Abstract
Character displacement, or a shift in traits where species co-occur, is one of the most common ecological patterns to result from interactions between closely related species. Usually, character displacement is associated to divergence in traits, though, they might be convergent, especially when used for aggressive interference between species. In the context of animal communication, territorial calls are predicted to converge in order to increase context recognition and decrease the costs of ecological interference competition. However, such signals might also be adapted to characteristics of the shared environment. In this study, we used data from 15 groups of two parapatric tamarins, Saguinus midas and S. bicolor, to test for similarities in long calls among sympatric and allopatric groups. We hypothesized that calls would converge in sympatric areas, as it would be mutually beneficial if both species recognize territorial contexts, but that convergence would depend on forest type due to acoustic adaptation. As predicted, long calls converged in sympatry, with S. midas shifting its calls towards S. bicolor’s acoustic pattern. However, this shift only occurred in primary forest. In sympatric areas, S. midas produced sounds with narrower bandwidths in primary than in secondary forest, consistent with optimization of sound propagation while both species produced longer calls in primary forests independently of geographic location (i.e. sympatry and allopatry). Our results suggest that both social and environmental pressures are important in shaping tamarin sounds. As their effects can interact, analyses, which assume that these ecological pressures act independently, are likely to miss important patterns.
Significance statement
Territorial signals between closely related sympatric species are expected to be convergent to increase context recognition and decrease the costs of interference competition. However, such signals might also be adapted to characteristics of the shared environment, such as forest structure characteristics. We analysed vocalisations from two parapatric tamarins and found that, though their long calls asymmetrically converged in sympatry, only red-handed tamarins shifted towards pied tamarin call type, and this only occurred in primary forest. Our results suggest that both social and environmental pressures are important in shaping primate calls. Because their effects can interact, analyses which assume that these pressures act independently, are likely to miss important patterns.
Similar content being viewed by others
Data availability
Data are available as supplementary material.
References
Allen WL, Stevens M, Higham JP (2014) Character displacement of Cercopithecini primate visual signals. Nat Commun 5:4266. https://doi.org/10.1038/ncomms5266
Ayres JM, Mittermeier RA, Constable ID (1982) Brazilian tamarins on the way to extinction? Oryx 16:329–333. https://doi.org/10.1017/S0030605300017786
Bicudo T, Anciães M, Benchimol M, Peres CA, Simões PI (2016) Insularization effects on acoustic signals of 2 suboscine Amazonian birds. Behav Ecol 27:1480–1490. https://doi.org/10.1093/beheco/arw070
Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Oxford University Press, Oxford
Breheny P, Burchett W (2017) Visualization of regression models using visreg. R J 9:56–71. https://doi.org/10.32614/rj-2017-046
Brockelman WY, Schilling D (1984) Inheritance of stereotyped gibbon calls. Nature 312:634–636. https://doi.org/10.1038/312634a0
Brown WL, Wilson EO (1956) Character displacement. Syst Zool 5:49–64. https://doi.org/10.2307/2411924
