Abstract
Many species are difficult to study either due to their rarity, elusiveness, difficult access to their area of occurrence, or any combination of these. This can be particularly problematic for threatened species. Passive acoustic monitoring (PAM) is a recently developed survey technique that has shown great potential in addressing this problem for species that communicate through vocalizations. However, the large amount of data it generates can be difficult to process manually. Here, we present an entirely automatic workflow to record and detect the vocalizations of a bird species that is both elusive (nocturnal) and restricted to difficult terrain in the most remote rainforests of an oceanic island: the recently discovered Principe Scops-Owl. Specifically, we evaluated (i) the performance of the workflow to monitor the presence of the owl, (ii) we assessed the most suitable time for monitoring it; and (iii) we examined the potential of this species to present detectable vocal individual signatures. For 12 days, we deployed omnidirectional recording stations (AudioMoth devices) in 72 points along 10 transects that were surveyed during one night at the same time by observers in the field. We trained TADARIDA, a machine learning software toolbox, to automatically detect owl calls. Results on the presence of the owl per site were similar for both methods. The automatic workflow showed that the owl is active during the whole night and the PAM recording setting should encompass at least the 21–23 h interval. Possibly, vocalizations had individual signatures—but the small sample size and temporal window prevented a definite conclusion. The automatic workflow developed here is an efficient method to monitor the Principe Scops-Owl and can be easily adapted for other elusive vocal species.
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Data availability
The datasets generated and analyzed during the current study, as well as R scripts and labelled audios are available at https://osf.io/a34vs/. Due to size constraints, the remaining audio data is only available on request from the corresponding author.
References
Abrahams C (2018) Bird Bioacoustic Surveys - developing a standard protocol. In Practice 20–23
Abrahams C, Geary M (2020) Combining bioacoustics and occupancy modelling for improved monitoring of rare breeding bird populations. Ecol Indic 112:106131. https://doi.org/10.1016/j.ecolind.2020.106131
Aide TM, Corrada-Bravo C, Campos-Cerqueira M et al (2013) Real-time bioacoustics monitoring and automated species identification. PeerJ 1:e103. https://doi.org/10.7717/peerj.103
Ancona S, Dénes FV, Krüger O et al (2017) Estimating adult sex ratios in nature. Philos Trans R Soc B 372:20160313. https://doi.org/10.1098/rstb.2016.0313
Bas Y, Bas D, Julien J-F (2017) Tadarida: a toolbox for animal detection on acoustic recordings. J Open Res Softw 5:6. https://doi.org/10.5334/jors.154
Bee MA, Kozich CE, Blackwell KJ, Gerhardt HC (2001) Individual variation in advertisement calls of territorial Male Green Frogs, Rana clamitans: implications for individual discrimination. Ethology 107:65–84. https://doi.org/10.1046/j.1439-0310.2001.00640.x
Borges SH, Magalli Henriques L, Carvalhaes A (2004) Density and habitat use by owls in two Amazonian forest types. J Field Ornithol 75:176–182. https://doi.org/10.1648/0273-8570-75.2.176
Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer Associates, Sunderland
Browning E, Gibb R, Glover-Kapfer P, Jones KE (2017) Passive acoustic monitoring in ecology and conservation. WWF Conserv Technol Series 1:1–75
Buchanan GM, Donald PF, Butchart SHM (2011) Identifying priority areas for conservation: a global assessment for forest-dependent birds. PLoS One 6:e29080. https://doi.org/10.1371/journal.pone.0029080
Buckland ST, Anderson DR, Burnham KP et al (2001) Introduction to Distance Sampling: Estimating Abundance of Biological Populations. Oxford University Press, Oxford
Campos-Cerqueira M, Aide TM (2016) Improving distribution data of threatened species by combining acoustic monitoring and occupancy modelling. Methods Ecol Evol 7:1340–1348. https://doi.org/10.1111/2041-210X.12599
Catchpole C, Slater PJB (2008) Bird song: biological themes and variations, 2nd edn. Cambridge University Press, Cambridge
Choi W, Lee J-H, Sung H-C (2019) A case study of male tawny owl (Strix aluco) vocalizations in South Korea: call feature, individuality, and the potential use for census. Animal Cells and Systems 23:90–96. https://doi.org/10.1080/19768354.2019.1592022
