- Email: [email protected]
Temperature selection by tropical bats roosting in caves
ARTICLE IN PRESS
Journal of Thermal Biology 28 (2003) 465–468
Temperature selection by tropical bats roosting in caves A. Rodr!ıguez-Dura! n*, J.A. Soto-Centeno ! PR 00957, USA Department of Natural Sciences, Inter American University, Rd. 830, No. 500, Bayamon, Received 14 June 2002; accepted 27 July 2002
Abstract The temperature preferences of the mormoopid and phyllostomid bats Pteronotus quadridens and Erophylla sezekorni, from the West Indies, were determined in the laboratory and compared to field observations. Pteronotus quadridens was invariably found within the deepest and hottest parts of caves, at temperatures between 28 C and 35 C, while E. sezekorni was found at temperatures from 25 C to 28 C. Temperatures selected by each species in a thermopreferendum chamber were similar to their respective roosting temperatures in the caves. These inter-specific differences are statistically significant. Our results support the hypothesis that roost temperature and differences in temperature preferences among species, are important in explaining multispecies associations and the spatial segregation within caves. r 2003 Elsevier Ltd. All rights reserved. Keywords: Bats; Temperature selection; Caves; West Indies; Roosting; Coexistence; Tropical; Temperature preference
1. Introduction Selection of appropriate roosting conditions may be of critical survival value for bats (Kunz, 1982; Maloney et al., 1999), although when it comes to tropical species this is an aspect of their ecology that is commonly underestimated. The literature on microclimatic preferences among bat species is scarce, and addresses mostly the problem of hibernation (e.g. Twente, 1955; Herreid, 1967; Daan and Wichers, 1968; Gaisler, 1970) or deals with tree (e.g. Sedgeley and O’Donnell, 1999) or atticroosting bats (e.g. Entwistle et al., 1997; Zahn, 1999) from temperate regions. Few studies address the matter of roost selection by tropical bats, and to our knowledge no other study examines selection of temperature as a mechanism promoting the coexistence of multispecies assemblages of tropical bats. Wilkinson (1985) suggested that microclimate might be one factor influencing roosting behavior of female Desmodus rotundus. Kunz et al. (1983) found no microclimatic differences between *Corresponding author. E-mail address: [email protected] (A. Rodr!ıguezDur!an).
occupied and vacant cavities in a cave inhabited by Artibeus jamaicensis. In both studies, microclimate selection was ruled out as a major factor influencing roost selection. Both D. rotundus and A. jamaicensis are medium sized bats that do not roost exclusively in caves and do not form large aggregations. The bat faunas of the West Indies are not random assemblages from the tropical mainland (Fleming, 1982; McFarlane, 1989; Genoways et al., 1998), and the presence of caves is one of several factors that may help define the packing patterns of these faunas (Rodr!ıguezDur!an and Kunz, 2001). Small mormoopid and phyllostomid bats roosting in hot caves exhibit high degrees of gregariousness and roost fidelity (SilvaTaboada, 1979; Rodr!ıguez-Dur!an, 1998), and face the problems associated with their reduced capacity to store fat and thermoregulate (Bonaccorso et al., 1992; Rodr!ıguez-Dur!an, 1995). Although up to nine species may occupy a single hot-cave, different species usually maintain spatial separation within the roost (SilvaTaboada, 1979). High frequencies of roosting aggregations have been reported for the hot-caves associations: Monophyllus redmani (Phyllostomidae)—Mormoops blainvilli—Pteronotus quadridens (Mormoopidae); and,
0306-4565/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0306-4565(03)00046-9
ARTICLE IN PRESS 466
! J.A. Soto-Centeno / Journal of Thermal Biology 28 (2003) 465–468 A. Rodr!ıguez-Duran,
Erophylla sezekorni (Phyllostomidae)—P. parnellii (Mormoopidae) (Rodr!ıguez-Dur!an, 1998), in which warm temperatures (26–40 C) resulted from high densities of bats. It has been proposed that intraspecific competition for access to the roost is what limits the species composition and population sizes in these caves (Bateman and Vaughan, 1974; Silva-Taboada, 1979; Rodr!ıguez-Dur!an and Lewis, 1987). However, this hypothesis does not explain the spatial separation of species within the cave. The purpose of this study is to assess the temperature preferences of P. quadridens and E. sezekorni as they relate to microclimatic differences within a cave.
