Calling for the future of conservation: a protocol for passive acoustic monitoring of small arboreal primates
DOI:
https://doi.org/10.32673/bjm.vie92.122Keywords:
Acoustic communication, Biodiversity monitoring, Remote recorders, Species detectionAbstract
Biodiversity conservation faces challenges due to a lack of accurate information on species occurrence. Various techniques have been used to survey species diversity and estimate population density, but monitoring species over large spatial and temporal scales remains challenging. Passive acoustic monitoring (PAM) has emerged as a cost-effective and non-invasive method for monitoring biodiversity. PAM utilizes autonomous recording units (ARUs) installed in different areas and is particularly relevant for monitoring threatened species in tropical forest regions. In the case of non-human primates, PAM has proven effective in detecting endangered species, monitoring populations, studying vocal behavior, and evaluating territory use. The black lion tamarin (Leontopithecus chrysopygus), an endangered species of the Atlantic Forest, relies on acoustic signals for communication. This study proposes a PAM protocol for monitoring arboreal primates using the black lion tamarin as a model. It reviews PAM's use in primate research and emphasizes defining target vocalizations. We recommend optimal recording conditions, including distance, height, and equipment. Recordings should be positioned high above the ground, considering the arboreal nature of primates. The choice of spatial distribution, including random placement, transects, and grids, depends on the research question and objectives. Lastly, the study addresses the recording schedule, considering periods of greater species activity, such as from sunrise to sunset. In summary, this study highlights PAM's potential for monitoring arboreal primates providing recommendations for vocalizations, recording conditions, equipment, spatial distribution, and schedules, contributing to effective monitoring, and supporting conservation efforts in tropical forests.
References
Aide TM, Corrada-Bravo C, Campos-Cerqueira M, Milan C, Vega G, Alvarez R. 2013. Real-time bioacoustics monitoring and automated species identification. PeerJ 1: e103. https://doi.org/10.7717/peerj.103.
Altmann SA. 1967. Social communication among primates. University of Chicago Press, Chicago.
Bastos M, Souto A, Jones G, Eason P, Bione C, Schiel N, Bezerra B. 2015. Vocal repertoire of wild blonde capuchins (Sapajus flavius) and contextual use of calls. American Journal of Primatology 77(6): 605-617. https://doi.org/10.1002/ajp.22384.
Bezerra BM, Souto A. 2008. Structure and usage of the vocal repertoire of Callithrix jacchus. International Journal of Primatology 29(3): 671-701. https://doi.org/10.1007/s10764-008-9250-0.
Buxton RT, Lendrum PE, Crooks KR, Wittemyer, G. 2018. Pairing camera traps and acoustic recorders to monitor the ecological impact of human disturbance. Global Ecology and Conservation 16: e00493. https://doi.org/10.1016/j.gecco.2018.e00493.
Campos-Cerqueira M, Aide, TM. 2016. Improving distribution data of threatened species by combining acoustic monitoring and occupancy modelling. Methods in Ecology and Evolution 7(11): 1340-1348. https://doi.org/10.1111/2041-210X.12599.
Cullen Jr L, Rudran R. 2009. Transectos lineares na estimativa de densidade de mamíferos e aves de médio e grande porte. Pp. 169-179, In: Cullen LJr, Rudran R, Valladares-Padua C (Orgs.), Métodos de estudos em biologia da conservação e manejo da vida silvestre. Editora UFPR, Curitiba.
Enari H, Enari HS, Okuda K, Maruyama T, Okuda KN. 2019. An evaluation of the efficiency of passive acoustic monitoring in detecting deer and primates in comparison with camera traps. Ecological Indicators 98: 753-762. https://doi.org/10.1016/j.ecolind.2018.11.062.
Heinicke S, Kalan AK, Wagner OJ, Mundry R, Lukashevich H, Kühl HS. 2015. Assessing the performance of a semi-automated acoustic monitoring system for primates. Methods in Ecology and Evolution 6: 753-763. https://doi.org/10.1111/2041-210X.12384.
Kalan AK, Mundry R, Wagner OJ, Heinicke S, Boesch C, Kühl HS. 2015. Towards the automated detection and occupancy estimation of primates using passive acoustic monitoring. Ecological Indicators 54: 217-226. https://doi.org/10.1016/j.ecolind.2015.02.023.
Kalan AK, Piel AK, Mundry R, Wittig RM, Boesch C, Kühl HS. 2016. Passive acoustic monitoring reveals group ranging and territory use: a case study of wild chimpanzees (Pan troglodytes). Frontiers in Zoology 13(1): 1-11. https://doi.org/10.1186/s12983-016-0167-8.
Kleiman DG, Hoage RJ, Green KM. 1988. The lion tamarins, genus Leontopithecus. Pp. 299-347, In Mittermeier RA, Rylands AB, Coimbra-Filho AF, Fonseca GAB (Eds.), Ecology and behaviour of neotropical primates. World Wildlife Fund, Washington.
K. Lisa Yang Center for Conservation Bioacoustics at the Cornell Lab of Ornithology. 2023. Raven Pro: Interactive Sound Analysis Software (Version 1.6.4). The Cornell Lab of Ornithology, Ithaca, NY. Available from https://ravensoundsoftware.com/.
