Aplicando técnicas de bioacústica a estudios de ornitología urbana: guía y recomendaciones

Rocío Bahía; Sergio A. Lambertucci; Karina L. Speziale

doi:10.56178/eh.v37i2.394

Methodologies and Supports in Research Published 01 December 2022 https://doi.org/10.56178/eh.v37i2.394

Applying bioacoustic techniques to urban ornithology studies: guidelines and recommendations

bioacoustics birds conservation passive acoustic monitoring research tool soundscape technology urban ecology

Rocío Bahía Grupo de Investigaciones en Biología de la Conservación (GRINBIC), Laboratorio Ecotono, INIBIOMA, Universidad Nacional del Comahue - CONICET, Quintral 1250 (R8400FRF), San Carlos de Bariloche, Argentina.

Sergio A. Lambertucci Grupo de Investigaciones en Biología de la Conservación (GRINBIC), Laboratorio Ecotono, INIBIOMA, Universidad Nacional del Comahue - CONICET, Quintral 1250 (R8400FRF), San Carlos de Bariloche, Argentina.

Karina L. Speziale Grupo de Investigaciones en Biología de la Conservación (GRINBIC), Laboratorio Ecotono, INIBIOMA, Universidad Nacional del Comahue - CONICET, Quintral 1250 (R8400FRF), San Carlos de Bariloche, Argentina.

Abstract

One of the main ways birds communicate, through the emission of sounds or vocalizations, can be affected by sounds produced by human activities in urban areas. These noises or disturbances interfere with bird communication, affecting mate identification, reproductive processes, territory defense, and even bird community richness and diversity. In this way, urban areas constitute complex sound environments for birds. Bioacoustics, through passive acoustic monitoring (PAM), is a growing tool with numerous advantages especially useful for urban ecology studies. PAM is a non-invasive and effective method for obtaining information autonomously, continuously, simultaneously and under various environmental conditions. Despite this, it is still an under-exploited tool in Neotropical countries. We here provide a methodological description showing the potential of PAM in bird research, particularly for birds living in urban and/or peri-urban environments. To this end, we conducted a non-systematic review of the existing literature presenting basic notions of sound and its recording process, options of microphone and recorders associated with the PAM, sampling designs, analyzes programs, and acoustic indexes. We also present examples of our research on monitoring urban environments in Patagonia. We highlight the value of this study tool for long-term research, complex study sites, monitoring programs and conservation projects.

