Pairing a user-friendly machine-learning animal sound detector with passive acoustic surveys for occupancy modeling of an endangered primate.

Szczegóły
Abstrakt

Tytuł:: Pairing a user-friendly machine-learning animal sound detector with passive acoustic surveys for occupancy modeling of an endangered primate.
Autorzy:: Wood CM; K. Lisa Yang Center for Conservation Bioacoustics, Cornell Lab of Ornithology, Cornell University, Ithaca, New York, USA.
Barceinas Cruz A; Nelson Institute for Environmental Studies, Department of Geography, University of Wisconsin-Madison, Madison, Wisconsin, USA.; Natura y Ecosistemas Mexicanos AC, Mexico City, Mexico.
Kahl S; K. Lisa Yang Center for Conservation Bioacoustics, Cornell Lab of Ornithology, Cornell University, Ithaca, New York, USA.
Źródło:: American journal of primatology [Am J Primatol] 2023 Aug; Vol. 85 (8), pp. e23507. Date of Electronic Publication: 2023 May 21.
Typ publikacji:: Journal Article
Język:: English
Imprint Name(s):: Publication: New York : Wiley-Blackwell
Original Publication: New York : Liss, c1981-
MeSH Terms:: Conservation of Natural Resources*
Ecosystem*
Animals ; Population Density ; Primates ; Acoustics
References:: Almeida-Rocha, J. M., Peres, C. A., Monsalvo, J. A. B., & Oliveira, L. D. C. (2020). Habitat determinants of golden-headed lion tamarin (Leontopithecus chrysomelas) occupancy of cacao agroforests: Gloomy conservation prospects for management intensification. American Journal of Primatology, 82, e23179.
Arce-Peña, N. P., Arroyo-Rodríguez, V., Dias, P. A. D., Franch-Pardo, I., & Andresen, E. (2019). Linking changes in landscape structure to population changes of an endangered primate. Landscape Ecology, 34, 2687-2701.
Arroyo-Rodríguez, V., González-Perez, I. M., Garmendia, A., Solà, M., & Estrada, A. (2013). The relative impact of forest patch and landscape attributes on black howler monkey populations in the fragmented Lacandona rainforest, Mexico. Landscape Ecology, 28, 1717-1727.
Arroyo-Rodríguez, V., Melo, F. P. L., Martínez-Ramos, M., Bongers, F., Chazdon, R. L., Meave, J. A., Norden, N., Santos, B. A., Leal, I. R., & Tabarelli, M. (2017). Multiple successional pathways in human-modified tropical landscapes: New insights from forest succession, forest fragmentation and landscape ecology research. Biological Reviews, 92, 326-340.
Austin, K. G., González-Roglich, M., Schaffer-Smith, D., Schwantes, A. M., & Swenson, J. J. (2017). Trends in size of tropical deforestation events signal increasing dominance of industrial-scale drivers. Environmental Research Letters, 12, 054009.
Batist, C. H., Razafindraibe, M. N., Randriamanantena, F., & Baden, A. L. (2022). Factors affecting call usage in wild black-and-White ruffed lemurs (Varecia variegata) at Mangevo, Ranomafana National Park. Primates, 63, 79-91.
Van Belle, S., Estrada, A., & Garber, P. A. (2013). Spatial and diurnal distribution of loud calling in Black Howlers (Alouatta pigra). International Journal of Primatology, 34, 1209-1224.
Brancalion, P. H. S., Broadbent, E. N., de-Miguel, S., Cardil, A., Rosa, M. R., Almeida, C. T., Almeida, D. R. A., Chakravarty, S., Zhou, M., Gamarra, J. G. P., Liang, J., Crouzeilles, R., Hérault, B., Aragão, L. E. O. C., Silva, C. A., & Almeyda-Zambrano, A. M. (2020). Emerging threats linking tropical deforestation and the COVID-19 pandemic. Perspectives in Ecology and Conservation, 18, 243-246.
Briseño-Jaramillo, M., Biquand, V., Estrada, A., & Lemasson, A. (2017). Vocal repertoire of free-ranging black howler monkeys' (Alouatta pigra): Call types, contexts, and sex-related contributions. American Journal of Primatology, 79, e22630.
Campos-Cerqueira, M., & Aide, T. M. (2016). Improving distribution data of threatened species by combining acoustic monitoring and occupancy modelling. Methods in Ecology and Evolution, 7, 1340-1348.
Chiarello, A. G. (1995). Role of loud calls in brown howlers, Alouatta fusca. American Journal of Primatology, 36, 213-222.
