Startseite The big brown bat (Eptesicus fuscus) reduces its body mass during winter in a tropical montane ecosystem of central Mexico
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The big brown bat (Eptesicus fuscus) reduces its body mass during winter in a tropical montane ecosystem of central Mexico

  • Kevin I. Medina-Bello , Rommy Vázquez-Fuerte und Jorge Ayala-Berdon EMAIL logo
Veröffentlicht/Copyright: 5. Dezember 2022
Mammalia
Aus der Zeitschrift Mammalia Band 87 Heft 2

Abstract

Most animals face changes in the availability of food and the environmental conditions in the places where they live. In response, they need to adjust their behavioral, physiological, and morphological traits. In temperate zones and high latitudes, bats increase their body mass (M b ) in autumn to store fat reserves and use them during hibernation. However, other small mammals decrease their M b prior to winter to reduce the energetic requirements of individuals. These changes are unknown for bats inhabiting other highly energetic demanding environments. We measured changes in M b of 84 non-reproductive males of Eptesicus fuscus inhabiting a tropical montane ecosystem in central Mexico over seasons. We also examined the relationship of bats’ M b with the minimum ambient temperature (T a , °C) and mean precipitation (mm). Bats presented an increase in M b from March to June, followed by a decrease from September to November and presented the lowest M b from November to March, in the dry-cold season. The results suggest that the pattern of changes in M b could be the result of two non-exclusive components related to the bats’ energy budget, the energetic demands experienced by the bats throughout the year and the morphological adaptations animals could display to reduce their energy requirements during the winter.


Corresponding author: Jorge Ayala-Berdon, CONACYT, Universidad Autónoma de Tlaxcala, código postal 90062, Tlaxcala de Xicohténcatl, Mexico, E-mail:

Acknowledgments

The authors wish to thank all the students that were involved in data collection, Justin Overstreet for reviewing the language of the manuscript, two anonymous reviewers and the associate editor for their comments and suggestions, and La Malinche biological station for logistical support.

  1. Author contributions: The three authors conceived the idea, acquired and processed data and wrote the manuscript.

  2. Research funding: No funding was received for the development of this work.

  3. Conflict of interest statement: The authors declare that they have no conflicts of interest regarding this article.

  4. Research ethics: Bat captures were performed under the permission of the Department of Wildlife Management granted to our institution (SEMARNAT 07019; SGPA/DGVS/00582/20).

References

Abouali, M., Nejadhashemi, A.P., Daneshvar, F., and Woznicki, S.A. (2016). Two-phase approach to improve stream health modeling. Ecol. Inf. 34: 13–21, https://doi.org/10.1016/j.ecoinf.2016.04.009.Suche in Google Scholar

Aguilar-Rodríguez, P.A., Vega-Gutiérrez, V.H., Méndez, R.S.M., Hernandez, A.A., Cabrera-Campos, I., and Ayala-Berdon, J. (2021). Winter occupation of two bat hibernacula in a montane ecosystem of central Mexico. Bol. Red. Latin. Car. Cons. Murc. 12: 3–9.Suche in Google Scholar

Ashton, K.G., Tracy, M.C., and Queiroz, A.D. (2000). Is Bergmann’s rule valid for mammals? Am. Nat. 156: 390–415, https://doi.org/10.1086/303400.Suche in Google Scholar PubMed

Ayala-Berdon, J., Schondube, J.E., and Stoner, K.E. (2009). Seasonal intake responses in the nectar-feeding bat Glossophaga soricina. J. Comp. Physiol., B 179: 553–562, https://doi.org/10.1007/s00360-008-0335-z.Suche in Google Scholar PubMed

Ayala-Berdon, J., Vázquez-Fuerte, R., Rodríguez-Peña, N., and Martínez-Gómez, M. (2017). Bat fauna associated with artificial ponds in La Malinche National Park, a mountain ecosystem of Mexico. Mammalia 81: 573–581, https://doi.org/10.1515/mammalia-2016-0055.Suche in Google Scholar

