The effect of female call on male howling in red howler monkeys(Alouatta seniculus)

Howler (Alouatta spp.)females often produce loud calls together with the males. Sometimes these howls are not heard above the much louder male call, but on other occasions most of the howls are produced by the females. Observations indicate that female howls are aggressive. Females howl at other troop females and at extratroop females; they also sit close to their mates and howl at other males. I suggest that howling by the females with their mate is important in strengthening the pair bond whereby the male recognizes his infants and acts protectively toward them. Playback experiments of female howls elicited more response from the males than did recordings of male/female and male-only howls, supporting the hypothesis that females howl in order to incite competition among the males.     

Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty,Madagascar

The mating behavior of ring-tailed lemurs at Berenty, Madagascar, was observed in April 1982. Although Troop A included five adult females, only two were observed to mate. The mating period covered two consecutive days, April 24 and 25. Each female was receptive for about 4 hr. Data from 47 copulations, of which 38 were with ejaculation, suggest that to be the first mating partner is of importance for male ring-tailed lemurs. Previously it has been suggested that male dominance is of little significance in determining mating partners. In this investigation it was observed that the second most dominant male MK was always the first mating partner. Only after several ejaculations and resultant fatigue did he lose possession of the female to lower ranking males, and the first ranking male was not seen to copulate with either female at any time. These results suggest that a male's mating success is partly, but not completely correlated with his dominance rank, and that other factors, including his length of residence in the group and female choice, also determine patterns of mating.     

Male Mate Choice in Lemur catta

Though females are generally more selective in mate choice, males may also derive reproductive benefits from exercising mate selectivity if one or more factors limit male reproductive success and females differ in reproductive potential. I used male mating effort as a proxy for male mate choice in ring-tailed lemurs (Lemur catta). I calculated mating effort as the rate of male-male agonism during each female's estrous period 30 min before and 30 min after the first and last mountings with intromission. I collected data on 1 free-ranging Lemur catta troop during 2 consecutive breeding seasons on St. Catherines Island, USA. In both yrs, male mating effort differed significantly among troop females once I adjusted male-male agonistic rates to reflect agonistic intensity, and I corrected for the number of observed mates per female (2000: χ² = 27.43, df = 3, p < 0.0001; 2001: χ² = 21.10, df = 3, p < 0.001). Results strongly suggest male mate choice. Contrary to expectation, males did not expend the greatest mating effort for females with the highest dominance status nor the highest reproductive success. Males preferred females that either: (1) belonged to the age class in which fecundity and infant survival is the highest at this site (4–9 yrs), or 2) were older females (≥10 yrs) with high reproductive success. Female reproductive potential appears to be an important variable determining male mating effort in Lemur catta.     

Sexual selection and adult male orangutan long calls

Long calls given by adult male orangutans (Pongo pygmaeus) have been hypothesized to mediate interindividual spacing among male orangutans and to attract female orangutans, to high-ranking mates over long distances. To test these two hypotheses I conducted observations of calling behaviour and a series of experimental playbacks of recorded long calls. The findings were consistent with the male-spacing hypothesis but did not support the mate-attraction hypothesis. Experimental playbacks demonstrate that long calls regulate spacing between males through an approach-avoidance system based on dominance relationships: the highest-ranking adult male approaches calls, while lower-ranking, males avoid calls. The results of playbacks also reveal that sexually active females do not move toward long calls, and therefore do not indicate that long calls function in attracting mates. This latter finding suggests that female mate choice may not have been an important selective factor during the evolution of long calls.     

Special relationships instead of female dominance for redfronted lemurs,Eulemur fulvus rufus

Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale–multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male–female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male–female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male–female affiliations illuminated developmental and functional aspects of male–female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male–female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male–female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate. Am. J. Primatol. 43:239–258, 1997. © 1997 Wiley-Liss, Inc.     

Copulatory Plug Displacement Evidences Sperm Competition in Lemur catta

Male displacement of copulatory (sperm) plugs from female vaginas provides further evidence for sperm competition in ring-tailed lemurs (Lemur catta), a gregarious prosimian species with a multimale, multifemale mating system. During two mating seasons, I studied two groups of free-ranging ring-tailed lemurs on St. Catherines Island, GA, USA. I observed 22 mating pairs in which males achieved penile intromission. Copulatory plug displacement by males occurred in 9 cases. Plugs were displaced during copulation by male penes upon withdrawl following deep vaginal thrusting. In every case of copulatory plug displacement, the male displacing a plug mated to ejaculation with the estrous female. In a mating system in which females typically mate with more than one male during estrous, often in succession, copulatory plug displacement may function to disrupt or preclude other males' successful insemination of estrous females. The effects of sperm plug displacement on paternity in Lemur catta are unknown, as no study had heretofore documented copulatory plug displacement in this species. The first-male mating advantage suggested for Lemur catta should be re-evaluated where mating order is known, and copulatory plug displacement during mating, or lack thereof, is identified. Because there is a tendency for first-mating males to mate-guard for longer periods of time in Lemur catta, the latency period between the first mate's ejaculation and that of subsequent mates may be an important determinant of male fertilization success.     

