Abstract
Effective survey methods are paramount to measure changes in species distribution, populations dynamics and to guide conservation. Mist-netting and passive acoustic monitoring are two of the most used techniques to sample bats assemblages. Yet, despite the great potential of low-cost autonomous ultrasound recorders in surveying bat assemblages, we lack thorough assessments of their performance in relation to more established survey methods. Taking advantage of the rich bat fauna of the northeastern Brazilian Amazon, we set out to i) investigate the complementarity of mist-netting and acoustic surveys in sampling bats in forest and savannah habitats in the Savannahs of Amapá and ii) undertake a cost-effectiveness evaluation of using one, two or three recorders per sampling site to simultaneously survey bat assemblages. The two methods show complementary, and overall species diversity recorded with mist nets was higher than with acoustic recorders. However, species diversity was higher with acoustic recorders than with mist nets when considering a reduced (n < 3) number of transects. In addition, we found a gain in species diversity when using more than one acoustic recorder in forest habitats, despite the low cost-effectiveness. However, there were no differences between the diversity using one, two or three acoustic recorders in savannah. Due to possible device malfunction, we recommend the use of at least two acoustic recorders in both habitats to reduce the likelihood of data loss. The use of low-cost bioacoustic recorders in bat surveys can help to address critical knowledge gaps for poorly known aerial-hawking insectivores and support evidence-based conservation strategies.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the author on request.
References
Aguiar, L. M. S., Pereira, M. J. R., Zortéa, M., & Machado, R. B. (2020). Where are the bats? An environmental complementary analysis in a megadiverse country. Diversity and Distribution, 26(11), 1510–1522. https://doi.org/10.1111/ddi.13137
Aguiar, L. M. S., Bueno-Rocha, I. D., Oliveira, G., Pires, E. S., Vasconcelos, S., Nunes, G. L., Frizzas, M. R., & Tofni, P. H. B. (2021). Going out for dinner – The consumption of agriculture pests by bats in urban areas. PLoS ONE, 16(10), e0258066. https://doi.org/10.1371/journal.pone.0258066
Appel, G., Capaverde, U. D., Jr., de Oliveira, L. Q., Pereira, L. G. A., Tavares, V. C., López-Baucells, A., Magnusson, W. E., Baccaro, F. B., & Bobrowiec, P. E. D. (2021). Use of complementary methods to sample bats in the Amazon. Acta Chiropterologica, 23(2), 499–511.
Arias-Aguilar, A., Hintze, F., Aguiar, L. M., Rufray, V., Bernard, E., & Pereira, M. J. R. (2018). Who’s calling? Acoustic identification of Brazilian bats. Mammal Research, 63(3), 231–253. https://doi.org/10.1007/s13364-018-0367-z
Arita, H. T., & Fenton, M. B. (1997). Flight and echolocation in the ecology and evolution of bats. Trends in Ecology & Evolution, 12(2), 53–58. https://doi.org/10.1016/S0169-5347(96)10058-6
Barnett, A. A., Sampaio, E. M., Kalko, E. K. V., Shapley, R. L., Fischer, E., Camargo, G., & Rodríguez-Herrera, B. (2006). Bats of Jaú National Park, central Amazônia, Brazil. Acta Chiropterologica, 8, 103–128. https://doi.org/10.3161/1733-5329(2006)8[103:BOJNPC]2.0.CO;2
Bernard, E., & Fenton, M. B. (2002). Species diversity of bats (Mammalia: Chiroptera) in forest fragments, primary forests, and savannas in central Amazonia, Brazil. Canadian Journal of Zoology, 80, 1124–1140. https://doi.org/10.1139/z02-094
Carrasco-Rueda, F., & Loiselle, B. A. (2020). Dimensions of phyllostomid bat diversity and assemblage composition in a tropical forest-agricultural landscape. Diversity. https://doi.org/10.3390/d12060238