Ayala-Berdon, J., Corona, C.G., and Martínez-Gómez, M. (2018). Seasonal intake responses could reflect digestive plasticity in the nectar-feeding bat Anoura geoffroyi. Mamm. Biol. 93: 118–123, https://doi.org/10.1016/j.mambio.2018.10.001.Suche in Google Scholar

Ayala-Berdon, J., Vázquez-Fuerte, R., Guillén-Servent, A., López-Cuamatzi, I.L., and Martínez-Gómez, M. (2022). Changes in activity along the year in a community of insectivorous bats inhabiting a montane ecosystem of central Mexico. Mammal Res. 67: 219–229, https://doi.org/10.1007/s13364-022-00620-y.Suche in Google Scholar

Banks, P.B. and Dickman, C.R. (2000). Effects of winter food supplementation on reproduction, body mass, and numbers of small mammals in montane Australia. Can. J. Zool. 78: 1775–1783, https://doi.org/10.1139/z00-110.Suche in Google Scholar

Barclay, R.M. (1991). Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. J. Anim. Ecol. 60: 165–178, https://doi.org/10.2307/5452.Suche in Google Scholar

Becker, N.I., Tschapka, M., Kalko, E.K., and Encarnaçao, J.A. (2013). Balancing the energy budget in free-ranging male Myotis daubentonii bats. Physiol. Biochem. Zool. 86: 361–369, https://doi.org/10.1086/670527.Suche in Google Scholar PubMed

Bernard, R.F., Willcox, E.V., Jackson, R.T., Brown, V.A., and McCracken, G.F. (2021). Feasting, not fasting: winter diets of cave hibernating bats in the United States. Front. Zool. 18: 48, https://doi.org/10.1186/s12983-021-00434-9.Suche in Google Scholar PubMed PubMed Central

Bonaccorso, F.J., Smythe, N., and Humphrey, S.R. (1976). Improved techniques for marking bats. J. Mammal. 57: 181–182, https://doi.org/10.2307/1379526.Suche in Google Scholar

Bozinovic, F., Cruz-Neto, A.P., Cortés, A., Diaz, G.B., Ojeda, R.A., and Giannoni, S.M. (2007). Physiological diversity in tolerance to water deprivation among species of South American desert rodents. J. Arid Eviron. 70: 427–442, https://doi.org/10.1086/physzool.63.6.30152641.Suche in Google Scholar

Bozinovic, F., Novoa, F.F., and Veloso, C. (1990). Seasonal changes in energy expenditure and digestive tract of Abrothrix andinus (Cricetidae) in the Andes range. Physiol. Zool. 63: 1216–1231, https://doi.org/10.1086/physzool.63.6.30152641.Suche in Google Scholar

Brunet-Rossinni, A.K. and Wilkinson, G.S. (2009). Methods for age estimation and the study of senescence. In: Kunz, T.H. and Parsons, S. (Eds.), Ecological and behavioral methods for the study of bats, 2nd ed. Johns Hopkins University Press, Baltimore, pp. 315–325.Suche in Google Scholar

Buck, C.L. and Barnes, B.M. (1999). Annual cycle of body composition and hibernation in free-living arctic ground squirrels. J. Mammal. 80: 430–442, https://doi.org/10.2307/1383291.Suche in Google Scholar

Cabrera-Campos, I., Carballo-Morales, J.D., Saldaña-Vázquez, R.A., Villalobos, F., and Ayala-Berdon, J. (2021). Body mass explains digestive traits in small vespertilionid bats. J. Comp. Physiol., B 191: 427–438, https://doi.org/10.1007/s00360-021-01348-y.Suche in Google Scholar PubMed

Chen, J.F., Zhong, W.Q., and Wang, D.H. (2012). Seasonal changes in body mass, energy intake and thermogenesis in Maximowiczi’s voles (Microtus maximowiczii) from the Inner Mongolian grassland. J. Comp. Physiol., B 182: 275–285, https://doi.org/10.1007/s00360-011-0608-9.Suche in Google Scholar PubMed