Clare, J. D. J., Townsend, P. A., & Zuckerberg, B. (2021). Generalized model-based solutions to false-positive error in species detection/nondetection data. Ecology, 102, e03241.
Clink, D. J., Hamid Ahmad, A., & Klinck, H. (2020). Gibbons 'aren't singing in the rain: Presence and amount of rainfall influences ape calling behavior in Sabah, Malaysia. Scientific Reports, 10, 1282.
Clink, D. J., & Klinck, H. (2019). GIBBONFINDR: An R package for the detection and classification of acoustic signals. https://arxiv.org/abs/1906.02572v2.
Clink, D. J., & Klinck, H. (2021). Unsupervised acoustic classification of individual gibbon females and the implications for passive acoustic monitoring. Methods in Ecology and Evolution, 12, 328-341.
Cortes-Ortíz, L., Rosales-Meda, L. K., Marsh, & Mittermeier, R. A (2020). Alouatta pigra. IUCN.
Crunchant, A.-S., Borchers, D., Kühl, H., & Piel, A. (2020). Listening and watching: Do camera traps or acoustic sensors more efficiently detect wild chimpanzees in an open habitat? Methods in Ecology and Evolution, 11, 542-552.
Darras, K. F. A., Pérez, N., Mauladi, Dilong, L., Hanf-Dressler, T., Markolf, M., & Wanger, T. C. (2023, March 1). ecoSound-web: An open-source, online platform for ecoacoustics [version 2; peer review: 2 approved]. F1000Research, 9, 1224. https://doi.org/10.12688/f1000research.26369.2.
Dufourq, E., Durbach, I., Hansford, J. P., Hoepfner, A., Ma, H., Bryant, J. V., Stender, C. S., Li, W., Liu, Z., Chen, Q., Zhou, Z., & Turvey, S. T. (2021). Automated detection of Hainan gibbon calls for passive acoustic monitoring. Remote Sensing in Ecology and Conservation, 7, 475-487.
Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Di Fiore, A., Nekaris, K. A.-I., Nijman, V., Heymann, E. W., Lambert, J. E., Rovero, F., Barelli, C., Setchell, J. M., Gillespie, T. R., Mittermeier, R. A., Arregoitia, L. V., de Guinea, M., Gouveia, S., Dobrovolski, R., … Li, B. (2017). Impending extinction crisis of the world's primates: Why primates matter. Science Advances, 3, e1600946.
Estrada, A., Mendoza, A., Castellanos, L., Pacheco, R., Van Belle, S., García, Y., & Muñoz, D. (2002). Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque, Chiapas, Mexico: A. Pigrain forest fragments. American Journal of Primatology, 58, 45-55.
Fiske, I., & Chandler, R. (2011). Unmarked: An R package for fitting hierarchical models of wildlife occurrence and abundance. Journal of Statistical Software, 43, 1-23.
Gallardo-Cruz, J. A., Peralta-Carreta, C., Solórzano, J. V., Fernández-Montes de Oca, A. I., Nava, L. F., Kauffer, E., & Carabias, J. (2021). Deforestation and trends of change in protected areas of the Usumacinta River basin (2000-2018), Mexico and Guatemala. Regional Environmental Change, 21, 97.
Heinicke, S., Kalan, A. K., Wagner, O. J. J., Mundry, R., Lukashevich, H., & Kühl, H. S. (2015). Assessing the performance of a semi-automated acoustic monitoring system for primates. Methods in Ecology and Evolution, 6, 753-763.
IUCN. (2012). IUCN Red list categories and criteria: Version 3.1 (p. iv + 32). IUCN.
Kahl, S., Wilhelm-Stein, T., Hussein, H., Klinck, H., Ritter, M., & Eibl, M (2017). Large-scale bird sound classification using convolutional neural networks (pp. 1-14). BirdCLEF.
Kahl, S., Wood, C. M., Eibl, M., & Klinck, H. (2021). BirdNET: A deep learning solution for avian diversity monitoring. Ecological Informatics, 61, 101236.
Kalan, A. K., Mundry, R., Wagner, O. J. J., Heinicke, S., Boesch, C., & Kühl, H. S. (2015). Towards the automated detection and occupancy estimation of primates using passive acoustic monitoring. Ecological Indicators, 54, 217-226.
Keane, A., Hobinjatovo, T., Razafimanahaka, H. J., Jenkins, R. K. B., & Jones, J. P. G. (2012). The potential of occupancy modelling as a tool for monitoring wild primate populations. Animal Conservation, 15, 457-465.
