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Call Repertoire of the Sahamalaza Sportive Lemur, Lepilemur sahamalazensis

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Abstract

The acoustic structure of primate loud calls can be used as a powerful, inexpensive, and noninvasive tool for intra- and interspecific comparative analyses, reconstruction of phylogeny, and primate surveys. Despite the range of possibilities offered by acoustic analysis, only few studies so far have focused on quantitative descriptions of the acoustic structure of primate loud call repertoires. Here we aimed to assess the vocal repertoire of the solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, and to investigate potential communication functions. We recorded every sportive lemur vocalization we heard during 1000 h of nocturnal observations of eight collared individuals, as well as opportunistic searches in the Ankarafa Forest, Sahamalaza Peninsula in northwest Madagascar. In addition, we used playback experiments with four call types to clarify call function. We measured both temporal and spectral properties to describe calls quantitatively and used cross-validated discriminant function analysis to validate call types that we identified from a preliminary qualitative inspection of the spectrograms of 107 calls. We identified six distinct loud call types with the possibility of a seventh call type, with six loud call types similar to those of Lepilemur edwardsi and two loud call types similar to those of four other sportive lemur species. The described call types most likely function in mate advertisement, offspring care, and territorial defense. Future studies of loud calling of the Sahamalaza sportive lemur are needed to clarify if certain call types are sex specific and if loud calls could be used for recognition of individuals to enable noninvasive density measurements and species monitoring.

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References

  • Ambrose, L. (2003). Three acoustic forms of Allen’s galagos (primates; Galagonidae) in the Central African region. Primates, 44, 25–39.

    PubMed  Google Scholar 

  • Anderson, M. J., Ambrose, L., Dixson, A. F., & Pullen, S. (2000). Intraspecific variation in the vocalizations and hand pad morphology of southern lesser bush babies (Galago moholi): A comparison with G. senegalensis. International Journal of Primatology, 21, 537–555.

    Article  Google Scholar 

  • Andriaholinirina, N., Fausser, J. L., Roos, C., Zinner, D., Thalmann, U., Rabarivola, C., Ravoarimanana, I., Ganzhorn, J. U., Meier, B., Hilgartner, R., Walter, L., Zaramody, A., Langer, C., Hahn, T., Zimmermann, E., Radespiel, U., Craul, M., Tomiuk, J., Tattersall, I., & Rumpler, Y. (2006). Molecular phylogeny and taxonomic revision of the sportive lemurs (Lepilemur, Primates). BMC Evolutionary Biology, 6, 17.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bearder, S. K., Honess, P. E., & Ambrose, L. (1995). Species diversity among galagos with special reference to mate recognition. In L. Alterman, G. A. Doyle, & M. K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 331–352). New York: Plenum Press.

    Chapter  Google Scholar 

  • Braune, P., Schmidt, S., & Zimmermann, E. (2005). Spacing and group coordination in a nocturnal primate, the golden brown mouse lemur (Microcebus ravelobensis): The role of olfactory and acoustic signals. Behavioural Ecology and Sociobiology, 58, 587–596.

    Article  Google Scholar 

  • Braune, P., Schmidt, S., & Zimmermann, E. (2008). Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus ssp.). BMC Biology, 6, 19.

  • Bridges, A. S., & Dorcas, M. E. (2000). Temporal variation in anuran calling behavior: Implications for surveys and monitoring programs. Copeia, 2, 587–592.

    Article  Google Scholar 

  • Brigham, R. M., Grindal, S. D., Firman, M. C., & Morissette, J. L. (1997). The influence of structural clutter on activity patterns of insectivorous bats. Journal of Zoology, 75, 131–136.

    Google Scholar 

  • Büsching, C. D., Heistermann, M., Hodges, J. K., & Zimmermann, E. (1998). Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatologica, 69, 295–308.

    Article  Google Scholar 

  • Cap, H., Deleporte, P., Joachim, J., & Reby, D. (2008). Male vocal behavior and phylogeny in deer. Cladistics, 24, 917–931.

    Article  Google Scholar 

  • Chokkalingam, U., de Jong, W. (2001). Secondary forest: a working definition and typology. International Forestry Review 3, 19–26.

  • Craul, M., Zimmermann, E., Rasoloharijaona, S., Randrianambinina, B., & Radespiel, U. (2007). Unexpected species diversity of Malagasy primates (Lepilemur spp.) in the same biogeographical zone: A morphological and molecular approach with the description of two new species. BMC Evolutionary Biology, 7, 83.