Cryan, P.M. (2003). Seasonal distribution of migratory tree bats (Lasiurus and Lasionycteris) in North America. J. Mammal. 84: 579–593, https://doi.org/10.1644/1545-1542(2003)084<0579:sdomtb>2.0.co;2.10.1644/1545-1542(2003)084<0579:SDOMTB>2.0.CO;2Suche in Google Scholar

Dark, J. and Zucker, I. (1983). Short photoperiods reduce winter energy requirements of the meadow vole, Microtus pennsylvanicus. Physiol. Behav. 31: 699–702, https://doi.org/10.1016/s0031-9384(83)80006-7.Suche in Google Scholar

Davis, W.H. and Reite, O.B. (1967). Responses of bats from temperate regions to changes in ambient temperature. Biol. Bull. 132: 320–328, https://doi.org/10.2307/1539637.Suche in Google Scholar

de Jong, J. and Ahlén, I. (1991). Factors affecting the distribution pattern of bats in Uppland, central Sweden. Ecography 14: 92–96, https://doi.org/10.1111/j.1600-0587.1991.tb00638.x.Suche in Google Scholar

Del Valle, J.C. and Busch, C. (2003). Body composition and gut length of Akodon azarae (Muridae: Sigmodontinae): relationship with energetic requirements. Acta Theriol. 48: 347–357, https://doi.org/10.1007/bf03194174.Suche in Google Scholar

Farias, T.D.O., Figueiredo, A.F.A., Wnuk, N.T., Ferraz, F.S., Talamoni, S.A., and Costa, G.M.J. (2020). Male reproductive morphofunctional evaluation of a Neotropical sperm-storing vespertilionid bat (Myotis levis) in an environmental context. Cell Tissue Res. 382: 639–656, https://doi.org/10.1007/s00441-020-03242-5.Suche in Google Scholar PubMed

Ferreyra-García, D., Saldaña-Vázquez, R.A., and Schondube, J.E. (2018). La estacionalidad climática no afecta la fenología de murciélagos cavernícolas con dieta omnívora. Rev. Mex. Biodivers. 89: 488–496, https://doi.org/10.22201/ib.20078706e.2018.2.2016.Suche in Google Scholar

Fleming, T.H. (2019). Bat migration. In: Chun, J.C. (Ed.). Encyclopedia of animal behavior. Elsevier, Amsterdam, pp. 605–610.10.1016/B978-0-12-809633-8.20764-4Suche in Google Scholar

Frick, W.F., Puechmaille, S.J., and Willis, C.K. (2016). White-nose syndrome in bats. In: Voigt, C.C. and Kingston, T. (Eds.), Bats in the Anthropocene: conservation of bats in a changing world. Springer, Cham, pp. 245–262.10.1007/978-3-319-25220-9_9Suche in Google Scholar

Haarsma, A.J. (2008). Manual for assessment of reproductive status, age and health in European vespertilionid bats. Electronic, Holland, Hillegom.Suche in Google Scholar

Hansen, S.K. (2020). Variation in basal metabolic rate within bats of the family Vespertilionidae. Master’s thesis. Trondheim, Norwegian University of Science and Technology.Suche in Google Scholar

Heldmaier, G., Ortmann, S., and Elvert, R. (2004). Natural hypometabolism during hibernation and daily torpor in mammals. Respir. Physiol. Neurobiol. 141: 317–329, https://doi.org/10.1016/j.resp.2004.03.014.Suche in Google Scholar PubMed

Herreid, C.F. and Schmidt-Nielsen, K. (1966). Oxygen consumption, temperature and water loss in bats from different environments. Am. J. Physiol. 211: 1108–1112, https://doi.org/10.1152/ajplegacy.1966.211.5.1108.Suche in Google Scholar PubMed

