieleman, Joseph B. Williams, and G. Henk Visser Submitted to Ecology ABSTRACT We compared physiological, demographic and ecological variables of larks to gain insights into life history variation along an aridity gradient, incorporating phylogenetic relationships in ana- lyses when appropriate. Quantifying field meta- bolic rate (FMR) and water flux (WF) of parents feeding nestlings as measures of parental effort, we found that parental FMR and WF were lower by 24-39% and 39-61%, respectively, in larks from arid environments compared with species from mesic areas. Water and energy requirements of 6-8 day old nestlings were reduced in desert species. Nestling growth rate, clutch size and number of clutches decreased with increasing ari- dity, and nest predation rates increased with increasing aridity. We combined FMR and WF of parents and chicks, energy and water accumula- ted during growth, and brood size to establish energy and water budgets of parent-brood units. Parent-offspring energy budgets equaled 101 kJ d-1 for Bar-tailed Desert Lark, 265 kJ d-1 for Hoopoe Lark, 162 kJ d-1 for Dunn’s Lark, 389 kJ d-1 for Skylark, and 345 kJ d-1 for Woodlark, a 28% reduction in the desert species when taking into account mass differences. Family unit water fluxes were 23.8 g d-1 for Bar-tailed Desert Lark, 48.6 g d-1 for Hoopoe Lark, 37.5 g d-1 for Dunn’s Lark, 101.4 g d-1 for Skylark, 82.8 g d-1 for Woodlark. Parent-brood units of arid-zone spe- cies used 28-50% less water per gram mass than species from mesic areas. These results support the hypothesis that decreasing food and water availability favor lower energy and water require- ments of parents and young, reduced growth rates, and smaller clutch sizes with increasing aridi- ty. The decrease in parental effort with increasing aridity might reflect a lower fitness value of a single brood for arid-zone species than for larks from mesic habitats, suggesting that the probabi- lity of adult survival is higher in arid than in mesic areas. ABSTRACT Introduction A central tenet of life history theory is that current reproductive investment is traded off against residual reproductive value (Williams 1966; Stearns 1992; Roff 1993). This trade-off, or cost of reproduction, is fundamental in predicting the optimal life history in a variety of environments. The difficulty of obtaining direct measures of fitness costs to demonstrate a cost of reproduction has stimu- lated investigators to find quantifiable currencies that are related to fitness. A frequently used measure of current reproductive investment is parental effort, the proportion of available resources devoted to reproduction as opposed to growth and maintenance (Reznick 1985), that can be expressed in terms of energy, assu- ming that life history trade-offs are the result of energy allocation (Drent & Daan 1980; Bryant 1988). Because separating resources allocated to reproduction and to maintenance is problematic in field studies on birds, many studies use total daily energy expenditure as a measure of parental effort (Bryant 1988; Weathers & Sullivan 1989; Tinbergen & Verhulst 2000). In this study we use parental energy and water expenditure in the field as proxy to quantify parental effort, and we relate these variables to basal metabolic rate and total evaporative water loss from laboratory studies. In addition, we investigate variation in clutch size as an independent measure of parental effort. Whereas clutch size is ultimately evaluated in light of parental fitness allocation to current and future reproduction (Perrins & Moss 1975; Boyce & Perrins 1987), it may also be viewed as the outcome of a trade-off between growth rate and nutrient requirements of the young, and depend on environmental condi- tions such as food availability and risk of nest predation. Lack (1968) argued that nestling mortality due to predation could be reduced by shortening the nestling period, but that this would require faster growth and result in higher energy demands of the young. He suggested that growth rates are a compromise between food availability and risk of predation. Environments with a higher predation risk should select for faster growing young, and thereby force parents to raise fewer young per nesting attempt. In contrast with this prediction however, high FIELD nest predation, slow growth, and small broods occur together in the tropics, THE whereas low nest predation, fast growth and large broods coincide in temperate IN zones (Skutch 1966; Ricklefs 1979). Adding knowledge of the relationships between LARKS growth rate, clutch size and nest predation over an environmental continuum of OF increasing aridity may provide new insights into the effect of environmental factors on demography and physiology. BUDGETS Deserts are characterized by high ambient temperatures (T ), unpredictable, low a TER A rainfall and reduced primary productivity, resulting in limited food and water W availability for their inhabitants. One might expect that birds exposed to these AND conditions require specific physiological and behavioral adaptations that permit survival and reproduction (Serventy 1971; Dawson 1984; Williams & Tieleman ENERGY 167 2001). Low food and water availability could constrain energy and water intake, and the thermal environment may limit time available for foraging and force birds to minimize activity during the middle part of the day (Williams et al. 1999; Tieleman & Williams 2002a). In such an environment, natural selection poten- tially favors individuals with low rates of energy expenditure and water loss (Louw & Seely 1982; Williams & Tieleman 2001). However, during the repro- ductive season, parents not only provide food and water for themselves, but also for their offspring, and may need to elevate their own energy and water require- ments in order to produce young. Whereas the amount of energy and water that can be invested per brood may be determined by the time available for foraging and the availability of food and water, the number of chicks that can be reared per brood depends also on the daily energy and water requirements per young. Reductions in these requirements could be accomplished by reducing nestling metabolism, growth rate, and evaporative and excretory water losses (Klaassen & Drent 1991). To date, few studies have investigated how energy and water are allocated to different components of the energy and water balance of a parent- brood complex in different environments. Early work on metabolism and water flux did not show any general physiological differences between desert and non-desert species (Bartholomew & Cade 1963; Dawson & Schmidt-Nielsen 1964; Serventy 1971; Dawson 1984). Subsequent studies, typically on single species of desert birds, have reported low basal meta- bolic rate (BMR), total evaporative water loss (TEWL) (Dawson & Bennett 1973; Weathers 1979; Arad & Marder 1982; Withers & Williams 1990), and low field metabolic rate (FMR) (Nagy 1987) and water flux (WF) (Nagy & Peterson 1988). More recently, across species comparisons between desert and non-desert species supported the hypothesis that arid-zone birds have on average lower BMR, FMR (Tieleman & Williams 2000) and TEWL (Williams 1996), also when taking into account phylogenetic relatedness among species. Results for comparisons of field water flux were equivocal, with conventional analysis showing differences between desert and non-desert species, but independent contrast analysis not (Tieleman & Williams 2000). Broad-scale interspecific comparisons of metabolism and water loss have the inherent problem that species differ not only in habitat but also in phylogenetic background, diet and behavior. Restricting comparative analyses to a small group of closely related species occurring in different environments provides the oppor- tunity for a more detailed examination of physiological adaptations while limi- ting complications due to dissimilar lifestyles or evolutionary history (Coddington 1988; Bennett 1988; Price 1991; Leroi 1994). The lark family (Alaudidae) has representatives living in environments ranging from hyperarid deserts to mesic grasslands (Cramp 1988; Pätzold 1994). Because all larks are ground-foraging birds that eat similar foods, a mixture of insects and seeds, beha- 168 vior and diet are not confounding factors in our analyses. In addition, know- ledge of the phylogeny of the lark family based on molecular evidence (Tieleman et al. 2002b) allows us to select species with phylogenetic relatedness in mind. This family provides an appropriate model to study physiological and behavioral adaptation to the environment (Williams & Tieleman 2000; Tieleman & Williams 2002b; Tieleman et al. 2002c; Tieleman et al. 2003). Among larks, BMR and TEWL decrease along a gradient of increasing aridity (Tieleman et al.