Skip to main content
Springer Nature Link
Log in

Mining noise affects loud call structures and emission patterns of wild black-fronted titi monkeys

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

Anthropogenic noise pollution is increasing and can constrain acoustic communication in animals. Our aim was to investigate if the acoustic parameters of loud calls and their diurnal pattern in the black-fronted titi monkey (Callicebus nigrifrons) are affected by noise produced by mining activity in a fragment of Atlantic Forest in Brazil. We installed two passive acoustic monitoring devices to record sound 24 h/day, 7 days every 2 months, for a year; one unit was close to an opencast mine and the other 2.5 km away from it. Both sites presented similar habitat structures and were inhabited by groups of black-fronted titi monkeys. We quantified the noise at both sites by measuring the equivalent continuous sound level every 2 months for 1 year and quantified the emission of loud calls by titi monkeys through visual inspection of the recordings. The close site presented higher ambient noise levels than the far site. The quantitative comparison of loud calls of black-fronted titi monkeys between the two sites showed less calling activity in the site close to the mine than in the site further away. Approximately 20 % of the calls detected at the site close to the mine were masked by noise from truck traffic. Loud calls were longer at the site far from the mine and the diurnal patterns of vocal activity differed in the amount of calling as well as in the timing of peak calling activity between the two sites. Our results indicate that mining noise may constrain titi monkeys’ long-distance vocal communication. Loud calls occupy a similar frequency band to mining noise, and an increase in ambient noise may be triggering black-fronted titi monkeys to adjust their long-distance communication patterns to avoid masking of their calls. Given that vocalizations are an important means of social interaction in this species, there are concerns about the impact of mining noise on populations exposed to this human activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2a, b
Fig. 3

Similar content being viewed by others

References

  • Alvarez-Berríos NL, Aide TM (2015) Global demand for gold is another threat for tropical forests. Environ Res Lett 10

  • Barber JR, Crooks KR, Fristrup KM (2009) The costs of chronic noise exposure for terrestrial organisms. Trends Ecol Evol 25:180–189

    Article  PubMed  Google Scholar 

  • Bayne EM, Habib L, Boutin S (2008) Impacts of chronic anthropogenic noise from energy-sector activity on abundance of songbirds in the boreal forest. Conserv Biol 22:1186–1193

    Article  PubMed  Google Scholar 

  • Bee MA, Swanson EM (2007) Auditory masking of anuran advertisement calls by road traffic noise. Anim Behav 74:1765–1776

    Article  Google Scholar 

  • Bejder L, Samuels A, Whitehead H, Gales N (2006) Interpreting short-term behavioural responses to disturbance within a longitudinal perspective. Anim Behav 72:1149–1158

    Article  Google Scholar 

  • Bertoluci J, Canelas MAS, Eisemberg CC, de Palmuti CFS, Montingelli GG (2009) Herpetofauna of Estação Ambiental de Peti, an Atlantic Rainforest fragment of Minas Gerais State, southeastern Brazil. Bio Neotrop 9:147–155

    Article  Google Scholar 

  • Brumm H (2004) The impact of environmental noise on song amplitude in a territorial bird. J Anim Ecol 73:434–440

    Article  Google Scholar 

  • Brumm H, Voss K, Köllmer I, Todt D (2004) Acoustic communication in noise: regulation of call characteristics in a New World monkey. J Exp Biol 207:443–448

    Article  PubMed  Google Scholar 

  • Brumm H, Schmidt R, Schrader L (2009) Noise-dependent vocal plasticity in domestic fowl. Anim Behav 78:741–746

    Article  Google Scholar 

  • Campo JL, Gil MG, Dávila SG (2005) Effects of specific noise and music stimuli on stress and fear levels of laying hens of several breeds. Appl Anim Behav Sci 91:75–84

    Article  Google Scholar 

  • Cäsar C, Byrne R, Young RJ, Zuberbühler K (2012) The alarm call system of wild black-fronted titi monkeys, Callicebus nigrifrons. Behav Ecol Sociobiol 66:653–667

    Article  Google Scholar 

  • Caselli CB, Setz EZF (2011) Feeding ecology and activity pattern of black-fronted titi monkeys (Callicebus nigrifrons) in a semideciduous tropical forest of southern Brazil. Primates 52:351

    Article  PubMed  Google Scholar 

  • Caselli CB, Mennill DJ, Bicca-Marques JC, Setz EZF (2014) Vocal behavior of black-fronted titi monkeys (Callicebus nigrifrons): acoustic properties and behavioral contexts of loud calls. Am J Primatol 76:788–800