2. Materials and methods Observations and captures at three caves (Rodr!ıguezDura! n, 1998) form the basis for the present study, although most efforts were concentrated at Bonita Cave. To establish the location of each species within each cave we made visual examinations using a headlamp and, when necessary, 7 35 binoculars. We obtained measurements of temperature of roosts used by P. quadridens (Mormoopidae) and E. sezekorni (=bombifrons) (Phyllostomidae) at Los Pe! rez, Cucaracha, and Bonita caves, using maximum/minimum thermometers in combination with a telescopic aluminium pole. We captured adult, non-reproductive individuals of both sexes (81 P. quadridens and 79 E. sezekorni) as they returned from foraging, using a harp-trap (Kunz and Kurta, 1988) set at the cave entrance. Laboratory experiments began 3–8 h following capture and were always terminated before the beginning of the normal foraging phase of the species. Prior to each experiment, all bats were housed in a temperature-controlled cabinet at a temperature of 27–30 C and a relative humidity of 80–90%. Temperature preference tests (Herreid, 1967) were conducted in a specially designed (180 30 30 cm3) aluminum chamber. This chamber contained a hardware cloth cage, and both the interior of the chamber and the cage were painted flat black. We arranged nine type-K thermocouples at 18 cm (SD=1.7 cm) intervals along the chamber at the same height as the bats roosted. The wire cage was insulated from the floor of the chamber by means of wooden legs so as to minimize thermal conductance. The outside of the chamber was insulated with 10.2-cm-thick, high-density, expandable polystyrene with a conductivity of K=0.27 J (s m C)1. We cooled one end of the chamber and heated the other, creating a 22–40 C thermal gradient. Single bats were placed in a previously established gradient and given 1.5 h to select their position, after which the chamber was opened and the temperature at the
thermocouple closest to the bat was recorded. To avoid potential problems associated with bats staying in the section of the gradient where they are introduced, we followed three variations of this protocol: (1) bats were placed in the middle of the gradient; (2) bats were placed in a subdivision of the cage on the hot section of the chamber and after they settled down, allowed access to the whole of the gradient; (3) bats were placed on the cool section of the gradient in the same manner as in (2). After each experiment, we cleaned (Lysol Scent) and blow-dried both the wire-cage and the floor of the chamber to eliminate any odor cue that might have been left from the previous bat. We compared the results using t-tests, or Mann– Whitney when the data failed to pass a normality test. We examined overall differences among species, sex differences within species, and differences due to whether the bats were released on the hot vs. cool end of the gradient.
3. Results Pteronotus quadridens was invariably found within the deepest and hottest parts of caves, at temperatures between 28 C and 35 C, while E. sezekorni was found near the heat trap, at temperatures ranging from 25 C to 28 C. Temperatures selected by each species in the thermopreferendum chamber were similar to their respective roosting temperatures in the caves. Twentyseven (34%) of the P. quadridens selected temperatures between 22 C and 27 C, while 39 (49%) selected temperatures between 31 C and 39 C (Fig. 1). The median temperature selected by P. quadridens was 29.5 C (N ¼ 81; Mean=30.2, SD=4.6). Thirty-two (41%) E. sezekorni selected temperatures between 22 C and 27 C, whereas 21(27%) selected temperatures between 31 C and 39 C (Fig. 1). The median temperature selected by
Fig. 1. Temperatures selected by P. quadridens and E. sezekorni in the thermopreferendum chamber. The difference is statistically significant (P ¼ 0:013; Mann–Whitney test).
ARTICLE IN PRESS ! J.A. Soto-Centeno / Journal of Thermal Biology 28 (2003) 465–468 A. Rodr!ıguez-Duran,
E. sezekorni was 28 C (N ¼ 79; Mean=28.2, SD=2.3). These differences in temperatures selected by each species in the thermopreferendum chamber are statistically significant (P ¼ 0:013; Mann–Whitney). Other tests revealed non-significant differences. There is no significant difference between temperatures selected by males and females P. quadridens (P ¼ 0:202; Mann–Whitney) or E. sezekorni (P ¼ 0:396; t-test). There is no significant difference between temperatures selected by P. quadridens (P ¼ 0:276; t-test) released in the hot vs. cool section of the chamber; the same holds true for E. sezekorni (P ¼ 0:350; t-test).