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References

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Alcocer I, Lima H, Sugai Lsm y Llusia D (2022). Acoustic indices as proxies for biodiversity: a meta-analysis. Biological Reviews 97:2209-2236.
Aronson MF, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, Warren PS, Williams NS, Cilliers S y Clarkson B (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proceedings of the Royal Society B: Biological Sciences 281:20133330.
Bahia R, Lambertucci SA, Plaza PI y Speziale KL (2021) Antagonistic-mutualistic interaction between parrots and plants in the context of global change: Biological introductions and novel ecosystems. Biological Conservation, 109399.
Bahia R, Speziale K y Lambertucci SA (2022). Sacar la voz: Tres especies de aves del Bosque Andino-Patagónico cambian sus vocalizaciones en respuesta al sonido antrópico. XIX Reunión Argentina de Ornitología, Puerto Madryn. doi: 10.13140/RG.2.2.27591.78241
Baker MC y Logue DM (2007) A comparison of three noise reduction procedures applied to bird vocal signals. Journal of Field Ornithology 78:240–253.
Blumstein DT, Mennill DJ, Clemins P, Girod L, Yao K, Patricelli G, Deppe JL, Krakauer AH, Clark C y Cortopassi KA (2011) Acoustic monitoring in terrestrial environments using microphone arrays: applications, technological considerations and prospectus. Journal of Applied Ecology 48:758–767.
Boelman NT, Asner GP, Hart PJ y Martin RE (2007) Multi‐trophic invasion resistance in Hawaii: bioacoustics, field surveys, and airborne remote sensing. Ecological Applications 17:2137–2144.
Borker AL, McKown MW, Ackerman JT, EAGLES‐SMITH CA, Tershy BR y Croll DA (2014) Vocal activity as a low cost and scalable index of seabird colony size. Conservation Biology 28: 1100–1108.
Bradbury J y Vehrencamp S (2011) Principles of animal communication, 2nd edn Sunderland. MA: Sinauer Associates.
Browning E, Gibb R, Glover-Kapfer P y Jones KE (2017) Passive acoustic monitoring in ecology and conservation. 76pp. WWF Conservation Technology Series 1(2).
Brumm H (2004) The impact of environmental noise on song amplitude in a territorial bird. Journal of Animal Ecology, 434–440.
Brumm H y Slabbekoorn H (2005) Acoustic communication in noise. Advances in the Study of Behavior 35:151–209.
Catchpole CK y Slater PJ (2003) Bird song: biological themes and variations. Cambridge University press.
Caycedo-Rosales PC, Ruiz-Muñoz JF y Orozco-Alzate M (2013) Reconocimiento automatizado de señales bioacústicas: Una revisión de métodos y aplicaciones. Ingeniería y Ciencia 9:171–195.
Chace JF y Walsh JJ (2006) Urban effects on native avifauna: a review. Landscape and Urban Planning 74:46–69.
Chambert T, Waddle JH, Miller DA, Walls SC y Nichols JD (2018) A new framework for analysing automated acoustic species detection data: Occupancy estimation and optimization of recordings post‐processing. Methods in Ecology and Evolution 9:560–570.
Cole JS, Michel NL, Emerson SA y Siegel RB (2022) Automated bird sound classifications of long-duration recordings produce occupancy model outputs similar to manually annotated data. Ornithological Applications 124:duac003.
Darras K, Furnas B, Fitriawan I, Mulyani Y y Tscharntke T (2018) Estimating bird detection distances in sound recordings for standardizing detection ranges and distance sampling. Methods in Ecology and Evolution 9:1928–1938.
Darras K, Pütz P, Rembold K y Tscharntke T (2016) Measuring sound detection spaces for acoustic animal sampling and monitoring. Biological Conservation 201:29–37.
Deichmann JL, Hernández-Serna A, Campos-Cerqueira M y Aide TM (2017) Soundscape analysis and acoustic monitoring document impacts of natural gas exploration on biodiversity in a tropical forest. Ecological Indicators 74:39–48.
Depraetere M, Pavoine S, Jiguet F, Gasc A, Duvail S y Sueur J (2012) Monitoring animal diversity using acoustic indices: implementation in a temperate woodland. Ecological Indicators 13:46–54.
Elizalde L y Lambertucci SA (2022). Private gardens in a town immersed in a National Park: Potential for conservation and highly valued under COVID lockdown. Landscape and Urban Planning 226:104481.
Figueira L, Tella JL, Camargo UM y Ferraz G (2015) Autonomous sound monitoring shows higher use of Amazon old growth than secondary forest by parrots. Biological Conservation 184:27–35.
Fischer JD, Schneider SC, Ahlers AA y Miller JR (2015) Categorizing wildlife responses to urbanization and conservation implications of terminology. Conservation Biology 29:1246–1248.
Fontana CS, Burger MI y Magnusson WE (2011) Bird diversity in a subtropical South-American City: effects of noise levels, arborisation and human population density. Urban Ecosystems 14:341–360.
Frommolt K-H (2017) Information obtained from long-term acoustic recordings: applying bioacoustic techniques for monitoring wetland birds during breeding season. Journal of Ornithology 158:659–668.
Garaffa PI, Filloy J y Bellocq MI (2009) Bird community responses along urban–rural gradients: does the size of the urbanized area matter? Landscape and Urban Planning 90:33–41.
Gasc A, Francomano D, Dunning JB y Pijanowski BC (2017) Future directions for soundscape ecology: The importance of ornithological contributions. The Auk: Ornithological Advances 134:215–228.
Gil D y Brumm H (2014) Avian urban ecology. Oxford University Press.
Gil D, Honarmand M, Pascual J, Pérez-Mena E y Macías Garcia C (2015) Birds living near airports advance their dawn chorus and reduce overlap with aircraft noise. Behavioral Ecology 26:435–443.
Goddard MA, Ikin K y Lerman SB (2017). Ecological and social factors determining the diversity of birds in residential yards and gardens. Pp: 371-397. In: Ecology and conservation of birds in urban environments. Springer, Cham.
Gomes L, Solé M, Sousa-Lima RS y Baumgarten JE (2022) influence of anthropogenic sounds on insect, anuran and bird acoustic signals: A Meta-Analysis. Frontiers in Ecology and Evolution 10:827440.
Gonçalves SF, de Paula Lourenco AC, de Sousa Bueno Filho JS y de Toledo MCB (2021) Characteristics of residential backyards that contribute to conservation and diversity of urban birds: A case study in a Southeastern Brazilian city. Urban Forestry & Urban Greening, 61:127095.
Goyette JL, Howe RW, Wolf AT y Robinson WD (2011) Detecting tropical nocturnal birds using automated audio recordings. Journal of Field Ornithology 82:279–287.
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Harding HR, Gordon TA, Eastcott E, Simpson SD y Radford AN (2019) Causes and consequences of intraspecific variation in animal responses to anthropogenic noise. Behavioral Ecology 30:1501–1511.
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Hu Y y Cardoso GC (2010) Which birds adjust the frequency of vocalizations in urban noise? Animal Behaviour 79:863–867.
Kasten EP, Gage SH, Fox J y Joo W (2012) The remote environmental assessment laboratory’s acoustic library: An archive for studying soundscape ecology. Ecological informatics 12:50–67.
Kowarik I (2011) Novel urban ecosystems, biodiversity, and conservation. Environmental Pollution 159:1974–1983.
Kułaga K y Budka M (2019) Bird species detection by an observer and an autonomous sound recorder in two different environments: Forest and farmland. PLoS One 14: e0211970.
Laiolo P (2010) The emerging significance of bioacoustics in animal species conservation. Biological Conservation 143:1635–1645.
Lambert KT y McDonald PG (2014) A low‐cost, yet simple and highly repeatable system for acoustically surveying cryptic species. Austral Ecology 39:779–785.
León E, Beltzer A y Quiroga M (2014) El jilguero dorado (Sicalis flaveola) modifica la estructura de sus vocalizaciones para adaptarse a hábitats urbanos. Revista mexicana de Biodiversidad 85:546–552.
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How to cite

