Aplicaciones del monitoreo acústico activo y pasivo para conservación de primates neotropicales
DOI:
https://doi.org/10.62015/np.2023.v29.784Keywords:
Bioacoustics, conservation technology, soundscapes, wildlife monitoringAbstract
Most Neotropical primates are very vocal, and many species use long–distance calls for intra– and inter–group communication. The use of field methods based on acoustic signaling holds promise for Neotropical primate population studies when combined with remote sampling techniques. However, if assumptions are not met, these methods may be ineffective or provide misleading results. We will address the use of passive and active acoustic monitoring (playback) for the survey and monitoring of primate populations. We discuss the suitability of each method in terms of the target species and project objectives, data analysis approaches, team considerations, research design, and other factors affecting primate detection in the field.
References
Blumstein, D. T., Mennill, D. J., Clemins, P., Girod, L., Yao, K., Patricelli, G., Deppe, J. L., Krakauer, Clark, C., Cortopass, K. A., Hanser, S. F., McCowan, B., Ali, A. M. y Kirschel, A. N. G. 2011. Acoustic monitoring in terrestrial environments using microphone arrays: Applications, technological considerations and prospectus. J. Appl. Ecol. 48: 758–767. https://doi.org/10.1111/j.1365-2664.2011.01993.x.
Buckland, S. T., Plumptre, A. J., Thomas, L. y Rexstad, E. A. 2010. Design and analysis of line transect surveys for primates. Int. J. Primatol. 31: 833–847. https://doi.org/10.1007/s10764-010-9431-5.
Buckland, S. T., Rexstad, E. A., Marques, T. A. y Oedeko- ven, C. S. 2015. Distance sampling: Methods and applications, Vol. 431. Springer, Nueva York.
Buckland, S. T., Summers, R. W., Borchers, D. L. y Tho- mas, L. 2006. Point transect sampling with traps or lures. J. Appl. Ecol. 43(2): 377–384. https://www.jstor.org/stable/3505930.
Campbell, G., Head, J., Junker, J., Nekaris, K. A. I., Wich, S. y Marshall, A. 2016. Primate abundance and distribution: Background concepts and methods. In: An Introduction to Primate Conservation. S. A. Wich, A. J. Marshall (eds.) pp.79–110.
Caselli, C. B., Ayres, P. H. B., Castro, S. C. N., Souto, A., Schiel, N. y Miller, C. T. 2018a. The role of extragroup encounters in a neotropical, cooperative breeding primate, the common marmoset: A field playback experiment. Anim. Behav. 136: 137–146. https://doi.org/10.1016/j.anbehav.2017.12.009.
Caselli, C. B., Romano, V., Ruiz–Miranda, C. R. y da Cunha, R. G. T. 2018b. Las voces de los primates neo- tropicales:¿ qué dicen? En: La Primatología en Latinoa- mérica 2 – A Primatologia na America Latina 2. Tomo I Argentina–Colombia., B. Urbani, M. Kowalewski, R. G. T. Cunha, S. de la Torre y L. Cortés–Ortiz (eds.), pp.267–281. Ediciones Instituto Venezolano de Investigaciones Científicas (IVIC), Caracas.
Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, Escocia, Website: https://www.creem.st–andrews.ac.uk/distance–sampling–methods/.
Cleveland, J. y Snowdon, C. T. 1982. The complex vocal repertoire of the adult cotton–top tamarin (Saguinus oedipus oedipus). Z. Tierpsychol. 58: 231–270. https://doi.org/10.1111/j.1439-0310.1982.tb00320.x.
Coelho, I. P., Collins, S. J., Santos Junior, E. M., Valença‐ Montenegro, M. M., Jerusalinsky, L. y Alonso, A. C. 2020. Playback point counts and N‐mixture models suggest higher than expected abundance of the critically endangered blond titi monkey in northeastern Brazil. Am. J. Primatol. 82: e23126. https://doi.org/10.1002/ajp.23126.
Costa–Araújo, R., Luis Regolin, A., Martello, F., Pedro Souza–Alves, J., Hrbek, T. y Cezar Ribeiro, M. 2021. Occurrence and conservation of the vulnerable titi monkey Callicebus melanochir in fragmented landscapes of the Atlantic Forest hotspot. Oryx 55: 1–8. https://doi.org/10.1017/S0030605319001522.
de Cunha, R. G. T., de Oliveira, D. A. G., Holzmann, I., and Kitchen, D. M. 2015. Production of loud and quiet calls in howler monkeys. En: Howler Monkeys. Developments in Primatology: Progress and Prospects, M. Kowalewski, P. Garber, L. Cortés–Ortiz, B. Urbani, y D. Youlatos (eds.), pp.337–368. Springer, Nueva York.
Dacier, A., de Luna, A. G., Fernandez–Duque, E. y Di Fiore, A. 2011. Estimating population density of Amazonian titi monkeys (Callicebus discolor) via playback point counts. Biotropica 43(2): 135–140. https://www.jstor.org/stable/41057989.