4. Discussion Mormoopid and phyllostomid bats often share the same caves, forming some of the largest multispecies assemblages of mammals known (Bateman and Vaughan, 1974; Silva-Taboada, 1979; Rodr!ıguez-Dur!an and Lewis, 1987; Bonaccorso et al., 1992). The occurrence of these assemblages generate the question of whether or not their coexistence is promoted by the concomitant thermal gradient within the cave. Observations of bats hibernating in caves suggest that specific differences in behavior as to the choice of roosting site are commonly related to preferred ambient temperature (Ta ) (Daan and Wichers, 1968; Gaisler, 1970). Harmata (1969) reported a good agreement between laboratory experiments of thermopreference and observations made in the hibernacula of bats. The results from previous studies (Rodr!ıguez-Dura! n, 1995, 1998) suggest that physiological differences among species will influence which species coexist in a given cave in the tropical setting where this study was conducted. Given that E. sezekorni is one of the largest species using hot-caves, it is unlikely that other species would displace it by means of direct antagonism. However, direct antagonism would not be necessary to exclude E. sezekorni; sites that become too hot could exclude this species and favor P. quadridens or some other species in these multispecies assemblages. For bats roosting in bat boxes Kerth et al. (2001) found that roost selection was based on temperature and was affected by reproductive condition. Cave-dwelling microchiropterans in Australia have shown preference for different roost temperatures and humidities (Baudinette et al., 2000). Rodr!ıguez-Dur!an (1995) proposed that bats inhabiting hot roosts may show reduced basal metabolic rates as an adaptation to reduce endogenous heat loads and thus promote conservation of water, a proposition partly supported by the results of Maloney et al. (1999) and Rivera-Marchand and Rodr!ıguez-Dur!an (2001). High roost temperatures appear to have a profound effect on the energetic and behavioral strategies of cave-dwelling bats (Bonaccorso et al., 1992;
467
Rodr!ıguez-Dur!an, 1995; Bronner et al., 1999; RiveraMarchand and Rodr!ıguez-Dur!an, 2001). In the laboratory experiments E. sezekorni and P. quadridens choose significantly different temperatures, whether they were released from the hot or cool end of the gradient and irrespective of sex. These results argue against any artifact of the experimental setup being responsible for the differences. Erophylla sezekorni does not cluster when roosting at Ta ’s below TNZ (Rodr!ıguez-Dur!an, 1995), and in the thermopreference experiments it chooses lower Ta ’s than P. quadridens, suggesting the possibility that the potential for overheating in the hot roost may force this species to select lower temperatures. The lethal temperature (LD:50 in 2.5 h) for P. quadridens is 42 C whereas for E. sezekorni is 37 C (Rodr!ıguez-Dura! n, 1991). The correspondence between observed patterns of roost utilization (Rodr!ıguez-Dur!an, 1995; this study) and thermopreference in the laboratory supports the hypothesis that selection of roost-site within a cave by E. sezekorni and P. quadridens is influenced by temperature preferences. Microclimatic differences at a roost site, due to a variety of microstructures such as stalactites, solutional cavities, and other features of the cave’s architecture may contribute to patterns of association of bats. The associations of cave-dwelling bats in Puerto Rico is nonrandom (Rodr!ıguez-Dur!an, 1998). Although these patterns of association seem to be promoted by differences in patterns of activity of coexisting species (Bateman and Vaughan, 1974; Silva-Taboada, 1979; Rodr!ıguez-Dur!an and Lewis, 1987), our results support the hypothesis that roost temperature and differences in temperature preferences among species are important in explaining these associations and the spatial segregation within the cave.
Acknowledgements The National Science Foundation’s Puerto Rico Alliance for Minority Participation partly funded this study. Allen Kurta made helpful comments on an earlier version of the manuscript. Julio Reyes and B. RiveraMarchand helped with field work. The Puerto Rico Department of Natural Resources and Environment provided all necessary permits.
References Bateman, G.C., Vaughan, T.A., 1974. Night activities of mormoopid bats. J. Mamm. 55, 45–65. Baudinette, R.V., Churchill, S.K., Christian, K.A., Nelson, J.E., Hudson, P.J., 2000. Energy, water balance and the roost microenvironment in three Australian cave-dwelling bats (Microchiroptera). J. Comp. Physiol. B 170, 439–446.