Collen B, Pettorelli N, Baillie JEM, Durant SM (2013) Biodiversity Monitoring and Conservation: Bridging the Gap between Global Commitment and Local Action. Wiley-Blackwell, Oxford, UK
D’Amelio PB, Klumb M, Adreani MN et al (2017) Individual recognition of opposite sex vocalizations in the zebra finch. Sci Rep 7:5579. https://doi.org/10.1038/s41598-017-05982-x
Darras K, Batáry P, Furnas BJ et al (2019) Autonomous sound recording outperforms human observation for sampling birds: a systematic map and user guide. Ecol Appl 29:e01954. https://doi.org/10.1002/eap.1954
Delport W, Kemp AC, Ferguson JWH (2002) Vocal identification of individual African Wood Owls Strix woodfordii: a technique to monitor long-term adult turnover and residency: Hoot-calls of African Wood Owls. Ibis 144:30–39. https://doi.org/10.1046/j.0019-1019.2001.00019.x
Dowle M, Srinivasan A (2019) data.table: Extension of `data.frame`. Version R package version 1.12.2.URL https://CRAN.R-project.org/package=data.table
Dragonetti M (2007) Individuality in Scops Owl Otus scops Vocalisations. Bioacoustics 16:147–172. https://doi.org/10.1080/09524622.2007.9753573
Feng J-J, Cui L-W, Ma C-Y et al (2014) Individuality and stability in Male songs of Cao Vit Gibbons (Nomascus nasutus) with potential to monitor population dynamics. PLoS One 9:e96317. https://doi.org/10.1371/journal.pone.0096317
Freitas B, Melo M, do Bom Jesus C, et al (2023) The recently discovered Principe Scops-owl is highly threatened: distribution, habitat associations, and population estimates. Bird Conserv Int 33:e39. https://doi.org/10.1017/S0959270922000429
Galeotti P, Sacchi R (2001) Turnover of territorial Scops Owls Otus scops as estimated by spectrographic analyses of male hoots. J Avian Biol 32:256–262. https://doi.org/10.1111/j.0908-8857.2001.320308.x
Gilbert G, Tyler GA, Smith KW (2002) Local annual survival of booming male Great Bittern Botaurus stellaris in Britain, in the period 1990–1999: survival of booming male Great Bittern. Ibis 144:51–61. https://doi.org/10.1046/j.0019-1019.2001.00012.x
Hill AP, Prince P, Piña Covarrubias E et al (2018) AudioMoth: evaluation of a smart open acoustic device for monitoring biodiversity and the environment. Methods Ecol Evol 9:1199–1211. https://doi.org/10.1111/2041-210X.12955
Hill AP, Prince P, Snaddon JL et al (2019) AudioMoth: a low-cost acoustic device for monitoring biodiversity and the environment. HardwareX 6:e00073. https://doi.org/10.1016/j.ohx.2019.e00073
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
IUCN (2020) The IUCN Red List of Threatened Species. 2020–2. https://www.iucnredlist.org. Downloaded on July 2020.
Jones PJ (1994) Biodiversity in the Gulf of Guinea: an overview. Biodivers Conserv 3:772–784. https://doi.org/10.1007/BF00129657
Jones P, Tye A (2006) The Birds of São Tomé and Príncipe, with Annobón: Islands of the Gulf of Guinea. British Ornithologists’ Union and British Ornithologists’ Club, Oxford
Kahl S, Wood CM, Eibl M, Klinck H (2021) BirdNET: a deep learning solution for avian diversity monitoring. Ecol Inform 61:101236. https://doi.org/10.1016/j.ecoinf.2021.101236
Kassambara A, Mundt F (2017) factoextra: extract and visualize the results of multivariate data analyses. Version R package version 1.0.5URL https://CRAN.R-project.org/package=factoextra
König C, Weick F (2008) Owls of the World, 2nd edn. Yale University Press, New Haven
Lê S, Josse J, Husson F (2008) FactoMineR: an R Package for multivariate analysis. J Stat Softw 25:1–18. https://doi.org/10.18637/jss.v025.i01
Le Saout S, Hoffmann M, Shi Y et al (2013) Protected areas and effective biodiversity conservation. Science 342:803–805. https://doi.org/10.1126/science.1239268
Lengagne T (2001) Temporal stability in the individual features in the calls of Eagle Owls (Bubo bubo). Behaviour 138:1407–1419
Lengagne T, Lauga J, Jouventin P (1997) A method of independent time and frequency decomposition of bioacoustic signals: inter-individual recognition in four species of penguins. Comptes Rendus De L’Académie Des Sciences - Series III - Sciences De La Vie 320:885–891. https://doi.org/10.1016/S0764-4469(97)80873-6
Liaw A, Wiener M (2002) Classification and regression by randomForest. R news 2:18–22
Madeira B (2018) Sexual dimorphism and reproductive phenology of common birds in São Tomé Island - conservation implications. MSc Thesis, Universidade de Lisboa