Rocío Bahía, Sergio A. Lambertucci, Karina L. Speziale (2022). Applying bioacoustic techniques to urban ornithology studies: guidelines and recommendations. El Hornero, Vol. 37 No. 2 (2022), 47-64. https://doi.org/10.56178/eh.v37i2.394

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[1] Aide TM, Corrada-Bravo C, Campos-Cerqueira M, Milan C, Vega G y Alvarez R (2013) Real-time bioacoustics monitoring and automated species identification. PeerJ 1:e103.

[2] Alcocer I, Lima H, Sugai Lsm y Llusia D (2022). Acoustic indices as proxies for biodiversity: a meta-analysis. Biological Reviews 97:2209-2236.

[3] Aronson MF, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, Warren PS, Williams NS, Cilliers S y Clarkson B (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proceedings of the Royal Society B: Biological Sciences 281:20133330.

[4] Bahia R, Lambertucci SA, Plaza PI y Speziale KL (2021) Antagonistic-mutualistic interaction between parrots and plants in the context of global change: Biological introductions and novel ecosystems. Biological Conservation, 109399.

[5] Bahia R, Speziale K y Lambertucci SA (2022). Sacar la voz: Tres especies de aves del Bosque Andino-Patagónico cambian sus vocalizaciones en respuesta al sonido antrópico. XIX Reunión Argentina de Ornitología, Puerto Madryn. doi: 10.13140/RG.2.2.27591.78241

[6] Baker MC y Logue DM (2007) A comparison of three noise reduction procedures applied to bird vocal signals. Journal of Field Ornithology 78:240–253.

[7] Blumstein DT, Mennill DJ, Clemins P, Girod L, Yao K, Patricelli G, Deppe JL, Krakauer AH, Clark C y Cortopassi KA (2011) Acoustic monitoring in terrestrial environments using microphone arrays: applications, technological considerations and prospectus. Journal of Applied Ecology 48:758–767.

[8] Boelman NT, Asner GP, Hart PJ y Martin RE (2007) Multi‐trophic invasion resistance in Hawaii: bioacoustics, field surveys, and airborne remote sensing. Ecological Applications 17:2137–2144.

[9] Borker AL, McKown MW, Ackerman JT, EAGLES‐SMITH CA, Tershy BR y Croll DA (2014) Vocal activity as a low cost and scalable index of seabird colony size. Conservation Biology 28: 1100–1108.

[10] Bradbury J y Vehrencamp S (2011) Principles of animal communication, 2nd edn Sunderland. MA: Sinauer Associates.