    Article  PubMed  Google Scholar 

  • Chan AAY-H, Giraldo-Perez P, Smith S, Blumstein DT (2010) Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis. Biol Lett 6:458–461

    Article  PubMed  PubMed Central  Google Scholar 

  • Delaney DK, Gurbb TG, Seibr P, Pater LL, Reiser MH (1999) Effects of helicopter noise on Mexican spotted owls. J Wildl Manage 63:60–76

    Article  Google Scholar 

  • Duarte MHL, Vecci MA, Hirsch A, Young RJ (2011) Noisy human neighbours affect where urban monkeys live. Biol Lett 7:840–842

    Article  PubMed  PubMed Central  Google Scholar 

  • Duarte MHL, Sousa-Lima RS, Young RJ, Farina A, Vasconcelos M, Rodrigues M, Pieretti N (2015) The impact of noise from opencast mining on Atlantic Forest biophony. Biol Conserv 191:623–631

    Article  Google Scholar 

  • Estrada A (2009) Primate conservation in South America: the human and ecological dimensions of the problem. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates. Springer, New York, pp 463–505

    Chapter  Google Scholar 

  • Faria CM, Rodrigues M, do Amaral FQ, Módena É (2006) Aves de um fragmento de Mata Atlântica no alto Rio Doce, Minas Gerais: colonização e extinção. Rev Bras Zool 23:1217–1230

    Article  Google Scholar 

  • Foote AD, Osborne RW, Hoelzel AR (2004) Whale-call response to masking boat noise. Nature 428:910

    Article  CAS  PubMed  Google Scholar 

  • Francis CD, Ortega CP, Cruz A (2009) Noise pollution changes avian communities and species interactions. Curr Biol 19:1415–1419

    Article  CAS  PubMed  Google Scholar 

  • Fuller RA, Warren PH, Gaston KJ (2007) Day time noise predicts nocturnal singing in urban robins. Biol Lett 3:368–370

    Article  PubMed  PubMed Central  Google Scholar 

  • Geissmann T, Mütschler T (2006) Diurnal distribution of loud calls in sympatric wild indri (Indri indri) and ruffed lemurs (Varecia variegata): implications for call functions. Primates 47:393–396

    Article  PubMed  Google Scholar 

  • Gestich CC, Caselli CB, Nagy-Reis MB, Setz EZF, da Cunha RGT (2016) Estimating primate population densities: the systematic use of playbacks along transects in population surveys. Am J Primatol 9999:1–9

    Google Scholar 

  • Hage SR, Jiang T, Berquist SW, Feng J, Metzner W (2013) Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats. Proc Natl Acad Sci USA 110:4063–4068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bicca-Marques JC, Heymann EW (2013) Ecology and behavior of titi monkeys (genus Callicebus). In: Veiga LM, Barnett AA, Ferrari SF, Norconk MA (eds) Evolutionary biology and conservation of titis, sakis, and uacaris. Cambridge University, Cambridge, pp 196–207

    Chapter  Google Scholar 

  • Karp DS, Root TL (2009) Sound the stressor: how hoatzins (Opisthocomus hoazin) react to ecotourist conversation. Biodiv Conserv 18:3733–3742

    Article  Google Scholar 

  • Kight CR, Swaddle JP (2011) How and why environmental noise impacts animals: an integrative, mechanistic review: environmental noise and animals. Ecol Lett 14:1052–1061

    Article  PubMed  Google Scholar 

  • Kinzey WG, Robinson JG (1983) Intergroup loud calls, range size, and spacing in Callicebus torquatus. Am J Phys Anthropol 60:539–544

    Article  CAS  PubMed  Google Scholar 

  • Kinzey WG, Rosenberger AL, Heisler PS, Prowse DL, Trilling JS (1977) A preliminary field investigation of the yellow handed titi monkey, Callicebus torquatus torquatus, in northern Peru. Primates 18:159–181

    Article  Google Scholar 

  • Laiolo P (2010) The merging significance of bioacoustics in animal species conservation. Biol Conserv 143:1635–1645

    Article  Google Scholar 

  • León E, Beltzer A, Quiroga M (2014) El jilguero dorado (Sicalis flaveola) modifica la estructura de sus vocalizaciones para adaptar se a hábitats urbanos. Rev Mex Biod 85:546–552

    Article  Google Scholar 

  • Lohr B, Wright TF, Dooling RJ (2003) Detection and discrimination of natural calls in masking noise by birds: estimating the active space signal. Anim Behav 65:763–777