    Article  PubMed Central  PubMed  Google Scholar 

  • Davies, N., & Schwitzer, C. (2013). Lemur conservation status review: An overview of the lemur Red-Listing results 2012. In C. Schwitzer, R. A. Mittermeier, N. Davies, S. Johnson, J. Ratsimbazafy, J. Razafindramanana, E. E. Louis, Jr., & Rajaobelina, S. (Eds.), Lemurs of Madagascar: A strategy for their conservation 2013–2016 (pp. 13–28). IUCN SSC Primate Specialist Group; Bristol Conservation and Science Foundation; Conservation International.

  • Davila-Ross, M., & Geissmann, T. (2007). Call diversity of wild male orangutans: A phylogenetic approach. American Journal of Primatology, 69, 305–324.

    Article  Google Scholar 

  • Farnsworth, A., & Lovette, I. J. (2008). Phylogenetic and ecological effects on interspecific variation in structurally simple avian vocalizations. Biological Journal of the Linnean Society, 94, 155–173.

    Article  Google Scholar 

  • Fichtel, C., & Hammerschmidt, K. (2002). Responses of redfronted lemurs to experimentally modified alarm calls: Evidence for urgency-based changes in call structure. Ethology, 108, 763–777.

    Article  Google Scholar 

  • Fischer, J., Hammerschmidt, K., & Todt, D. (1995). Factors affecting acoustic variation in Barbary macaque (Macaca sylvanus) disturbance calls. Ethology, 101, 51–66.

    Article  Google Scholar 

  • Fischer, J., Metz, M., Cheney, D. L., & Seyfarth, R. M. (2001). Categorical responses of Chacma baboons to graded bark variants? Animal Behaviour, 61, 925–931.

    Article  Google Scholar 

  • Gamba, M., & Giacoma, C. (2006). Vocal tract modeling in a prosimian primate: The black and white ruffed lemur. Acta Acustica united with Acustica, 92, 749–755.

    Google Scholar 

  • Gamba, M., & Giacoma, C. (2007). Quantitative acoustic analysis of the vocal repertoire of the crowned lemur. Ethology Ecology and Evolution, 19, 323–343.

    Article  Google Scholar 

  • Gautier, J. P. (1988). Interspecific affinities among guenons as deduced from vocalizations. In A. Gautier-Hion, F. Bouliére, & J. P. Gautier (Eds.), A primate radiation: Evolutionary biology of the African guenons (pp. 195–226). New York: Cambridge University Press.

    Google Scholar 

  • Geissmann, T., & Nijman, V. (2006). Calling behavior of wild silvery gibbons (Hylobates moloch) in Java (Indonesia). American Journal Primatology, 68, 1–19.

    Article  Google Scholar 

  • Hafen, T., Neveu, H., Rumpler, Y., Wilden, I., & Zimmermann, E. (1998). Acoustically dimorphic advertisement calls separate morphologically and genetically homogenous populations of the grey mouse lemur (Microcebus murinus). Folia Primatologica, 69, 342–356.

    Article  Google Scholar 

  • Harcourt, C., & Thornback, J. (1990). Lemurs of Madagascar and the Comoros. The IUCN Red Data Book. Gland, Switzerland, and Cambridge, U.K: IUCN.

    Google Scholar 

  • Harper, G., Steininger, M., Tucker, C., Juhn, D., Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation 34, 325–333.

  • IUCN Red List of Threatened Species. Version 2014.2. www.iucnredlist.org/ (Accessed July 25, 2014).

  • Kalko, E. K. V. (1995). Echolocation signal design, foraging habitats and guild structure in six Neotropical sheath-tailed bats (Emballonuridae). In P. A. Racey & S. M. Swift (Eds.), Ecology, evolution and behaviour of bats. Oxford: The Zoological Society of London and Clarendon Press.

    Google Scholar 

  • Lehner, P. N. (1998). Handbook of Ethological Methods. Cambridge: Cambridge University Press, 694 p.

  • Lehtinen, R. M., Wojtowicz, E. A., & Hailey, A. (2011). Male vocalizations, female discrimination and molecular phylogeny: Multiple perspectives on the taxonomic status of a critically endangered Caribbean frog. Journal of Zoology, 283, 117–125.