INEGI (1987). Anexo cartográfico del estado de Tlaxcala. Tlaxcala.Suche in Google Scholar

Jackson, D.M., Hambly, C., Trayhurn, P., and Speakman, J.R. (2001). Associations between energetics and over-winter survival in the short-tailed field vole Microtus agrestis. J. Anim. Ecol. 70: 633–640, https://doi.org/10.1046/j.1365-2656.2001.00518.x.Suche in Google Scholar

Jackson, R.T., Willcox, E.V., Zobel, J.M., and Bernard, R.F. (2022). Emergence activity at hibernacula differs among four bat species affected by white nose syndrome. Ecol. Evol. 12: e9113, https://doi.org/10.1002/ece3.9113.Suche in Google Scholar PubMed PubMed Central

Jansky, L., Haddad, G., Pospisilova, D., and Dvorak, P. (1986). Effect of external factors on gonadal activity and body mass of male golden hamsters (Mesocricetus auratus). J. Comp. Physiol., B 156: 717–725, https://doi.org/10.1007/bf00692750.Suche in Google Scholar PubMed

Kunz, T.H., Wrazen, J.A., and Burnett, C.D. (1998). Changes in body mass and fat reserves in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5: 8–17, https://doi.org/10.1080/11956860.1998.11682443.Suche in Google Scholar

Kurta, A. and Baker, R.H. (1990). Eptesicus fuscus. Mamm. Species 356: 1–10, https://doi.org/10.2307/3504258.Suche in Google Scholar

Li, X.S. and Wang, D.H. (2005). Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): the roles of short photoperiod and cold. J. Comp. Physiol., B 175: 593–600, https://doi.org/10.1007/s00360-005-0022-2.Suche in Google Scholar PubMed

López-Domínguez, J.C. and Acosta, R. (2005). Descripción del parque nacional Malinche. In: Fernández, J.A. and López, J.C. (Eds.), Biodiversidad del Parque Nacional La Malinche, Mexico (J). Coordinación General de Ecología. Gobierno del Estado de Tlaxcala, Mexico, pp. 3–24.Suche in Google Scholar

McGuire, L.P. and Boyle, W.A. (2013). Altitudinal migration in bats: evidence, patterns, and drivers. Biol. Rev. 88: 767–786, https://doi.org/10.1111/brv.12024.Suche in Google Scholar PubMed

McNab, B.K. (1969). The economics of temperature regulation in Neotropical bats. Comp. Biochem. Physiol. 31: 227–268, https://doi.org/10.1016/0010-406x(69)91651-x.Suche in Google Scholar PubMed

McNab, B.K. (1986). The influence of food habits on the energetics of eutherian mammals. Ecol. Monogr. 56: 1–19, https://doi.org/10.2307/2937268.Suche in Google Scholar

McNab, B.K. (2012). Extreme measures. University of Chicago Press, Chicago.10.7208/chicago/9780226561240.001.0001Suche in Google Scholar

Merritt, J.F., Zegers, D.A., and Rose, L.R. (2001). Seasonal thermogenesis of southern flying squirrels (Glaucomys volans). J. Mammal. 82: 51–64, https://doi.org/10.1093/jmammal/82.1.51.Suche in Google Scholar

Medellín, R.A., Arita, H.T., and Sanchez-Herrera, O. (2008). Identificación de los murciélagos de México: clave de campo. Asociación Mexicana de Mastozoología, México.Suche in Google Scholar

Moosman, P.R., Warner, D.P., Hendren, R.H., and Hosler, M.J. (2015). Potential for monitoring eastern small-footed bats on talus slopes. Northeast Nat. 22: 1–13, https://doi.org/10.1656/045.022.0102.Suche in Google Scholar

Nagy, T.R., Gower, B.A., and Stetson, M.H. (1995). Endocrine correlates of seasonal body mass dynamics in the collared lemming (Dicrostonyx groenlandicus). Am. Zool. 35: 246–258, https://doi.org/10.1093/icb/35.3.246.Suche in Google Scholar