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Bonaccorso, F.J., Arends, A., Genoud, M., Cantoni, D., Morton, T., 1992. Thermal ecology of moustached and ghost-faced bats (Mormoopidae) in Venezuela. J. Mamm. 73, 365–378. Bronner, G.N., Maloney, S.K., Buffenstein, R., 1999. Survival tactics within thermally-challenging roosts: heat tolerance and cold sensitivity in the Angolan free-tailed bat, Mops condylurus. S. Afr. J. Zool. 34, 1–10. Daan, S., Wichers, H.J., 1968. Habitat selection of bats hibernating in a limestone cave. Sonderdruck (aus) Z. F. Saugetierkunde Bd. 33, 262–287. Entwistle, A.C., Racey, P.A., Speakman, J.R., 1977. Roost selection by the brown long-eared bat Plecotus auritus. J. Appl. Ecol. 34, 399–408. Fleming, T.H., 1982. Parallel trends in species diversity of West Indian birds and bats. Oecologia 53, 56–60. Gaisler, J., 1970. Remarks on the thermopreferendum of paleartic bats in their natural habitats. Bijdr. Dierkd. 40, 33–35. Genoways, H.H., Phillips, C.J., Baker, R.J., 1998. Bats of the Antillean island of Grenada: a new zoogeographic perspective. Occas. Pap. Mus. Texas Tech. Univ. 177, 1–28. Harmata, W., 1969. The thermopreferendum of some species of bats (Chiroptera). Acta Theriol. 14, 49–62. Herreid, C.F., 1967. Temperature regulation, temperature preference and tolerance, and metabolism of young and adult free-tailded bats. Physiol. Zool. 40, 1–22. Kerth, G., Weissmann, K., Konig, B., 2001. Day roost selection in female Bechstein’s bat (Myotis bechsteinii): a field experiment to determine the influence of roost temperature. Oecologia 126, 1–9. Kunz, T.H., 1982. Roosting ecology of bats. In: Kunz, T.H. (Ed.), Ecology of Bats. Plenum Press, New York, pp. 1–55. Kunz, T.H., Kurta, A., 1988. Capture methods and holding devices. In: Kunz, T.H. (Ed.), Ecological and Behavioural Methods for the Study of Bats. Smithsonian Institution, Washington, DC, pp. 1–30. Kunz, T.H., August, P.V., Burnett, C.D., 1983. Harem social organization in cave roosting Artibeus jamaicensis (Chiroptera: Phyllostomidae). Biotropica 152, 133–138.
Maloney, S.K., Bronner, G.N., Buffenstein, R., 1999. Thermoregulation in the Angolan free-tailed bat Mops condylurus: a small mammal that uses hot rosts. Physiol. Biochem. Zool. 72, 385–396. McFarlane, D.A., 1989. Patterns of species co-occurrence in the Antillean bat fauna. Mammalia 53, 59–66. Rivera-Marchand, B., Rodr!ıguez-Dur!an, A., 2001. Preliminary observations on the renal adaptations of bats roosting in hot caves in Puerto Rico. Caribb. J. Sci. 37, 272–274. Rodr!ıguez-Dur!an, A., 1991. Comparative environmental physiology of bats roosting in hot caves. Unpublished Ph.D. Thesis, Boston University, Boston, MA. Rodr!ıguez-Dur!an, A., 1995. Metabolic rates and thermal conductance in four species of Neotropical bats roosting in hot caves. Comp. Biochem. Physiol. 110A, 347–355. Rodr!ıguez-Dur!an, A., 1998. Nonrandom aggregations and distribution of cave dwelling bats in Puerto Rico. J. Mamm. 79, 141–146. Rodr!ıguez-Dur!an, A., Kunz, T.H., 2001. Biogeography of West Indian bats: an ecological perspective. In: Woods, C.A., Sergile, F.E. (Eds.), Biogeography of the West Indies: Patterns and Perspectives. CRC Press, New York, pp. 355–368. Rodr!ıguez-Dur!an, A., Lewis, A.R., 1987. Patterns of population size, diet and activity time for a multispecies assemblage of bats at a cave in Puerto Rico. Caribb. J. Sci. 23, 352–360. Sedgeley, J.A., O’Donnell, C.F.J., 1999. Factors influencing the selection of roost cavities by a temperate rainforest bat (Vespertilionidae: Chalinolobus tuberculatus) in New Zealand. J. Zool. London 249, 437–446. Silva-Taboada, G., 1979. Los Murci!elagos de Cuba. Editorial Academia, La Habana, Cuba. Twente, J.W., 1955. Some aspects of habitat selection and other behavior of cavern-dwelling bats. Ecology 36, 706–732. Wilkinson, G.S., 1985. The social organization of the common vampire bat. I. Pattern and cause of association. Behav. Ecol. Sociobiol. 17, 111–121. Zahn, A., 1999. Reproductive success, colony size, and roost temperature in attic-dwelling bat Myotis myotis. J. Zool. London 247, 275–280.
