It has been proposed that primates use advertisement calls exclusively to negotiate spacing, but the function of female calls has rarely been studied. Here, we investigated the function of male and female advertisement calls in the northern giant mouse lemur (Mirza zaza),a non-gregarious nocturnal primate from north-western Madagascar. We recorded advertisement calls and associated behaviours of 35 M. zaza individuals at the Duke University Lemur Center. We found that females of M. zaza exclusively use their advertisement calls to advertise oestrus. In contrast, male advertisement calls appeared to be used in a spacing context. These findings show that primates can use their advertisement calls for both spacing and mate attraction, and that the sexes may differ in how they use these calls. The novel find of females of M. zaza attracting mates with loud advertisement calls contrasts with many non-primate taxa, where acoustic mate attraction is usually a function of male advertisement calls, and with other primates, where females use visual and olfactory cues to attract males. The loud female advertisement calls of M. zaza likely ensure mating success during the short receptive phase in this non-gregariously foraging, nocturnal primate.

Keywords:
Northern giant mouse lemur, Mirza zaza, Vocalisation, Oestrus cycle, Spacing, Mate attraction
1.
Alexander RD, Marshall DC, Cooley JR (1997). Evolutionary perspectives on insect mating. In Mating Systems in Insects and Arachnids (Choe JC, Crespi BJ, eds.), pp 4–31. Cambridge, Cambridge University Press.
2.
Andersson MB (1994). Sexual Selection. Princeton, Princeton University Press.
3.
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 Sociobiology58: 587–596.
4.
Braune P, Schmidt S, Zimmermann E (2008). Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus ssp.). BMC Biology6: 19.
5.
Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998). Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatologica 69: 295–308.
6.
Charles-Dominique P (1977). Ecology and Behaviour of Nocturnal Primates. New York, Columbia University Press.
7.
Charles-Dominique P, Petter JJ (1980). Ecology and social life of Phaner furcifer. In Nocturnal Malagasy Primates (Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rosseaux A, Schilling A, eds.), pp 75–95. New York, Academic Press.
8.
Cheney DL, Seyfarth RM (1982). Recognition of individuals within and between groups of free-ranging vervet monkeys. American Zoologist 22: 519–529.
9.
Cox CR, Le Boeuf BJ (1977). Female incitation of male competition: a mechanism in sexual selection. American Naturalist 111: 317–335.
10.
Daly M (1978). The cost of mating. American Naturalist 112: 771–774.
11.
Dammhahn M, Kappeler PM (2005). Social system of Microcebus berthae, the world’s smallest primate. International Journal of Primatology26: 407–435.
12.
Delgado RA (2006). Sexual selection in the loud calls of male primates: signal content and function. International Journal of Primatology 27: 5–25.
13.
Eberle M, Kappeler PM (2004). Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behavioural Ecology and Sociobiology57: 77–90.
14.
Falls JB (1992). Playback: a historical perspective. In Playback and Studies of Animal Communication (McGregor PK, ed.), pp 11–33. New York, Plenum Press.
15.
Fernandez-Duque E (2007). Social monogamy in the only nocturnal haplorhines. In Primates in Perspective(Campbell C, Fuentes A, Mackinnon K, Bearder S, Stumpf E, eds.),pp 140–154. Oxford, Oxford University Press.
16.
Fichtel C, Van Schaik CP (2006). Semantic differences in sifaka (Propithecus verreauxi) alarm calls: a reflection of genetic or cultural differences? Ethology112:839–849.
17.
Gamba M, Giacoma C (2007). Quantitative acoustic analysis of the vocal repertoire of the crowned lemur. Ethology, Ecology and Evolution19: 323–343.
18.
Garner RL (1892). The Speech of Monkeys. London, Heinemann.
19.
Gerhardt HC, Huber F (2002). Acoustic Communication in Insects and Anurans: Common Problems and Diverse Solutions. Chicago, University of Chicago Press.
20.
Glatson ARH (1979). Reproduction and Behaviour of the Lesser Mouse Lemur ( Microcebus murinus, Miller, 1777). PhD thesis, University of London.
21.
Hall KRL, Boelkins RC, Goswell MJ (1965). Behavior of patas monkeys, Erythrocebus patas, in captivity, with notes on the natural habitat. Folia Primatologica 3: 22–47.
22.
Hill CM (1994). The role of female Diana monkeys, Cercopithecus diana, in territorial defense. Animal Behaviour 47: 425–431.
23.