Nickerson, D.M., Facey, D.E., and Grossman, G.D. (1989). Estimating physiological thresholds with continuous two-phase regression. Physiol. Zool. 62: 866–887, https://doi.org/10.1086/physzool.62.4.30157934.Suche in Google Scholar

Palacios, D. and Vázquez-Selem, L. (1996). Geomorphic effects of the retreat of Jamapa glacier, Pico de Orizaba volcano (Mexico). Geogr. Ann. 78: 19–34, https://doi.org/10.1080/04353676.1996.11880449.Suche in Google Scholar

Patterson, B.D., Pacheco, V., and Solari, S. (1996). Distribution of bats along an elevational gradient in the Andes of south eastern Peru. J. Zool. 240: 637–658, https://doi.org/10.1111/j.1469-7998.1996.tb05313.x.Suche in Google Scholar

Powell, C.S., Blaylock, M.L., Wang, R., Hunter, H.L., Johanning, G.L., and Nagy, T.R. (2002). Effects of energy expenditure and Ucp1 on photoperiod-induced weight gain in collard lemmings. Obes. Res. 10: 541–550, https://doi.org/10.1038/oby.2002.73.Suche in Google Scholar PubMed

Racey, P.A. (1982). Ecology of bat reproduction. In: Kunz, T.H. (Ed.). Ecology of bats. Plenum Press, New York, pp. 57–104.10.1007/978-1-4613-3421-7_2Suche in Google Scholar

Ransome, R.D. (1990). The natural history of hibernating bats. Christopher Helm, London.Suche in Google Scholar

R Core Team (2020). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.Suche in Google Scholar

Ruf, T., Klingenspor, M., Preis, H., and Heldmaier, G. (1991). Daily torpor in the Djungarian hamster (Phodopus sungorus): interactions with food intake, activity, and social behaviour. J. Comp. Physiol., B 160: 609–615, https://doi.org/10.1007/bf00571257.Suche in Google Scholar

Rughetti, M. and Toffoli, R. (2014). Sex-specific seasonal change in body mass in two species of vespertilionid bats. Acta Chiropterol. 16: 149–155, https://doi.org/10.3161/150811014x683363.Suche in Google Scholar

Sánchez Cordero, V. (2001). Elevation gradients of diversity for rodents and bats in Oaxaca, Mexico. Global Ecol. Biogeogr. 10: 63–76, https://doi.org/10.1046/j.1466-822x.2001.00235.x.Suche in Google Scholar

Scholander, P.F., Hock, R., Walters, V., Johnson, F., and Irving, L. (1950). Heat regulation in some arctic and tropical mammals and birds. Biol. Bull. 99: 237–258, https://doi.org/10.2307/1538741.Suche in Google Scholar PubMed

Silva Taboada, G. (1979). Los murciélagos de Cuba. Editorial Academia, Havana.Suche in Google Scholar

Solow, A.R. (1987). Testing for climate change: an application of the two-phase regression model. J. Appl. Meteorol. Climatol. 26: 1401–1405, https://doi.org/10.1175/1520-0450(1987)026<1401:tfccaa>2.0.co;2.10.1175/1520-0450(1987)026<1401:TFCCAA>2.0.CO;2Suche in Google Scholar

Speakman, J.R. (2005). Body size, energy metabolism and lifespan. J. Exp. Biol. 208: 1717–1730, https://doi.org/10.1242/jeb.01556.Suche in Google Scholar PubMed

Speakman, J.R. and Rowland, A. (1999). Preparing for inactivity: how insectivorous bats deposit a fat store for hibernation. Proc. Nutr. Soc. 58: 123–131, https://doi.org/10.1079/pns19990017.Suche in Google Scholar PubMed

