Exploring the potential of occupancy modelling using passive acoustics in Coua gigas and Coua coquereli



Passive acoustic monitoring, Kirindy forest, Madagascar, surveillance acoustique passive, monitoring biodiversity, population dynamics


In highly threatened habitats such as the dry deciduous forests of western Madagascar, it is essential to develop new approaches to detect population changes and evaluate conservation measures. Passive acoustic monitoring (PAM) is such a promising approach. This method has many advantages over conventional methods, such as time efficiency, money savings, and reduced wildlife disturbance. It is especially suitable for studying occupancy and activity patterns of vocalizing species such as birds. Our study analyzed data recorded with autonomous sound recorders in 2018 in Kirindy Forest for the territorial calls of Coua gigas and Coua coquereli. We modeled occupancy and detection probability for both species in the study area. We also examined activity patterns and found that the peak of vocal activity for Coua coquereli is at 0700h and for Coua gigas at 1100h. To also test the value of PAM in relation to ecological factors we modeled occupancy and included logging status as a site covariate. We detected a positive influence of logging in occupancy of Coua gigas. Our study provides guidelines for future occupancy studies using PAM in the two coua species. We conclude that PAM will improve the ecological monitoring of soniferous animals in Madagascar.



Dans les habitats très menacés tels que les forêts sèches à feuilles caduques de l'ouest de Madagascar, il est essentiel de développer de nouvelles approches pour détecter les changements de population et évaluer les mesures de conservation. La surveillance acoustique passive (PAM) est une approche prometteuse. Cette méthode présente de nombreux avantages par rapport aux méthodes conventionnelles, comme le gain de temps, l'économie d'argent et la réduction des perturbations de la faune. Elle est particulièrement adaptée à l'étude des modèles d'occupation et d'activité des espèces vocalisantes telles que les oiseaux. Notre étude a analysé les données enregistrées avec des enregistreurs sonores autonomes en 2018 dans la forêt de Kirindy pour les vocalisations territoriaux de Coua gigas et Coua coquereli. Nous avons modélisé l'occupation et la probabilité de détection des deux espèces dans la zone d'étude. Nous avons également examiné les schémas d'activité et constaté que le pic d'activité vocale de Coua coquereli se situe à 0700h et celui de Coua gigas à 1100h. Pour tester également la valeur de la PAM par rapport aux facteurs écologiques, nous avons modélisé l'occupation et inclus le statut d'exploitation forestière en tant que covariable du site. Nous avons détecté une influence positive de l'exploitation forestière sur l'occupation de Coua gigas. Notre étude fournit des lignes directrices pour les futures études d'occupation utilisant la PAM pour les deux espèces de coua. Nous concluons que la PAM améliorera le suivi écologique des animaux sonifères à Madagascar.

Author Biography

Matthias Markolf, Chances for Nature; Cologne Zoo

Chances for Nature, Goettingen, Germany

Cologne Zoo, Cologne, Germany


Astaras, C., Linder, J. M., Wrenge, P., Orume, R., Johnson, P. J. and Macdonald, D. W. 2020. Boots on the ground: The role of passive acoustic monitoring in evaluating anti-poaching patrols. Environmental Conservation 47, 3: 213–216. <https://doi.org/10.1017/S0376892920000193>

Bailey, L. L., MacKenzie, D. I. and Nichols, J. D. 2014. Advances and applications of occupancy models. Methods in Ecology and Evolution 5, 12: 1269–1279. <https://doi.org/10.1111/2041-210X.12100>

Bardeli, R., Wolff, D., Kurth, F., Koch, M., Tauchert, K.-H. and Frommolt, K.-H. 2010. Detecting bird sounds in a complex acoustic environment and application to bioacoustic monitoring. Pattern Recognition Letters 31, 12: 1524–1534. <https://doi.org/10.1016/j.patrec.2009.09.014>

