Abstract
We provide a preliminary case study in red-bellied lemurs (Eulemur rubriventer) to illustrate a multimodal approach to understanding communication strategies within a species with obligate pair-bonds. From June to August 2012, we observed and analyzed signaling behaviors across three established red-bellied lemur pairs at Duke Lemur Center (Durham, NC, USA). Our aim was to assess how individuals combine signal modalities to communicate with pair-mates, and to determine whether these strategies vary by time of day, sex, or pair. We analyzed rates of occurrence of touch (allogrooming, mutual grooming, physical contact, and huddling), scent (scent marking and allomarking), and sound (close-distance contact calls) using Wilcoxon rank sum and exact binomial tests. Time of day impacted rates of occurrence across signal modalities, with higher rates of combined signaling within each modality occurring earlier in the day (p < 0.03). Across time periods, all pairs used auditory signals most frequently, followed by olfactory signals, and finally tactile and tactile-olfactory signals (p < 0.01, all comparisons). In fact, auditory signals frequently overlapped the olfactory signaling modality, and travel rarely occurred without accompanying vocalizations. However, red-bellied lemurs spent the highest percentage of their observed time in tactile signaling bouts (on average, 19.5% of total observed time across pairs). Males and females participated equally in most signaling behaviors (p > 0.1), with the exception of scent marking, which males used more frequently (p < 0.01). The results of this study will aid in developing methods and hypotheses to determine how wild red-bellied lemurs communicate to form, maintain, and advertise their pair-bonds.
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References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–265. https://doi.org/10.1163/156853974X00534
Carter CS (2006) Biological perspectives on social attachment and bonding. In: Carter CS, Ahnert L, Grossmann KE, Hrdy SB, Lamb ME, Porges SW, Sachser N (eds) Attachment and bonding: a new synthesis. MIT Press, Massachusetts, pp 85–100
Curtis D, Zaramody A (1999) Social structure and seasonal variation in the behavior of Eulemur mongoz. Folia Primatol 70:79–96. https://doi.org/10.1159/000021679
Dunbar RIM (1991) Functional significance of social grooming in primates. Folia Primatol 57:121–131. https://doi.org/10.1159/000156574
Endler J (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153. https://doi.org/10.1086/285308
Epple G (1986) Communication by chemical signals. In: Mitchell G, Erwin J (eds) Comparative primate biology, vol 2. Behavior, conservation and ecology. A.R. Liss, New York, pp 531–580
Eppley TM, Ganzhorn JU, Donati G (2016) Latrine behaviour as a multimodal communicatory signal station in wild lemurs: the case of Hapalemur meridionalis. Anim Behav 111:57–67. https://doi.org/10.1016/j.anbehav.2015.10.012
Erhart EM, Overdorff DJ (2008) Rates of agonism by diurnal lemuroids: implications for female social relationships. Int J Primatol 29:1227–1247. https://doi.org/10.1007/s10764-008-9287-0
Fernandez-Duque E (2012) Owl monkeys Aotus spp in the wild and in captivity. Int Zoo Yearb 46:80–94. https://doi.org/10.1111/j.1748-1090.2011.00156.x
Forrest T (1994) From sender to receiver: propagation and environmental effects on acoustic signals. Am Zool 34:644–654. https://doi.org/10.1093/icb/34.6.644
Fröhlich M, van Schaik CP (2018) The function of primate multimodal communication. Anim Cogn 21:619–629. https://doi.org/10.1007/s10071-018-1197-8
Fuentes A (2002) Patterns and trends in primate pair bonds. Int J Primatol 23:953–978. https://doi.org/10.1023/A:1019647514080
Gamba M, Colombo C, Giacoma C (2012) Acoustic cues to caller identity in lemurs: a case study. J Ethol 30:191–196. https://doi.org/10.1007/s10164-011-0291-z
Hebets E, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214. https://doi.org/10.1007/s00265-004-0865-7
Higham J, Hebets E (2013) An introduction to multimodal communication. Behav Ecol Sociobiol 67:1381–1388. https://doi.org/10.1007/s00265-013-1590-x
Hilgartner R, Fitchel C, Kappeler PM, Zinner D (2012) Determinants of pair-living in red-tailed sportive lemurs (Lepilemur ruficaudatus). Ethology 118:466–479. https://doi.org/10.1111/j.1439-0310.2012.02033.x
