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Allometric escape and acoustic signal features facilitate high-frequency communication in an endemic Chinese primate

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Abstract

The principle of acoustic allometry—the larger the animal, the lower its calls' fundamental frequency—is generally observed across terrestrial mammals. Moreover, according to the Acoustic Adaptation Hypothesis, open habitats favor the propagation of high-frequency calls compared to habitats with complex vegetational structures. We carried out playback experiments in which the calls of the Guizhou snub-nosed monkey (Rhinopithecus brelichi) were used as stimuli in sound attenuation and degradation experiments to test the hypothesis that propagation of Guizhou snub-nosed monkey calls is favored above vs through the forest floor vegetation. We found that low-pitched Guizhou snub-nosed monkey vocalizations suffered less attenuation than its high-pitched calls. Guizhou snub-nosed monkeys were observed emitting high-pitched calls from 1.5 to 5.0 m above the ground. The use of high-pitched calls from these heights coupled with the concomitant behavior of moving about above the understory may provide a signal for receivers which maximizes potential transmission and efficacy. Our results support the Acoustic Adaptation Hypothesis and suggest that by uncoupling its vocal output from its size, this monkey can produce a high-pitched call with a broad spectral bandwidth, thereby increasing both its saliency and the frequency range over which the animal may more effectively communicate in its natural habitat.

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Abbreviations

HPC:

High-pitched call

RMS:

Root mean square

SPL:

Sound pressure level

GLMM:

Generalized Linear Mixed Model

References

  • Altmann SA (1967) The structure of primate social communication. In: Altmann SA (eds) Social communication among primates. University of Chicago Press, Chicago

  • Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267

    Article  CAS  Google Scholar 

  • Arak A, Eiriksson T (1992) Choice of singing sites by male bushcrickets (Tettigonia viridissima) in relation to signal propagation. Behav Ecol Sociobiol 30:365–372

    Google Scholar 

  • Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278

    Google Scholar 

  • Bleisch WV, Xie JH (1998) Ecology and behaviour of the Guizhou snub-nosed langur (Rhinopithecus brelichi), with a discussion of socioecology in the genus. The natural history of the doucs and snub-nosed monkeys. World Scientific Press, Singapore, pp 217–241

    Google Scholar 

  • Bleisch W, Cheng AS, Ren XD, Xie JH (1993) Preliminary results from a field study of wild Guizhou snub-nosed monkeys (Rhinopithecus brelichi). Folia Primatol 60:72–82

    CAS  Google Scholar 

  • Boersma P (2001) Praat, a system for doing phonetics by computer. Glot Int 5:341–345

    Google Scholar 

  • Bowling DL, Garcia M, Dunn JC, Ruprecht R, Stewart A, Frommolt K-H, Fitch WT (2017) Body size and vocalization in primates and carnivores. Sci Rep 7:41070

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bowling DL, Dunn JC, Smaers JB, Garcia M, Sato A, Hantke G, Handschuh S, Dengg S, Kerney M, Kitchener AC, Gumpenberger M, Fitch WT (2020) Rapid evolution of the primate larynx? PLoS Biol 18:e3000764

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brenowitz EA (1982) The active space of red-winged blackbird song. J Comp Physiol A 147:511–522

    Google Scholar 

  • Bretz F, Hothorn T, Westfall P (2010) Multiple comparisons using R. Chapman & Hall/CRC Press, Boca Raton

    Google Scholar 

  • Castellano S, Giacoma C, Ryan MJ (2003) Call degradation in diploid and tetraploid green toads. Biol J Linn Soc 78:11–26

    Google Scholar 

  • Charlton BD, Reby D (2016) The evolution of acoustic size exaggeration in terrestrial mammals. Nat Commun 7:12739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Charlton BD, Owen MA, Swaisgood RR (2019) Coevolution of vocal signal characteristics and hearing sensitivity in forest mammals. Nat Commun 10(1):2778

    PubMed  PubMed Central  Google Scholar 

  • Clarke E, Reichard UH, Zuberbühler K (2006) The syntax and meaning of wild gibbon songs. PLoS ONE 1(1):e73

