Crypsis, including visual and auditory concealment, usually manifests in primates as an antipredator strategy. Other factors may also influence cryptic communication style, including habitat structure and phylogenetic history. Compared to less cryptic lowland Sulawesian tarsiers, montane pygmy tarsiers (Tarsius pumilus) exhibit a communication style that lacks scent marks and lower-frequency vocalisations. This study examines why auditory crypsis occurs in montane tarsiers more so than in larger tarsier species and presents the only known spectrograms of T. pumilus in the field. T. pumilus regularly exhibited calls with a dominant frequency of 60–80 kHz (n = 4) in both social situations (duet calls) and stressed contexts. These results indicate that highland, smaller-bodied tarsiers habitually communicate at high frequencies in contexts where Sulawesian and Philippine tarsiers use lower frequencies. While predation threats and habitat acoustics may influence the use of high-frequency vocalisations, this study found that T. pumilus shows an expected relationship between vocal frequency and body mass. These traits may represent a retention of primitive haplorhine traits rather than derived adaptations to a montane environment.

Keywords:
Crypsis, Ultrasonic vocalisation, Body size, Communication, Antipredator strategy, Tarsius
1.
Arch VS, Narins PM (2008). “Silent” signals: selective forces acting on ultrasonic communication systems in terrestrial vertebrates. Animal Behaviour 76: 1423–1428.
2.
Arlettaz R, Jones G, Racey PA (2001). Effect of acoustic clutter on prey detection by bats. Nature 414: 742–745.
3.
Barclay RM, Brigham RM (1991). Prey detection, dietary niche breadth, and body size in bats: why are aerial insectivorous bats so small? The American Naturalist137: 693–703.
4.
Blackburn TM, Gaston KJ, Loder N (1999). Geographic gradients in body size: a clarification of Bergmann’s rule. Diversity and Distributions 5: 165–174.
5.
Brown RM, Weghorst JA, Olson KV, Duya MR, Barley AJ, Duya MV, Shekelle M, Neri-Arboleda I, Esselstyn J, Dominy N, Ong PS, Moritz GL, Luczon A, Diesmos MLL, Diesmos AC, Siler CD (2014). Conservation genetics of the Philippine tarsier: cryptic genetic variation restructures conservation priorities for an island archipelago primate. PLoS One 9: e104340.
6.
Burton JA, Nietsch A (2010). Geographical variation in duet songs of Sulawesi tarsiers: evidence for new cryptic species in south and southeast Sulawesi. International Journal of Primatology 31: 1123–1146.
7.
Cartmill M (1972). Arboreal adaptations and the origin of the order Primates. In The Functional and Evolutionary Biology of Primates (Tuttle R, ed.), pp 97–122. Chicago, Aldine Atherton.
8.
Cherry JA, Izard MK, Simons EL (1987). Description of ultrasonic vocalizations of the mouse lemur (Microcebus murinus) and the fat-tailed dwarf lemur (Cheirogaleus medius). American Journal of Primatology 13: 181–185.
9.
Chown SL, Klok CJ (2003). Altitudinal body size clines: latitudinal effects associated with changing seasonality. Ecography 26: 445–455.
10.
Clutton-Brock TH, Harvey PH (1977). Primate ecology and social organization. Journal of Zoology 183: 1–39.
11.
Coleman MN (2009). What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. International Journal of Primatology 30: 55–91.
12.
Coleman MN, Colbert MW (2010). Correlations between auditory structures and hearing sensitivity in non-human primates. Journal of Morphology 271: 511–532.
13.
Crompton RH (1995). “Visual predation,” habitat structure, and the ancestral primate niche. In Creatures of the Dark (Alterman L, Doyle GA, Izard MK, eds.), pp 11–30. Boston, Springer.
14.
Curtis DJ, Rasmussen MA (2003). Cathemerality in lemurs. Evolutionary Anthropology 11(suppl 1): 83–86.
15.
de la Torre S, Snowdon CT (2002). Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea. Animal Behaviour 63: 847–856.
16.
Frazer GW, Canham CD, Lertzman KP (1999). Gap light analyzer (GLA): imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, user’s manual and program documentation. Burnaby, Simon Fraser University/Millbrook, Institute of Ecosystem Studies.
17.