Journal of Thermal Biology 28 (2003) 465–468
Temperature selection by tropical bats roosting in caves A. Rodr!ıguez-Dura! n*, J.A. Soto-Centeno ! PR 00957, USA Department of Natural Sciences, Inter American University, Rd. 830, No. 500, Bayamon, Received 14 June 2002; accepted 27 July 2002
Abstract The temperature preferences of the mormoopid and phyllostomid bats Pteronotus quadridens and Erophylla sezekorni, from the West Indies, were determined in the laboratory and compared to field observations. Pteronotus quadridens was invariably found within the deepest and hottest parts of caves, at temperatures between 28 C and 35 C, while E. sezekorni was found at temperatures from 25 C to 28 C. Temperatures selected by each species in a thermopreferendum chamber were similar to their respective roosting temperatures in the caves. These inter-specific differences are statistically significant. Our results support the hypothesis that roost temperature and differences in temperature preferences among species, are important in explaining multispecies associations and the spatial segregation within caves. r 2003 Elsevier Ltd. All rights reserved. Keywords: Bats; Temperature selection; Caves; West Indies; Roosting; Coexistence; Tropical; Temperature preference
1. Introduction Selection of appropriate roosting conditions may be of critical survival value for bats (Kunz, 1982; Maloney et al., 1999), although when it comes to tropical species this is an aspect of their ecology that is commonly underestimated. The literature on microclimatic preferences among bat species is scarce, and addresses mostly the problem of hibernation (e.g. Twente, 1955; Herreid, 1967; Daan and Wichers, 1968; Gaisler, 1970) or deals with tree (e.g. Sedgeley and O’Donnell, 1999) or atticroosting bats (e.g. Entwistle et al., 1997; Zahn, 1999) from temperate regions. Few studies address the matter of roost selection by tropical bats, and to our knowledge no other study examines selection of temperature as a mechanism promoting the coexistence of multispecies assemblages of tropical bats. Wilkinson (1985) suggested that microclimate might be one factor influencing roosting behavior of female Desmodus rotundus. Kunz et al. (1983) found no microclimatic differences between *Corresponding author. E-mail address: [email protected] (A. Rodr!ıguezDur!an).
occupied and vacant cavities in a cave inhabited by Artibeus jamaicensis. In both studies, microclimate selection was ruled out as a major factor influencing roost selection. Both D. rotundus and A. jamaicensis are medium sized bats that do not roost exclusively in caves and do not form large aggregations. The bat faunas of the West Indies are not random assemblages from the tropical mainland (Fleming, 1982; McFarlane, 1989; Genoways et al., 1998), and the presence of caves is one of several factors that may help define the packing patterns of these faunas (Rodr!ıguezDur!an and Kunz, 2001). Small mormoopid and phyllostomid bats roosting in hot caves exhibit high degrees of gregariousness and roost fidelity (SilvaTaboada, 1979; Rodr!ıguez-Dur!an, 1998), and face the problems associated with their reduced capacity to store fat and thermoregulate (Bonaccorso et al., 1992; Rodr!ıguez-Dur!an, 1995). Although up to nine species may occupy a single hot-cave, different species usually maintain spatial separation within the roost (SilvaTaboada, 1979). High frequencies of roosting aggregations have been reported for the hot-caves associations: Monophyllus redmani (Phyllostomidae)—Mormoops blainvilli—Pteronotus quadridens (Mormoopidae); and,
0306-4565/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0306-4565(03)00046-9
ARTICLE IN PRESS 466
! J.A. Soto-Centeno / Journal of Thermal Biology 28 (2003) 465–468 A. Rodr!ıguez-Duran,
Erophylla sezekorni (Phyllostomidae)—P. parnellii (Mormoopidae) (Rodr!ıguez-Dur!an, 1998), in which warm temperatures (26–40 C) resulted from high densities of bats. It has been proposed that intraspecific competition for access to the roost is what limits the species composition and population sizes in these caves (Bateman and Vaughan, 1974; Silva-Taboada, 1979; Rodr!ıguez-Dur!an and Lewis, 1987). However, this hypothesis does not explain the spatial separation of species within the cave. The purpose of this study is to assess the temperature preferences of P. quadridens and E. sezekorni as they relate to microclimatic differences within a cave.
