Cutaneous and Respiratory Water Loss in Larks from Arid and Mesic Environments
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590 Cutaneous and Respiratory Water Loss in Larks from Arid and Mesic Environments B. Irene Tieleman1,* avenue of water loss in birds and of major importance in main- Joseph B. Williams2 taining heat balance, especially for birds living in hot and dry 1Zoological Laboratory, University of Groningen, P.O. Box environments (Bartholomew 1972; Dawson 1982; Williams and 14, 9750 AA Haren, The Netherlands; 2Department of Tieleman 2001). Birds from deserts generally have lower TEWL Evolution, Ecology, and Organismal Biology, Ohio State than species from mesic areas (Williams 1996), although the University, 1735 Neil Avenue, Columbus, Ohio 43210 mechanisms responsible for this finding remain unresolved. Understanding these mechanisms might provide insights into Accepted 7/24/02 the evolutionary processes that underlie the correlation between TEWL and environment. The variation in physiological traits such as TEWL and their adjustment to environmental condi- tions may be the result of genetic differences or phenotypic ABSTRACT plasticity. Forms of plasticity include acclimatization or phe- Birds from deserts generally have lower total evaporative water notypic flexibility of adult phenotypes in response to changing loss (TEWL), the sum of cutaneous (CWL) and respiratory environments and developmental plasticity that can determine water loss (RWL), than species from mesic areas. We investi- an individual’s phenotype during ontogeny. Genetic variation gated the role of CWL and RWL as a function of air temperature in physiological traits may result from natural selection or ge- (Ta) in hoopoe larks (Alaemon alaudipes) and Dunn’s larks netic drift or may be a consequence of phylogenetic constraint (Eremalauda dunni) from the Arabian Desert and skylarks (Gould and Lewontin 1979). (Alauda arvensis) and woodlarks (Lullula arborea) from tem- To minimize the confounding effect of phylogenetic factors, perate mesic grasslands. The proportional contribution of CWL we compared TEWL and basal metabolic rate (BMR) within a to TEWL in all larks at moderate Ta ranged from 50% to 70%. closely related group of birds, all members of the lark family Њ Њ At high Ta (40 –45 C), larks enhanced CWL by only 45%–78% (Alaudidae), that are distributed over a gradient from mesic to and relied on an increase in RWL by 676%–2,733% for evap- arid habitats. We found a decline in TEWL and BMR with orative cooling. Surface-specific CWL at 25ЊC was 29% lower increasing aridity (Tieleman et al. 2002a, 2002b). To investigate in the arid-zone species than in the mesic larks. When accli- the extent to which interspecific differences in TEWL and BMR Њ mated to constant Ta,15C-acclimated hoopoe larks increased result from acclimatization, we acclimated five species of larks CWL by 22% compared with 35ЊC-acclimated birds, but the to 15ЊC and 35ЊC (Tieleman et al. 2003). Hoopoe larks (Alae- other species did not change CWL. This study is consistent mon alaudipes) and Dunn’s larks (Eremalauda dunni) live in with the hypothesis that larks from deserts have a reduced CWL arid deserts, spike-heeled larks (Chersomanes albofasciata)in- at moderate and low Ta but provided no support for the hy- habit semiarid areas, and skylarks (Alauda arvensis) and wood- pothesis that at high Ta larks from arid regions rely more on larks (Lullula arborea) dwell in mesic environments. When CWL than larks from mesic environments. Interspecific dif- measured at 25ЊC, the 15ЊC-acclimated hoopoe larks increased ferences in CWL cannot be attributed to acclimation to envi- their mass-specific TEWL by 23% compared with the 35ЊC- ronmental temperature and are possibly the result of genetic acclimated individuals, but the other species did not alter their differences due to natural selection or of phenotypically plastic TEWL in response to acclimation (Williams and Tieleman 2000; responses to divergent environments during ontogeny. Tieleman et al. 2003). All species increased their BMR when acclimated to 15ЊC compared with 35ЊC. If metabolic rate is correlated with RWL, and therefore RWL has increased in the 15ЊC-acclimated birds, the fractional contributions of CWL and Introduction RWL to TEWL may have changed in these larks, even if TEWL Total evaporative water loss (TEWL), the sum of cutaneous is not different. water loss (CWL) and respiratory water loss (RWL), is the main Several mechanisms have been proposed to explain the re- duced TEWL in desert birds: hyperthermia (Calder and King * Corresponding author; e-mail: [email protected]. 1974; Weathers 1981; Dawson 1984), countercurrent heat Physiological and Biochemical Zoology 75(6):590–599. 2002. ᭧ 2002 by The exchange in the nasal passages that lowers RWL (Schmidt- University of Chicago. All rights reserved. 