Copulation Calls in Male Formosan Macaques: Honest Signals of Male Quality?

 Brief Report

Folia Primatol 729   Received: May 10, 2002 Accepted: June 23, 2002

Copulation Calls in Male Formosan
Macaques: Honest Signals of Male
Quality?
Minna J. Hsu^a Jin-Fu Lin^b Li-Ming Chen^a

Govindasamy Agoramoorthy^a

^aDepartment of Biological Sciences, National Sun Yat-sen University, and
^bShi-Pu Junior High School, Kaohsiung, Taiwan, ROC

Key Words
Communication ` Dominance ` Sexual behavior ` Sonogram ` Calling

Introduction

Male copulation calls are found in a number of polygynous primate species, but their functions still represent a puzzle [1]. It has been proposed that among rhesus macaques, male copulation calls are sexually selected handicap signals that females can use to evaluate male quality on account of the cost to males of calling (specifically increased aggression shown to callers) [2]. Evidence in favor of this hypothesis is inconclusive, however, and an alternative explanation of their occur­rence is that the calls simply reflect overall levels of male courtship intensity [3]. This report describes for the first time the acoustic structure and pattern of occur­rence of male copulation calls among the little-studied Formosan macaques. This study also evaluates whether calling is related to male rank and leads to increased levels of aggressive harassment received by mating males, as predicted by the handicap signal hypothesis.

Methods

A long-term study to investigate the population dynamics and social behavior of For­mosan macaques at Mt. Longevity began in July 1993[4?6]. Investigations of vocal behav­iors started from October 1999 [7], and a systematic survey of copulatory calls was con-ducted on 21 social troops between April 2001 and April 2002. Behavioral data and sound recordings were gathered using focal animal sampling and scan sampling methods[8]. Each social group was followed 2?4 times per week for at least 30 min on each follow. Sound

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0015?5713/02/0000?0000$18.50/0 Sun Yat-sen University, PO Box 59-157 Fax +41 61 306 12 34 Kaohsiung 80424, Taiwan (ROC) E-Mail karger@karger.ch Accessible online at: Fax +886 7 5253623 www.karger.com www.karger.com/journals/fpr E-Mail agoram@mail.nsysu.edu.tw

Fig. 1. The occurrence of male copulation calls produced at least once in single- (a) and multiple-mount/thrusting (b) series of Formosan macaques during the 2001?2002 mating season. OTM = Other troop adult males; NTM = nontroop adult males.

recordings were made within a range of few meters, using a Sony professional cassette re-corder (TC-D5 PRO II) and a directional microphone (Sennheiser MKH 460). Spectro­graphic analyses were carried out using a Macintosh computer (G3/350 kHz) and the Canary software package (version 1.2.4).

Results and Discussion

Copulations were observed 401 times between 300 different heterosexual dy­ads, formed by 94 males and 180 females. Males called during copulations with their lips slightly parted but their jaws closed, as is seen in lion-tailed and long-tailed macaques [9]. The tonal units of the whistle-like sounds uttered in irregular trains were well-structured phrases containing up to 4 pulses.The units consisted of 4?7 discrete frequency bands (1.5?19.5 kHz) with low degrees of modulation (fig. 1). Copulation calls were only made by adult males; subadult males never made this call. Copulation calls were given much less frequently by adult males than by females (calls given in 39.2 vs. 88.8% of copulations, respectively, χ² = 214.2,

d.f. = 1, p < 0.001).The occurrence of male copulation calls in Formosan macaques is related to the copulation type: males were observed to call more frequently in a multiple-mount series (67.3% of matings) than in single-mount matings (29.5%; fig. 1), which is consistent with the mate intensity hypothesis.

Little evidence was found that male copulation calls in Formosan macaques functioned as a handicap signal of male quality, which increases the likelihood of calling males receiving aggression. Alpha males did not call in a greater proportion of copulations than other troop or nontroop males, either in single-(χ² = 1.57, d.f.= 2, p > 0.45) or multiple-mount/mating series (χ² = 0.32, d.f. = 2, p > 0.85, fig. 2).

