Mammalian Biology

, Volume 81, Issue 6, pp 623–627 | Cite as

Tracking the origin of the smearing behavior in long-nosed bats (Leptonycteris spp.)

  • Jafet M. Nassar
  • Rubén Galicia
  • Ana Ibarra
  • Rodrigo A. MedellinEmail author
Original investigation


A unique and novel stereotypic ‘smearing’ behavior and the formation of an odoriferous dorsal patch have been recently described in two species of long-nosed bats, Leptonycteris curasoae and L. yerbabuenae (Glossophaginae: Phyllostomidae). It has been hypothesized that this structure represents a mechanism involved in female mate choice mediated through odor, and that it has only evolved within the genus Leptonycteris. No evidence has been published indicating whether the smearing behavior and the dorsal patch occur in L. nivalis, the third extant species within the genus. We reviewed the available data on the mating behavior of L. nivalis and conducted four surveys on the only mating colony known for this species at Cueva del Diablo, Tepoztlan, Morelos, Mexico, searching for evidence of both the smearing behavior and the dorsal patch in reproductive males of this species. Our findings indicate that L. nivalis does not display the smearing behavior or the dorsal patch, suggesting that this trait and its role in mate choice by females must have evolved from a common ancestor of L. yerbabuenae and L. curasoae after it separated from L. nivalis, between 1.0 and 0.5 million years ago. We propose a possible hypothetical scenario for the evolution of the smearing behavior, based on differential levels of ectoparasitic pressure acting on bat populations established at locations with markedly different environmental temperatures.


Behavior Dorsal patch Ectoparasites Leptonycteris nivalis Odor signals Sexual selection 