Grow N (2013a). Altitudinal Effects on the Behavior and Morphology of Pygmy Tarsiers ( Tarsiuspumilus) in Central Sulawesi, Indonesia. PhD dissertation, Texas A&M University.
18.
Grow N (2013b). Altitudinal distribution and ranging patterns of pygmy tarsiers. In High Altitude Primates (Grow N, Gursky-Doyen S, Krzton A, eds.), pp 43–59. New York, Springer.
19.
Grow N, Gursky-Doyen S (2010). Preliminary data on the behavior, ecology, and morphology of pygmy tarsiers (Tarsius pumilus). International Journal of Primatology31: 1174–1191.
20.
Grow N, Gursky S, Duma Y (2013). Altitude and forest edges influence the density and distribution of pygmy tarsiers (Tarsius pumilus). American Journal of Primatology 75: 464–477.
21.
Grow NB, Bailey K, Gursky S (2016). Ultrasonic vocalizations by montane pygmy tarsiers (Tarsius pumilus) in Sulawesi, Indonesia. American Journal of Physical Anthropology159(suppl 62): 162–163.
22.
Gursky S (1997). Modeling Maternal Time Budgets: The Impact of Lactation and Infant Transport on the Time Budget of the Spectral Tarsier. PhD dissertation, State University of New York at Stony Brook.
23.
Gursky S (2000). Sociality in the spectral tarsier, Tarsius spectrum. American Journal of Primatology 51: 89–101.
24.
Gursky S (2003). Predation experiments on infant spectral tarsiers (Tarsius spectrum). Folia Primatologica 74: 272–284.
25.
Gursky S (2005). Predator mobbing in Tarsius spectrum. International Journal of Primatology 26: 207–221.
26.
Gursky S (2013). Acoustic characterization of ultrasonic vocalizations by a nocturnal primate Tarsius syrichta. Primates 54: 293–299.
27.
Gursky S (2015). Ultrasonic vocalizations by the spectral tarsier, Tarsius spectrum. Folia Primatologica 86: 153–163.
28.
Gursky SL (2007). The response of spectral tarsiers toward avian and terrestrial predators. In Primate Anti-Predator Strategies (Gursky S, Nekaris KAI, eds.), pp 241–252. Boston, Springer.
29.
Gursky S, Moser C (2018). Echolocation in a nocturnal primate? American Journal of Physical Anthropology165(suppl 66): 109.
30.
Gursky S, Grow N, Fields L (2017). Tarsiiformes. In The International Encyclopedia of Primatology, volume III (Fuentes A, ed.), pp 1364–1368. New York, Wiley Blackwell.
31.
Hauser MD (1993). The evolution of nonhuman primate vocalizations: effects of phylogeny, body weight, and social context. American Naturalist 142: 528–542.
32.
Heffner RS (2004). Primate hearing from a mammalian perspective. The Anatomical Record Part A 281A: 1111–1122.
33.
Jachowski DS, Pizarras C (2005). Introducing an innovative semi-captive environment for the Philippine tarsier (Tarsius syrichta). Zoo Biology 24: 101–109.
34.
Lahann P, Schmid J, Ganzhorn JU (2006). Geographic variation in populations of Microcebus murinus in Madagascar: resource seasonality or Bergmann’s rule? International Journal of Primatology 27: 983–999.
35.
Liao JC, Liu NF (2008). Altitudinal variations of acoustic organs in anurans: A case study from China. Italian Journal of Zoology 75: 125–134.
36.
Liao J, Zhang Z, Liu N (2006). Altitudinal variation of skull size in Daurian pika (Ochotona daurica Pallas, 1868). Acta Zoologica Academiae Scientiarum Hungaricae 52: 319–329.
37.
MacKinnon J, MacKinnon K (1980). The behavior of wild spectral tarsiers. International Journal of Primatology 1: 361–379.
38.
Marler P (1955). Characteristics of some animal calls. Nature 176: 6−8.
39.
Marten K, Marler P (1977). Sound transmission and its significance for animal vocalization. Behavioral Ecology and Sociobiology 2: 271–290.
40.
McGrew WC, Marchant LF, Phillips CA (2009). Standardised protocol for primate faecal analysis. Primates 50: 363–366.
41.
Merker S, Yustian I (2008). Habitat use analysis of Dian’s tarsier (Tarsius dianae) in a mixed-species plantation in Sulawesi, Indonesia. Primates 49: 161–164.