2. Materials and methods Observations and captures at three caves (Rodr!ıguezDura! n, 1998) form the basis for the present study, although most efforts were concentrated at Bonita Cave. To establish the location of each species within each cave we made visual examinations using a headlamp and, when necessary, 7 35 binoculars. We obtained measurements of temperature of roosts used by P. quadridens (Mormoopidae) and E. sezekorni (=bombifrons) (Phyllostomidae) at Los Pe! rez, Cucaracha, and Bonita caves, using maximum/minimum thermometers in combination with a telescopic aluminium pole. We captured adult, non-reproductive individuals of both sexes (81 P. quadridens and 79 E. sezekorni) as they returned from foraging, using a harp-trap (Kunz and Kurta, 1988) set at the cave entrance. Laboratory experiments began 3–8 h following capture and were always terminated before the beginning of the normal foraging phase of the species. Prior to each experiment, all bats were housed in a temperature-controlled cabinet at a temperature of 27–30 C and a relative humidity of 80–90%. Temperature preference tests (Herreid, 1967) were conducted in a specially designed (180 30 30 cm3) aluminum chamber. This chamber contained a hardware cloth cage, and both the interior of the chamber and the cage were painted flat black. We arranged nine type-K thermocouples at 18 cm (SD=1.7 cm) intervals along the chamber at the same height as the bats roosted. The wire cage was insulated from the floor of the chamber by means of wooden legs so as to minimize thermal conductance. The outside of the chamber was insulated with 10.2-cm-thick, high-density, expandable polystyrene with a conductivity of K=0.27 J (s m C)1. We cooled one end of the chamber and heated the other, creating a 22–40 C thermal gradient. Single bats were placed in a previously established gradient and given 1.5 h to select their position, after which the chamber was opened and the temperature at the
thermocouple closest to the bat was recorded. To avoid potential problems associated with bats staying in the section of the gradient where they are introduced, we followed three variations of this protocol: (1) bats were placed in the middle of the gradient; (2) bats were placed in a subdivision of the cage on the hot section of the chamber and after they settled down, allowed access to the whole of the gradient; (3) bats were placed on the cool section of the gradient in the same manner as in (2). After each experiment, we cleaned (Lysol Scent) and blow-dried both the wire-cage and the floor of the chamber to eliminate any odor cue that might have been left from the previous bat. We compared the results using t-tests, or Mann– Whitney when the data failed to pass a normality test. We examined overall differences among species, sex differences within species, and differences due to whether the bats were released on the hot vs. cool end of the gradient.
3. Results Pteronotus quadridens was invariably found within the deepest and hottest parts of caves, at temperatures between 28 C and 35 C, while E. sezekorni was found near the heat trap, at temperatures ranging from 25 C to 28 C. Temperatures selected by each species in the thermopreferendum chamber were similar to their respective roosting temperatures in the caves. Twentyseven (34%) of the P. quadridens selected temperatures between 22 C and 27 C, while 39 (49%) selected temperatures between 31 C and 39 C (Fig. 1). The median temperature selected by P. quadridens was 29.5 C (N ¼ 81; Mean=30.2, SD=4.6). Thirty-two (41%) E. sezekorni selected temperatures between 22 C and 27 C, whereas 21(27%) selected temperatures between 31 C and 39 C (Fig. 1). The median temperature selected by
Fig. 1. Temperatures selected by P. quadridens and E. sezekorni in the thermopreferendum chamber. The difference is statistically significant (P ¼ 0:013; Mann–Whitney test).
ARTICLE IN PRESS ! J.A. Soto-Centeno / Journal of Thermal Biology 28 (2003) 465–468 A. Rodr!ıguez-Duran,
E. sezekorni was 28 C (N ¼ 79; Mean=28.2, SD=2.3). These differences in temperatures selected by each species in the thermopreferendum chamber are statistically significant (P ¼ 0:013; Mann–Whitney). Other tests revealed non-significant differences. There is no significant difference between temperatures selected by males and females P. quadridens (P ¼ 0:202; Mann–Whitney) or E. sezekorni (P ¼ 0:396; t-test). There is no significant difference between temperatures selected by P. quadridens (P ¼ 0:276; t-test) released in the hot vs. cool section of the chamber; the same holds true for E. sezekorni (P ¼ 0:350; t-test).
