Evaporative water loss in Kuhl's pipistrelles declines along an environmental gradient, from mesic to hyperarid

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Highlights

  • Cutaneous evaporative water loss (CWL) is the main avenue of water loss in many bat species.

  • We measured total evaporative water loss (TEWL) in three groups of Pipistrellus kuhlii from mesic, desert, and hyperarid habitats.

  • TEWL in the hyperarid group was significantly lower than in the other two groups at high ambient temperature.

  • We attributed the differences in TEWL to CWL, and suggest that this may be due to modification of the lipids in the dermis.

Abstract

Intraspecific variation in animal energy and water balances may play an important role in local adaptation of populations to specific habitats such as deserts. We examined Kuhl's pipistrelle (Pipistrellus kuhlii), a common bat in Israel that ranges in distribution from mesic Mediterranean to hyperarid desert habitats, for intraspecific differences in metabolic rate (MR) and evaporative water loss (EWL) among populations along a climatic gradient. We tested the prediction that EWL, especially at high ambient temperatures is lower in Kuhl's pipistrelles from desert habitats than from mesic habitats. We measured MR and total evaporative water loss (TEWL) at four ambient temperatures (10 °C, 20 °C, 30 °C and 35 °C) in three groups of bats using open-flow respirometry. We fitted the bats with a mask to separate cutaneous water loss (CWL) from respiratory water loss (RWL) at 35 °C. At 35 °C, mean TEWL in the southernmost group, from the hyperarid location, was significantly lower than in the other two groups, with no apparent difference in mean MR. The source of difference TEWL was that the southern group had significantly lower CWL than the other two groups; RWL did not differ among them. This suggests that there are mechanisms that reduce EWL from the skin of the bats; a likely candidate is modification of the lipids in the outer layer of the dermis that make the skin possibly less permeable to water as has been described in birds and a few other species of bat.

Graphical abstract

Evaporative water loss in three sample groups of populations of Pipistrellus kuhlii along a climactic gradient from mesic Mediterranean, to desert, and hyperarid desert habitats were measured. Total evaporative water loss (TEWL) in the group from the hyperarid habitat was significantly lower than in the other two groups at high ambient temperatures. The differences observed in TEWL are due to differences in measured cutaneous evaporative water loss.

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Introduction

All mammals regulate water loss to maintain water balance; a central principle of physiological homeostasis that is often a challenge for cursorial mammals, especially small species. Bats, as a group, are more susceptible to water loss though trans-cutaneous evaporation than cursorial mammals of their body size because of their large membranous wings, which are highly vascularized, and relatively large naked ears (Poole, 1936; Studier, 1970). In addition, flapping flight necessitates a high metabolic rate (MR; Thomas, 1987), which translates into accelerated respiratory gas exchange. Accordingly, respiratory evaporation is also likely to be high (Webb, 1995) and therefore bats likely have higher water turnover rates than similar-sized, non-volant mammals (Studier, 1970; Neuweiler, 2000).

Indeed, total evaporative water loss (TEWL) in bats so far studied contributes up to 85% of their total water loss, the remainder being excretory in non-lactating animals (Studier, 1970; Arad and Korine, 1993; Minnaar et al., 2014). This is about twice as much as in other mammals of the same body mass (Studier, 1970; Webb, 1995; Neuweiler, 2000). One might therefore assume that bats have efficient behavioral and physiological mechanisms to reduce both respiratory water loss (RWL) and cutaneous water loss (CWL) that are of adaptive advantage to survive and reproduce in dry environments.