Carvalho, W. D., & Mustin, K. (2017). The little known, highly threatened and under-protected Amazonian Savannas. Nature Ecology and Evolution, 1(4), 100. https://doi.org/10.1038/s41559-017-0100
Carvalho, W. D., Rosalino, L. M., Adania, C. H., & Esbérard, C. E. (2016a). Mammal inventories in Seasonal Neotropical Forests: Traditional approaches still compensate drawbacks of modern technologies. Iheringia, Série Zoologia, 106, e2016005. https://doi.org/10.1590/1678-4766e2016005
Carvalho, W. D., Norris, D., & Michalski, F. (2016b). Opportunistic predation of a common scale-backed Antbird (Willisornis poecilinotus) by a Goliath bird-eating spider (Theraphosa blondi) in the eastern Brazilian Amazon. Studies on Neotropical Fauna and Environment, 51, 239–241. https://doi.org/10.1080/01650521.2016.1237802
Carvalho, W. D., Gomes, L. A. C., Castro, I. J., Martins, A. C., Esbérard, C. E. L., & Mustin, K. (2018). Beyond the Amazon forest: Richness, abundance and flight height of bats in the understory of savannahs, campinaranas and terra firme forest. Acta Chiroptorologica, 20, 407–419. https://doi.org/10.3161/15081109ACC2018.20.2.011
Carvalho, W. D., Meyer, C. F. J., Xavier, B. S., Mustin, K., Castro, I. J., Silvestre, S. M., Pathek, D. B., Capaverde, U. D., Jr., Hilário, R., & Toledo, J. J. (2020). Consequences of replacing native savannahs with acacia plantations for the taxonomic, functional, and phylogenetic ⍺- and β-diversity of bats in the Northern Brazilian Amazon. Frontiers in Ecology and Evolution. https://doi.org/10.3389/fevo.2020.609214
Carvalho, W. D., Mustin, K., Farneda, F. Z., de Castro, I. J., Hilário, R. R., Martins, A. C. M., Miguel, J. D., Xavier, B. S., & de Toledo, J. J. (2021). Taxonomic, functional and phylogenetic bat diversity decrease from more to less complex natural habitats in the Amazon. Oecologia, 197, 223–239. https://doi.org/10.1007/s00442-021-05009-3
Chao A, Chiu CH (2016) Nonparametric estimation and comparison of species richness. eLS. https://doi.org/10.1002/9780470015902.a0026329
Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H., Colwell, R. K., & Ellison, A. M. (2014). Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecological Monographs, 84, 45–67. https://doi.org/10.1890/13-0133.1
Costa-Neto, S. V. (2014) Fitofisionomia e florística de savanas do Amapá. PhD thesis, Universidade Federal Rural da Amazônia.
Cumming, G., & Finch, S. (2005). Inference by eye: Confidence intervals and how to read pictures of data. American Psychologist, 60(2), 170–180. https://doi.org/10.1037/0003-066X.60.2.170
Da Silva, L. C. N., Vieira, T. B., Oliveira, A. S. Q. A., Mendes, P., Peixoto, F. P., Oprea, M., & Aguiar, L. M. S. (2022). Bat species of a karstic region in the Brazilian savanna and extension of the Hsunycteris thomasi (Phyllostomidae: Lonchophyllinae). Mammalia, 86(1), 27–36. https://doi.org/10.1515/mammalia-2021-0019
Darras, K. F. A., Yusti, E., Huang, J.C.-C., Zemp, D.-C., Kartono, A. P., & Wanger, T. C. (2021). Bat point counts: A novel sampling method shines light on flying bat communities. Ecology and Evolution, 11(23), 17179–17190. https://doi.org/10.1002/ece3.8356
Delgado-Jaramillo, M., Aguiar, L. M., Machado, R. B., & Bernard, E. (2020). Assessing the distribution of a species-rich group in a continental-sized megadiverse country: Bats in Brazil. Diversity and Distributions, 26(5), 632–643. https://doi.org/10.1111/ddi.13043
Ferreira, D. F., Gibb, R., López-Baucells, A., Nunes, N. J., Jones, K. E., & Rocha, R. (2022). Species-specific responses to land- use change in island insectivorous bats. Journal of Nature Conservation, 67, 126177. https://doi.org/10.1016/j.jnc.2022.126177