    Article  Google Scholar 

  • Machado RB, Fonseca GAB (2000) The avifauna of Rio Doce Valley, southeastern Brazil, a highly fragmented area. Biotropica 32:914–924

    Article  Google Scholar 

  • Madliger CL (2012) Toward improved conservation management: a consideration of sensory ecology. Biodivers Conserv 21:3277–3286

    Article  Google Scholar 

  • Melo FR, Mendes SL (2000) Emissão de gritos longos por grupos de Callicebus nigrifrons e suas reações a playbacks. In: Alonso C, Langgut A (eds) A Primatologia no Brasil—7. Sociedade Brasileira de Primatologia and Editora Universitária, João Pessoa, pp 215–222

    Google Scholar 

  • Miksis-Olds JL, Tyack PL (2009) Manatee (Thichechus manatus) vocalization usage in relation to environmental noise levels. J Acoust Soc Am 125:1806–1815

    Article  PubMed  Google Scholar 

  • Mitani JC (1985) Gibbon song duets and intergroup spacing. Behaviour 92:59–96

    Article  Google Scholar 

  • Nemeth E, Brumm H (2009) Blackbirds sing higher-pitched songs in cities: adaptation to habitat acoustics or side-effect of urbanization? Anim Behav 78:637–641

    Article  Google Scholar 

  • Paglia AP, Lopes MOG, Perini FA, Cunha HM (2005) Mammals of the Estação de Preservação e Desenvolvimento Ambiental de Peti (EPDA-Peti), São Gonçalo do Rio Abaixo, Minas Gerais, Brazil. Lundiana 6:89–96

    Google Scholar 

  • Parks ES, Clark CW, Tyack PL (2007) Short-and long-term changes in right whale calling behavior: the potential effects of noise on acoustic communication. J Acoust Soc Am 122:3725–3731

    Article  PubMed  Google Scholar 

  • Pieretti N, Duarte MHL, Sousa-Lima RS, Young RJ, Rodrigues M, Farina A (2015) Determining temporal sampling schemes for passive acoustic studies in different tropical environments. Trop Conserv Sci 8:215–234

    Article  Google Scholar 

  • Proppe DS, Sturdy CB, St Clair CC (2013) Anthropogenic noise decreases urban songbird diversity and may contribute to homogenization. Glob Chang Biol 19:1075–1084

    Article  PubMed  Google Scholar 

  • Rabin LA, McCowan B, Hooper SL, Owings DH (2003) Anthropogenic noise and its effect on animal communication: an interface between comparative psychology and conservation biology. Int J Psychol 16:172–192

    Google Scholar 

  • Reijen R, Foppen R, Braak CT, Thissen J (1998) The effects of car traffic and breeding bird populations in woodland. III. Reduction of density in relation to the proximity of main roads. J Appl Ecol 32:187–202

    Article  Google Scholar 

  • Rheindt FE (2003) The impact of roads on birds: does song frequency play a role in determining susceptibility to noise pollution? J Ornithol 144:295–306

    Article  Google Scholar 

  • Roberto JB (2010) Influência dos diversos tipos litológicos nas operações de concentração da instalação de beneficiamento de Brucutu. Master’s dissertation, Universidade Federal de Minas Gerais (available at http://www.bibliotecadigital.ufmg.br/dspace/handle/1843/BUOS-8DJFVY)

  • Robinson JG (1979) Vocal regulation of use of space by groups of titi monkeys Callicebus moloch. Behav Ecol Sociobiol 5:1–15

    Article  Google Scholar 

  • Robinson JG (1981) Vocal regulation of inter- and intra-group spacing during boundary encounters in the titi monkey, Callicebus moloch. Primates 22:161–172

    Article  Google Scholar 

  • Santos RV (2012) Área de vida e uso do espaço por Callicebus nigrifrons Spix, 1823 (Primates: Pitheciidae). Master’s dissertation, Pontifícia Universidade Católica de Minas Gerais

  • Santos GP, Galvão C, Young RJ (2012) The diet of wild black-fronted titi monkeys Callicebus nigrifrons during a bamboo masting year. Primates 53:265–272

    Article  PubMed  Google Scholar 

  • Schaub A, Ostwald J, Siemers BM (2008) Foraging bats avoid noise. J Exp Biol 211:3174–3180

    Article  PubMed  Google Scholar 

  • Schroeder J, Nakagawa S, Cleasby IR, Burke T (2012) Passerine birds breeding under chronic noise experience reduced fitness. PLoS One 7