    Article  Google Scholar 

  • Lei, R. H., Engberg, S. E., Andriantompohavana, R., McGuire, S. M., Mittermeier, R. A., Zaonarivelo, J. R., Brenneman, R. A., Louis, E. E. J. (2008). Nocturnal lemur diversity at Masoala National Park. Texas Tech University Museum Special Publications, 53,1-41.

  • Louis, E. E. J., Engberg, S. E., Lei, R., Geng, H., Sommer, J. A., Randriamampionona, R., Randriamanana, J. C., Zaonarivelo, J. R., Andriantompohavana, R., Randria, G., Prosper, P., Ramaromilanto, B., Rakotoarisoa, G., Rooney, A., Brenneman, R. A. (2006). Molecular and morphological analyses of the sportive lemurs (family Megaladapidae: genus Lepilemur) reveals 11 previously unrecognized species. Texas Tech University Museum Special Publications, 49, 1–49.

  • Macedonia, J. M., & Stanger, K. F. (1994). Phylogeny of the lemuridae revisited: Evidence from communication signals. Folia Primatologica, 63, 1–43.

    Article  CAS  Google Scholar 

  • Masters, J. C. (1991). Loud calls of Galago crassicaudatus and G. garnettii and their relation to habitat structure. Primates, 32, 153–167.

    Article  Google Scholar 

  • Mayr, E. (1978). Darwin and natural selection. American Scientific, 65, 312–327.

    Google Scholar 

  • Méndez-Cárdenas, M., Randrianambinina, B., Rabesandratana, A., Rasoloharijaona, S., & Zimmermann, E. (2008). Geographic variation in loud calls of sportive lemurs (Lepilemur ssp.) and their implications for conservation. American Journal of Primatology, 70, 828–838.

    Article  PubMed  Google Scholar 

  • Méndez-Cárdenas, M., & Zimmermann, E. (2009). Duetting: A mechanism to strengthen pair bonds in a dispersed pair-living primate (Lepilemur edwardsi)? American Journal of Physical Anthropology, 139, 523–532.

    Article  PubMed  Google Scholar 

  • Merker, S., & Groves, C. P. (2006). Tarsius lariang: A new primate species from Western Central Sulawesi. International Journal of Primatology, 27, 465–485.

    Article  Google Scholar 

  • Mittermeier, R. A., Ratsimbazafy, J., & Rylands, A. B. (2007). Primates in peril: The world’s 25 Most Endangered Primates 2006–2008. Primate Conservation, 22, 1–40.

    Article  Google Scholar 

  • Nietsch, A., & Kopp, M. L. (1998). Role of vocalization in species differentiation of Sulawesi Tarsiers. Folia Primatologica, 69, 371–378.

    Article  Google Scholar 

  • Oates, J. F., Bocian, C. M., & Terranova, C. J. (2000). The loud calls of black-and-white colobus monkeys: Their adaptive and taxonomic significance in light of new data. In P. F. Whitehead & C. J. Jolly (Eds.), Old World monkeys (pp. 431–452). Cambridge, U.K.: Cambridge University Press.

    Chapter  Google Scholar 

  • Oates, J. F., & Trocco, T. F. (1983). Taxonomy and phylogeny of black- and-white colobus monkeys: Inferences from an analysis of loud call variation. Folia Primatologica, 40, 83–113.

    Article  CAS  Google Scholar 

  • O’Farrell, M. J. (1997). Use of echolocation calls for the identification of free-flying bats. Transactions of the Western Section of the Wildlife Society, 33, 1–8.

    Google Scholar 

  • Olivieri, G., Zimmermann, E., Randrianambinina, B., Rasoloharijaona, S., Rakotondravony, D., Guschanski, K., Radespiel, U. (2007). The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Molecular Phylogenetics and Evolution, 43, 309–327.

  • Owings, D. H., & Morton, E. S. (1998). Animal vocal communication: A new approach. Cambridge, U.K.: Cambridge University Press.

    Book  Google Scholar 

  • Peters, G., & Tonkin-Leyhausen, B. A. (1999). Evolution of acoustic communication signals of mammals: Friendly close-range vocalizations in Felidae (Carnivora). Journal of Mammalian Evolution, 2, 129–159.

    Article  Google Scholar 

  • Ploog, D. (1974). Phylogenetic and ontogenetic aspects of vocal behavior in squirrel monkeys. Neuroscience Research Program Bulletin, 12, 611–618.