K. Lisa Yang Center for Conservation Bioacoustics. (2017). Raven Pro: Interactive Sound Analysis Software. Cornell Lab of Ornithology.
Kong, Q., Cao, Y., Iqbal, T., Wang, Y., Wang, W., & Plumbley, M. D (2020). PANNs: Large-scale pretrained audio neural networks for audio pattern recognition. arXiv. https://arxiv.org/abs/1912.10211.
MacKenzie, D. I., Nichols, J. D., Lachman, G. B., Droege, S., Andrew Royle, J., & Langtimm, C. A. (2002). Estimating site occupancy rates when detection probabilities are less than one. Ecology, 83, 2248-2255.
MacKenzie, D. I., Nichols, J. D., Royle, J. A., Pollock, K. H., Bailey, L., & Hines, J. E. (2017). Occupancy estimation and modeling: Inferring patterns and dynamics of species occurrence (2nd ed.). Academic Press.
Markolf, M., Zinowsky, M., Keller, J. K., Borys, J., Cillov, A., & Schülke, O. (2022). Toward passive acoustic monitoring of lemurs: Using an affordable open-source system to monitor phaner vocal activity and density. International Journal of Primatology, 43, 409-433.
McGinn, K., Kahl, S., Peery, M. Z., Klinck, H., & Wood, C. M. (2023). Feature embeddings from the BirdNET algorithm provide insights into avian ecology. Ecological Informatics, 74, 101995.
Do Nascimento, L. A., Pérez-Granados, C., & Beard, K. H. (2021). Passive acoustic monitoring and automatic detection of diel patterns and acoustic structure of Howler Monkey Roars. Diversity, 13, 566.
Neilson, E., Nijman, V., & Nekaris, K. A. I. (2013). Conservation assessments of arboreal mammals in difficult terrain: Occupancy modeling of pileated gibbons (Hylobates pileatus). International Journal of Primatology, 34, 823-835.
Nichols, J. D., Hines, J. E., MacKenzie, D. I., Seamans, M. E., & Gutiérrez, R. J. (2007). Occupancy estimation and modeling with multiple states and state uncertainty. Ecology, 88, 1395-1400.
Pérez-Granados, C., & Schuchmann, K.-L. (2021). Passive acoustic monitoring of the diel and annual vocal behavior of the black and gold Howler monkey. American Journal of Primatology, 83, e23241.
Piel, A. K., Crunchant, A., Knot, I. E., Chalmers, C., Fergus, P., Mulero-Pázmány, M., & Wich, S. A. (2022). Noninvasive technologies for primate conservation in the 21st century. International Journal of Primatology, 43, 133-167.
R Core Development Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Ravaglia, D., Ferrario, V., De Gregorio, C., Carugati, F., Raimondi, T., Cristiano, W., Torti, V., Hardenberg, A. V., Ratsimbazafy, J., Valente, D., Giacoma, C., & Gamba, M. (2023). There you are! automated detection of Indris’ Songs on features extracted from passive acoustic recordings. Animals: An Open Access Journal from MDPI, 13, 241.
Reid, D. S., Wood, C. M., Whitmore, S. A., Berigan, W. J., Keane, J. J., Sawyer, S. C., Shaklee, P. A., Kramer, H. A., Kelly, K. G., Reiss, A., Kryshak, N., Gutiérrez, R. J., Klinck, H., & Peery, M. Z. (2021). Noisy neighbors and reticent residents: Distinguishing resident from non-resident individuals to improve passive acoustic monitoring. Global Ecology and Conservation, 28, e01710.
Ruggiero, P. G. C., Pfaff, A., Nichols, E., Rosa, M., & Metzger, J. P. (2021). Election cycles affect deforestation within Brazil's Atlantic Forest. Conservation Letters, 14, e12818.
Rylands, A. B., Groves, C. P., Mittermeier, R. A., Cortés-Ortiz, L., & Hines, J. J. H. (2006). Taxonomy and Distributions of Mesoamerican Primates. In A. Estrada, P. A. Garber, M. S. M. Pavelka, & L. Luecke (Eds.), New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior, and Conservation (pp. 29-79). Springer US.
Schön, M. A. (1971). The anatomy of the resonating mechanism in howling monkeys. Folia Primatologica. International Journal of Primatology, 15, 117-132.
Schön Ybarra, M. A. (1986). Loud calls of adult male red howling monkeys (Alouatta seniculus). Folia Primatologica, 47, 204-216.
Seymour, F., & Harris, N. L. (2019). Reducing tropical deforestation. Science, 365, 756-757.