Beaudrot, L., Ahumada, J., O’Brien, T. G. and Jansen, P. A. 2019. Detecting tropical wildlife declines through camera-trap monitoring: An evaluation of the Tropical Ecology Assessment and Monitoring protocol. Oryx 53, 1: 126–129. <https://doi.org/10.1017/S0030605318000546>

Bessone, M., Kühl, H. S., Hohmann, G., Herbinger, I., N‘Goran, K. P., et al. 2020. Drawn out of the shadows: Surveying secretive forest species with camera trap distance sampling. Journal of Applied Ecology 57, 5: 963–974. <https://doi.org/10.1111/1365-2664.13602>

Brooks, T. M., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B., Rylands, A. B., et al. 2002. Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology 16, 4: 909–923. <https://doi.org/10.1046/j.1523-1739.2002.00530.x>

Campos-Cerqueira, M. and 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. <https://doi.org/10.1111/2041-210X.12599>

Celis-Murillo, A., Deppe, J. L. and Ward, M. P. 2012. Effectiveness and utility of acoustic recordings for surveying tropical birds. Journal of Field Ornithology 83, 2: 166–179. <https://doi.org/10.1111/j.1557-9263.2012.00366.x>

Chalmers, C., Fergus, P., Wich, S. and Longmore, S. N. 2021. Modelling Animal Biodiversity Using Acoustic Monitoring and Deep Learning. In: International Joint Conference on Neural Networks, Cornell University, New York. Available online <https://doi.org/10.1109/IJCNN52387.2021.9534195>

Chiatante, G. 2021. Spatial distribution of an assemblage of an endemic genus of birds: An example from Madagascar. African Journal of Ecology 60, 1: 13–26. <https://doi.org/10.1111/aje.12917>

Chouteau, P. 2004. The impacts of logging on the microhabitats used by two species of couas in the western forest of Madagascar. Comptes Rendus Biologies 327, 12: 1157–1170. <https://doi.org/10.1016/j.crvi.2004.09.011>

Chouteau, P. 2006. Influences of the season and the habitat structure on the foraging ecology of two coua species in the western dry forest of Madagascar. Comptes Rendus Biologies 329: 691–701. <https://doi.org/10.1016/j.crvi.2006.06.005>

Chouteau, P. 2007. The impact of burning on the microhabitat used by two species of couas in the western dry forest of Madagascar. Ostrich 78, 1: 43–49. <https://doi.org/10.2989/OSTRICH.2007.>

Chouteau, P. 2009. Impact of logging on the foraging behaviour of two sympatric species of Couas (Coua coquereli and Coua gigas) in the western dry forest of Madagascar. Comptes Rendus Biologies 332, 6: 567–578. <https://doi.org/10.1016/j.crvi.2009.01.005>

Chouteau, P., Fenosoa, R. and Rakotoarimanana, V. 2004. Habitat selection and density of couas in Madagascar: Implication for their conservation. Comptes Rendus Biologies 327, 1: 37–50. <https://doi.org/10.1016/j.crvi.2003.10.006>

Chouteau, P. and Pedrono, M. 2009. Breeding biology of Coquerel’s Coua (Coua coquereli) in western Madagascar. Journal of Ornithology 150: 55–60. <https://doi.org/10.1007/s10336-008-0317-7>

Darras, K., Batáry, P., Furnas, B., Celis‐Murillo, A., Van Wilgenburg, S. L., et al. 2018. Comparing the sampling performance of sound recorders versus point counts in bird surveys: A meta‐analysis. Journal of Applied Ecology 55, 6: 2575–2586. <https://doi.org/10.1111/1365-2664.13229>

Darras, K., Batáry, P., Furnas, B. J., Grass, I., Mulyani, Y. A. and Tscharntke, T. 2019. Autonomous sound recording outperforms human observation for sampling birds: A systematic map and user guide. Ecological Applications 29, 6: e01954. <https://doi.org/10.1002/eap.1954>

Dobson, A. J. and Barnett, A. G. 2018. An Introduction to Generalized Linear Models, 4th ed. Chapman and Hall, CRC Press, Taylor & Francis Group, Boca Raton, FL.