Lisboa CA, Mendes FDC, Silveira M, Aguiar LMS. 2021. The vocal repertoire of the bearded capuchin (Cebidae: Sapajus libidinosus): implications for understanding the complexity of neotropical primate communication. Folia Primatologica 92(3): 151-163. https://doi.org/10.1159/000517917.
Lobão-Cruz E. 2009. Estrutura e uso do repertório vocal de Leontopithecus chrysomelas (Primates: Callitrichidae) em cativeiro. Master's thesis in Animal Biology, Program in Animal Biology, Federal University of Pernambuco, Brazil.
Lomolino MV. 2004. Conservation biogeography. Pp. 293-296, In Lomolino MV, Heaney LR (Eds.), Frontiers of Biogeography: new directions in the geography of nature. Sunderland, MA: Sinauer.
Magurran AE. 2004. Measuring biological diversity. Blackwell, Maldan, MA.
Mendes SL, Vielliard JME, Marco P. 2009. The vocal identity of the Callithrix species (Primates, Callitrichidae). Pp. 63-84 In The smallest anthropoids (pp. 63-84). Springer.
Nascimento et al., 2021
Oliveira DAG, Ades C. 2004. Long-distance calls in Neotropical primates. Anais da Academia Brasileira de Ciências 76(2): 393-398. https://doi.org/10.1590/S0001-37652004000200031.
Pardini R, Ditt EH, Cullen L Jr, Bassi C, Rudran R. 2009. Levantamento rápido de mamíferos terrestres de médio e grande porte. Pp. 181-201, In: Cullen L Jr, Rudran R, Valladares-Padua C (Orgs.), Métodos de estudos em biologia da conservação e manejo da vida silvestre. Editora UFPR, Curitiba.
Pérez-Granados C, Schuchmann KL. 2021. Passive acoustic monitoring of the diel and annual vocal behavior of the Black and Gold Howler Monkey. American Journal of Primatology 83(3): e23241. https://doi.org/10.1002/ajp.23241.
Rezende G, Knogge C, Passos F, Ludwig G, Oliveira LC, Jerusalinsky L, Mittermeier RA. 2020. Leontopithecus chrysopygus. The IUCN Red List of Threatened Species 2020, e.T11505A17935400.
Ruiz-Miranda CR, Archer CA, Kleiman DG. 2002. Acoustic differences between spontaneous and induced long calls of golden lion tamarins, Leontopithecus rosalia. Folia primatologica 73(2-3): 124-131. 10.1159/000064791.
Sabatini V, Ruiz-Miranda CR. 2008. Acoustical aspects of the propagation of long calls of wild Leontopithecus rosalia. International Journal of Primatology 29: 207-223. https://doi.org/10.1007/s10764-008-9240-2.
Scarpelli MD, Ribeiro MC, Teixeira FZ, Young RJ, Teixeira CP. (2020). Gaps in terrestrial soundscape research: it's time to focus on tropical wildlife. Science of the Total Environment 707: 135403. https://doi.org/10.1016/j.scitotenv.2019.135403.
Snowdon CT. 1993. A vocal taxonomy of the callitrichids. In: Rylands AB (Ed.), Marmosets and tamarins: systematics, behaviour, and ecology. Oxford University Press, Oxford.
Sugai LSM, Silva TSF, Ribeiro JW Jr, Llusia D. 2019a. Terrestrial passive acoustic monitoring: review and perspectives. BioScience 69(1): 15-25. https://doi.org/10.1093/biosci/biy147.
Sugai LSM, Desjonquères C, Silva TSF, Llusia D. 2019b. A roadmap for survey designs in terrestrial acoustic monitoring. Remote Sensing in Ecology and Conservation 6: 220-235. https://doi.org/10.1002/rse2.131.
Teixeira-Cunha RG, Byrne RW. 2009. The use of vocal communication in keeping the spatial cohesion of groups: intentionality and specific functions. Pp. 341-363, In: South American Primates. Springer, New York.
Teixeira-Cunha RG, Oliveira DAG, Holzmann I, Kitchen DM. 2015. Production of loud and quiet calls in Howler Monkeys. Pp. 337-368, In: Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (Eds.), Howler monkeys: adaptive radiation, systematics, and morphology. Springer, New York
Vu TT, Tran LM. 2019. An application of autonomous recorders for gibbon monitoring. International Journal of Primatology 40(2): 169-186. https://doi.org/10.1007/s10764-018-0073-3.
Whitehead JM. 1995. Vox Alouattinae: A Preliminary Survey of the Acoustic Characteristics of Long-Distance Calls of Howling Monkeys. International Journal of Primatology 16(1): 121-144. https://doi.org/10.1007/BF02700156.
Whittaker RJ, Araújo MB, Jepson P, Ladle RJ, Watson JE, Willis KJ. 2005. Conservation biogeography: assessment and prospect. Diversity and distributions 11(1): 3-23. https://doi.org/10.1111/j.1366-9516.2005.00143.x.
Wrege PH, Rowland ED, Keen S, Shiu Y. 2017. Acoustic monitoring for conservation in tropical forests: examples from forest elephants. Methods in Ecology and Evolution 8(10): 1292-1301. https://doi.org/10.1111/2041-210X.12730.
Zambolli AH, Manzano MCR, Honda LK, Rezende GC, Culot L. 2022. Performance of autonomous recorders to detect a cryptic and endangered primate species, the black lion-tamarin (Leontopithecus chrysopygus). American Journal of Primatology 85: e23454. https://doi.org/10.1002/ajp.23454.
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