[11] Browning E, Gibb R, Glover-Kapfer P y Jones KE (2017) Passive acoustic monitoring in ecology and conservation. 76pp. WWF Conservation Technology Series 1(2).

[12] Brumm H (2004) The impact of environmental noise on song amplitude in a territorial bird. Journal of Animal Ecology, 434–440.

[13] Brumm H y Slabbekoorn H (2005) Acoustic communication in noise. Advances in the Study of Behavior 35:151–209.

[14] Catchpole CK y Slater PJ (2003) Bird song: biological themes and variations. Cambridge University press.

[15] Caycedo-Rosales PC, Ruiz-Muñoz JF y Orozco-Alzate M (2013) Reconocimiento automatizado de señales bioacústicas: Una revisión de métodos y aplicaciones. Ingeniería y Ciencia 9:171–195.

[16] Chace JF y Walsh JJ (2006) Urban effects on native avifauna: a review. Landscape and Urban Planning 74:46–69.

[17] Chambert T, Waddle JH, Miller DA, Walls SC y Nichols JD (2018) A new framework for analysing automated acoustic species detection data: Occupancy estimation and optimization of recordings post‐processing. Methods in Ecology and Evolution 9:560–570.

[18] Cole JS, Michel NL, Emerson SA y Siegel RB (2022) Automated bird sound classifications of long-duration recordings produce occupancy model outputs similar to manually annotated data. Ornithological Applications 124:duac003.

[19] Darras K, Furnas B, Fitriawan I, Mulyani Y y Tscharntke T (2018) Estimating bird detection distances in sound recordings for standardizing detection ranges and distance sampling. Methods in Ecology and Evolution 9:1928–1938.

[20] Darras K, Pütz P, Rembold K y Tscharntke T (2016) Measuring sound detection spaces for acoustic animal sampling and monitoring. Biological Conservation 201:29–37.

[21] Deichmann JL, Hernández-Serna A, Campos-Cerqueira M y Aide TM (2017) Soundscape analysis and acoustic monitoring document impacts of natural gas exploration on biodiversity in a tropical forest. Ecological Indicators 74:39–48.

[22] Depraetere M, Pavoine S, Jiguet F, Gasc A, Duvail S y Sueur J (2012) Monitoring animal diversity using acoustic indices: implementation in a temperate woodland. Ecological Indicators 13:46–54.

[23] Elizalde L y Lambertucci SA (2022). Private gardens in a town immersed in a National Park: Potential for conservation and highly valued under COVID lockdown. Landscape and Urban Planning 226:104481.

[24] Figueira L, Tella JL, Camargo UM y Ferraz G (2015) Autonomous sound monitoring shows higher use of Amazon old growth than secondary forest by parrots. Biological Conservation 184:27–35.

[25] Fischer JD, Schneider SC, Ahlers AA y Miller JR (2015) Categorizing wildlife responses to urbanization and conservation implications of terminology. Conservation Biology 29:1246–1248.

[26] Fontana CS, Burger MI y Magnusson WE (2011) Bird diversity in a subtropical South-American City: effects of noise levels, arborisation and human population density. Urban Ecosystems 14:341–360.

[27] Frommolt K-H (2017) Information obtained from long-term acoustic recordings: applying bioacoustic techniques for monitoring wetland birds during breeding season. Journal of Ornithology 158:659–668.

[28] Garaffa PI, Filloy J y Bellocq MI (2009) Bird community responses along urban–rural gradients: does the size of the urbanized area matter? Landscape and Urban Planning 90:33–41.

[29] Gasc A, Francomano D, Dunning JB y Pijanowski BC (2017) Future directions for soundscape ecology: The importance of ornithological contributions. The Auk: Ornithological Advances 134:215–228.

[30] Gil D y Brumm H (2014) Avian urban ecology. Oxford University Press.

[31] Gil D, Honarmand M, Pascual J, Pérez-Mena E y Macías Garcia C (2015) Birds living near airports advance their dawn chorus and reduce overlap with aircraft noise. Behavioral Ecology 26:435–443.

[32] Goddard MA, Ikin K y Lerman SB (2017). Ecological and social factors determining the diversity of birds in residential yards and gardens. Pp: 371-397. In: Ecology and conservation of birds in urban environments. Springer, Cham.