Favre, J.-C. 1996. Traditional utilization of the forest. In: Ecology and Economy of Dry Forests in Madagascar. J. U. Ganzhorn and J.-P. Sorg (eds.), pp 33–40. Primate Report Special Issue 46, 1.

Fiske, I. J. and Chandler, R. B. 2011. unmarked: An R package for fitting hierarchical models of wildlife occurrence and abundance. Journal of Statistical Software 43, 10: 1 – 23. <https://doi.org/10.18637/jss.v043.i10>

Ganzhorn, J. U. 1995. Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology 76, 7: 2084–2096. <https://doi.org/10.2307/1941683>

Ganzhorn, J. U., Ganzhorn, A. W., Abraham, J.-P., Andriamanarivo, L. and Ramananjatovo, A. 1990. The impact of selective logging on forest structure and tenrec populations in western Madagascar. Oecologia 84, 1: 126–133. <https://doi.org/10.1007/bf00665606>

Ganzhorn, J. U., Lowry, P. P., Schatz, G. E. and Sommer, S. 2001. The biodiversity of Madagascar: One of the world’s hottest hotspots on its way out. Oryx 35, 4: 346–348. <https://doi.org/10.1046/j.1365-3008.2001.00201.x>

Goodman, S. M. 2020. Coquerel’s Coua & Giant Coua. In: The Birds of Africa: The Malagasy Region. Volume 8. R. Safford, F. Hawkins and D. J. Pearson (eds.), pp 550-555. Christopher Helm, London.

Gibb, R., Browning, E., Glover-Kapfer, P. and Jones, K. E. 2019. Emerging opportunities and challenges for passive acoustics in ecological assessment and monitoring. Methods in Ecology and Evolution 10, 2: 169–185. <https://doi.org/10.1111/2041-210X.13101>

Guisan, A. and Thuiller, W. 2005. Predicting species distribution: Offering more than simple habitat models. Ecology Letters 8: 993–1009. <https://doi.org/10.1111/j.1461-0248.2005.00792.x>

Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D. and Hawkins, F. 2007. Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation 34, 4: 325–333. <https://doi.org/10.1017/S0376892907004262>

Hawkins, A. F. A. and Wilmé, L. 1996. Effects of logging on forest birds. In: Ecology and Economy of Dry Forests in Madagascar. J. U. Ganzhorn and J.-P. Sorg (eds.), pp 57–80. Primate Report Special Issue 46, 1.

Hawkins, F., Safford, R., Skerrett, A., Gale, J. and Small, B. E. 2015. Birds of Madagascar and the Indian Ocean islands: Seychelles, Comoros, Mauritius, Reunion, and Rodrigues. Christopher Helm, London.

Honrado, J. P., Pereira, H. M. and Guisan, A. 2016. Fostering integration between biodiversity monitoring and modelling. Journal of Applied Ecology 53 ,5: 1299–1304. <https://doi.org/10.1111/1365-2664.12777>

IUCN. 2016. Coua gigas. The IUCN Red List of Threatened Species. International Union for Conservation of Nature. Online <https://www.iucnredlist.org/search?query=Coua%20gigas&searchType=species>

IUCN. 2018. Coua coquereli. The IUCN Red List of Threatened Species. International Union for Conservation of Nature. Online <https://www.iucnredlist.org/search?query=Coua%20gigas&searchType=species>

Kalan, A. K., Mundry, R., Wagner, O. J. J., Heinicke, S., Boesch, C. and Kühl, H. S. 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>

Langrand, O. and Wilmé, L. 1997. Effects of forest fragmentation on extinction patterns of the endemic avifauna on the Central High Plateau of Madagascar. In: Natural Change and Human Impact in Madagascar. S. M. Goodmann and B. D. Patterson (eds.), pp 280–306. Smithsonian Institution Press, Washington.