    PubMed  PubMed Central  Google Scholar 

  • Dobson AJ (2002) An introduction to generalized linear models, 2nd edn. Chapman & Hall/CRC Press, Boca Raton

    Google Scholar 

  • Erb WM, Hodges JK, Hammerschmidt K (2013) Individual, contextual, and age-related acoustic variation in Simakobu (Simias concolor) loud calls. PLoS ONE 8:e83131

    PubMed  PubMed Central  Google Scholar 

  • Estienne V, Stephens C, Boesch C (2017) Extraction of honey from underground bee nests by central African chimpanzees (Pan troglodytes troglodytes) in Loango National Park, Gabon: Techniques and individual differences. Am J Primatol 79:e22672

    Google Scholar 

  • Ey E, Fischer J (2009) The “acoustic adaptation hypothesis”—a review of the evidence from birds, anurans and mammals. Bioacoustics 19:21–48

    Google Scholar 

  • Fan P, Liu X, Liu R, Li F, Huang T, Wu F, Yao H, Liu D (2018) Vocal repertoire of free-ranging adult golden snub-nosed monkeys (Rhinopithecus roxellana). Am J Primatol 80:e22869

    PubMed  PubMed Central  Google Scholar 

  • Favaro L, Ozella L, Pessani D (2014) The vocal repertoire of the African penguin (Spheniscus demersus): structure and function of calls. PLoS ONE 9(7):e103460

    PubMed  PubMed Central  Google Scholar 

  • Feng AS, Narins PM, Xu CH, Lin WY, Yu ZL, Qiu Q, Xu ZM, Shen JX (2006) Ultrasonic communication in frogs. Nature 440:333–336

    CAS  PubMed  Google Scholar 

  • Fischer J, Hammerschmidt K (2002) An overview of the Barbary macaque, Macaca sylvanus, vocal repertoire. Folia Primatol 73:32–45

    Google Scholar 

  • Forrest TG (1994) From sender to receiver: propagation and environmental effects on acoustic signals. Am Zool 34:644–654

    Google Scholar 

  • Forstmeier W, Schielzeth H (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol 65:47–55

    PubMed  Google Scholar 

  • Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. SAGE Publications Inc, Thousand Oaks

    Google Scholar 

  • Furrer RD, Manser MB (2009) The evolution of urgency-based and functionally referential alarm calls in ground-dwelling species. Am Nat 173(3):400–410

    PubMed  Google Scholar 

  • Gamba M, Giacoma C (2005) Key issues in the study of primate acoustic signals. J Anthropol Sci 83:61–87

    Google Scholar 

  • Gamba M, Colombo C, Giacoma C (2012a) Acoustic cues to caller identity in lemurs: a case study. J Ethol 30:191–196

    Google Scholar 

  • Gamba M, Friard O, Giacoma C (2012b) Vocal tract morphology determines species-specific features in vocal signals of lemurs (Eulemur). Int J Primatol 33:1453–1466

    Google Scholar 

  • Garcia M, Ravignani A (2020) Acoustic allometry and vocal learning in mammals. Biol Lett 16:20200081

    PubMed  Google Scholar 

  • Garcia M, Christian T, Herbst CT, Bowling DL, Dunn JC, Fitch WT (2017) Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production. Sci Rep 7:10450

    PubMed  PubMed Central  Google Scholar 

  • Grawunder S, Crockford C, Clay Z, Kalan AK, Stevens JMG, Stoessel A, Hohmann G (2018) Higher fundamental frequency in bonobos is explained by larynx morphology. Curr Biol 28:R1188–R1189

    CAS  PubMed  Google Scholar 

  • Grüter CC (2003) Social behaviour of Yunnan snub-nosed monkeys (Rhinopithecus bieti). Dissertation, University of Zurich

  • Halfwerk W, Lea AM, Guerra MA, Page RA, Ryan MJ (2016) Vocal responses to noise reveal the presence of the Lombard effect in a frog. Behav Ecol 27:669–676

    Google Scholar 

  • Holman SD, Seale WTC (1991) Ontogeny of sexually dimorphic ultrasonic vocalizations in Mongolian gerbils. Dev Psychobiol 24:103–115