Dietz, J. M., Hankerson, S. J., Alexandre, B. R., Henry, M. D., Martins, A. F., Ferraz, L. P. y Ruiz–Miranda, C. R. 2019. Yellow fever in Brazil threatens successful recovery of endangered golden lion tamarins. Sci. Rep. 9: 12926. https://doi.org/10.1038/s41598-019-49199-6.
de Morais Jr., M. M. 2005. Metodologias de amostragem de populações: Aplicação e comparação em populações de mico–leão–dourado (Leontopithecus rosalia) e sagüis (Callithrix spp.) na bacia do Rio São João. Tesis de Maestría, Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Rio de Janeiro.
Delgado, R. A. 2006. Sexual selection in the loud calls of male primates: Signal content and function. Int. J. Primatol. 27: 5–25. https://doi.org/10.1007/s10764-005-9001-4.
do Nascimento, L. A., Pérez–Granados, C. y Beard, K. H. 2021. Passive acoustic monitoring and automatic detection of diel patterns and acoustic structure of howler monkey roars. Diversity 13: 566. https://doi.org/10.3390/d13110566.
Enari, H., Enari, H. S., Okuda, K., Maruyama, T. y Oku- da, K. N. 2019. An evaluation of the efficiency of passive acoustic monitoring in detecting deer and primates in comparison with camera traps. Ecol. Indic. 98: 753–762. https://doi.org/10.1016/j.ecolind.2018.11.062.
Fischer, J., Noser, R. y Hammerschmidt, K. 2013. Bioacoustic field research: a primer to acoustic analyses and playback experiments with primates. Am. J. Primatol. 75: 643–63. https://doi.org/10.1002/ajp.22153.
French, J. A., Schaffner, C. M., Shepherd, R. E. y Miller, M. E. 1995. Familiarity with intruders modulates agonism towards outgroup conspecifics in Wied’s black‐tufted‐ear marmoset (Callithrix kuhli: Primates, Callitrichidae). Ethol. 99: 24–38. https://doi.org/10.1111/j.1439-0310.1995.tb01086.x.
Gestich, C. C., Arroyo–Rodríguez, V., Ribeiro, M. C., da Cunha, R. G. T. y Setz, E. Z. F. 2019. Unraveling the scales of effect of landscape structure on primate species richness and density of titi monkeys (Callicebus nigrifrons). Ecol. Res. 34: 150–159. https://doi.org/10.1111/1440-1703.1009.
Gestich, C. C., Caselli, C. B., Nagy‐Reis, M. B., Setz, E. Z. y da Cunha, R. G. 2017. Estimating primate population densities: The systematic use of playbacks along transects in population surveys. Am. J. Primatol. 79: e22586. https://doi.org/10.1002/ajp.22586.
Heinicke, S., Kalan, A. K., Wagner, O. J. J., Mundry, R., Lukashevich, H., Kühl, H. S. y Jones, K. 2015. Assessing the performance of a semi‐automated acoustic monitoring system for primates. Methods Ecol. Evol. 6: 753–763. https://doi.org/10.1111/2041-210X.12384.
Jerusalinsky, L., Oliveira, M. M., Pereira, R. F., Santana, V., Bastos, P. C. R. y Ferrari, S. F. 2006. Preliminary evaluation of the conservation status of Callicebus coimbrai Kobayashi and Langguth, 1999 in the Brazilian state of Sergipe. Primate Conserv. 2006(21): 25–32. https://doi.org/10.1896/0898-6207.21.1.25.
Kalan, A. K., Mundry, R., Wagner, O. J. J., Heinicke, S., Boesch, C. y Kühl, H. S. 2015. Towards the automated detection and occupancy estimation of primates using passive acoustic monitoring. Ecol. Indic. 54: 217–226. https://doi.org/10.1016/j.ecolind.2015.02.02.
Kiffner, C., Waltert, M., Meyer, B. y Mühlenberg, M. 2008. Response of lions (Panthera leo Linnaeus 1758) and spotted hyaenas (Crocuta crocuta Erxleben 1777) to sound playbacks. Afr. J. Ecol. 46: 223–226. https://doi.org/10.1111/j.1365-2028.2007.00813.x.
Kierulff, M. C. M. y Rylands, A. B. 2003. Census and distribution of the golden lion tamarin (Leontopithecus rosalia). Am. J. Primatol. 59: 29–44. https://doi.org/10.1002/ajp.10064.
Kirchhof, J. y Hammerschmidt, K. 2006. Functionally referential alarm calls in tamarins (Saguinus fuscicollis and Saguinus mystax): evidence from playback experiments. Ethol. 112: 346–354. https://doi.org/10.1111/j.1439-0310.2006.01165.x.