MacKenzie, D. I. and Bailey, L. L. 2004. Assessing the fit of site-occupancy models. Journal of Agricultural, Biological, and Environmental Statistics 9: 300–318. <https://doi.org/10.1198/108571104X3361>

MacKenzie, D. I., Nichols, J. D., Lachman, G. B., Droege, S., Andrew Royle, J. and Langtimm, C. A. 2002. Estimating site occupancy rates when detection probabilities are less than one. Ecology 83, 8: 2248–2255. <https://doi.org/10.1890/0012-9658(2002)083[2248:ESORWD]2.0.CO;2>

MacKenzie, D. I., Nichols, J. D., Royle J. A., Pollock, K. H., Bailey, L. L., Hines, J. E. 2017. Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence (Second edition). Academic Press, London.

Markolf, M., Zinowsky, M., Keller, J. K., Borys, J., Cillov, A. and 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. <https://doi.org/10.1007/s10764-022-00285-z>

Meredith, M. and Ridout, M. 2016. Overview of the overlap package. Biology, Environmental Science. Available online <https://cran.microsoft.com/snapshot/2016-08-05/web/packages/overlap/vignettes/overlap.pdf>

Mielke, A. and Zuberbühler, K. 2013. A method for automated individual, species and call type recognition in free-ranging animals. Animal Behaviour 86, 2: 475–482. <https://doi.org/10.1016/j.anbehav.2013.04.017>

Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. and Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858. <https://doi.org/10.1038/35002501>

Oppel, S., Hervias, S., Oliveira, N., Pipa, T., Silva, C., et al. 2014. Estimating population size of a nocturnal burrow-nesting seabird using acoustic monitoring and habitat mapping. Nature Conservation 7: 1–13. <https://doi.org/10.3897/natureconservation.7.6890>

Pérez-Granados, C., Bota, G., Giralt, D. and Traba, J. 2018. A cost-effective protocol for monitoring birds using autonomous recording units: A case study with a night-time singing passerine. Bird Study 65, 3: 338–345. <https://doi.org/10.1080/00063657.2018.1511682>

Pérez-Granados, C. and Schuchmann, K.-L. 2021. Passive acoustic monitoring of Chaco chachalaca (Ortalis canicollis) over a year: vocal activity pattern and monitoring recommendations. Tropical Conservation Science 14. <https://doi.org/10.1177/19400829211058295>

Plumptre, A. J. 2000. Monitoring mammal populations with line transect techniques in African forests. Journal of Applied Ecology 37, 2: 356–368. <https://doi.org/10.1046/j.1365-2664.2000.00499.x>

Pollock, K. H., Nichols, J. D., Simons, T. R., Farnsworth, G. L., Bailey, L. L. and Sauer, J. R. 2002. Large scale wildlife monitoring studies: Statistical methods for design and analysis. Environmetrics 13, 2: 105–119. <https://doi.org/10.1002/env.514>

Priyadarshani, N., Marsland, S. and Castro, I. 2018. Automated birdsong recognition in complex acoustic environments: A review. Journal of Avian Biology 49, 5: 01447. <https://doi.org/10.1111/jav.01447>

Rajaonarivelo, J. A., Andrianarimisa A., Raherilalao M. J. and Goodman S. 2020. Vertical distribution and daily patterns of birds in the dry deciduous forests of central western Madagascar. Tropical Zoology 33, (1: 36–52. <https://doi.org/10.4081/tz.2020.66>

Ralimanana, H., Perrigo, A. L., Smith, R. J., Borrell, J. S., Faurby, S., et al. 2022. Madagascar’s extraordinary biodiversity: Threats and opportunities. Science 378, 6623: eadf1466. <https://doi.org/10.1126/science.adf1466>

