The crust of a male: does size matter when females are fertile?

Abstract

Mammalian odors are frequently sexually dimorphic, with males often exhibiting a stronger, or otherwise distinct, odor relative to females, which can be especially useful for nocturnal species with reduced use of vision. Some male bats exhibit intense odors to attract females and reproduce, presumably as a consequence of a high concentration of testosterone. This usually coincides with the fertile period of females, which can be difficult to recognize visually because female mammals rarely advertise their precise reproductive condition. Recently, a novel odorous crust was discovered on the forearms of adult male fringe-lipped bats, Trachops cirrhosus. To understand its reproductive significance, we explored potential relationships between the size of the crust and testosterone concentration, testes size, female reproductive state, ectoparasite load, and body condition. We sampled bats during the mating season and determined crust size, testosterone concentration (plasma), testes volume, precise reproductive status of females (vaginal smears), body condition (ratio of body mass and forearm length), and ectoparasite load. Crust size (0–38 mm2) was positively correlated both to testosterone concentration (0.7–36.4 ng mL−1) and to relative testes volume (6.3–349.1 mm3). During the sampling period, vaginal smears confirmed that all females were in estrus. Ectoparasite load in males was significantly lower than in females, although both sexes were in similar body condition. Our results suggest that testosterone concentration is a key factor in the exhibition of a larger crust and presumably a stronger odorous signal to estrus females during the reproductive season.

Significance statement

Male secondary sexual characteristics are critical for attracting females for mating. Male odor, in particular, can be indispensable in nocturnal species, as visual signals may lose their effectiveness under dark conditions. The most important male hormone, testosterone, increases the development of male exclusive traits, including odors. In the Neotropics, reproductive male fringe-lipped bats exhibit large odorous crusts on their forearms. The largest male crusts correspond with the highest concentration of testosterone, a relationship we find in the mating season, when vaginal smears confirm females are fertile. We also show that males with crusts have low ectoparasite loads. Our results suggest that the male crust could potentially reveal critical information. Our research highlights the significance of testosterone in the expression of male exclusive traits.

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Acknowledgments

For their invaluable field assistance, we thank Gregg Cohen, Nikolaj Meyer, Ram Mohan, Marie Guggenberger, Marjorie Dixon, Amanda Savage, Brian Leavell, Amber Litterer, and Dineilys Aparicio. We are grateful for the support and infrastructure of the Smithsonian Tropical Research Institute, in particular the Gamboa Bat Lab. We thank Ioana Chiver (Smithsonian Tropical Research Institute), Astolfo Mata (Instituto Venezolano de Investigaciones Científicas), and Rosa De Jesus (Instituto de Investigaciones Científicas y Servicios de Alta Tecnología) for their guidance in hormone determination; Carmenza Spadafora and Laura Pineda (Instituto de Investigaciones Científicas y Servicios de Alta Tecnología), and Marta Vargas (STRI-Naos) for allowing us to use laboratory equipment. We thank G. S. Wilkinson, Associate Editor, and two anonymous reviewers for their meticulous reading and their helpful, insightful comments.

Funding

This research was supported by a Smithsonian Tropical Research Institute (STRI) short-term fellowship to MMR, with additional STRI support to cover materials.

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Correspondence to Mariana Muñoz-Romo.

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The research with bats was carried out in accordance with permits from the STRI Institutional Animal Care and Use Committee (IACUC: 2018-0901-2021) and the Panamanian Ministry of the Environment (Ministerio del Ambiente: SE/A-78-18). Procedures were also consistent with the guidelines of the American Society of Mammalogists for the capture, management and care of mammals (Sikes and the Animal Care and Use Committee of the American Society of Mammalogists 2016), and the Association for the Study of Animal Behaviour.

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Muñoz-Romo, M., Flores, V., Ramoni-Perazzi, P. et al. The crust of a male: does size matter when females are fertile?. Behav Ecol Sociobiol 74, 151 (2020). https://doi.org/10.1007/s00265-020-02914-0

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Keywords

  • Odor
  • Testosterone
  • Sexual dimorphism
  • Trachops cirrhosus
  • Mate attraction
  • Chiroptera