4. Discussion Mormoopid and phyllostomid bats often share the same caves, forming some of the largest multispecies assemblages of mammals known (Bateman and Vaughan, 1974; Silva-Taboada, 1979; Rodr!ıguez-Dur!an and Lewis, 1987; Bonaccorso et al., 1992). The occurrence of these assemblages generate the question of whether or not their coexistence is promoted by the concomitant thermal gradient within the cave. Observations of bats hibernating in caves suggest that specific differences in behavior as to the choice of roosting site are commonly related to preferred ambient temperature (Ta ) (Daan and Wichers, 1968; Gaisler, 1970). Harmata (1969) reported a good agreement between laboratory experiments of thermopreference and observations made in the hibernacula of bats. The results from previous studies (Rodr!ıguez-Dura! n, 1995, 1998) suggest that physiological differences among species will influence which species coexist in a given cave in the tropical setting where this study was conducted. Given that E. sezekorni is one of the largest species using hot-caves, it is unlikely that other species would displace it by means of direct antagonism. However, direct antagonism would not be necessary to exclude E. sezekorni; sites that become too hot could exclude this species and favor P. quadridens or some other species in these multispecies assemblages. For bats roosting in bat boxes Kerth et al. (2001) found that roost selection was based on temperature and was affected by reproductive condition. Cave-dwelling microchiropterans in Australia have shown preference for different roost temperatures and humidities (Baudinette et al., 2000). Rodr!ıguez-Dur!an (1995) proposed that bats inhabiting hot roosts may show reduced basal metabolic rates as an adaptation to reduce endogenous heat loads and thus promote conservation of water, a proposition partly supported by the results of Maloney et al. (1999) and Rivera-Marchand and Rodr!ıguez-Dur!an (2001). High roost temperatures appear to have a profound effect on the energetic and behavioral strategies of cave-dwelling bats (Bonaccorso et al., 1992;
467
Rodr!ıguez-Dur!an, 1995; Bronner et al., 1999; RiveraMarchand and Rodr!ıguez-Dur!an, 2001). In the laboratory experiments E. sezekorni and P. quadridens choose significantly different temperatures, whether they were released from the hot or cool end of the gradient and irrespective of sex. These results argue against any artifact of the experimental setup being responsible for the differences. Erophylla sezekorni does not cluster when roosting at Ta ’s below TNZ (Rodr!ıguez-Dur!an, 1995), and in the thermopreference experiments it chooses lower Ta ’s than P. quadridens, suggesting the possibility that the potential for overheating in the hot roost may force this species to select lower temperatures. The lethal temperature (LD:50 in 2.5 h) for P. quadridens is 42 C whereas for E. sezekorni is 37 C (Rodr!ıguez-Dura! n, 1991). The correspondence between observed patterns of roost utilization (Rodr!ıguez-Dur!an, 1995; this study) and thermopreference in the laboratory supports the hypothesis that selection of roost-site within a cave by E. sezekorni and P. quadridens is influenced by temperature preferences. Microclimatic differences at a roost site, due to a variety of microstructures such as stalactites, solutional cavities, and other features of the cave’s architecture may contribute to patterns of association of bats. The associations of cave-dwelling bats in Puerto Rico is nonrandom (Rodr!ıguez-Dur!an, 1998). Although these patterns of association seem to be promoted by differences in patterns of activity of coexisting species (Bateman and Vaughan, 1974; Silva-Taboada, 1979; Rodr!ıguez-Dur!an and Lewis, 1987), our results support the hypothesis that roost temperature and differences in temperature preferences among species are important in explaining these associations and the spatial segregation within the cave.
Acknowledgements The National Science Foundation’s Puerto Rico Alliance for Minority Participation partly funded this study. Allen Kurta made helpful comments on an earlier version of the manuscript. Julio Reyes and B. RiveraMarchand helped with field work. The Puerto Rico Department of Natural Resources and Environment provided all necessary permits.
References Bateman, G.C., Vaughan, T.A., 1974. Night activities of mormoopid bats. J. Mamm. 55, 45–65. Baudinette, R.V., Churchill, S.K., Christian, K.A., Nelson, J.E., Hudson, P.J., 2000. Energy, water balance and the roost microenvironment in three Australian cave-dwelling bats (Microchiroptera). J. Comp. Physiol. B 170, 439–446.