Revilla-Martín, N., Budinski, I., Puig-Montserrat, X., Flaquer, C. and López-Baucells, A. 2021. Monitoring cave-dwelling bats using remote passive acoustic detectors: A new approach for cave monitoring. Bioacoustics 30, 5: 527–542. <https://doi.org/10.1080/09524622.2020.1816492>

Rosenthal, G. G. and Ryan, M. J. 2000. Visual and acoustic communication in non-human animals: A comparison. Journal of Biosciences 25: 285–290. <https://doi.org/10.1007/BF02703937>

Ross, S. R. J., O'Connell, D. P., Deichmann, J. L., Desjonquères, C., Gasc, A., et al. 2023. Passive acoustic monitoring provides a fresh perspective on fundamental ecological questions. Functional Ecology 37, 4: 959–975. <https://doi.org/10.1111/1365-2435.14275>

Slingerland, W. 2021. Passive Acoustic Monitoring in Ranomafana National Park—Characterizing the Soundscape and Acoustic Niche Overlap of Frugivorous Bird Species. Unpublished Master thesis, Utrecht University, Utrecht. Available online <https://studenttheses.uu.nl/handle/20.500.12932/299>

Stowell, D., Wood, M. D., Pamuła, H., Stylianou, Y. and Glotin, H. 2019. Automatic acoustic detection of birds through deep learning: The first Bird Audio Detection challenge. Methods in Ecology and Evolution 10, 3: 368–380. <https://doi.org/10.1111/2041-210X.13103>

Sugai, L. S. M. and Llusia, D. 2019. Bioacoustic time capsules: Using acoustic monitoring to document biodiversity. Ecological Indicators 99: 149–152. <https://doi.org/10.1016/j.ecolind.2018.12.021>

Sugai, L. S. M., Silva, T. S. F., Ribeiro, J. W. and Llusia, D. 2019. Terrestrial passive acoustic monitoring: review and perspectives. BioScience 69, 1: 15–25. <https://doi.org/10.1093/biosci/biy147>

Todd, N. R. E., Cronin, M., Luck, C., Bennison, A., Jessopp, M. and Kavanagh, A. S. 2020. Using passive acoustic monitoring to investigate the occurrence of cetaceans in a protected marine area in northwest Ireland. Estuarine, Coastal and Shelf Science 232: 106509. <https://doi.org/10.1016/j.ecss.2019.106509>

Vieilledent, G., Clovis G., Rakotomalala F. A., Ranaivosoa R., Rakotoarijaona J.-R., et al. 2018. Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Biological Conservation 222: 189–197. <https://doi.org/10.1016/j.biocon.2018.04.008>

Waeber, P. O., Wilmé, L., Ramamonjisoa, B., Garcia, C., Rakotomalala, D., et al. 2015. Dry forests in Madagascar, neglected and under pressure. International Forestry Review 17, S2: 127–148. <https://doi.org/10.1505/146554815815834822>

Wilmé, L. 1996. Composition and characteristics of bird communities in Madagascar. In: Biogéographie de Madagascar. Actes du Colloque international biogéographie de Madagascar. W. R. Lourenco (ed.), pp 349–362. ORSTOM, Paris. Available online <https://www.documentation.ird.fr/hor/fdi:010008477>

Wood, C. M. and Peery, M. Z. 2022. What does ‘occupancy’ mean in passive acoustic surveys? Ibis 164, 4: 1295-1300. <https://doi.org/10.1111/ibi.13092>

Zwerts, J. A., Stephenson, P. J., Maisels, F., Rowcliffe, M., Astaras, C., et al. 2021. Methods for wildlife monitoring in tropical forests: Comparing human observations, camera traps, and passive acoustic sensors. Conservation Science and Practice 3, 12: e568. <https://doi.org/10.1111/csp2.568>

Coua coquereli. Plate 58 In: Milne Edwards, A., Grandidier, A. 1876. Histoire Physique, Naturelle et Politique de Madagascar, Volume XIII: Histoire Naturelle des Oiseaux. Tome II. Atlas I. Imprimerie Nationale, Paris.