    Google Scholar 

  • Rabarivola, C., Zaramody, A., Fausser, J. L., Andriaholinirina, N., Roos, C., Zinner, D., Rumpler, Y. (2006). Cytogenetic and molecular characteristics of a new species of Lepilemur from Northern Madagascar. Lemur News, 11, 45–49.

  • Rabesandratana, A. Z. (2006). Variation microgeographiques et bioacoustiques de Lepilemur edwardsi (Geoffroy, 1850) dans le Parc National Ankarafantsika (region nord-ouest de Madagascar). Doctoral dissertation, Universite´ d’Antananarivo, Madagascar.

  • Ramaromilanto, B., Lei, R. H., Engberg, S. E., Johnson, S. E., Sitzmann, B. D., & Jouis, E. E. J. (2009). Sportive lemur diversity at Mananara-Nord Biosphere Reserve, Madagascar. Occasional Papers of the Museum of Texas Tech University, 286, 1–22.

    Google Scholar 

  • Rasoloharijaona, S., Rakotosamimanana, B., Zimmermann, E. (2000). Infanticide by a male Milne-Edwards' sportive lemur (Lepilemur edwardsi) in Ampijoroa, NW-Madagascar. International Journal of  Primatology, 21, 41–45.

  • Rasoloharijaona, S., Randrianambinina, B., Braune, P., & Zimmermann, E. (2006). Loud calling, spacing, and cohesiveness in a nocturnal primate, the Milne Edwards’ sportive lemur (Lepilemur edwardsi). American Journal of Physical Anthropology, 129, 591–600.

    Article  PubMed  Google Scholar 

  • Riede, K. (1998). Acoustic monitoring of Orthoptera and its potential for conservation. Journal of Insect Conservation, 2, 217–223.

    Article  Google Scholar 

  • Ryan, M. J., & Kime, N. M. (2003). Selection on long-distance acoustic signals. In A. M. Simmons, A. N. Popper, & R. R. Fay (Eds.), Acoustic communication (pp. 225–274). New York: Springer-Verlag.

    Chapter  Google Scholar 

  • Saunders, M. B., & Barclay, R. M. R. (1992). Ecomorphology of insectivorous bats: A test of predictions using two morphologically similar species. Ecology, 73, 1335–1345.

    Article  Google Scholar 

  • Schrader, L., & Todt, D. (1993). Contact call parameters covary with social context in common marmosets, Callithrix j. jacchus. Animal Behaviour, 46, 1026–1028.

    Article  Google Scholar 

  • Schwitzer, C., Schwitzer, N., Randriatahina, G. H., Rabarivola, C., & Kaumanns, W. (2006). “Programme Sahamalaza”: New perspectives for the in situ and ex situ study and conservation of the blue-eyed black lemur (Eulemur macaco flavifrons) in a fragmented habitat. In C. Schwitzer, S. Brandt, O. Ramilijaona, M. Rakotomalala Razanahoera, D. Ackermand, T. Razakamanana, J. U. Ganzhorn (Eds.), Proceedings of the German-Malagasy research cooperation in life and earth sciences (pp. 135–149). Berlin: Concept Verlag.

  • Schwitzer, N., Kaumanns, W., Seitz, P. C., & Schwitzer, C. (2007a). Cathemeral activity patterns of the blue-eyed black lemur Eulemur macaco flavifrons in intact and degraded forest fragments. Endangered Species Research, 3, 293–247.

    Google Scholar 

  • Schwitzer, N., Randriatahina, G. H., Kaumanns, W., Hoffmeister, D., & Schwitzer, C. (2007b). Habitat utilization of blue-eyed black lemurs, Eulemur macaco flavifrons (Gray, 1867), in primary and altered forest fragments. Primate Conservation, 22, 79–87.

    Article  Google Scholar 

  • Seiler, M., Holderied, M., & Schwitzer, C. (2013). Anti-predator behaviour of Sahamalaza sportive lemurs, Lepilemur sahamalazensis, at diurnal sleeping sites. Contributions to Zoology, 82, 131–143.

    Google Scholar 

  • Seiler, M., Holderied, M., & Schwitzer, C. (2014). Habitat selection and use in the Critically Endangered Sahamalaza sportive lemur, Lepilemur sahamalazensis, in altered habitat. Endangered Species Research, 24, 273–286.