Jacobs RL, Frankel DC, Rice RJ, Kiefer VJ, Bradley BJ (2018) Parentage complexity in socially monogamous lemurs (Eulemur rubriventer): integrating genetic and observational data. Am J Primatol 80:e22738. https://doi.org/10.1002/ajp.22738
Liebal K, Waller BM, Slocombe KE, Burrows AM (2013) Primate communication: a multimodal approach. Cambridge University Press, Cambridge
Marlof B, McElligott AG, Müeller AE (2007) Female social dominance in two Eulemur species with different social organizations. Zoo Biol 26:201–214. https://doi.org/10.1002/zoo.20135
Merenlender AM (1993) The effects of sociality on the demography and genetic structure of Lemur fulvus rufus (polygamous) and Lemur rubriventer (monogamous) and the conservation implications. Dissertation, University of Rochester
Overdorff DJ (1988) Preliminary report on the activity cycle and diet of the red-bellied lemur (Lemur rubriventer) in Madagascar. Am J Primatol 16:143–153. https://doi.org/10.1002/ajp.1350160205
Overdorff DJ (1991) Ecological correlates to social structure in two prosimian primates: Eulemur fulvus rufus and Eulemur rubriventer in Madagascar. Dissertation, Duke
Overdorff DJ (1992) Territoriality and home range use by red-bellied lemurs (Eulemur rubriventer) in Madagascar. Am J Phys Anthropol 35:129
Overdorff DJ, Tecot SR (2006) Social pair-bonding and resource defense in wild red-bellied lemurs (Eulemur rubriventer). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Developments in primatology: progress and prospects. Springer, New York, pp 235–254
Rigaill L et al (2015) Multimodal advertisement of pregnancy in free-ranging female Japanese macaques (Macaca fuscata). PLoS One 10:e0135127. https://doi.org/10.1371/journal.pone.0135127
Snowdon CT (2017) Vocal communication in family-living and pair-bonded primates. In: Quam RM, Ramsier MA, Fay RR, Popper AN (eds) Primate hearing and communication. Springer handbook of auditory research, vol 63. Springer, Cham, pp 141–174. https://doi.org/10.1007/978-3-319-59478-1
Tecot SR (2008) Seasonality and predictability: The hormonal and behavioral responses of the red-bellied lemur in SE Madagascar. Dissertation, UT-Austin
Tecot SR, Singletary B, Eadie E (2016) Why “monogamy” isn’t good enough. Am J Primatol 78:340–354. https://doi.org/10.1002/ajp.22412
Wilke C, Kavanagh E, Donnellan E, Waller BM, Machanda ZP, Slocombe KE (2017) Production of and responses to unimodal and multimodal signals in wild chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 123:305–316. https://doi.org/10.1016/j.anbehav.2016.10.024
Zahavi A (1977) The testing of a bond. Anim Behav 25:246–247
Zahavi A (1987) The theory of signal selection and some of its implications. In: Delfino VP (ed) International symposium of biological evolution, vol 120. Adriatic Editrice, Bari, pp 305–327
Acknowledgements
This work was supported by the University of Arizona’s School of Anthropology via the W. & N. Sullivan Scholarship Fund. We are grateful to Erin Ehmke and Duke Lemur Center for access and support. We thank Drs. H. D. and N. Steklis for lending us audio recording equipment, Drs. Borgstrom and Torabi for statistical assistance, and N. Cortes and M. Silva for dedicated assistance in data collection and entry. We thank Drs. Papaj, Raichlen, and Pike for their comments on previous drafts. B. Singletary also thanks C. McPherson, J. Webber, and J. Wilson for their support. Research protocols were approved by University of Arizona and Duke University Animal Care and Use Committees.
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All applicable international, national, and institutional guidelines for the care and use of animals were followed. All study procedures conformed to the ethical standards of University of Arizona and Duke University Animal Care and Use Committees (IACUC# A-203-11-627 08). This article does not contain studies with human participants.
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Singletary, B., Tecot, S. Signaling across the senses: a captive case study in pair-bonded red-bellied lemurs (Eulemur rubriventer) at the Duke Lemur Center, NC, USA. Primates 60, 499–505 (2019). https://doi.org/10.1007/s10329-019-00770-9
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DOI: https://doi.org/10.1007/s10329-019-00770-9