Relative Dominance and Resource Availability Mediate Mantled Howler (Alouatta palliata) Spatial Responses to Neighbors’ Loud Calls

Many animals generate long-distance vocalizations (“loud calls”) that have been hypothesized to mediate spatial interactions. Howls by mantled howlers (Alouatta palliata), specifically, are hypothesized to function in group spacing, but the mechanism by which this is accomplished remains unclear. In this study, I evaluated the role of naturally occurring howls in mediating mantled howler intergroup spatial interactions on Barro Colorado Island, Panama. Multivariate analyses examined relationships between social and environmental contextual variables and the likelihood that a group would approach or avoid a neighboring group’s howl. Mantled howlers were more likely to approach howling neighbors when fruit and flower availability was limited. Relative dominance was also a highly significant predictor of approach, though the relationship ran contrary to expectations. Groups were more likely to approach howling neighbors higher in the established dominance hierarchy than those lower down, possibly reflecting priority access of more dominant groups to higher quality resources. Other variables tested, including numeric odds, vocalization intensity, infanticide risk, and location of the howling group, were not significant predictors of spatial response. These findings are consistent with the assertion that howls contain identifying information and highlight the importance of including contextual variables in multivariate analyses of spatial responses to loud calls. These results also indicate potential contrasts between observational and playback studies by suggesting that howl location may play a greater role in responses to simulated intruders than to known neighbor groups, and that relative dominance may provide a more salient measure of competitive ability than numeric odds among groups with interaction histories.     

Scent marking as resource defense by female Lemur catta

Because ring-tailed lemurs (Lemur catta) are a female-dominant, female-philopatric species in which the females provide the majority of parental care and troop defense, resource defense is a possible function of female lemur scent marking. To test this hypothesis, I conducted three studies. First, I presented captive, individually housed females with a series of samples of female scent, each from a different female, to determine whether they would respond to those samples and discriminate between them. Second, I reanalyzed data from a focal animal study of four females in two adjacent troops in Berenty Reserve, Madagascar, to determine female marking rates before, during, and after the mating season, and to clarify the relationship among positions of feeding, intertroop defense, and scent marking. The third study was based on ad libitum observations of the sniffing and marking behavior of a troop in Berenty Reserve during a year when they traveled far out of their home range. The females in study 1 investigated female scent samples but provided no evidence that they discriminated between them. In study 2 the wild females marked throughout the study and did not limit their marking to the mating season. They deposited significantly more of their marks in a zone of confrontation with adjacent troops, where they also did the majority of their feeding, and they increased their rate of marking during agonistic intertroop confrontations. The females determined the positions of their scent marks and deposited the first mark in the majority of countermarking sequences. When the females traveled out of their defended range in study 3, they significantly decreased their rate of marking and increased their rate of sniffing spots but not marking them. All evidence gathered so far supports the hypothesis that one function of female ring-tailed lemur scent marking is to provide intergroup information that is then used to reinforce the border of the defended resource.     

Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve,Madagascar

Observations of reproductive behavior in free-ranging Lemur catta were carried out during one annual cycle. Variability in the behavior of female ringtailed lemurs during parturition appears to be mainly a function of the female's parity and thus her experience. Females within a troop show estrous asynchrony and characteristically mate with more than one male. Females also exhibit proceptive behavior toward and mate with some males from other troops and with transferring males. The potential for a male to monopolize mating opportunities during a female's short estrous period is therefore limited. Male mating strategies in ringtailed lemurs can be seen as adaptations to female mate choice during a highly restricted breeding season. In this species the dominance hierarchy does not break down with regard to the order of mating. The highest ranking male (central male) mates first and shows precopulatory guarding and longer postejaculatory guarding, which may increase his chances of siring the offspring. Subsequent mating partners have developed various counterstrategies to mitigate mating order effects.     

Intergroup encounters in wild white-faced capuchins (Cebus capucinus)

Wrangham (1980) hypothesized that knowledge of the nature of intergroup encounters is crucial to understanding primate social relationships and social organization. I studied a single social group of wild white-faced capuchins over a period of 26 months and observed 44 encounters between social groups during 3703 hr of observation. All intergroup encounters consisted of predominantly hostile social interactions. However, nonaggressive interactions between males of different social groups occurred in a few cases. Adult males were the sole participants in 39 encounters and the primary participants in all 44 encounters. The alpha male was the most frequent participant. High-ranking females participated aggressively in five encounters, and low-ranking females never participated. There was no stable intergroup dominance hierarchy. I hypothesize that the need for male-male cooperation in intergroup aggression is an important factor influencing the quality of intragroup male-male relationships. Behavior during intergroup encounters is consistent with the idea that intergroup behavior is related to male reproductive strategies, but inconsistent with the idea that intergroup aggression is related to female defense of resources. The possibility that males are “hired guns” (Wrangham, 1980) cannot be ruled out.     