Marsland S, Priyadarshani N, Juodakis J, Castro I (2019) AviaNZ: A future-proofed program for annotation and recognition of animal sounds in long-time field recordings. Methods Ecol Evol 10:1189–1195. https://doi.org/10.1111/2041-210X.13213
Melo M, Dallimer M (2009) Is there an undiscovered endemic scops owl Otus sp. on Príncipe Island? Malimbus 31:109–115
Melo M, Freitas B, Verbelen P et al (2022) A new species of scops-owl (Aves, Strigiformes, Strigidae, Otus) from Príncipe Island (Gulf of Guinea, Africa) and novel insights into the systematic affinities within Otus. ZK 1126:1–54. https://doi.org/10.3897/zookeys.1126.87635
Mennill DJ, Vehrencamp SL (2008) Context-dependent functions of avian duets revealed by microphone-array recordings and multispeaker playback. Curr Biol 18:1314–1319. https://doi.org/10.1016/j.cub.2008.07.073
Metcalf OC, Barlow J, Bas Y et al (2022) Detecting and reducing heterogeneity of error in acoustic classification. Methods Ecol Evol. https://doi.org/10.1111/2041-210X.13967
Mishima Y, Morisaka T, Itoh M et al (2015) Individuality embedded in the isolation calls of captive beluga whales (Delphinapterus leucas). Zool Lett 1:27. https://doi.org/10.1186/s40851-015-0028-x
Nagy CM, Rockwell RF (2012) Identification of individual Eastern Screech-Owls Megascops asio via vocalization analysis. Bioacoustics 21:127–140. https://doi.org/10.1080/09524622.2011.651829
Najmi-Hanis Z, Puan CL, Zakaria M, Azhar B (2016) Home range and activity patterns of Sunda scops owl in Peninsular Malaysia. Raffles Bull Zool 64:28–32
Odom K, Mennill D (2010) Vocal duets in a nonpasserine: an examination of territory defence and neighbour–stranger discrimination in a neighbourhood of barred Owls. Behav 147:619–639. https://doi.org/10.1163/000579510X12632972452424
Odom KJ, Slaght JC, Gutiérrez RJ (2013) Distinctiveness in the territorial calls of great Horned Owls within and among years. J Raptor Res 47:21–30. https://doi.org/10.3356/JRR-12-11.1
Pilla P, Puan CL, Lim V-C et al (2018) Sunda Scops-Owl density estimation via distance sampling and call playback. Sains Malaysiana 47:441–446. https://doi.org/10.17576/jsm-2018-4703-03
Pinheiro J, Bates D (2023) nlme: Linear and Nonlinear Mixed Effects Models. Version R package version 3.1–162URL https://CRAN.R-project.org/package=nlme
R Core Team (2017) R: A language and environment for statistical computing v.3.6. Version 3.6. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
Ripley B, Hornik K, Gebhardt A (2020) MASS: support functions and datasets for Venables and Ripley’s MASS. Version R package version 7.3–58.1URL https://stat.ethz.ch/R-manual/R-devel/library/MASS/html/00Index.html
Robert A, Lengagne T, Melo M et al (2019) The theory of island biogeography and soundscapes: species diversity and the organization of acoustic communities. J Biogeogr 46:1901–1911. https://doi.org/10.1111/jbi.13611
Robin X, Turck N, Hainard A et al (2011) pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12:77. https://doi.org/10.1186/1471-2105-12-77
Robisson P, Aubin T, Bremond J-C (1993) Individuality in the voice of the Emperor Penguin Aptenodytes forsteri: adaptation to a noisy environment. Ethology 94:279–290. https://doi.org/10.1111/j.1439-0310.1993.tb00445.x
Roemer C, Julien J, Bas Y (2021) An automatic classifier of bat sonotypes around the world. Methods Ecol Evol 12:2432–2444. https://doi.org/10.1111/2041-210X.13721
RStudio Team (2015) RStudio: Integrated development environment for R. Version Version 1.1.447. RStudio Inc., Boston
Scherrer B (1984) Biostatistique. Gaetan Morin Editeur. Chicoutimi, Québec
Stattersfield AJ, Crosby MJ, Long AJ, Wege DC (1998) Endemic Bird Areas of the World: Priorities for Biodiversity Conservation. BirdLife International, Cambridge
Stutchbury BJ, Morton ES (2001) Behavioral Ecology of Tropical Birds. Academic Press, San Diego
Sueur J, Gasc A, Grandcolas P, Pavoine S (2012) Global estimation of animal diversity using automatic acoustic sensors. In: Le Galliard J-F, Guarini J-M, Gaill F (eds) Sensors for ecology: towards integrated knowledge of ecosystems. CNRS-[Institut écologie et environnement], Paris
Terry AM, Peake TM, McGregor PK (2005) The role of vocal individuality in conservation. Front Zool 2:10. https://doi.org/10.1186/1742-9994-2-10
Thornton IWB (2007) Island colonization: the origin and development of island communities. Cambridge University Press, Cambridge