    CAS  PubMed  Google Scholar 

  • Kirkpatrick RC (1998) Ecology and behaviour in snub-nosed and douc langurs. In: Jablonski NG (ed) The natural history of the doucs and snub-nosed monkeys. World Scientific Publishing, Singapore, pp 155–190

    Google Scholar 

  • Kirkpatrick RC, Grueter CC (2010) Snub-nosed monkeys: multilevel societies across varied environments. Evol Anthropol 19:98–113

    Google Scholar 

  • Li B, Chen F, Luo S, Xie W (1993) Major categories of vocal behaviour in wild Sichuan golden monkey (Rhinopithecus roxellana). Acta Theriol Sin 13:181–187

    Google Scholar 

  • Liedigk R, Yang M, Jablonski NG, Momberg F, Geissmann T, Lwin N et al (2012) Evolutionary history of the odd-nosed monkeys and the phylogenetic position of the newly described Myanmar snub-nosed monkey Rhinopithecus strykeri. PLoS ONE 7:e37418

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34

    Google Scholar 

  • Narins PM, Feng AS, Schnitzler H-U, Denzinger A, Suthers RA, Lin W, Xu C-H (2004) Old World frog and bird vocalizations contain prominent ultrasonic harmonics. J Acoust Soc Am 115:910–913

    PubMed  Google Scholar 

  • Niu K, Tan CL, Yang Y (2010) Altitudinal movements of Guizhou snub-nosed monkeys (Rhinopithecus brelichi) in Fanjingshan National Nature Reserve, China: implications for conservation management of a flagship species. Folia Primatol 81:233–244

    Google Scholar 

  • Niu K, Tan CL, Cui D, Shi L, Yang M, Qui Y, Zhang W, Yang Y (2014) Utilization of food on snow-covered ground by Guizhou snub-nosed monkeys (Rhinopithecus brelichi) in Fanjingshan National Nature Reserve, China. Chin J Wildl 35:31–37

    Google Scholar 

  • Rendall D, Rodman PS, Emond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015

    Google Scholar 

  • Richards DG, Wiley RH (1980) Reverberations and amplitude fluctuations in the propagation of sound in a forest: Implications for animal communication. Am Nat 115:381–399

    Google Scholar 

  • Römer H, Lewald J (1992) High-frequency sound transmission in natural habitats: implications for the evolution of insect acoustic communication. Behav Ecol Sociobiol 29:437–444

    Google Scholar 

  • Röper KM, Scheumann M, Wiechert AB, Nathan S, Goossens B, Owren MJ, Zimmermann E (2014) Vocal acoustics in the endangered proboscis monkey (Nasalis larvatus). Am J Primatol 76:192–201

    PubMed  Google Scholar 

  • Shen J-X, Xu Z-M, Feng AS, Narins PM (2011) Large odorous frogs (Odorrana graminea) produce ultrasonic calls. J Comp Physiol 197:1027–1030

    Google Scholar 

  • Snowdon CT, Cleveland J (1980) Individual recognition of contact calls by pygmy marmosets. Anim Behav 28:717–727

    Google Scholar 

  • Srivathsan A, Meier R (2011) Proboscis monkeys (Nasalis larvatus (Wurmb, 1787)) have unusually high-pitched vocalizations. Raffles J Zool 59:319–323

    Google Scholar 

  • Todt D, Goedeking P, Symmes D (eds) (2012) Primate vocal communication. Springer Science & Business Media, New York

    Google Scholar 

  • Tonini JFR, Provete DB, Maciel NM, Morais AR, Goutte S, Toledo LF, Pyron RA (2020) Allometric escape from acoustic constraints is rare for frog calls. Ecol Evol 10:3686–3695

    PubMed  PubMed Central  Google Scholar 

  • Torti V, Bonadonna G, De Gregorio C, Valente D, Randrianarison RM, Friard O, Gamba M, Giacoma C (2017) An intra-population analysis of the indris’ song dissimilarity in the light of genetic distance. Sci Rep 7:1–12

    CAS  Google Scholar 

  • Waser PM (1977) Individual recognition, intragroup cohesion and intergroup spacing: evidence from sound playback to forest monkeys. Behaviour 60:28–74