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  1. Arita, H.T., 1991. Spatial segregation in long-nosed bats, Leptonycteris nivalis and Leptonycteris curasoae, in Mexico. J. Mammal. 72, 706–714.CrossRefGoogle Scholar
  2. Arroyo-Cabrales, J., Polaco, O.J., 2003. Caves and the Pleistocene vertebrate paleontology of Mexico. In: Schubert, B.W., Mead, J.I., Graham, R.W. (Eds.), Studies of Vertebrate Cave Life During the North American Ice Age. Indiana University Press, Indiana, pp. 273–291.Google Scholar
  3. Axelrod, D.I., 1979. Age and origin of the Sonoran desert vegetation. Occas. Pap. Calif. Acad. Sci. 132, 1–74.Google Scholar
  4. Ayala-Berdon, J., Galicia, R., Flores-Ortíz, C., Medellín, R., Schondube, J.E., 2013. Digestive capacities allow the Mexican long-nosed bat (Leptonycteris nivalis) to live in cold environments. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 164, 622–628.CrossRefGoogle Scholar
  5. Bordes, F., Morand, S., Ricardo, G., 2008. Bat fly species richness in Neotropical bats: correlations with host ecology and host brain. Oecologia 158, 109–116.CrossRefGoogle Scholar
  6. Brown, CM., 2008. Natural History and Population Genetics of the Endangered Mexican Long-Nosed Bat, Leptonycteris nivalis (Chiroptera: Phyllostomidae). Master Thesis. Angelo State University, US, 64 pps.Google Scholar
  7. Caballero-Martínez, LA., 2004. Observaciones sobre la conducta reproductiva de Leptonycteris nivalis (Chiroptera: Phyllostomidae) enTepoztlán, Morelos, México. Licenciatura Thesis. Facultad de Ciencias, UAEM, Mexico, 118 pps.Google Scholar
  8. Ceballos, G., Fleming, T.H., Chávez, C., Nassar, J.M., 1997. Population dynamics of Leptonycteris curasoae (Chiroptera: Phyllostomidae) in Jalisco, Mexico. J. Mammal. 78, 1220–1230.CrossRefGoogle Scholar
  9. Christe, P., Arlettaz, R., Vogel, P., 2000. Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol. Lett. 3, 212–307.CrossRefGoogle Scholar
  10. Cole, F.R., Wilson, D.E., 2006. Leptonycteris yerbabuenae. Mammal. Species 797, 1–7.CrossRefGoogle Scholar
  11. Gray, J.S., Dautel, H., Estrada-Peña, A., Kahl, O., Lindgren, E., 2009. Effects of climate change on ticks and tick-borne diseases in Europe. Interdiscip. Perspect. Infect. Dis., Scholar
  12. Hensley, A.P., Wilkins, K.T., 1988. Leptonycteris nivalis. Mammal. Species 307, 1–4.CrossRefGoogle Scholar
  13. Hoffman, A., Palacios-Vargas, J.G., Morales-Malacara, J.B., 1986. Manual de Bioespeleología (Con nuevas aportaciones de Morelos y Guerrero, México), 2nd ed. UNAM, Mexico.Google Scholar
  14. IUCN, 2016. IUCN Red List, (accessed 05.03.16. López-Segurajáuregui, G., Toledo-Gutiérrez, K., Medellín, R.A., 2006. Cueva del Diablo: a Bat cave inTepoztlán. AMCS Bull. 19/SMES Bol. 7, 264–270.
  15. Lourenco, S., Palmeirim, J.M., 2008. Which factors regulate the reproduction of ectoparasites of temperate-zone cave-dwelling bats? Parasitol. Res. 104, 127–134.Google Scholar
  16. Marshall, A.G., 1982. Ecology of ectoparasitic insects on bats. In: Kunz, T.H. (Ed.), Ecology of Bats. Plenum Publishing Corporation, New York, London, pp. 369–399.CrossRefGoogle Scholar
  17. Merino, S., Potti, J., 1996. Weather dependent effects of nest ectoparasites on their bird hosts. Ecography 19, 107–113.CrossRefGoogle Scholar
  18. Moreno-Valdéz, A., Honeycutt, R.L., Grant, W.E., 2004. Colony dynamics of Leptonycteris nivalis (Mexican long-nosed bat) related to flowering Agave in northern Mexico. J. Mammal. 85, 453–459.CrossRefGoogle Scholar
  19. Muñoz-Romo, M., Kunz, T.H., 2009. Dorsal patch and chemical signaling in males of the long-nosed bat, Leptonycteris curasoae (Chiroptera: Phyllostomidae). J. Mammal. 90, 1139–1147.CrossRefGoogle Scholar
  20. Muñoz-Romo, M., Burgos, J.F., Kunz, T.H., 2011a. Smearing behaviour of male Leptonycteris curasoae (Chiroptera) and female responses to the odour of dorsal patches. Behaviour 148, 461–483.CrossRefGoogle Scholar
  21. Muñoz-Romo, M., Burgos, J.F., Kunz, T.H., 2011b. The dorsal patch of males of the Curañaoan long-nosed bat, Leptonycteris curasoae (Phyllostomidae: Glossophaginae) as a visual signal. Acta Chiropterol. 13, 207–215.CrossRefGoogle Scholar