Flaquer, C., Torre, I., & Arrizabalaga, A. (2007). Comparison of sampling methods for inventory of bat communities. Journal of Mammalogy, 88(2), 526–533. https://doi.org/10.1644/06-MAMM-A-135R1.1
Froidevaux, J. S. P., Roemer, C., Lemarchand, C., Martí-Carreras, J., Maes, P., Rufray, V., Uriot, Q., Uriot, S., & López-Baucells, A. (2020). Second capture of Promops centralis (Chiroptera) in French Guiana after 28 years of mist-netting and description of its echolocation and distress calls. Acta Amazonica, 50(4), 327–334. https://doi.org/10.1590/1809-4392202001451
Furey, N. M., Mackie, I. J., & Racey, P. A. (2009). The role of ultrasonic bat detectors in improving inventory and monitoring surveys in Vietnamese karst bat assemblages. Current Zoology, 55(5), 327–341. https://doi.org/10.1093/czoolo/55.5.327
Garbino GST, Gregorin R, Lima IP, Loureiro L, Moras LM, Moratelli R, Nogueira MR, Pavan AC, Tavares VC, Peracchi AL (2020) Updated checklist of Brazilian bats: versão 2020. Comitê da Lista de Morcegos do Brasil—CLMB. Sociedade Brasileira para o Estudo de Quirópteros (Sbeq). https://www.sbeq.net/lista-de-especies. Accessed 11 February 2022
Gardner, T. A., Barlow, J., Araujo, I. S., Ávila-Pires, T. C., Bonaldo, A. B., Costa, J. E., Esposito, M. C., Ferreira, L. V., Hawes, J., Hernandez, M. I. M., Hoogmoed, M. S., Leite, R. N., Lo-Man-Hung, N. F., Malcolm, J. R., Martins, M. B., Mestre, L. A. M., Miranda-Santos, R., Overal, W. L., Parry, L., … Peres, C. A. (2008). The cost-effectiveness of biodiversity surveys in tropical forests. Ecology Letters, 11(2), 139–150. https://doi.org/10.1111/j.1461-0248.2007.01133.x
Hart, A. G., Dawson, M., Fourie, R., et al. (2022). Comparing the effectiveness of camera trapping, driven transects and ad hoc records for surveying nocturnal mammals against a known species assemblage. COMMUNITY ECOLOGY. https://doi.org/10.1007/s42974-021-00070-7
Hill, M. O. (1973). Diversity and evenness: A unifying notation and its consequences. Ecology, 54, 427–432. https://doi.org/10.2307/1934352
Hill, A. P., Prince, P., Covarrubias, E. P., Doncaster, C. P., Snaddon, J. L., & Rogers, A. (2018). AudioMoth: Evaluation of a smart open acoustic device for monitoring biodiversity and the environment. Methods in Ecology and Evolution, 9(5), 1199–1211. https://doi.org/10.1111/2041-210X.12955
Hsieh, T. C., Ma, K. H., & Chao, A. (2016). iNEXT: An R package for rarefaction and extrapolation of species diversity (H ill numbers). Methods in Ecology and Evolution, 7(12), 1451–1456. https://doi.org/10.1111/2041-210X.12613
Joermann, G., Schmidt, U., & Schmidt, C. (1988). The mode of orientation during flight and approach to landing in two phyllostomid bats. Ethology, 78, 332–340. https://doi.org/10.1111/j.1439-0310.1988.tb00242.x
Korine, C., & Kalko, E. K. V. (2005). Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): Echolocation call design and olfaction. Behavioral Ecology and Sociobiology, 59, 12–23. https://doi.org/10.1007/s00265-005-0003-1
Kunz, T. H., de Torrez, E. B., Bauer, D., Lobova, T., & Fleming, T. H. (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences, 1223(1), 1–38. https://doi.org/10.1111/j.1749-6632.2011.06004.x
Lim, B. K., & Engstrom, M. D. (2001). Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: Implications for conservation. Biodiversity and Conservation, 10, 613–657. https://doi.org/10.1023/A:1016660123189
López-Baucells, A., Rocha, R., Bobrowiec, P., Bernard, E., Palmeirim, J., & Meyer, C. F. J. (2018). Field guide to the Bats of the Amazon. Pelagic Publishing.
