Abstract
Many animal species respond less aggressively to calls emitted by neighbors in comparison with strangers, an asymmetry known as the “dear enemy” effect. The adaptive significance of having “dear enemies” would be to minimize defensive costs towards less-threatening individuals (like neighbors). The opposite situation, in which known neighbors become untrustworthy, representing an even greater menace than strangers, is call “nasty neighbor effect”. In addition to these neighbor-stranger discrimination abilities, some species are also capable of recognizing neighbors individually, allowing them to avoid risky encounters based on identity and past experiences, minimizing the probability of losing an encounter. In this study we tested if black-and-gold howler monkey (Alouatta caraya) males can recognize neighbors individually and investigated the nature of long-term relationships under the dear enemy/nasty neighbors hypotheses. We conducted 36 playback experiments on four dominant males in “El Cachapé” reserve, in Argentina. We exposed each male to three different treatments, consisting of roars from: 1- Neighbors from the area of home range overlap, 2- Misplaced neighbors from the opposite side to the area of home range overlap, and 3- Strangers, quantifying eight response variables during each experiment. Our results showed that dominant males recognize neighbors individually (by roaring longer in response to misplaced neighbors), clearly reacting more aggressively to neighbors who violate mutual agreements (like home range boundaries). Also, dominant males displayed a longer roar duration and closer approach to the sound source when hearing roars from strangers, supporting the hypothesis that neighbors are dear enemies in this species. Our results show that neighbor vocal recognition is key to understanding the configuration of areas of collective use and navigation decision in primates and that strangers exert the major threat to group stability in howler monkeys.
Significance statement
Behavioral traits like individual vocal recognition and neighbor-stranger discrimination can help to minimize costs of aggressive interactions, based mostly on familiarity and/or past experiences. We examined the ability of black-and-gold howler monkey males to discriminate between neighbors (known individuals who respect home range boundaries, considered as “dear enemies”), untrustworthy neighbors (known individuals who violate home range boundaries, considered as “nasty neighbors”) and strangers (unknown individuals in search of a home range to settle). Males reacted more aggressively to strangers (roaring for longer and exhibiting closer approach to the sound source), in comparison to neighbors. Males also demonstrated to recognize neighbors individually, reacting differently (roaring for longer) to the same neighbor when acting as untrustworthy. Vocal recognition of long-range vocalizations is a key component of long-term relationships in species that occupy stable home ranges throughout the years, reducing physical interactions and probabilities of getting hurt.
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Data availability
Dataset analyzed in our study is in Table 2 and in the online resource.
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Acknowledgements
We want to extend our gratitude to the Bolo-Bolaño family, the owners from “El Cachapé” private Reserve: Don Eduardo, Santiago, Maru, Emi and Leónidas. Special thanks also to Tati and Cacho. All these people highly contribute to this long-term project. Thanks also to all the field assistants: C. Márques, A. Córdoba, M. Fernández, L. Vivas, S. Benavente, C. Lobo, C. Del Basso and N. Bejarano. Special thanks to C. Bianchi for home ranges spatial analyses and F. Reckziegel for invaluable help with statistical analyses and GLMM model building. We are grateful with our colleagues from the ECOSON lab for valuable suggestions, especially to Nacho Areta, who greatly contribute to the manuscript. Finally, we want to extend our gratitude to both reviewers and the associate editor who contributed with comments and suggestions that highly improved the manuscript.
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This project was carried out with the financial support of FONCyT (PICT 0223–2015), The Leakey Foundation and CONICET.
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IH: Conceptualization, methodology, field data collection, funding acquisition and writing. RSC: Field data collection, data analyses and writing.
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This research complied with the Best Practices for Field Primatology of the International Primatological Society (https://www.asp.org/resources/docs/Code of_Best_Practices Oct 2014.pdf) and adhered to the legal requirements of Argentina. Ethical approval from ethics committee was not required.
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Holzmann, I., Córdoba, R.S. Individual vocal recognition and dear enemy effect in the black-and-gold howler monkey (Alouatta caraya). Behav Ecol Sociobiol 78, 51 (2024). https://doi.org/10.1007/s00265-024-03469-0
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DOI: https://doi.org/10.1007/s00265-024-03469-0