1522-2152/2002/7506-2053$15.00 Nielsen et al. 1970), and adjustment of the lipid structure in Cutaneous and Respiratory Water Loss in Larks 591 the skin to reduce CWL (Menon et al. 1989, 1996). Previously, Netherlands. Data on the complete heat balance, including me- we explored the role of hyperthermia (Tieleman and Williams tabolism, TEWL, Tb, and the dry heat transfer coefficient per 1999) and of water recovery in the nasal turbinates in reducing species and on the phylogenetic relationships between these TEWL in birds (Tieleman et al. 1999). Based on this work, we four larks can be found in Tieleman et al. (2002b). We examined concluded that these factors could not account for the differ- if CWL and RWL at moderate Ta were lower in the two arid- ence in TEWL between desert and nondesert forms. zone larks than in the two mesic birds and if, when birds were Desert birds could reduce their TEWL by decreasing their heat stressed, CWL increased more in the arid-zone larks than CWL (Menon et al. 1989, 1996; Williams 1996). Although early in those from the mesic areas. In addition, we explored the investigators surmised that most evaporative cooling takes place phenotypic flexibility of CWL and RWL of all four species in in the respiratory passages (Rawles 1960; Bartholomew and response to acclimation to 15ЊC and 35ЊC. Cade 1963; Mount 1979), later work showed that CWL is an important avenue of water loss in the thermoregulatory process, Material and Methods at least at air temperatures (Ta) below body temperature (Bern- stein 1969; Smith 1969; Dawson 1982; Webster and Bernstein We mistnetted hoopoe larks (Alaemon alaudipes, mass ,g,n p 14 ) and Dunn’s larks (Eremalauda dunni 3.7 ע Webster and King 1987; Wolf and Walsberg 1996; Mi- 36.5 ;1987 g,n p 16 ) in Mahazat as-Sayd, a reserve in the 1.8 ע chaeli and Pinshow 2001). Collating data from the literature, 20.5 we were unable to identify any significant differences in CWL Arabian Desert (22Њ15ЈN, 41Њ50ЈE), and housed them in out- at thermally neutral Ta between species from arid and mesic door aviaries at the National Wildlife Research Center near environments (Williams and Tieleman 2001). However, con- Taif, Saudi Arabia. Average yearly rainfall in Mahazat equals 90 Њ clusions were tentative because data were few and were obtained mm, and maximum Ta in July averages 40.2 C with some daily in a variety of ways (Appleyard 1979; Marder and Ben-Asher maxima reaching 50ЊC (National Wildlife Research Center, un- 1983; Withers and Williams 1990). published data). Temperatures in Taif resemble those in Ma- Few studies have investigated CWL and RWL at high Ta when hazat during the summer. In the Netherlands, we netted sky- p ע Tb must be regulated below lethal limits solely by evaporative larks (Alauda arvensis,31.5 2.9 g,n 14 ) and woodlarks -g,n p 14 ) in the province of Dren 1.0 ע water loss from the skin and from the respiratory passages (Lullula arborea,25.5 (Marder and Ben-Asher 1983; Wolf and Walsberg 1996; Hoff- the (52Њ52ЈN, 06Њ20ЈE) and kept them in outdoor aviaries at man and Walsberg 1999). Some species, especially members of the Zoological Laboratory of the University of Groningen, 30 the Columbiformes, seem to rely primarily on CWL when Ta km from the capture site. In Drenthe, rainfall averages 750 mm Ϫ1 Њ exceeds Tb, whereas other species seem to emphasize the use yr , and mean maximum Ta in July is 21.7 C (Koninklijk of RWL, facilitated by panting or gular flutter (Bouverot et al. Nederlands Meteorologisch Instituut). We used an open-flow 1974; Wolf and Walsberg 1996; Hoffman and Walsberg 1999; system for indirect calorimetry to measure CWL, RWL, and Tieleman et al. 1999; Williams and Tieleman 2001). Our un- metabolic rate (MR) of all birds during daytime after they had derstanding of CWL and RWL at high Ta and how water loss been in captivity for 3–6 wk during June, July, or August of is partitioned remains rudimentary. 1999–2001. Larks were fed ad lib. a mixture of insects and Our hypothesis is that natural selection should have equipped seeds. In addition, larks in the Netherlands had access to water desert birds with a mechanism that impedes water loss through ad lib. Hoopoe larks and Dunn’s larks do not drink, even when the skin, at least at moderate Ta, to save water. Under heat provided with water or after rains when temporary pools are stress, when evaporative cooling is crucial for survival, evap- available (B. I. Tieleman and J. B. Williams, personal obser- oration through the skin should be elevated. Birds from mesic vation). environments, however, which experience neither water scarcity Previous investigators have used a two-compartment system nor high Ta, would not have been selected for reduced CWL with the head and neck of the bird extending through a dental- at moderate Ta or for the capacity to enhance evaporation at dam barrier to quantify CWL and RWL separately (Bernstein high Ta. Rates of CWL in desert birds may be governed by two 1971; Webster and King 1987; Wolf and Walsberg 1996; Hoff- selective pressures: a long-term requirement of minimizing man and Walsberg 1999).