Effects of spatial proximity and alliances on dominance relations among female ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar

In the present study, we describe a change in the dominance rank of the top-ranking female in a wild troop of ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. After the top-ranking female fell to the bottom-ranking position, she was able to outrank a low-ranking female with the support of her adult daughter or an unrelated high-ranking female. These results indicate that, as in cercopithecine monkeys such as macaques and baboons, close proximity and alliances influence dominance relations among adult females in a wild troop of ring-tailed lemurs.     

Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta)

The challenge hypothesis (J. C. Wingfield, R. E. Hegner, B. G. Ball, and A. M. Duffy, 1990, Am. Nat. 136, 829-846) proposes that in birds, reptiles, and fish, "the frequency or intensity of reproductive aggression as an effect of T[estosterone] is strongest in situations of social instability, such as during the formation of dominance relationships, the establishment of territorial boundaries, or challenges by a conspecific male for a territory or access to mates" (p. 833). To determine the extension of this hypothesis to mammalian species, we tested predictions of the hypothesis in a nonpaternal, seasonal breeding, prosimian primate (ring-tailed lemurs, Lemur catta). Semi-free-ranging males were studied during periods of social stability (premating period) and instability (mating period). The annual mating season consists of several days during which males fight for access to promiscuous group females as each individually becomes sexually receptive for 1 day. Male rates of aggression were compared to fecal testosterone levels within premating and mating periods. In the premating period male rate of aggression was not significantly correlated with testosterone level. By contrast, during the mating season testosterone and aggression levels were positively and significantly correlated. However, on days just preceding estrus, male rate of aggression was not significantly correlated with testosterone, but on days of estrus, when aggressive challenges peaked sharply, testosterone and aggression were highly positively correlated. These results suggest that the challenge hypothesis applies to mammals as well as to birds, reptiles, and fish. In addition, elevations in testosterone were tightly circumscribed around days of estrus, suggesting a compromise between costs and benefits of elevated testosterone levels.     

Calling,Courtship, and Condition in the Fall Field Cricket,Gryllus pennsylvanicus

Theoretically, sexual signals should provide honest information about mating benefits and many sexually reproducing species use honest signals when signalling to potential mates. Male crickets produce two types of acoustic mating signals: a long-distance mate attraction call and a short-range courtship call. We tested whether wild-caught fall field cricket (Gryllus pennsylvanicus) males in high condition (high residual mass or large body size) produce higher effort calls (in support of the honest signalling hypothesis). We also tested an alternative hypothesis, whether low condition males produce higher effort calls (in support of the terminal investment hypothesis). Several components of long-distance mate attraction calls honestly reflected male body size, with larger males producing louder mate attraction calls at lower carrier frequencies. Long-distance mate attraction chirp rate dishonestly signalled body size, with small males producing faster chirp rates. Short-range courtship calls dishonestly reflected male residual mass, as chirp rate and pulse rate were best explained by a curvilinear function of residual mass. By producing long-distance mate attraction calls and courtship calls with similar or higher effort compared to high condition males, low condition males (low residual mass or small body size) may increase their effort in current reproductive success at the expense of their future reproductive success, suggesting that not all sexual signals are honest.     

Adult Male Scent-Marking in Lemur catta and Eulemur fulvus rufus

Scent-marking and olfactory communication are used extensively by prosimians and can provide spatial and temporal records of group movement and behavior. We compare rates of male scent-marking in relation to reproductive seasons, male dominance rank, and habitat use in two related prosimians: Lemur catta and Eulemur fulvus rufus. We collected scent-marking data on adult male Lemur catta at Beza-Mahafaly Reserve (dry forest), and on Eulemur fulvus rufus at Ranomafana National Park (rainforest), Madagascar. In Lemur, rates of overall scent-marking differed significantly by reproductive season, with higher rates occurring in mating and lactation/migration periods, whereas in Eulemur, reproductive season did not appear to affect scent-marking rates. Dominance rank of male Lemur catta did not affect rates of scent-marking. Among male Eulemur fulvus, dominance relations were not apparent; however, 2 of the 5 focal males scent-marked somewhat more frequently during the mating season and also experienced greater mating success. In Lemur catta, higher rates of scent-marking in the mating season may relate to indirect reproductive competition during a period of high aggression, while such mating competition was not as marked in Eulemur fulvus. Furthermore, higher rates of marking in resident male Lemur catta during male migration may correlate with vigilance toward immigrating males. Greater overall scent-marking rates in ring-tailed lemurs may relate to extensive intergroup home range overlap and no area of exclusive use, whereas the red-fronted lemur groups tended to forage in areas of their home range where little-to-no intergroup overlap occurred.     