Campbell P, Pasch B, Pino JL, Crino OL, Phillips M, Phelps SM (2010) Geographic variation in the songs of neotropical singing mice: testing the relative importance of drift and local adaptation. Evolution 64:1955–1972. https://doi.org/10.1111/j.1558-5646.2010.00962.x
Cardoso GC, Price TD (2010) Community convergence in bird song. Evol Ecol 24:447–461. https://doi.org/10.1007/s10682-009-9317-1
Chazdon R (2014) Second growth: the promise of tropical forest regeneration in an age of deforestation. Chicago Press, Chicago
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. https://doi.org/10.1146/annurev.ecolsys.31.1.343
Christensen C, Radford AN (2018) Dear enemies or nasty neighbors? Causes and consequences of variation in the responses of group-living species to territorial intrusions. Behav Ecol 29:1004–1013. https://doi.org/10.1093/beheco/ary010
Cody ML (1969) Convergent characteristics in sympatric species: a possible relation to interspecific competition and aggression. Condor 71:223–239. https://doi.org/10.2307/1366300
Cowen MC, Drury JP, Grether GF (2020) Multiple routes to interspecific territoriality in sister species of North American perching birds. Evolution 74:2134–2148. https://doi.org/10.1111/evo.14068
Crist E, Mora C, Engelman R (2017) The interaction of human population, food production, and biodiversity protection. Science 356:260–264. https://doi.org/10.1126/science.aal2011
Crockford C, Herbinger I, Vigilant L, Boesch C (2004) Wild chimpanzees produce group-specific calls: a case for vocal learning? Ethology 110:221–243. https://doi.org/10.1111/j.1439-0310.2004.00968.x
Curé C, Mathevon N, Mundry R, Aubin T (2012) Acoustic cues used for species recognition can differ between sexes and sibling species: evidence in shearwaters. Anim Behav 84:239–250
Dabelsteen T, Larsen ON, Pedersen SB (1993) Habitat-induced degradation of sound signals: quantifying the effects of communication sounds and bird location on blur ratio, excess attenuation, and signal-to-noise ratio in blackbird song. J Acoust Soc Am 93:2206. https://doi.org/10.1121/1.406682
Daniel JC, Blumstein DT (1998) A test of the acoustic adaptation hypothesis in four species of marmots. Anim Behav 56:1517–1528. https://doi.org/10.1006/anbe.1998.0929
Day RT, Elwood RW (1999) Sleeping site selection by the golden-handed tamarin Saguinus midas midas: the role of predation risk, proximity to feeding sites, and territorial defence. Ethology 105:1035–1051. https://doi.org/10.1046/j.1439-0310.1999.10512492.x
de Moura Bubadué J, Cáceres N, dos Santos CR, Sponchiado J, Passaro F, Saggese F, Mondanaro A, Raia P, Carotenuto F (2016) Character displacement under influence of bergmann’s rule in Cerdocyon thous (Mammalia: Canidae). Hystrix 27:83–90. https://doi.org/10.4404/hystrix-27.2-11433
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x
Drury JP, Cowen MC, Grether GF (2020) Competition and hybridization drive interspecific territoriality in birds. P Natl Acad Sci USA 117:12923–12930. https://doi.org/10.1073/pnas.1921380117
Egnor SER, Hauser MD (2004) A paradox in the evolution of primate vocal learning. Trends Neurosci 27:649–654. https://doi.org/10.1016/j.tins.2004.08.009
Estrada A, Garber PA, Mittermeier RA et al (2018) Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation. PeerJ 6:e4869. https://doi.org/10.7717/peerj.4869
Ey E, Fischer J (2009) The “acoustic adaptation hypothesis”—a review of the evidence from birds, anurans and mammals. Bioacoustics 19:21–48. https://doi.org/10.1080/09524622.2009.9753613
Freitas M de O, Toledo LF (2020) Treefrogs with distinct advertisement calls produce similar territorial signals. Bioacoustics (published online, https://doi.org/10.1080/09524622.2020.1791733)