López-Baucells, A., Rowley, S., Rocha, R., Bobrowiec, P. E., Palmeirim, J. M., Farneda, F. Z., & Meyer, C. F. J. (2022). Interplay between local and landscape-scale effects on the taxonomic, functional and phylogenetic diversity of aerial insectivorous Neotropical bats. Landscape Ecology (in Press). https://doi.org/10.1007/s10980-022-01493-x
López-Baucells, A., Torrent, L., Rocha, R., Bobrowiec, P. E., Palmeirim, J. M., & Meyer, C. F. (2019). Stronger together: Combining automated classifiers with manual post-validation optimizes the workload vs reliability trade-off of species identification in bat acoustic surveys. Ecological Informatics, 49, 45–53. https://doi.org/10.1016/j.ecoinf.2018.11.004
López-Baucells, A., Yoh, N., Rocha, R., Bobrowiec, P. E. D., Palmeirim, J. M., & Meyer, C. F. J. (2021). Optimising bat bioacoustic surveys in human-modified neotropical landscapes. Ecological Applications, 31(6), e02366. https://doi.org/10.1002/eap.2366
MacGregor-Fors, I., & Payton, M. E. (2013). Contrasting diversity values: Statistical inferences based on overlapping confidence intervals. PLoS ONE. https://doi.org/10.1371/journal.pone.0056794
MacSwiney, G. M. C., Clarke, F. M., & Racey, P. A. (2008). What you see is not what you get: The role of ultrasonic detectors in increasing inventory completeness in Neotropical bat assemblages. Journal of Applied Ecology, 45(5), 1364–1371. https://doi.org/10.1111/j.1365-2664.2008.01531.x
Mancini MCS, Hintze F, Laurindo RS, Mello RM, Gregorin R (2022) Tradition vs. innovation: comparing bioacoustics and mist-net results to bat sampling. Bioacoustics 31(5):575–593. https://doi.org/10.1080/09524622.2021.2008494
Marques, J. T., Ramos-Pereira, M. J., Marques, T. A., Santos, C. D., Santana, J., Beja, P., & Palmeirim, J. M. (2013). Optimising sampling design to deal with mist-net avoidance in Amazonian birds and bats. PLoS ONE. https://doi.org/10.1371/journal.pone.0074505
Marques, J. T., Ramos-Pereira, M. J., & Palmeirim, J. M. (2016). Patterns in the use of rainforest vertical space by Neotropical aerial insectivorous bats: All the action is up in the canopy. Ecography, 39(5), 476–486. https://doi.org/10.1111/ecog.01453
Martins, A. C., Oliveira, H. F., Zimbres, B., Sá-Neto, R. J., & Marinho-Filho, J. (2022). Environmental heterogeneity and water availability shape the structure of phyllostomid bat assemblages (Mammalia: Chiroptera) in the north-eastern Amazon forest. Forest Ecology and Management. https://doi.org/10.1016/j.foreco.2021.119863
Meyer, C. F. (2015). Methodological challenges in monitoring bat population-and assemblage-level changes for anthropogenic impact assessment. Mammalian Biology, 80(3), 159–169. https://doi.org/10.1016/j.mambio.2014.11.002
Meyer, C. F. J., Aguiar, L. M. S., Aguirre, L. F., et al. (2015). Species undersampling in tropical bat surveys: Effects on emerging biodiversity patterns. Journal of Animal Ecology, 84, 113–123. https://doi.org/10.1111/1365-2656.12261
Meyer CF, Struebig MJ, Willig MR (2016) Responses of tropical bats to habitat fragmentation, logging, and deforestation. In: Voigt C, Kingston T (ed) Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer Nature, Cham, pp 63–103.