Being nocturnal leads to lower EWL in active bats, as does careful daytime roost selection in resting ones (Chew and Dammann, 1961; Studier, 1970; Gaffen and Ross, 1999; Herreid and Schmidt-Nielsen, 1966; Toussaint and McKechnie, 2012). In addition, physiological adaptations also contribute to reduce EWL. For example, temporal countercurrent heat exchange within the nares reduces RWL in several species of small mammals including bats (Schmid, 1976) and vasodilation and vasoconstriction can change rates of CWL, as has been observed in birds (Marder and Raber, 1989) and inferred in bats (Reeder and Cowles, 1951). Furthermore, many species, and in particular bats that inhabit temperate regions, can decrease their body temperature (Tb) by 5 to 10 °C on a daily basis when entering torpor (e.g., Reeder and Cowles, 1951; McNab, 2002; Geiser, 2004). Reduced MR and Tb during torpor lead reduced RWL (e.g. Thomas and Geiser, 1997; Willis et al., 2011). Muñoz-Garcia et al. (2012a) studied the relative contributions of RWL and CWL to total evaporative water loss (TEWL) in bats in different thermoregulatory states and found that both were lower in torpid than in normothermic bats. However, bats in deep torpor had similar or higher CWL than bats in shallow torpor, suggesting they exert less effective physiological control over CWL when in deep torpor (Muñoz-Garcia et al., 2012a). Muñoz-Garcia et al. (2016) measured surface-specific CWL in Hemprich's long-eared bat (Otonycteris hemprichii) a species found only in extremely dry deserts; two species of bats from arid environments, Christi's big-eared bat, and Botta's serotine (Plecotus christii and Eptesicus bottae); and one species, Kuhl's pipistrelle (Pipistrellus kuhlii) that inhabits both Mediterranean and desert habitats. As expected, the rates of CWL were lower in Hemprich's long-eared bat and higher in Kuhl's pipistrelle at moderate ambient temperatures. However, at 35 °C the desert-dwelling species, Christi's big-eared bat and Botta's serotine, had higher CWL than Kuhl's pipistrelle, implying that desert species might use CWL to thermoregulate to a greater extent than mesic species.

While there is evidence that some desert-dwelling bats have lower EWL than non-desert species (Herreid and Schmidt-Nielsen, 1966; Marom et al., 2006; Toussaint and McKechnie, 2012), the question remains whether there are differences in EWL among populations of a single species that inhabits both mesic and desert habitats. An example is Kuhl's pipistrelle that has recently expanded its range southward through Israel (Yom-Tov and Mendelssohn, 1988) and is now common throughout the country, with habitats ranging from mesic Mediterranean to hyperarid desert (Korine and Pinshow, 2004). In this light, we hypothesized that populations of Kuhl's pipistrelle from habitats with different climates have phenotypic differences that reflect the climatic conditions of their habitat and tested the prediction that TEWL and particular CWL, especially at high ambient temperatures (Ta), is lower in bats from desert habitats.

Section snippets

Animals

We collected P. kuhlii from three populations in Israel, on a north-to-south gradient. Our capture sites were Lachish (31°33′ N, 34°50′ E), a Mediterranean habitat, Mashabei Sadeh (31°00′ N, 34°47′ E) an arid area, and Eilat (29°34′ N, 34°58′ E) that is in hyperarid desert (Table 1).

We captured eight to ten bats at each location using mist nets, and brought them to holding facilities at the Mitrani Department of Desert Ecology at the Jacob Blaustein Institutes for Desert Research, Midreshet

Results

Body masses of all the animals were between 4.8 and 7.8 g and were not significantly different among individuals or groups (mean mb for Lachish, Mashabei Sadeh and Eilat were 6.32 ± 0.04 g, 5.92 ± 0.05 g and 6.48 ± 0.17 g, respectively). Overall, TEWL varied significantly among the three habitat groups (F4,46 = 4.49, p = .004), and both MR and TEWL varied significantly among Tas (F6,18 = 99.13, p < .001 and F6,18 = 117.42, p < .001; respectively). However, except for Ta = 10 °C, where bats from

Discussion

The low average rates of TEWL in P. kuhlii from Eilat (hyperarid desert) compared to those from Lachish (Mediterranean) and Mashabei Sadeh (desert), combined with the lack of significant differences in MR among the groups, indicate that the lower TEWL in the Eilat group was not due to correspondingly low MR. We therefore infer that TEWL was not lower by virtue of lower Tb. Low TEWL in bats from the Eilat group at 35 °C was also not due to low RWL; rather, the Eilat group had significantly lower

Declaration of Competing Interest

We declare no conflict of interest.

Acknowledgements

This research was funded by grant number 2008469 from the United States - Israel Binational Science Foundation to Carmi Korine and Joseph B. Williams. We thank Miri Ben-Hamo for her invaluable help in the experiments and Justin. B. Boyles for constructive criticism on a draft of this MS. This research was done under permit 34615 to Carmi Korine from the Israel Nature and Parks Authority and under permit IL-71-12-2010 from the Ben-Gurion University Committee for the Ethical care and use of

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