Garber PA (1997) One for all and breeding for one: Cooperation and competition as a tamarin reproductive strategy. Evol Anthropol 5:187–199. https://doi.org/10.1002/(sici)1520-6505(1997)5:6%3c187::aid-evan1%3e3.0.co;2-a
Garber PA, Pruetz JD, Isaacson J (1993) Patterns of range use, range defense, and intergroup spacing in moustached tamarin monkeys (Saguinus mystax). Primates 34:11–25. https://doi.org/10.1007/BF02381276
Garbino GST, Martins-Junior AMG (2018) Phenotypic evolution in marmoset and tamarin monkeys (Cebidae, Callitrichinae) and a revised genus-level classification. Mol Phylogenet Evol 118:156–171. https://doi.org/10.1016/j.ympev.2017.10.002
Gasc A, Sueur J, Jiguet F, Devictor V, Grandcolas P, Burrow C, Depraete M, Pavoine S (2013) Assessing biodiversity with sound: do acoustic diversity indices reflect phylogenetic and functional diversities of bird communities? Ecol Indic 25:279–287. https://doi.org/10.1016/j.ecolind.2012.10.009
Germain RM, Williams JL, Schluter D, Angert AL (2018) Moving character displacement beyond characters using contemporary coexistence theory. Trends Ecol Evol 33:74–84. https://doi.org/10.1016/j.tree.2017.11.002
Gordo M (2012) Ecologia e conservação do sauim-de-coleira, Saguinus bicolor (Primates; Callitrichidae). PhD thesis, Museu Paraense Emílio Goeldii
Gordo M, Calleia FO, Vasconcelos SA et al (2013) The challenges of survival in a concrete jungle: conservation of the pied tamarin (Saguinus bicolor) in the urban landscape of manaus, Brazil. In: Marsh L, Chapman CA (eds) Primates in Fragments: Complexity and Resilience. Springer, New York, pp 357–370
Gordo M, Jerusalinsky L, Mittermeier RA, Röhe F, Boubli JP, Subirá RJ, Vidal MD (2019a) Saguinus bicolor. IUCN Red List Threat Species. https://doi.org/10.2305/IUCN.UK.2019-3.RLTS.T40644A17931870.en
Gordo M, Lagroteria D, Röhe F, Jerusalinsky J, Azevedo RB, Vidal MD, Hrbek T, Farias I, Rylands AB (2019b) Pied tamarin: Saguinus bicolor Spix, 1823 Brazil. In: Schwitzer C, Mittermeier RA, Rylands AB (eds) Primates in Peril: the world’s 25 most endangered primates 2018–2020. International Primatological Society, Global Wildlife Conservation and Bristol Zoological Society, Washington DC, IUCN SSC Primate Specialist Group, pp 82–85
Gordo M, Rodrigues LF, Vidal MD, Spironello WR (2008) Primatas. In: Oliveira M, Baccaro FB, Braga-Neto R, Magnusson WE (eds) Reserva Ducke–a Biodiversidade amazônica através de uma Grade. Átema design editorial, Manaus, pp 39–49
Gordo M, Subirá RJ, Vidal MD, Röhe F, Spironello WR, Valente LM, Oliveira JB, Pissinatti A, Wormell D (2017) Contextualização do Sauim-de-coleira. In: Jerusalinsky L, Azevedo R, Gordo M (eds) Plano de ação nacional para a conservação do sauim-de-coleira. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, pp 25–44
Grant PR (1972) Convergent and divergent character displacement. Biol J Linn Soc 4:39–68. https://doi.org/10.1111/j.1095-8312.1972.tb00690.x
Grether GF (2011) The neuroecology of competitor recognition. Integr Comp Biol 51:807–818. https://doi.org/10.1093/icb/icr060
Grether GF (2020) Convergent and divergent selection drive plumage evolution in woodpeckers. Nat Commun 11:144. https://doi.org/10.1038/s41467-019-14006-3
Grether GF, Drury JP, Okamoto KW, McEachin S, Anderson CN (2020) Predicting evolutionary responses to interspecific interference in the wild. Ecol Lett 23:221–230. https://doi.org/10.1111/ele.13395
Grether GF, Losin N, Anderson CN, Okamoto KW (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol Rev 84:617–635
Grether GF, Peiman KS, Tobias JA, Robinson BW (2017) Causes and consequences of behavioral interference between species. Trends Ecol Evol 32:760–772. https://doi.org/10.1016/j.tree.2017.07.004