Mustin, K., Carvalho, W. D., Hilário, R. R., et al. (2017). Biodiversity, threats and conservation challenges in the “Cerrado of Amapá”, an Amazonian savanna. Nature Conservation, 22, 107–127. https://doi.org/10.3897/natureconservation.22.13823
O’Farrell, M. J., & Gannon, W. L. (1999). A comparison of acoustic versus capture techniques for the inventory of bats. Journal of Mammalogy, 80, 24–30. https://doi.org/10.2307/1383204
Oliveira, L. Q., Marciente, R., Magnusson, W. E., & Bobrowiec, P. E. D. (2015). Activity of the insectivorous bat Pteronotus parnellii relative to insect resources and vegetation structure. Journal of Mammalogy, 96, 1036–1044. https://doi.org/10.1093/jmammal/gyv108
Palmeirim, A. F., Benchimol, M., Peres, C. A., & Vieira, M. V. (2019). Moving forward on the sampling efficiency of neotropical small mammals: Insights from pitfall and camera trapping over traditional live trapping. Mammal Research, 64, 445–454. https://doi.org/10.1007/s13364-019-00429-2
Patriquin, K. J., Hogberg, L. K., Chruszcz, B. J., Barclay, R. M. R., & Barclay, R. M. B. (2003). The influence of habitat structure on the ability to detect ultrasound using bat detectors. Wildlife Society Bulletin, 31, 475–481.
Pech-Canche JM, MacSwiney CG, Estrella E (2010) Importancia de los detectores ultrasónicos para mejorar los inventários de murciélagos Neotropicales. Therya 1(3):221–228. https://doi.org/10.12933/therya-10-17
Prance GT (1996) Islands in Amazonia. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 351(1341): 823–33. https://doi.org/10.1098/rstb.1996.0077
R Core Team (2020) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. R v.4.0.3, 2020. https://www.R-project.org. Accessed 11 February 2022
Reis, N. R., Peracchi, A. L., Batista, C. B., & Lima, I. P. (2017). História natural dos morcegos brasileiros: Chave de identificação de espécies. Technical Books Livraria LTDA.
Ribeiro-Júnior, M. A., Gardner, T. A., & Ávila-Pires, T. C. S. (2008). Evaluating the effectiveness of herpetofaunal sampling techniques across a gradient of habitat change in a Tropical forest landscape. Journal of Herpetology, 42(4), 733–749. https://doi.org/10.1670/07-097R3.1
Rodrigues, R., & Prado, P. I. (2018). Sampling methods affect observed response of bird species richness to vegetation structure in Brazilian savannas. The Condor: Ornithological Applications, 120(2), 402–413. https://doi.org/10.1650/CONDOR-17-190.1
Schnitzler, H. U., & Kalko, E. K. V. (2001). Echolocation by insect-eating bats. BioScience, 51, 557–569. https://doi.org/10.1111/oik.07202
Sikes RS, the Animal Care and Use Committee of the American Society of Mammalogists. (2016). Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy, 97, 663–688. https://doi.org/10.1093/jmammal/gyw078
Silva, C. R., & Bernard, E. (2017). Bioacoustics as an Important Complementary Tool in Bat Inventories in the Caatinga Drylands of Brazil. Acta Chiropterologica, 19(2), 409–418. https://doi.org/10.3161/15081109ACC2017.19.2.017
Silva, C. R., Martins, A. C. M., Castro, I. J., Bernard, E., Cardoso, E. M., Santos, D. L., Gregorin, R., Rossi, R. V., Percequillo, A. R., & Cruz, K. C. (2013). Mammals of Amapá State, Eastern Brazilian Amazonia: A revised taxonomic list with comments on species distributions. Mammalia, 77, 409–424. https://doi.org/10.1515/mammalia-2012-0121
Sousa, J. C., Toledo, J. J., Carvalho, W. D., & Silva, J. M. C. (2022). Bird species responses to forest-savanna boundaries in an Amazonian savanna. Avian Conservation and Ecology, 17(1), 30. https://doi.org/10.5751/ACE-02138-170130
Souza E, Cunha A (2010) Climatologia de precipitação no Amapá e mecanismos climáticos de grande escala. In: Cunha AC, Souza EB, Cunha HFA (ed) Tempo, Clima e Recursos Hídricos: Resultados do Projeto REMETAP no Estado do Amapá. Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá - IEPA, Macapá, pp 177–195.