  • Slabbekoorn H, den Boer-Visser A (2006) Cities change the songs of birds. Curr Biol 16:2326–2331

    Article  CAS  PubMed  Google Scholar 

  • Slabbekoorn H, Peet M (2003) Birds sing at a higher pitch in urban noise. Nature 424:267

    Article  CAS  PubMed  Google Scholar 

  • Slabbekoorn H, Ripmeester EA (2008) Birdsong and anthropogenic noise: implications and applications for conservation. Mol Ecol 17:72–83

    Article  PubMed  Google Scholar 

  • Sousa-Lima R, Clark C (2008) Modeling the effect of boat traffic on the fluctuation of humpback whale singing activity in the Abrolhos National Park, Brazil. Can Acoust 36:174–181

    Google Scholar 

  • Sousa-Lima RS, Clark CW (2009) Whale sound recording technology as a tool for assessing the effects of boat noise in a Brazilian marine park. Park Sci 26:59

    Google Scholar 

  • Sun JWC, Narins PM (2005) Anthropogenic sounds differentially affect amphibian call rate. Biol Conserv 121:419–427

    Article  Google Scholar 

  • Vargas-Salinas GM, Cunnington A, Amézquita L Fahrig (2014) Does traffic noise alter calling time in frogs and toads? A case study of anurans in eastern Ontario, Canada. Urban Ecosyst 17:945–953

    Article  Google Scholar 

  • Veiga LM, Kierulff CM, de Oliveira MM, Mendes SL (2008) Callicebus nigrifrons. The IUCN Red List of threatened species version 20143 http://www.iucnredlist.org. Accessed 17 December 2014

  • Warren PS, Katti M, Brazel Ermann M (2006) Urban bioacoustics: it’s not just noise. Anim Behav 71:491–502

    Article  Google Scholar 

  • Weiss DJ, Hotchkin CF, Parks SE (2014) Modification of spectral features by nonhuman primates. Behav Brain Sci 37:574–576

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiley RH, Richards DG (1978) Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav Ecol Soc 3:69–94

    Article  Google Scholar 

  • Zuberbuehler K, Noe R, Seyfarth RM (1997) Diana monkey long-distance calls: messages for conspecifics and predators. Anim Behav 53:589–604

    Article  Google Scholar 

Download references

Acknowledgements

We thank all the staff at the Peti Environmental Station, especially Leotacílio da Fonseca. We are also grateful to Luane Ferreira for help with the analyses and figures, Marina Scarpelli and Renan Duarte for their help during data acquisition, and engineer Krisdany Cavalcante for help with the noise measurements. We are grateful to Martin Fisher and two anonymous reviewers for comments on the manuscript. M. H. L. D. and M. C. K. were supported by CAPES (PNPD) and the Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG/VALE). M. R., R. J. Y. and R. S. L. received financial support from FAPEMIG/VALE and the Conselho Nacional de Pesquisa (CNPq).

Author information

Authors and Affiliations

  1. Conservation, Ecology and Animal Behaviour Group-Laboratory of Bioacoustics, Post-Graduate Program in Vertebrate Biology and Museum of Natural Sciences, Pontifical Catholic University of Minas Gerais, Avenida Dom José Gaspar, 290, Bairro Coração Eucarístico, Belo Horizonte, Minas Gerais, 30535-901, Brazil

    M. H. L. Duarte & M. C. Kaizer

  2. Laboratory of Ornithology, Department of Zoology, Federal University of Minas Gerais, Avenida Presidente Antônio Carlos, 6627, Bairro Pampulha, Belo Horizonte, Minas Gerais, 31270-901, Brazil

    M. H. L. Duarte & M. Rodrigues

  3. School of Environment and Life Sciences, Peel Building, University of Salford Manchester, Salford, M5 4WT, UK

    M. C. Kaizer & R. J. Young

  4. Laboratory of Bioacoustics (LaB), Department of Physiology and Behavior, Federal University of Rio Grande do Norte, Avenida Senador Salgado Filho, 3000, Bairro Lagoa Nova, Natal, RN, 59078-970, Brazil

    R. S. Sousa-Lima

Authors
  1. M. H. L. Duarte
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. M. C. Kaizer
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. R. J. Young
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. M. Rodrigues
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. R. S. Sousa-Lima
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to M. H. L. Duarte.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Duarte, M.H.L., Kaizer, M.C., Young, R.J. et al. Mining noise affects loud call structures and emission patterns of wild black-fronted titi monkeys. Primates 59, 89–97 (2018). https://doi.org/10.1007/s10329-017-0629-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-017-0629-4

Keywords