    Article  Google Scholar 

  • Seiler, M., Randriatahina, G. H., & Schwitzer, C. (2010). Ongoing threats to lemurs and their habitat inside the Sahamalaza – Iles Radama National Park. Lemur News, 15, 7–9.

    Google Scholar 

  • Seiler, M., Randriatahina, G. H., & Schwitzer, C. (2012). The rapid boost of forest destruction and poaching of lemurs inside the Sahamalaza – Iles Radama National Park. Lemur News, 16, 28–30.

    Google Scholar 

  • Stanger, K. (1995). Vocalizations of some cheirogaleid prosimians evaluated in a phylogenetic context. In L. Alterman, G. Doyle, & M. Izard (Eds.), Creatures of the dark (pp. 353–376). New York: Plenum Press.

    Chapter  Google Scholar 

  • Tattersall, I. (1982). The primates of Madagascar. New York: Columbia University Press.

    Google Scholar 

  • Templeton, A. R. (1998). The role of molecular genetics in speciation studies. In R. DeSalle & B. Schierwater (Eds.), Molecular approaches to ecology and evolution (pp. 131–156). Basel: Birkhäuser.

    Chapter  Google Scholar 

  • Thomassen, H. A., & Povel, G. D. E. (2006). Comparative and phylogenetic analysis of the echo clicks and social vocalizations of swiftlets (Aves: Apodidae). Biological Journal of the Linnean Society, 88, 631–643.

    Article  Google Scholar 

  • Whitehead, J. M. (1995). Vox Alouattinae: A preliminary survey of acoustic characteristics of long-distance calls of howling monkeys. International Journal of Primatology, 16, 121–144.

    Article  Google Scholar 

  • Zimmermann, E. (1990). Differentiation of vocalizations on bushbabies (Galaginae, Prosimiae, Primates) and significance for assessing phylogenetic relationships. Journal of Zoological Systematics and Evolutionary Research, 28, 217–239.

    Article  Google Scholar 

  • Zimmermann, E., Bearder, S. K., Doyle, G. A., & Andersson, A. B. (1988). Variations in vocal patterns of Senegal and South African lesser bushbabies and their implications for taxonomic relationships. Folia Primatologica, 51, 87–105.

    Article  CAS  Google Scholar 

  • Zimmermann, E., & Lerch, C. (1993). The complex acoustic design of an advertisement call in male mouse lemurs (Microcebus murinus, Prosimii, Primates) and sources of its variation. Ethology, 93, 211–224.

    Article  Google Scholar 

  • Zimmermann, E., Vorobieva, E., Wrogemann, D., & Hafen, T. (2000). Use of vocal fingerprinting for specific discrimination of gray (Microcebus murinus) and rufous mouse lemurs (Microcebus rufus). International Journal of Primatology, 21, 837–852.

    Article  Google Scholar 

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Acknowledgments

We thank Madagascar National Parks (MNP), especially the director of Sahamalaza – Iles Radama National Park, M. Isaia Raymond, for their continuing collaboration. Thank you also to the DGEF and CAFF/CORE for granting us research permits for our work in Sahamalaza, and to Prof. Rabarivola Clément for his ongoing help. Tantely Nirina Ralantoharijaona, Bronwen Daniel, Chris Ingold, Sam Gatley, Jeremy Cusack, Lucy Todd, Lisa Knudsen, and Gabby Bell, along with all Ankarafa field guides, contributed substantially to the data collection. We further thank the editor and two anonymous reviewers for valuable comments on a former version of the manuscript. M. Seiler was funded by Bristol Conservation and Science Foundation, Association Européenne pour l’Etude et la Conservation des Lémuriens (AEECL), Conservation International Primate Action Fund, Margot Marsh Biodiversity Foundation, Mohamed bin Zayed Species Conservation Fund, International Primatological Society, and Christian-Vogel-Fonds.

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  1. Bristol Zoological Society, c/o Bristol Zoo Gardens, Bristol, BS8 3HA, United Kingdom

    Melanie Seiler & Christoph Schwitzer

  2. School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, United Kingdom

    Melanie Seiler & Marc Holderied

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  1. Melanie Seiler
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Seiler, M., Schwitzer, C. & Holderied, M. Call Repertoire of the Sahamalaza Sportive Lemur, Lepilemur sahamalazensis . Int J Primatol 36, 647–665 (2015). https://doi.org/10.1007/s10764-015-9846-0

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