Straube, F. C., & Bianconi, G. V. (2002). Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical, 8, 150–152.
Tavares, J. P. N. (2014). Características da climatologia de Macapá-AP. Caminhos De Geografia, 15, 138–151.
Tuttle, M. D., Ryan, M. J., & Belwood, J. J. (1985). Acoustical resource partitioning by two species of phyllostomid bats (Trachops cirrhosus and Tonatia silvicola). Animal Behaviour, 33, 1369–1370. https://doi.org/10.1016/S0003-3472(85)80204-9
Wilson, D. E., Mittermeier, R. A. (2019) Handbook of the Mammals of the World, Volume 9: Bats. Lynx Edicions, Barcelona.
Wordley, C. F. R., Sankaran, M., Mudappa, D., & Altringham, J. D. (2018). Heard but not seen: Comparing bat assemblages and study methods in a mosaic landscape in the Western Ghats of India. Ecology and Evolution, 8, 3883–3894. https://doi.org/10.1002/ece3.3942
Yoh, N., Clarke, J. A., López-Baucells, L., Mas, M., Bobrowiec, P. E. D., Rocha, R., & Meyer, C. F. J. (2022). Edge effects and vertical stratification of aerial insectivorous bats across the interface of primary-secondary Amazonian rainforest. PLoS ONE, 17(9), e0274637. https://doi.org/10.1371/journal.pone.0274637
Acknowledgements
William Douglas Carvalho was supported by post-doctoral (PNPD/CAPES) scholarships of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, until early 2020 (CAPES/PNPD—Finance Code 001). Currently, WDC is supported by ‘Ayudas Maria Zambrano’ (CA3/RSUE/2021-00197) funded by the Spanish Ministry of Universities. Bruna Xavier is supported by doctoral scholarships of the CAPES. Funding to Ricardo Rocha was provided by the Portuguese Foundation for Science and Technology (2020.01129.CEECIND/CP1601/CT0004). The fieldwork was authorised by the appropriate Brazilian authority, namely the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA; Collection licenses n° 55867-1). We are grateful to our field assistants Karen Mustin, Daniela Rato, Cledinaldo Marques, Cremilson Marques, Gustavo Silveira, Joandro Pandilha, Jackson Souza and Luís Miguel Rosalino. We also thank Dona Deusa, Dona Damiana, Dona Sônia (comunidade da Ressaca do Pedreira), Mateus (Quilombo do Curiaú), Márcilio e Ceará (Balneário do Alegre), Raizé Domingues, Juliano, José (comunidade do Abacate da Pedreira) e Ivori for allowing us to sample in their areas, for overnight stays and assistance during field activities.
Author information
Authors and Affiliations
Contributions
WDC, ALB, RR and JMP originally formulated the idea; WDC, JDM, BSX and IJC conducted fieldwork; JDM and ALB performed the acoustic identification; WDC and JDM performed statistical analyses and WDC, JDM and BSX wrote the drafts of the main manuscript and the online resources. All authors contributed critically to the manuscript and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Ethics approval
Not applicable.
Consent to participate
All co-authors agree.
Consent for publication
All co-authors agree.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Carvalho, W.D., Miguel, J.D., da Silva Xavier, B. et al. Complementarity between mist-netting and low-cost acoustic recorders to sample bats in Amazonian rainforests and savannahs. COMMUNITY ECOLOGY 24, 47–60 (2023). https://doi.org/10.1007/s42974-022-00131-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42974-022-00131-5