Folia Primatol Hsu/Lin/Chen/Agoramoorthy

Fig. 2. Male copulation call produced by an adult with a phrase of 5 compound units. The noise background approximately at a frequency of 0.45 kHz should be ignored.

Table 1. Association between calling and male type of 88 males (excluding 6 switched ranks) of Formosan macaques in the breeding season 2001?2002 at Mt. Longevity

Alpha males	20	1	21
Other troop males	23	5	28
Nontroop males	18	16	34
Subadult males	0	5	5

Alpha males of social groups called in a similar proportion (86/213) to other troop males (41/102) and nontroop males (30/79), and the difference was not statistically significant between these three groups(χ² = 0.15, d.f. = 2, p > 0.93, Fisher‘s exact probability >0.95). There was, however, a rank effect on the likelihood of calling during copulation at least once in the mating season: 95.2% of alpha males were seen to call, while only 82.1% of other troop males and 52.9% of nontroop males did so (table 1; χ² = 13.55, d.f. = 2, p < 0.01, ψ = 0.404, n = 83). A post hoc test revealed that no difference was found between alpha and other troop males (Fisher‘s exact probability = 1.92, p > 0.17). Nontroop males are a special case, as they want to remain inconspicuous. Importantly, in contradiction to the handicap signal hypothesis, males were never observed to experience mating interruptions/ harassment or physical attacks either during or 5 min after the end of a mount/ mating series.

Copulatory Calls in Male Formosan Macaques Folia Primatol 3

The function of male copulation calls in primate species remains a key area of investigation. What this study has shown, however, is that among Formosan ma­caques, such calls do not function as honest handicap signals of male quality. Such calls may serve to strengthen the pair bond [10], decreasing the likelihood of the female soliciting another male before successful ejaculation occurs. Calls may alter-natively hasten the culmination of a mating sequence via self-stimulation; reducing the time to ejaculation may free the male to begin courting other ovulating females.

Acknowledgments

This research was partially funded by the National Science Council‘s grant (NSC 90-2311-B-110-008) awarded to M.J.H. We thank Stuart Semple, Charlie Nunn and Paul Vasey for their critical comments on earlier versions of the manuscript.

References

1 Zahavi A: Mate selection: A selection for a handicap. J Theor Biol 1975;53:205?214. 2 Hauser MD: Rhesus monkey copulation calls: Honest signal for female choice. Proc R Soc Lond B 1993;254:93?96. 3 Manson JH: Rhesus macaque copulation calls: Re-evaluating the ”honest signal‘ hypothesis. Primates 1996;37:145?154. 4 Hsu MJ, Agoramoorthy G, Lin JF: Interbirth interval in wild Formosan macaques, Macaca cyclopis, at Mt. Longevity, Taiwan. Primates 2001;42:15?25. 5 Hsu MJ, Lin JF. Troop size and structure in free-ranging Formosan macaques (Macaca cyclopis)at Mt. Longevity, Taiwan. Zool Stud 2001;40:49?60. 6 Hsu MJ, Lin JF, Agoramoorthy G: Occurrence of twins in wild Formosan macaques, Macaca cyclopis, at Mt. Longevity, Taiwan. Folia Primatol 2000;71:154?156. 7 Chen LM: Vocal Patterns in Wild Formosan Macaques (Macaca cyclopis); master thesis, Kao­

hsiung, National Sun Yat-sen University, 2001, p 86. 8 Altmann J: Observational study of behavior: Sampling methods. Behaviour 1974;49:227-265. 9 Hohmann GM, Herzog MO: Vocal communication in lion-tailed macaques (Macaca silenus).

Folia Primatol 1985;45:148?178. 10 Hamilton WT, Arrowood PC: Copulatory vocalizations of chacma baboons (Papio ursinus), gibbons (Hylobates hoolock) and humans. Science 1978;200:1405?1409.

Folia Primatol Hsu/Lin/Chen/Agoramoorthy