Guariguata MR, Ostertag R (2001) Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manage 148:185–206. https://doi.org/10.1016/S0378-1127(00)00535-1
Hedwig D, Mundry R, Robbins MM, Boesch C (2015) Audience effects, but not environmental influences, explain variation in gorilla close distance vocalizations—a test of the acoustic adaptation hypothesis. Am J Primatol 77:1239–1252. https://doi.org/10.1002/ajp.22462
Hershkovitz P (1977) Living New World Monkeys (Platyrrhini). Primates, vol. 1. Chicago University Press, Chicago
Holland J, Dabelsteen T, Pedersen SB, Larsen ON (1998) Degradation of wren Troglodytes troglodytes song: implications for information transfer and ranging. J Acoust Soc Am 103:2154–2166. https://doi.org/10.1121/1.421361
Holzmann I, Areta JI (2020) Reduced geographic variation in roars in different habitats rejects the acoustic adaptation hypothesis in the black-and-gold howler monkey (Alouatta caraya). Ethology 126:76–87. https://doi.org/10.1111/eth.12962
Janik VM, Slater PJB (1997) Vocal learning in mammals. Adv Stud Behav 26:59–99
Kirschel ANG, Nwankwo EC, Seal N, Grether GF (2020) Time spent together and time spent apart affect song, feather colour and range overlap in tinkerbirds. Biol J Linn Soc 129:439–458. https://doi.org/10.1093/biolinnean/blz191
Kirschel ANG, Seddon N, Tobias JA (2019) Range-wide spatial mapping reveals convergent character displacement of bird song. Proc R Soc B 286:20190443. https://doi.org/10.1098/rspb.2019.0443
Kitchen DM, Bergman TJ, Dias PAD, Ho L, Canales-Espinoza D, Cortés-Otiz L (2019) Temporal but not acoustic plasticity in hybrid howler monkey (Alouatta palliata × A. pigra) loud calls. Int J Primatol 40:132–152. https://doi.org/10.1007/s10764-017-0004-8
Laiolo P (2012) Interspecific interactions drive cultural co-evolution and acoustic convergence in syntopic species. J Anim Ecol 81:594–604. https://doi.org/10.1111/j.1365-2656.2011.01946.x
Leary CJ (2001) Evidence of convergent character displacement in release vocalizations of Bufo fowleri and Bufo terrestris (Anura; Bufonidae). Anim Behav 61:431–438. https://doi.org/10.1006/anbe.2000.1597
Lenz BB, Jack KM, Spironello WR (2014) Edge effects in the primate community of the biological dynamics of forest fragments project, Amazonas, Brazil. Am J Phys Anthropol 155:436–446. https://doi.org/10.1002/ajpa.22590
Long AM, Moore NP, Hayden TJ (1998) Vocalizations in red deer (Cervus elaphus), sika deer (Cervus nippon), and red x sika hybrids. J Zool 244:123–134. https://doi.org/10.1017/S0952836998001149
McConnell P, Snowdon CT (1986) Vocal interactions between unfamiliar groups of captive cotton-top tamarins. Behaviour 97:273–296. https://doi.org/10.1163/156853986X00649
McFarlane SE, Pemberton JM (2019) Detecting the true extent of introgression during anthropogenic hybridization. Trends Ecol Evol 34:315–326
McGregor PK (1993) Signalling in territorial systems: a context for individual identification, ranging and eavesdropping. Phil Trans R Soc B 340:237–244. https://doi.org/10.1098/rstb.1993.0063
Mesquita RCG, Ickes K, Ganade G, Bruce Williamson G (2001) Alternative successional pathways in the Amazon Basin. J Ecol 89:528–537. https://doi.org/10.1046/j.1365-2745.2001.00583.x
Miller CT, Scarl J, Hauser MD (2004) Sensory biases underlie sex differences in tamarin long call structure. Anim Behav 68:713–720. https://doi.org/10.1016/j.anbehav.2003.10.028
Miller ET, Leighton GM, Freeman BG, Lees AC, Ligon RA (2019) Ecological and geographical overlap drive plumage evolution and mimicry in woodpeckers. Nat Commun 10:1602. https://doi.org/10.1038/s41467-019-09721-w
Monteiro-Neto BD (2015) Área e uso do espaço de Saguinus bicolor (Primates: Callitrichidae). Master Thesis, Universidade Federal do Amazonas