Speakman, J.R. and Thomas, D.W. (2003). Physiological ecology and energetics of bats. In: Kunz, T.H. and Brock-Fenton, M. (Eds.), Bat ecology. University of Chicago Press, Chicago, pp. 430–490.Suche in Google Scholar

Steinlechner, S., Heldmaier, G., and Becker, H. (1983). The seasonal cycle of body weight in the Djungarian hamster: photoperiodic control and the influence of starvation and melatonin. Oecologia 60: 401–405, https://doi.org/10.1007/bf00376859.Suche in Google Scholar PubMed

Terrien, J., Perret, M., and Aujard, F. (2011). Behavioral thermoregulation in mammals: a review. Front. Biosci. 16: 1428–1444, https://doi.org/10.2741/3797.Suche in Google Scholar PubMed

Villers, R.L., Rojas, F., and Tenorio, P. (2006). Guía botánica del Parque Nacional Malinche, Tlaxcala-Puebla. Universidad Nacional Autónoma de México, Mexico.Suche in Google Scholar

Voigt, C.C., Schneeberger, K., Voigt-Heucke, S.L., and Lewanzik, D. (2011). Rain increases the energy cost of bat flight. Biol. Lett. 7: 793–795, https://doi.org/10.1098/rsbl.2011.0313.Suche in Google Scholar PubMed PubMed Central

Wade, G.N. and Bartness, T.J. (1984). Effects of photoperiod and gonadectomy on food intake, body weight, and body composition in Siberian hamsters. Am. J. Physiol. 246: R26–R30, https://doi.org/10.1152/ajpregu.1984.246.1.r26.Suche in Google Scholar

Walther, B. and Gosler, A. (2001). The effects of food availability and distance to protective cover on the winter foraging behaviour of tits (Aves: Parus). Oecologia 129: 312–320, https://doi.org/10.1007/s004420100713.Suche in Google Scholar PubMed

Whitaker, J.O. and Gummer, S.L. (1992). Hibernation of the big brown bat, Eptesicus fuscus, in buildings. J. Mammal. 73: 312–316, https://doi.org/10.2307/1382062.Suche in Google Scholar

Wolf, L.K. (2020). Modeling the spread of Pseudogymnoascus destructans in Texas and Mexican karst regions. Master’s thesis. College Station, Texas A&M University.Suche in Google Scholar

Xue, Y., Tanaka, K., Yu, H., Chen, Y., Guan, L., Li, Z., Yu, H., Xu, B., Ren, Y., and Wan, R. (2018). Using a new framework of two-phase generalized additive models to incorporate prey abundance in spatial distribution models of juvenile slender lizardfish in Haizhou Bay, China. Mar. Biol. Res. 14: 508–523, https://doi.org/10.1080/17451000.2018.1447673.Suche in Google Scholar

Zhu, W.L., Jia, T., Lian, X., and Wang, Z.K. (2008). Evaporative water loss and energy metabolic in two small mammals, voles (Eothenomys miletus) and mice (Apodemus chevrieri), in Hengduan mountains region. J. Therm. Biol. 33: 324–331, https://doi.org/10.1016/j.jtherbio.2008.04.002.Suche in Google Scholar

Zhu, W.L., Jia, T., Cai, J.H., Xiao, L., and Wang, Z.K. (2012a). The effect of cold-acclimation on energy strategies of Apodemus draco in Hengduan Mountain region. J. Therm. Biol. 37: 41–46, https://doi.org/10.1016/j.jtherbio.2011.10.008.Suche in Google Scholar

Zhu, W.L., Zhang, H., and Wang, Z.K. (2012b). Seasonal changes in body mass and thermogenesis in tree shrews (Tupaia belangeri): the roles of photoperiod and cold. J. Therm. Biol. 37: 479–484, https://doi.org/10.1016/j.jtherbio.2012.04.007.Suche in Google Scholar


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/mammalia-2022-0031).


Received: 2022-03-11
Accepted: 2022-11-17
Published Online: 2022-12-05
Published in Print: 2023-03-28

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