Lima, N. B. 2012. Análise da estrutura acústica do chamado longo de duas frases do mico leão dourado (Leontopithecus rosalia) selvagem para obtenção de informações sobre sexo, região e indivíduo. Tesis de Maestría, Ecologia e Recursos Naturais, Universidade Estadual do Norte Fluminense, Rio de Janeiro.
MacKenzie, D. I. 2012. Presence user manual. Dunedin, New Zealand: Proteus Wildlife Research Consultants.
Marques, T. A., Thomas, L., Martin, S. W., Mellinger, D. K., Ward, J. A., Moretti, D. J., Harris, D. y Tyack, P. L. 2013. Estimating animal population density using passive acoustics. Biol. Rev. Camb. Philos. Soc. 88: 287–309. https://doi.org/10.1111/brv.12001.
McConnell, P. B. y Snowdon, C. T. 1986. Vocal interactions between unfamiliar groups of captive cotton-top tamarins. Behaviour 97: 273–296. https://www.jstor.org/stable/4534532.
Ogutu, J. y Dublin, H. 1998. The response of lions and spotted hyaenas to sound playbacks as a technique for estimating population size. Afr. J. Ecol. 36: 83–95. https://doi.org/10.1046/j.1365-2028.1998.113-89113.x.
Perez–Granados, C. y Schuchmann, K. L. 2021. Passive acoustic monitoring of the diel and annual vocal behavior of the black and gold howler monkey. Am. J. Pri- matol. 83: e23241. https://doi.org/10.1002/ajp.23241.
Robinson, J. G. 1979a. An analysis of the organization of vocal communication in the titi monkey Callicebus moloch. Z. Tierpsychol. 49: 381–405. https://doi.org/10.1111/j.1439-0310.1979.tb00300.x.
Robinson, J. G. 1979b. Vocal regulation of use of space by groups of titi monkeys Callicebus moloch. Behav. Ecol. Sociobiol. 5: 1–15. https://doi.org/10.1007/BF00302691.
Robinson, J. G. 1982. Vocal systems regulating within–group spacing. In: Primate communication, C. T. Snowdon, C. H. Brown y M. Peterson (eds.), pp.94–116. Cambridge University Press, Cambridge.
Robinson, J. G., Wright, P. C. y Kinzey, W. G. 1987. Monogamous cebids and their relatives: Intergroup calls and spacing. En: Primate Societies, T. T. Struhsaker (ed.), pp.44–53. University of Chicago Press, Chicago.
Ruiz–Miranda, C. R., de Morais, M. M., Jr., Dietz, L. A., Rocha Alexandre, B., Martins, A. F., Ferraz, L. P., Mickelberg, J., Handerson, S. J., Dietz y J. M. 2019. Estimating population sizes to evaluate progress in conservation of endangered golden lion tamarins (Leontopithecus rosalia). PloS ONE 14(6): e0216664. https://doi.org/10.1371/journal.pone.0216664.
Sabatini, V., Ruiz–Miranda, C. R. y Dabelsteen, T. 2011. Degradation characteristics of golden lion tamarin Leontopithecus rosalia two–phrase long calls: implications for call detection and ranging in the evergreen forest. Bioacoustics 20: 137–158. https://doi.org/10.1080/09524622.2011.9753640.
Sabatini, V. y Ruiz Miranda, C. R. 2008. Acoustical aspects of the propagation of long calls of wild Leontopithecus rosalia. Int. J. Primatol. 29: 207–223. https://doi.org/10.1007/s10764-008-9240-2.
Salcedo A. R., Mejia, M., Slocombe, K., y Papworth, S. 2014. Two case studies using playbacks to census Neotropical primates: Callicebus discolor and Alouatta palliata aequatorialis. Neotrop. Primates 21: 200–204. https://doi.org/10.1896/044.021.0209.
Savage, A., Thomas, L., Feilen, K. L., Kidney, D., Soto, L. H., Pearson, M., Medina, F. S., Emeris, G., Guillen y R. R. 2016. An assessment of the population of cotton–top tamarins (Saguinus oedipus) and their habitat in Colombia. PloS ONE 11: e0168324. https://doi.org/10.1371/journal.pone.0168324.
Savage, A., Thomas, L., Leighty, K. A., Soto, L. H. y Medina, F. S. 2010. Novel survey method finds dramatic decline of wild cotton–top tamarin population. Nat. Commun. 1: 30. https://doi.org/10.1038/ncomms1030.
Snowdon, C. T. 1989. Vocal communication in New World monkeys. J. Hum. Evol. 18: 611–633. https://doi.org/10.1016/0047-2484(89)90097-3.
Whitby, M. D., Carter, T. C., Britzke, E. R. y Bergeson, S. M. 2014. Evaluation of mobile acoustic techniques for bat population monitoring. Acta Chiropt. 16: 223–230. https://doi.org/10.3161/150811014X683417.
Downloads
Published
Issue
Section
License
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