  22. Muñoz-Romo, M., Nielsen, L.T., Nassar, J.M., Kunz, T.H., 2012. Chemical composition of the substances from dorsal patches of males of the Curañaoan long-nosed bat, Leptonycteris curasoae (Phyllostomidae: Glossophaginae). Acta Chiropterol. 14, 213–224.CrossRefGoogle Scholar
  23. Nassar, J.M., Salazar, M.V., Quintero, A., Stoner, K.E., Gómez, M., Cabrera, A., Jaffe, K., 2008. Seasonal sebaceous patch in the nectar-feeding bats Leptonycteris curasoae and L. yerbabuenae (Phyllostomidae: Glossophaginae): phenological, histological, and preliminary chemical characterization. Zoology 111, 363–376.PubMedGoogle Scholar
  24. Patterson, D.B., Dick, W.C., Dittmar, K., 2007. Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae).J. Trop. Ecol. 23, 177–189.CrossRefGoogle Scholar
  25. Pilosof, S., Dick, C.W., Korine, C., Patterson, B.D., Krasnov, B.R., 2012. Effects of anthropogenic disturbance and climate on patterns of bat fly parasitism. PLoS One 7, e41487.CrossRefGoogle Scholar
  26. Reid, F.R., 1997. A Field Guide to the Mammals of Central America and Southeast Mexico. Oxford University Press, New York.Google Scholar
  27. Rincón-Vargas, F., Stoner, K.E., Vigueras-Villaseñor, R.M., Nassar, J.M., Cháves, O.M., Hudson, R., 2013. Internal and external indicators of the male reproductive cycle in the long-nosed bat Leptonycteris yerbabuenae. J. Mammal. 94, 488–496.CrossRefGoogle Scholar
  28. Schad, J., Dechmann, D.K.N., Voigt, C.C., Sommer, S., 2012. Evidence for the ‘good genes’ model: association of MHC class II DRB alleles with ectoparasitism and reproductive state in the neotropical lesser bulldog bat, Noctilio albiventris. PLoS One, 7, Scholar
  29. SEMARNAT, 2010. Norma Oficial Mexicana NOM-059-SEMARNAT-2010. (2010). Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. Diario Oficial de la Federación 30/12/2010.Google Scholar
  30. Stoner, K.E., Salazar, K.A.O., Fernández, R.C.R., Quesada, M., 2003. Population dynamics, reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation. Biodivers. Conserv. 12, 357–373.CrossRefGoogle Scholar
  31. Téllez, J.G., 2001. Migración de los murciélagos-hocicudos (Leptonycteris) en el trópico mexicano. Tesis de licenciatura para obtener el grado de Biólogo. Universidad Nacional Autónoma de México (UNAM), 146 pps.Google Scholar
  32. Tlapaya-Romero, L., Horvath, A., Gallina-Tessaro, S., Naranjo, E.J., Gómez, B., 2015. Prevalencia y abundancia de moscas parásitas asociadas a una comunidad de murciélagos cavernícolas en La Trinitaria, Chiapas, Mexico. Rev. Mex. Biodivers. 86, 377–385.CrossRefGoogle Scholar
  33. Toledo-Gutiérrez, K.P., 2009. Hábitos reproductivos del murciélago magueyero mayor Leptonycteris nivalis (Chiroptera: Phyllostomidae) en la Cueva del Diablo, Tepoztlán, Morelos, México. Licenciatura Thesis. Universidad Nacional Auntónoma de México, Mexico.Google Scholar
  34. U.S. Fish and Wildlife Service, 1994. Plan de recuperación del murciélago magueyero (Leptonycteris nivalis). Albuquerque, Nuevo México.Google Scholar
  35. Villa-R, B., 1967. Los murciélagos de México. Instituto de Biología, Universidad Nacional Autónoma de México, Mexico.Google Scholar
  36. Wilkinson, G.S., Fleming, T.H., 1996. Migration and evolution of lesser long-nosed bats Leptonycteris curasoae: inferred from mitochondrial DNA. Mol. Ecol. 5, 329–339.CrossRefGoogle Scholar
  37. Wilson, D.E., Medellín, R.A., Lanning, D.V., Arita, H.T., 1985. Los murciélagos del noreste de México, con una lista de especies. Acta Zool. Mex. (Nueva serie) 8, 1–26.Google Scholar
  38. ter Hofstede, H.M., Fenton, M.B., 2005. Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. J. Zool. (London) 266, 333–340.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2016

Authors and Affiliations

  • Jafet M. Nassar
    • 1
  • Rubén Galicia
    • 2
  • Ana Ibarra
    • 2
  • Rodrigo A. Medellin
    • 2
    Email author
  1. 1.Centro de EcologíaInstituto Venezolano de Investigaciones CientíficasCaracasVenezuela
  2. 2.Instituto de EcologíaUNAMMexico

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