Montgomery RA, Chazdon RL (2001) Forest structure, canopy architecture, and light transmittance in tropical wet forests. Ecology 82:2707–2718. https://doi.org/10.1890/0012-9658(2001)082[2707:FSCAAL]2.0.CO;2
Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34. https://doi.org/10.1086/282971
Müller-Schwarze D (2006) Chemical ecology of vertebrates. Cambridge University Press, Cambridge
Mumm CAS, Knörnschild M (2017) Territorial choruses of giant otter groups (Pteronura brasiliensis) encode information on group identity. PLoS ONE 12:e0185733. https://doi.org/10.1371/journal.pone.0185733
Naugler CT, Ratcliffe L (1994) Character release in bird song: a test of the acoustic competition hypothesis using american tree sparrows Spizella arborea. J Avian Biol 25:142. https://doi.org/10.2307/3677033
Okamoto KW, Grether GF (2013) The evolution of species recognition in competitive and mating contexts: the relative efficacy of alternative mechanisms of character displacement. Ecol Lett 16:670–678. https://doi.org/10.1111/ele.12100
Oliveira DAG, Ades C (2004) Long-distance calls in neotropical primates. An Acad Bras Cienc 76:393–398. https://doi.org/10.1590/S0001-37652004000200031
Oliveira ML, Baccaro FB, Braga-neto R, Magnusson WE (2008) Reserva Ducke: A Biodiversidade Amazônica través de uma grade. Editora INPA, Manaus
Ortiz-Barrientos D, Counterman BA, Noor MAF (2004) The genetics of speciation by reinforcement. PLoS Biol 2:e416. https://doi.org/10.1371/journal.pbio.0020416
Partan SR (2017) Multimodal shifts in noise: switching channels to communicate through rapid environmental change. Anim Behav 124:325–337. https://doi.org/10.1016/j.anbehav.2016.08.003
Pasch B, Sanford R, Phelps SM (2017) Agonistic character displacement in social cognition of advertisement signals. Anim Cogn 20:267–273. https://doi.org/10.1007/s10071-016-1046-6
Peiman KS, Robinson BW (2010) Ecology and evolution of resource-related heterospecific aggression. Q Rev Biol 85:133–158. https://doi.org/10.1086/652374
Peres-Neto PR, Jackson DA, Somers KM (2005) How many principal components? Stopping rules for determining the number of non-trivial axes revisited. Comput Stat Data Anal 49:974–997. https://doi.org/10.1016/j.csda.2004.06.015
Peters G, Peters MK (2010) Long-distance call evolution in the Felidae: effects of body weight, habitat, and phylogeny. Biol J Linn Soc 101:487–500. https://doi.org/10.1111/j.1095-8312.2010.01520.x
Pfennig DW, Pfennig KS (2012) Development and evolution of character displacement. Ann NY Acad Sci 1256:89–107. https://doi.org/10.1111/j.1749-6632.2011.06381.x
Pfennig DW, Rice AM, Martin RA (2006) Ecological opportunity and phenotypic plasticity interact to promote character displacement and species coexistence. Ecology 87:769–779. https://doi.org/10.1890/05-0787
Pfennig KS, Pfennig DW (2009) Character displacement: ecological and reproductive responses to a common evolutionary problem. Q Rev Biol 84:253–276. https://doi.org/10.1086/605079
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) Package “nlme”: linear and nonlinear mixed effects models, https://CRAN.R-project.org/package=nlme. Accessed 29 June 2020
Pureswaran DS, Hofstetter RW, Sullivan BT, Potter KA (2016) The role of multimodal signals in species recognition between tree-killing bark beetles in a narrow sympatric zone. Environ Entomol 45:582–591. https://doi.org/10.1093/ee/nvw022
R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org
Riede T, Bronson E, Hatzikirou H, Zuberbühler K (2005) Vocal production mechanisms in a non-human primate: morphological data and a model. J Hum Evol 48:85–96. https://doi.org/10.1016/j.jhevol.2004.10.002