Janson CH (1984). Female choice and mating system of the brown capuchin monkey Cebus apella (Primates: Cebidae). Ethology65: 177–200.
24.
Jolly A (1966). Lemur Behavior. Chicago, Chicago University Press.
25.
Kappeler PM (1997). Intrasexual selection in Mirza coquereli: evidence for scramble competition polygyny in a solitary primate. Behavioral Ecology and Sociobiology 45: 115–127.
26.
Kappeler PM, Wimmer B, Zinner D, Tautz D (2002). The hidden matrilineal structure of a solitary lemur: implications for primate social evolution. Proceedings of the Royal Society of London B 269: 1755–1763.
27.
Kappeler PM, Rasoloarison RM, Razafimanantsoa L, Walter L, Roos C (2005). Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray 1870, with description of a new species. Primate Report 71: 3–26.
28.
Langmore NE, Davies NB, Hatchwell BJ, Hartley IR (1996). Female song attracts males in the alpine accentor Prunella collaris. Proceedings of the Royal Society of London B263: 141–146.
29.
Marler P (1965). Communication in monkeys and apes. In Primate Behaviour: Field Studies in Monkeys and Apes (DeVore I, ed.), pp 544–584. New York, Holt, Rinehart & Winston.
30.
Marler P (1968). Aggregation and dispersal: two functions in primate communication. In Primates: Studies in Adaptation and Variability (Jay P, ed.), pp 420–438. New York, Holt, Rinehart & Winston.
31.
Marler P (1969). Colobus guereza: territoriality and group composition. Science 163: 93–95.
32.
Marler P, Mitani J (1988). Vocal communication in primates and birds: parallels and contrasts. In Primate Vocal Communication (Todt D, Goedeking P, Symmes D, eds.), pp 3–14. Berlin, Springer.
33.
Masataka N (1988). The response of red-chested moustached tamarins to long calls from their natal and alien populations. Animal Behaviour 36: 55–61.
34.
Masataka N, Biben M (1987). Temporal rules regulating affiliative vocal exchanges of squirrel monkeys. Behaviour 101: 311–319.
35.
Méndez-Cárdenas MG, Zimmermann E (2009). Duetting – a mechanism to strengthen pair bonds in a dispersed pair-living primate (Lepilemur edwardsi). American Journal of Physical Anthropology139: 523–532.
36.
Mitani JC (1990). Experimental field studies of Asian ape social systems. International Journal of Primatology 11: 102–126.
37.
Pages E (1978). Home range, behaviour and tactile communication in a nocturnal Malagasy lemur Mirza coquereli. In Recent Advances in Primatology (Chivers J, Herbert J, eds.), pp 171–177. New York, Academic Press.
38.
Pages E (1980). Ethoecology of Microcebus coquereli during the dry season. In Nocturnal Malagasy Primates (Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rosseaux A, Schilling A, eds.), pp 97–116. New York, Academic Press.
39.
Pradhan GR, Engelhardt A, van Schaik CP, Maestripieri D (2006). The evolution in female copulation calls of primates: a review and a new model. Behavioural Ecology and Sociobiology59: 333–343.
40.
Radick G (2005). Primate language and the playback experiment, in 1890 and 1980. Journal of the History of Biology38: 461–493.
41.
Raemakers JJ, Raemakers PM (1985). Field playback of loud calls to gibbons, Hylobates lar: sex-specific and species-specific responses. Animal Behaviour 33: 481–493.
42.
Radespiel U (2000). Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. American Journal of Primatology51: 21–40.
43.
Rasoloharijaona S, Randrianambinina B, Braune P, Zimmermann E (2006). Loud calling, spacing and cohesiveness in a nocturnal primate, the Milne Edward’s sportive lemur (Lepilemur edwardsi). American Journal of Physical Anthropology129: 591–600.
44.
Rode EJ, Nekaris KAI, Kappeler PM, Schwitzer C (2015). The largest relative testes size among primates and aseasonal reproduction in a nocturnal lemur, Mirza zaza. American Journal of Physical Anthropology158: 165–169.
45.
Rode EJ, Nekaris KAI, Markolf M, Schliehe-Diecks S, Seiler M, Radespiel U, Schwitzer C (2013). Social organization of the northern giant mouse lemur Mirza zaza in Sahamalaza, north western Madagascar, inferred from nest group composition and genetic relatedness. Contributions to Zoology82: 71–83.
46.