Torben D, Mathevon N (2002) Why do songbirds sing intensively at dawn? A test of the acoustic transmission hypothesis. Acta Ethologica 4:65–72. https://doi.org/10.1007/s10211-001-0056-8
Tripp TM, Otter KA (2006) Vocal individuality as a potential long-term monitoring tool for Western Screech-Owls, Megascops kennicottii. Can J Zool 84:744–753. https://doi.org/10.1139/z06-055
Ulloa JS, Gasc A, Gaucher P et al (2016) Screening large audio datasets to determine the time and space distribution of Screaming Piha birds in a tropical forest. Eco Inform 31:91–99. https://doi.org/10.1016/j.ecoinf.2015.11.012
UNESCO (2012) The Island of Príncipe. http://www.unesco.org/new/en/natural-sciences/environment/ecological-sciences/biosphere-reserves/africa/sao-tome-and-principe/the-island-of-principe. Accessed 22 Jul 2019
Valente L, Phillimore AB, Melo M et al (2020) A simple dynamic model explains the diversity of island birds worldwide. Nature 579:92–96. https://doi.org/10.1038/s41586-020-2022-5
Venables WN, Ripley BD, Venables WN (2002) Modern applied statistics with S, 4th edn. Springer, New York
Verbelen P, Melo M, Sangster G, Spina F (2016) A 90-year-old mystery solved: a potentially new species of owl from Príncipe. Oryx 50:581. https://doi.org/10.1017/S0030605316000831
Whittaker RJ, Fernández-Palacios JM, Matthews TJ et al (2017) Island biogeography: taking the long view of nature’s laboratories. Science 357:eaam8326. https://doi.org/10.1126/science.aam8326
Wickham H (2016) ggplot2: elegant graphics for data analysis, 2nd edn. Springer, Cham
Winkler DW, Billerman SM, Lovette IJ (2020) Owls (Strigidae). In: Billerman SM, Keeney BK, Rodewald PG, Schulenberg TS (eds) Birds of the World. Cornell Lab of Ornithology, New York
Wrege PH, Rowland ED, Keen S, Shiu Y (2017) Acoustic monitoring for conservation in tropical forests: examples from forest elephants. Methods Ecol Evol 8:1292–1301. https://doi.org/10.1111/2041-210X.12730
Yee SA, Puan CL, Chang PK, Azhar B (2016) Vocal individuality of Sunda Scops-Owl (Otus lempiji) in Peninsular Malaysia. J Raptor Res 50:379–390. https://doi.org/10.3356/JRR-15-76.1
Zhou B, Xia C-W, Chen Z-R, Deng W-H (2020) Individual identification of Male Ural Owls based on territorial calls. J Raptor Res 54:57. https://doi.org/10.3356/0892-1016-54.1.57
Acknowledgements
We thank everyone at Forever Príncipe for the full logistic support of the field expeditions and in particular: Rombout and Ella Swanborn, Myles Oates, Walter Jubber, and everyone at Roça Belo Monte. We thank the additional logistic support from the Príncipe Foundation, of its director Estrela Matilde and staff. We are extremely thankful to our field assistants Ceciliano do Bom Jesus, Sátiro Costa, Dy, Ni and Nidi, without whom field work would not have been possible. We also thank the two anonymous reviewers for their insightful comments, which greatly improved the manuscript.
Funding
Fieldwork was supported by Forever Príncipe and the National Geographic Society (Early career grant—EC-364C-18 attributed to BF), and was developed in collaboration with the Príncipe Obô Natural Park and Príncipe Foundation, which provided key logistic support. This project was also supported via the European Union Horizon’s 2020 research and innovation program under grant agreement 854248 and through the Erasmus + program of the European Union (grant attributed to BF: SMT192047023). The Portuguese Foundation for Science and Technology (Fundação para a Ciência e a Tecnologia—FCT) provided structural funding to CIBIO (UIDB/50027/2020).
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Conceptualization: BF, MM; Methodology: BF, YB, AR, CD, MM; Formal analysis: BF, YB; Investigation: BF, MM; Writing—original draft preparation: BF; Writing—review & editing: YB, AR, CD, MM; Funding acquisition: BF, MM; Supervision: YB, CD, MM.
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Fieldwork in Príncipe Obô Natural Park was authorised by Arlindo Carvalho, director of the Department of the Environment of São Tomé and Príncipe, Daniel Ramos, director of the Príncipe Obô Natural Park and Plácida Lopes, Director of the Príncipe Biosphere Reserve.
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Freitas, B., Bas, Y., Robert, A. et al. Passive acoustic monitoring in difficult terrains: the case of the Principe Scops-Owl. Biodivers Conserv 32, 3109–3132 (2023). https://doi.org/10.1007/s10531-023-02642-7
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DOI: https://doi.org/10.1007/s10531-023-02642-7