42.
Merker S, Driller C, Perwitasari-Farajallah D, Pamungkas J, Zischler H (2009). Elucidating geological and biological processes underlying the diversification of Sulawesi tarsiers. Proceedings of the National Academy of Sciences of the United States of America 106: 8459–8464.
43.
Merker S, Yustian I, Mühlenberg M (2005). Responding to forest degradation: altered habitat use by Dian’s tarsier Tarsius dianae in Sulawesi, Indonesia. Oryx 39: 189–195.
44.
Miller LA, Surlykke A (2001). How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator: evolutionarily speaking, insects have responded to selective pressure from bats with new evasive mechanisms, and these very responses in turn put pressure on bats to “improve” their tactics. AIBS Bulletin 51: 570–581.
45.
Müller AE (1999). Aspects of social life in the fat-tailed dwarf lemur (Cheirogaleus medius): Inferences from body weights and trapping data. American Journal of Primatology49: 265–280.
46.
Musser G, Dagosto M (1987). The identity of Tarsius pumilus, a pygmy species endemic to the montane mossy forests of Central Sulawesi. American Museum Novitates 2867: 1–53.
47.
Nekaris KAI, Pimley ER, Ablard KM (2007). Predator defense by slender lorises and pottos. In Primate Anti-Predator Strategies (Gursky S, Nekaris KAI, eds.), pp 222–240. Boston, Springer.
48.
Nietsch A (1999). Duet vocalizations among different populations of Sulawesi tarsiers. International Journal of Primatology 20: 567–583.
49.
Pangau-Adam MZ (2003). Avian Nest Predation in Forest Margin Areas in Lore Lindu National Park, Central Sulawesi, Indonesia. PhD dissertation, Georg-August University of Göttingen.
50.
Ramsier MA, Cunningham AJ, Finneran JJ, Dominy NJ (2012a). Social drive and the evolution of primate hearing. Philosophical Transactions of the Royal Society B 367: 1860–1868.
51.
Ramsier MA, Cunningham AJ, Mortiz GL, Finneran JJ, Williams CV, Ong PS, Gursky-Doyen SL, Dominy NL (2012b). Primate communication in the pure ultrasound. Biology Letters 8: 508–511.
52.
Rosenberger AL (2010). The skull of Tarsius: functional morphology, eyeballs, and the nonpursuit predatory lifestyle. International Journal of Primatology 31: 1032–1054.
53.
Sales G, Pye D (1974a). Ultrasound in rodents. In Ultrasonic Communication by Animals (Sales G, Pye D, eds.), pp 149–201. London, Chapman & Hall.
54.
Sales G, Pye D (1974b). Ultrasonic Communication by Animals. London, Chapman & Hall.
55.
Shekelle M (2008). The history and mystery of the mountain tarsier, Tarsius pumilus. Primate Conservation23: 121–124.
56.
Stanford CB (2002). Avoiding predators: expectations and evidence in primate antipredator behavior. International Journal of Primatology 23: 741–757.
57.
Sugiura H, Tanaka T, Masataka N (2006). Sound transmission in the habitats of Japanese macaques and its possible effect on population differences in coo calls. Behaviour 143: 993–1012.
58.
Waser P, Brown C (1986). Habitat acoustics and primate communication. American Journal of Primatology 10: 135–154.
59.
Whitten T, Mustafa M, Henderson GS (2002). The Ecology of Sulawesi. Cambridge, Cambridge University Press.
60.
Wilson DR, Hare JF (2006). The adaptive utility of Richardson’s ground squirrel (Spermophilus richardsonii) short-range ultrasonic alarm signals. Canadian Journal of Zoology 84: 1322–1330.
61.
Wood SR, Sanderson KJ, Evans CS (2000). Perception of terrestrial and aerial alarm calls by honeyeaters and falcons. Australian Journal of Zoology48:127–134.
62.
Zimmermann E (1981). First record of ultrasound in two prosimian species. Naturwissenschaften 68: 531–532.
63.
Zimmermann E (1996). Castration affects the emission of an ultrasonic vocalization in a nocturnal primate, the grey mouse lemur (Microcebus murinus). Physiology and Behavior 60: 693–697.
© 2019 S. Karger AG, Basel
2019
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.