Rode-Margono EJ, Schwitzer C, Nekaris KAI (2016). Morphology, behavior, ranging patterns and habitat use of the northern giant mouse lemur Mirza zaza in Sahamalaza, northwestern Madagascar. In The Dwarf and Mouse Lemurs of Madagascar: Biology, Behavior and Conservation Biogeography of the Cheirogaleidae(Lehman S, Radespiel U, Zimmermann E, eds.),pp 235–254. Cambridge, Cambridge University Press.
47.
Ryan MT (1998). Sexual selection, receiver biases, and the evolution of sex differences. Science281: 1999–2003.
48.
Scheun J, Nowack J, Bennett NC, Ganswindt A (2016) Female reproductive activity and its endocrine correlates in the African lesser bushbaby, Galago moholi. Journal of Comparative Physiology B186: 255–264.
49.
Scordato ES, Drea CM (2007) Scents and sensibility: information content of olfactory signals in the ringtailed lemur, Lemur catta. Animal Behaviour73: 301–314.
50.
Searcy WA, Andersson M (1986). Sexual selection and the evolution of song. Annual Review of Ecology and Systematics 17: 507–533.
51.
Semple S (2001) Individuality and male discrimination of female copulation calls in the yellow baboon. Animal Behaviour61: 1023–1028.
52.
Semple S, McComb K (2000). Perception of female reproductive state from vocal cues in a mammal species. Proceedings of the Royal Society of London B 267: 707–712.
53.
Smith HJ, Newman JD, Bernhards DE, Symmes D (1983). Effects of reproductive state on vocalizations in squirrel monkeys (Saimiri sciureus). Folia Primatologica 40: 233–246.
54.
Stallmann RR, Froehlich JW (2000). Primate sexual swellings as coevolved signal systems. Primates41: 1–16.
55.
Stanger KF (1988). Lautrepertoire und begleitendes Verhalten von nachtaktiven Halbaffen. Eine Untersuchung an Galago demidovii (Zwerggalago), Microcebus murinus (Mausmaki) und Cheirogaleus medius (Katzenmaki) in Gefangenschaft. Master thesis, Eberhardt-Karls Universität Tübingen.
56.
Stanger KF (1993). Structure and Function of the Vocalizations of Nocturnal Prosimians (Cheirogaleidae). PhD thesis, Eberhardt-Karls Universität Tübingen.
57.
Stanger KF (1995). Vocalizations of some cheirogaleid prosimians evaluated in a phylogenetic context. In Creatures of the Dark: The Nocturnal Prosimians (Alterman L, Doyle GA, Izard MK, eds.), pp 353–376. New York, Plenum Press.
58.
Stanger KF, Coffman BS, Izard MK (1995). Reproduction in Coquerel’s dwarf lemur (Mirza coquereli). American Journal of Primatology 36: 223–237.
59.
Sterling EJ, McCreless EE (2006). Adaptation in the aye-aye: a review. In Lemurs: Ecology and Adaptation (Gould L, Sauther ML, eds.), pp 59–184. New York, Springer.
60.
Uster D, Zuberbühler K (2001). The functional significance of Dana monkey “clear” calls. Behaviour138:741–756.
61.
Wallner B, Aspernig D, Millesi E, Machatschke IH (2011). Non-lactating versus lactating females: a comparison of sex steroids, sexual coloration and sexual behavior in Japanese macaques. Primates52: 69–75.
62.
Waser P (1975). Experimental playbacks show vocal mediation of intergroup avoidance in a forest monkey. Nature 255: 56–58.
63.
Waser P (1977). Individual recognition, intragroup cohesion and intergroup spacing: evidence from sound playback to forest monkeys. Behaviour 60: 28–74.
64.
Wiley RH, Richards DG (1978). Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behavioral Ecology and Sociobiology 3: 69–94.
65.
Wrangham RW (1987). Evolution of social structure. In Primate Societies (Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, eds.), pp 282–297. Chicago, University of Chicago Press.
66.
Xiong R, Matsui M, Nishikawa K, Jiang J (2015). Advertisement calls of two horned frogs, Megophrys kuatunensis and M. huangshanensis, from China (Anura, Megophryidae). Current Herpetology34: 51–59.
67.
Zimmermann E (1989). Aspects of reproduction and behavioral and vocal development in Senegal bushbabies (Galago senegalensis). International Journal of Primatology10: 1–16.
68.
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. Ethology93: 211–224.
69.
Zimmermann E, Vorobieva E, Wrogemann D, Hafen T (2000). Use of vocal fingerprinting for specific communication of gray (Microcebus murinus) and rufous mouse lemurs (Microcebus rufus). International Journal of Primatology21: 837–852.
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