    Google Scholar 

  • Waser PM, Waser MS (1977) Experimental studies of primate vocalization: specializations for long-distance propagation. Z für Tierpsychol 43:239–263

    Google Scholar 

  • Wiley RH (2015) Noise matters. Harvard, Cambridge

    Google Scholar 

  • 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

    Google Scholar 

  • Xie JH, Liu YM, Yang YQ (1982) Preliminary survey of the ecological conditions of the Guizhou golden monkey. Scientific Survey of the Mt Fanjing Reserve, pp 215–221

  • Yang YQ, Lei XP, Yang CD (2002) Fanjingshan Research: ecology of the wild Guizhou Snub-nosed monkey. Guizhou Science Press, Guiyang

    Google Scholar 

  • Yang H-L, Li D-Q, Duo H-R, Ma J (2010) Vegetation distribution in Fanjing Mountain National Nature Reserve and habitat selection of Guizhou golden monkey (in Chinese with English abstract). Forest Res 23:393–398

    Google Scholar 

  • Yanqing G, Baoping R, Qiang D, Jun Z, Garber PA, Jiang Z (2020) Habitat stimates reveal that there are fewer than 400 Guizhou snub-nosed monkeys, Rhinopithecus brelichi, remaining in the wild. Glob Ecol Conserv 24:e01181

    Google Scholar 

  • Zhu SQ, Yang YQ (1990) Fanjingshan forest types. In: Zhou ZX, Yang YQ (eds) Research on the Fanjing mountain. Guizhou People’s Publishing House, Guiyang, pp 95–252

    Google Scholar 

  • Ziegler L, Arim M, Narins PM (2011) Linking amphibian call structure to the environment: the interplay of phenotypic flexibility and individual attributes. Behav Ecol 22:520–526

    PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

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Acknowledgements

We thank the Fanjingshan National Nature Reserve Administration for permission to carry out this study. Field assistants J. Li, X. Dong and Y. Feng helped with the experiments while H. Wang and J. Chen provided critical support for the vocal data collection. We thank A. Cobo-Cuan for help with producing Fig. 1, O. Friard for assistance with the cross-correlation calculations, and S. Castellano, M.J. Ryan and W. Halfwerk for helpful discussions of the analysis of the attenuation experiments. We would like to thank two anonymous reviewers for their suggestions and comments. Supported by grants from the Margot Marsh Biodiversity Foundation and the Offield Family Foundation to C.L.T., the Fanjingshan National Nature Reserve Project of China’s Ministry of Foreign Affairs Funding (Guizhou), and a Senior Scientist Research Fellowship from the U. Torino International Program to P.M.N. I.R., M.G., C.L.T., K.N. and C.G. carried out the field work and contributed to the design and data collection for this study. Y.Y. facilitated the study by obtaining proper authorizations from the Guizhou Forestry Dept., I.R., M.G., C.G. and P.M.N. drafted the manuscript, and all authors revised it for accuracy and content. All procedures were performed in agreement with the regulations of the Fanjingshan National Nature Reserve Administration. All authors agreed to be held accountable for the content and approved the final version of the manuscript.

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Authors and Affiliations

  1. Department of Life Sciences and Systems Biology, University of Torino, 10123, Torino, Italy

    Isidoro Riondato, Marco Gamba, Kefeng Niu & Cristina Giacoma

  2. LVDI International, San Marcos, CA, 92078, USA

    Chia L. Tan

  3. Forest Ally, Wellness, Science and Technology Co., Ltd., Shenzhen, 518112, Guangdong, China

    Kefeng Niu

  4. Departments of Integrative Biology and Physiology, and Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, 90095, USA

    Peter M. Narins

  5. Nonhuman Primate Conservation Research Institute, Tongren University, Tongren, Guizhou, 554300, People’s Republic of China

    Chia L. Tan, Kefeng Niu & Yeqin Yang

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  1. Isidoro Riondato
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Correspondence to Marco Gamba.

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Riondato, I., Gamba, M., Tan, C.L. et al. Allometric escape and acoustic signal features facilitate high-frequency communication in an endemic Chinese primate. J Comp Physiol A 207, 327–336 (2021). https://doi.org/10.1007/s00359-021-01465-7

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