Ritschard M, van Oers K, Naguib M, Brumm H (2012) Song amplitude of rival males modulates the territorial behaviour of great tits during the fertile period of their mates. Ethology 118:197–202. https://doi.org/10.1111/j.1439-0310.2011.01999.x
Röhe F (2006) Área de contato entre as distribuições geográficas de Saguinus midas e Saguinus bicolor (Callitrichidae-Primates): a importância de interações e fatores ecológicos. Master Thesis, Instituto Nacional de Pesquisas da Amazônia
Rozendaal DMA, Bongers F, Aide TM et al (2019) Biodiversity recovery of Neotropical secondary forests. Sci Adv 5:eaau3114. https://doi.org/10.1126/sciadv.aau3114
Rylands AB, Heymann EW, Lynch Alfaro J, Buckner JC, Roos C, Boubli JP, Sampaio R, Mittermeier RA (2016) Taxonomic review of the New World tamarins (Primates: Callitrichidae). Zool J Linn Soc 177:1003–1028. https://doi.org/10.1111/zoj.12386
Sabatini V, Ruiz-miranda CR (2010) Does the golden lion tamarin, Leontopithecus rosalia ( Primates : Callitrichidae ), select a location whithin the forest strata for long distance communication ? Zoologia 27:179–183. https://doi.org/10.1590/S1984-46702010000200004
Schluter D (2001) Ecological character displacement. In: Fox CW, Roff DA, Fairbairn DJ (eds) Evolutionary ecology: concepts and case studies. Oxford University Press, New York, pp 265–276
Scott JJ, Carlson KL, Snowdon CT (2006) Labile sex differences in long calling in cotton-top tamarins. Am J Primatol 68:153–160. https://doi.org/10.1002/ajp.20213
Secondi J, Bretagnolle V, Compagnon C, Faivre B (2003) Species-specific song convergence in a moving hybrid zone between two passerines. Biol J Linn Soc 80:507–517. https://doi.org/10.1046/j.1095-8312.2003.00248.x
Seddon N, Tobias JA (2010) Character displacement from the receiver’s perspective: species and mate recognition despite convergent signals in suboscine birds. Proc R Soc Lond B 277:2475–2483. https://doi.org/10.1098/rspb.2010.0210
Sicsú P, Manica LT, Maia R, Macedo RH (2013) Here comes the sun: multimodal displays are associated with sunlight incidence. Behav Ecol Sociobiol 67:1633–1642. https://doi.org/10.1007/s00265-013-1574-x
Snowdon CT (1989) Vocal communication in New World monkeys. J Hum Evol 18:611–633. https://doi.org/10.1016/0047-2484(89)90097-3
Snowdon CT (2017a) Learning from monkey “talk.” Science 355:1120–1122. https://doi.org/10.1126/science.aam7443
Snowdon CT (2017b) Vocal communication in family-living and pair-bonded primates. In: Quam RM, Ramsier MA, Fay RR, Popper AN (eds) Primate Hearing and Communication. Springer, Cham, pp 141–174
Snowdon CT, Cleveland J, French JA (1983) Responses to context- and individual-specific cues in cotton-top tamarin long calls. Anim Behav 31:92–101. https://doi.org/10.1016/S0003-3472(83)80177-8
Snowdon CT, de la Torre S (2002) Multiple environmental contexts and communication in pygmy marmosets (Cebuella pygmaea). J Comp Psychol 116:182–188. https://doi.org/10.1037/0735-7036.116.2.182
Sobroza TV, Cerqueda LS, Simões PI, Gordo M (2017) Vocal repertoire and its behavioral contexts in the pied tamarin, Saguinus bicolor. Int J Primatol 38:642–655. https://doi.org/10.1007/s10764-017-9971-z
Sobroza TV, Gordo M, Barnett APA, Boubli JP, Spironello WR (2021) Parapatric pied and red-handed tamarin responses to congeneric and conspecific calls. Acta Oecol 110:103688. https://doi.org/10.1016/j.actao.2020.103688
Stuart YE, Inkpen SA, Hopkins R, Bolnick DI (2017) Character displacement is a pattern: so, what causes it? Biol J Linn Soc 121:711–715. https://doi.org/10.1093/biolinnean/blx013
Tobias JA, Planqué R, Cram DL, Seddon N (2014) Species interactions and the structure of complex communication networks. P Natl Acad Sci USA 111:1020–1025. https://doi.org/10.1073/pnas.1314337111