[33] Gomes L, Solé M, Sousa-Lima RS y Baumgarten JE (2022) influence of anthropogenic sounds on insect, anuran and bird acoustic signals: A Meta-Analysis. Frontiers in Ecology and Evolution 10:827440.

[34] Gonçalves SF, de Paula Lourenco AC, de Sousa Bueno Filho JS y de Toledo MCB (2021) Characteristics of residential backyards that contribute to conservation and diversity of urban birds: A case study in a Southeastern Brazilian city. Urban Forestry & Urban Greening, 61:127095.

[35] Goyette JL, Howe RW, Wolf AT y Robinson WD (2011) Detecting tropical nocturnal birds using automated audio recordings. Journal of Field Ornithology 82:279–287.

[36] Hansen AJ, Knight RL, Marzluff JM, Powell S, Brown K, Gude PH y Jones K (2005) Effects of exurban development on biodiversity: patterns, mechanisms, and research needs. Ecological Applications 15:1893–1905.

[37] Harding HR, Gordon TA, Eastcott E, Simpson SD y Radford AN (2019) Causes and consequences of intraspecific variation in animal responses to anthropogenic noise. Behavioral Ecology 30:1501–1511.

[38] Herrera F (2002) Ecolocalización en guácharos: volando en la oscuridad. Boletín de la sociedad Venezolana de Espeleología 36:6–10.

[39] Hu Y y Cardoso GC (2010) Which birds adjust the frequency of vocalizations in urban noise? Animal Behaviour 79:863–867.

[40] Kasten EP, Gage SH, Fox J y Joo W (2012) The remote environmental assessment laboratory’s acoustic library: An archive for studying soundscape ecology. Ecological informatics 12:50–67.

[41] Kowarik I (2011) Novel urban ecosystems, biodiversity, and conservation. Environmental Pollution 159:1974–1983.

[42] Kułaga K y Budka M (2019) Bird species detection by an observer and an autonomous sound recorder in two different environments: Forest and farmland. PLoS One 14: e0211970.

[43] Laiolo P (2010) The emerging significance of bioacoustics in animal species conservation. Biological Conservation 143:1635–1645.

[44] Lambert KT y McDonald PG (2014) A low‐cost, yet simple and highly repeatable system for acoustically surveying cryptic species. Austral Ecology 39:779–785.

[45] León E, Beltzer A y Quiroga M (2014) El jilguero dorado (Sicalis flaveola) modifica la estructura de sus vocalizaciones para adaptarse a hábitats urbanos. Revista mexicana de Biodiversidad 85:546–552.

[46] de Magalhães Tolentino VC, Baesse CQ y de Melo C (2018) Dominant frequency of songs in tropical bird species is higher in sites with high noise pollution. Environmental Pollution 235:983–992.

[47] Manzano R, Bota G, Brotons L, Soto-Largo E y Pérez-Granados C (2022) Low-cost open-source recorders and ready-to-use machine learning approaches provide effective monitoring of threatened species. Ecological Informatics 101910.

[48] McClure CJ, Ware HE, Carlisle J, Kaltenecker G y Barber JR (2013) An experimental investigation into the effects of traffic noise on distributions of birds: avoiding the phantom road. Proceedings of the Royal Society B: Biological Sciences 280:20132290.

[49] Mendes S, Colino-Rabanal VJ y Peris SJ (2011) Diferencias en el canto de la ratona común (Troglodytes musculus) en ambientes con distintos niveles de influencia humana. Hornero 26:85–93.

[50] Merchant ND, Fristrup KM, Johnson, MP, Tyack PL, Witt MJ, Blondel P y Parks SE (2015) Measuring acoustic habitats. Methods in Ecology and Evolution 6:257–265.

[51] Munro J, Williamson I y Fuller S (2018) Traffic noise impacts on urban forest soundscapes in south‐eastern Australia. Austral Ecology 43:180–190.

[52] Nemeth E, Pieretti N, Zollinger SA, Geberzahn N, Partecke, J, Miranda AC y Brumm H (2013) Bird song and anthropogenic noise: vocal constraints may explain why birds sing higher-frequency songs in cities. Proceedings of the Royal Society B: Biological Sciences 280: 20122798.

[53] Newman G, Wiggins A, Crall A, Graham E, Newman S y Crowston K (2012) The future of citizen science: emerging technologies and shifting paradigms. Frontiers in Ecology and the Environment 10:298–304.

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