Stevenson, B. C., Dam-Bates, P., Young, C. K. Y., & Measey, J. (2021). A spatial capture-recapture model to estimate call rate and population density from passive acoustic surveys. Methods in Ecology and Evolution, 12, 432-442.
Symes, W. S., Edwards, D. P., Miettinen, J., Rheindt, F. E., & Carrasco, L. R. (2018). Combined impacts of deforestation and wildlife trade on tropical biodiversity are severely underestimated. Nature Communications, 9, 4052.
Torti, V., Valente, D., De Gregorio, C., Comazzi, C., Miaretsoa, L., Ratsimbazafy, J., Giacoma, C., & Gamba, M. (2018). Call and be counted! Can we reliably estimate the number of callers in the indri's (Indri indri) song? PLoS One, 13, e0201664.
Tyre, A. J., Tenhumberg, B., Field, S. A., Niejalke, D., Parris, K., & Possingham, H. P. (2003). Improving precision and reducing bias in biological surveys: Estimating false-negative error rates. Ecological Applications, 13, 1790-1801.
De Vos, J. (2002). Una tierra para sembrar sueños. Historia reciente de la Selva Lacandona, 1950-2000. Fondo de Cultura Económica.
Vu, T. T., Hoa Anh, N. Q., Rawson, B. M., Tran, D. V., Nguyen, H. T., & Van, T. N. (2020). Monitoring occurrence, extinction, and colonization probabilities for gibbon populations. American Journal of Primatology, 82, e23171.
Wood, C. M., Champion, J., Brown, C., Brommelsiek, W., Laredo, I., Rogers, R., & Chaopricha, P. (2023). Challenges and opportunities for bioacoustics in the study of rare species in remote environments. Conservation Science and Practice, e12941.
Wood, C. M., Kahl, S., Chaon, P., Peery, M. Z., & Klinck, H. (2021). Survey coverage, recording duration and community composition affect observed species richness in passive acoustic surveys. Methods in Ecology and Evolution, 12, 885-896.
Wood, C. M., Klinck, H., Gustafson, M., Keane, J. J., Sawyer, S. C., Gutiérrez, R. J., & Peery, M. Z. (2020). Using the ecological significance of animal vocalizations to improve inference in acoustic monitoring programs. Conservation Biology, 35, 336-345.
Wood, C. M., & Peery, M. Z. (2022). What does ‘occupancy’ mean in passive acoustic surveys? Ibis, 164, 1295-1300.
Wood, C. M., Popescu, V. D., Klinck, H., Keane, J. J., Gutiérrez, R. J., Sawyer, S. C., & Peery, M. Z. (2019). Detecting small changes in populations at landscape scales: A bioacoustic site-occupancy framework. Ecological Indicators, 98, 492-507.
Zambolli, A. H., Manzano, M. C. R., Honda, L. K., Rezende, G. C., & 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.
Contributed Indexing:: Keywords: BirdNET; Chiapas; Mexico; artificial intelligence; fragmentation; monitoring; tropical forest
Entry Date(s):: Date Created: 20230522 Date Completed: 20230718 Latest Revision: 20230719
Update Code:: 20240105
DOI:: 10.1002/ajp.23507
PMID:: 37211970
: Czasopismo naukowe

Full Text Finder

Population declines and range contractions due to habitat loss are pervasive among nonhuman primates, with 60% of species threatened with extinction. However, the extensive vocal activity displayed by many primates makes them excellent candidates for passive acoustic surveys. Passive acoustic survey data is increasingly being used to support occupancy models, which have proven to be an efficient means of estimating both population trends and distributions. Passive acoustic surveys can be conducted relatively quickly and at broad scales, but efficient audio data processing has long proven elusive. The machine learning algorithm BirdNET was originally developed for birds but was recently expanded to include nonavian taxa. We demonstrate that BirdNET can accurately and efficiently identify an endangered primate, the Yucatán black howler monkey (Alouatta pigra), by sound in passive acoustic survey data (collected in southeastern Chiapas, Mexico), enabling us to use a single-season occupancy model to inform further survey efforts. Importantly, we also generated data on up to 286 co-occurring bird species, demonstrating the value of integrated animal sound classification tools for biodiversity surveys. BirdNET is freely available, requires no computer science expertise to use, and can readily be expanded to include more species (e.g., its species list recently tripled to >3000), suggesting that passive acoustic surveys, and thus occupancy modeling, for primate conservation could rapidly become much more accessible. Importantly, the long history of bioacoustics in primate research has yielded a wealth of information about their vocal behavior, which can facilitate appropriate survey design and data interpretation.
(© 2023 Wiley Periodicals LLC.)

Informacja