ARTICLE IN PRESS 468
! J.A. Soto-Centeno / Journal of Thermal Biology 28 (2003) 465–468 A. Rodr!ıguez-Duran,
Bonaccorso, F.J., Arends, A., Genoud, M., Cantoni, D., Morton, T., 1992. Thermal ecology of moustached and ghost-faced bats (Mormoopidae) in Venezuela. J. Mamm. 73, 365–378. Bronner, G.N., Maloney, S.K., Buffenstein, R., 1999. Survival tactics within thermally-challenging roosts: heat tolerance and cold sensitivity in the Angolan free-tailed bat, Mops condylurus. S. Afr. J. Zool. 34, 1–10. Daan, S., Wichers, H.J., 1968. Habitat selection of bats hibernating in a limestone cave. Sonderdruck (aus) Z. F. Saugetierkunde Bd. 33, 262–287. Entwistle, A.C., Racey, P.A., Speakman, J.R., 1977. Roost selection by the brown long-eared bat Plecotus auritus. J. Appl. Ecol. 34, 399–408. Fleming, T.H., 1982. Parallel trends in species diversity of West Indian birds and bats. Oecologia 53, 56–60. Gaisler, J., 1970. Remarks on the thermopreferendum of paleartic bats in their natural habitats. Bijdr. Dierkd. 40, 33–35. Genoways, H.H., Phillips, C.J., Baker, R.J., 1998. Bats of the Antillean island of Grenada: a new zoogeographic perspective. Occas. Pap. Mus. Texas Tech. Univ. 177, 1–28. Harmata, W., 1969. The thermopreferendum of some species of bats (Chiroptera). Acta Theriol. 14, 49–62. Herreid, C.F., 1967. Temperature regulation, temperature preference and tolerance, and metabolism of young and adult free-tailded bats. Physiol. Zool. 40, 1–22. Kerth, G., Weissmann, K., Konig, B., 2001. Day roost selection in female Bechstein’s bat (Myotis bechsteinii): a field experiment to determine the influence of roost temperature. Oecologia 126, 1–9. Kunz, T.H., 1982. Roosting ecology of bats. In: Kunz, T.H. (Ed.), Ecology of Bats. Plenum Press, New York, pp. 1–55. Kunz, T.H., Kurta, A., 1988. Capture methods and holding devices. In: Kunz, T.H. (Ed.), Ecological and Behavioural Methods for the Study of Bats. Smithsonian Institution, Washington, DC, pp. 1–30. Kunz, T.H., August, P.V., Burnett, C.D., 1983. Harem social organization in cave roosting Artibeus jamaicensis (Chiroptera: Phyllostomidae). Biotropica 152, 133–138.
Maloney, S.K., Bronner, G.N., Buffenstein, R., 1999. Thermoregulation in the Angolan free-tailed bat Mops condylurus: a small mammal that uses hot rosts. Physiol. Biochem. Zool. 72, 385–396. McFarlane, D.A., 1989. Patterns of species co-occurrence in the Antillean bat fauna. Mammalia 53, 59–66. Rivera-Marchand, B., Rodr!ıguez-Dur!an, A., 2001. Preliminary observations on the renal adaptations of bats roosting in hot caves in Puerto Rico. Caribb. J. Sci. 37, 272–274. Rodr!ıguez-Dur!an, A., 1991. Comparative environmental physiology of bats roosting in hot caves. Unpublished Ph.D. Thesis, Boston University, Boston, MA. Rodr!ıguez-Dur!an, A., 1995. Metabolic rates and thermal conductance in four species of Neotropical bats roosting in hot caves. Comp. Biochem. Physiol. 110A, 347–355. Rodr!ıguez-Dur!an, A., 1998. Nonrandom aggregations and distribution of cave dwelling bats in Puerto Rico. J. Mamm. 79, 141–146. Rodr!ıguez-Dur!an, A., Kunz, T.H., 2001. Biogeography of West Indian bats: an ecological perspective. In: Woods, C.A., Sergile, F.E. (Eds.), Biogeography of the West Indies: Patterns and Perspectives. CRC Press, New York, pp. 355–368. Rodr!ıguez-Dur!an, A., Lewis, A.R., 1987. Patterns of population size, diet and activity time for a multispecies assemblage of bats at a cave in Puerto Rico. Caribb. J. Sci. 23, 352–360. Sedgeley, J.A., O’Donnell, C.F.J., 1999. Factors influencing the selection of roost cavities by a temperate rainforest bat (Vespertilionidae: Chalinolobus tuberculatus) in New Zealand. J. Zool. London 249, 437–446. Silva-Taboada, G., 1979. Los Murci!elagos de Cuba. Editorial Academia, La Habana, Cuba. Twente, J.W., 1955. Some aspects of habitat selection and other behavior of cavern-dwelling bats. Ecology 36, 706–732. Wilkinson, G.S., 1985. The social organization of the common vampire bat. I. Pattern and cause of association. Behav. Ecol. Sociobiol. 17, 111–121. Zahn, A., 1999. Reproductive success, colony size, and roost temperature in attic-dwelling bat Myotis myotis. J. Zool. London 247, 275–280.