Weber MG, Strauss SY (2016) Coexistence in close relatives: beyond competition and reproductive isolation in sister taxa. Annu Rev Ecol Evol S 47:359–381. https://doi.org/10.1146/annurev-ecolsys-112414-054048
Weiss DJ, Garibaldi BT, Hauser MD (2001) The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments. J Comp Psychol 115:258–271. https://doi.org/10.1037//0735-7036.115.3.258
West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183. https://doi.org/10.2307/2828804
Wich SA, Nunn CL (2002) Do male “long-distance calls” function in mate defense? A comparative study of long-distance calls in primates. Behav Ecol Sociobiol 52:474–484. https://doi.org/10.1007/s00265-002-0541-8
Wiley RH, Richards DG (1978) Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav Ecol Sociobiol 3:69–94. https://doi.org/10.1007/BF00300047
Wilkins MR, Seddon N, Safran RJ (2013) Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol 28:156–166. https://doi.org/10.1016/j.tree.2012.10.002
Yikweon J (2008) Asymmetry in reproductive character displacement. J Ecol Environ 31:255–260. https://doi.org/10.5141/jefb.2008.31.4.255
Zaccaroni M, Passilongo D, Buccianti A, Dessí-Fulgheri F, Facchini C, Gazzola A, Maggini I, Apollonio M (2012) Group specific vocal signature in free-ranging wolf packs. Ethol Ecol Evol 24:322–331. https://doi.org/10.1080/03949370.2012.664569
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
We thank Cristiane Rangel, Benedito Monteiro, Laynara Santos, Viviane Costa, Dayane Seyfarth, Guilherme Christo, Karina Solis, Arthur Citó, Gueviston Lima, and Gilberto for fieldwork help. We are also grateful to the Projeto Sauim-de-Coleira, UFAM, PARNA Viruá, LBA, BDFFP, Balbina Dam, Gonçalo Ferraz and the owners of private proprieties (especially Sra Ana and Sr. Dalton Valle) for field facilitation. We thank the editors and two anonymous reviewers for their helpful feedback, as well as Dr. Charles Snowdon for sharing his knowledge and impressions about the function of long calls in tamarin species. This is contribution 811 of the BDFFP Technical Series and 52 from the Amazonian Mammals Research group.
Funding
During the study TVS and received a scholarship from Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM) (062.01758/2018). RMR received a scholarship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (142352/2017–9). The study is part of a project supported by the "Primate Action Fund" (PAF 14–15; CI 1000796), Idea Wild and the Pignose Company.
Author information
Authors and Affiliations
Contributions
TVS originally formulated the research topic, collected data, and wrote the original draft. TVS, PACLP, JCD and RMR performed exploratory and current statistical analyses. AAPB, MG, and JCD supervised. TVS and WRS raised funds. AAPB and JCD checked the English. All authors contributed to the writing and reviewing.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
All applicable international, national, and/or institutional guidelines for the use of animals were followed. The study was non-invasive and complied with Brazilian law (permit for Viruá National Park access 47755–1; and for S. midas and S. bicolor research 10286 – 3 issued by SISBIO/Brazilian Ministry of Environment).
Conflicts of interest
The authors declare no competing interests.
Additional information
Communicated by M. A van Noordwijk.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sobroza, T.V., Gordo, M., Pequeno, P.A.C.L. et al. Convergent character displacement in sympatric tamarin calls (Saguinus spp.). Behav Ecol Sociobiol 75, 88 (2021). https://doi.org/10.1007/s00265-021-03028-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-021-03028-x