Experimental test of female black howler monkey (Alouatta Pigra) responses to loud calls from potentially infanticidal males: effects of numeric odds, vulnerable offspring, and companion behavior

During group defense, the contribution of female black howler monkeys (Alouatta pigra) may help deter male intruders; however, their involvement during natural intergroup encounters is facultative. Experimental playback trials simulating potentially infanticidal males were used to examine whether a female's reproductive investment and/or her group's relative fighting ability would influence her participation in loud call displays. Female howlers never responded to recordings without alpha male accompaniment, but their response patterns did not simply mimic his. For example, unlike alpha males, females with small, vulnerable offspring were no more likely than females without infants to participate in howling displays during playback trials. Further, although females without any small infants in their group got closer to speakers than females living in groups with small infants, males did not respond in the same way. To artificially simulate different "numeric odds" scenarios, recordings of one or three howling males (simulated intruders) were broadcast to females living in groups with 1-3 resident males. Responses were consistent with the hypothesis that females assessed intergroup fighting ability. As in alpha males, the weakest female responses occurred when the numeric odds were against their group. However, whereas alpha males participated most when numeric odds were in their favor, females had the most intense approach responses when the number of defending and intruding males was equal. Females appeared to use a cost-effective strategy, reserving their assistance for when their participation could have the greatest impact.     

Why Be Vigilant? The Case of the Alpha Animal

We compared patterns of vigilance behavior in a male- and a female-dominant species—white-faced capuchins and ring-tailed lemurs—and used the results to test four hypotheses to explain vigilance behavior in primates. Adult male white-faced capuchins spent significantly more time vigilant than females did, and much male vigilance appeared to be directed toward males from other social groups. This finding supports the protection of paternity hypothesis. No sex difference existed in vigilance behavior among the ring-tailed lemurs, and subjects of both sexes exhibited more vigilance toward predators/potential predators than toward extragroup conspecifics, which supports the predator detection hypothesis. A trade-off argument, suggesting that females tolerate males in a group in return for greater male vigilance, does not apply to ring-tailed lemurs in our study. In both the male-dominant capuchins and the female-dominant ring-tailed lemurs, the alpha subject in the majority of the study groups was significantly more vigilant than other group members were. In white-faced capuchins, the alpha male mates more often than subordinate males do; therefore, the greater degree of vigilance exhibited by the alpha male may correspond to the protection of his reproductive investment. In ring-tailed lemurs, there can be more than one matriline in a group. Thus, the greater amount of vigilance behavior exhibited by the alpha female may be related to protection of her matriline, which could ultimately lead to greater inclusive fitness. Alpha subjects in our study groups exhibited certain behaviors more frequently or exclusively. Accordingly, there may be a constellation of behaviors characteristic of alpha animals.     

Vigilance behavior during the birth and lactation season in naturally occurring ring-tailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

I examined the vigilance behavior of adult males and females in two groups of ring-tailed lemurs(Lemur catta)during the birth and lactation season at the Beza-Mahafaly Reserve, southwestern Madagascar. I found no sex difference with respect to the rates of overall vigilance, rates of vigilance toward a potential predator or unfamiliar sound, or rates of vigilance toward conspecifics from other social groups, nor were there sex differences in the percentage of time spent vigilant in any of the above categories. Higher-ranking females were vigilant significantly more often toward predators or potential predators than lower-ranking females were. I detected no relationship between vigilance behavior and dominance rank among adult males. The alpha female in each group exhibited significantly more vigilance behavior than all other members of her group. It was predicted that males should exhibit more vigilance behavior than females do, particularly during the birth and lactation season, when predator pressure is high, if they are benefiting females in this respect. I discuss the results in the context of this prediction and in terms of how ring-tailed lemur males benefit females, and why they may be tolerated in social groups.     

Androgen levels and female social dominance in Lemur catta

Morphological and behavioural traits which improve agonistic power are subject to intrasexual selection and, at the proximate level, are influenced by circulating androgens. Because intrasexual selection in mammals is more intense among males, they typically dominate females. Female social dominance is therefore unexpected and, indeed, rare. Ring-tailed lemurs (Lemur catta) are sexually monomorphic primates in which all adult females dominate all males. The goal of our study was to test the prediction that female dominance in this species is associated with high androgen levels. Using two captive groups, we collected data on agonistic behaviour and non-invasively assessed their androgen concentrations in faeces and saliva by enzyme immunoassay. We found that adult female L. catta do not have higher androgen levels than males. However, during the mating season there was a twofold increase in both the androgen levels and conflict rates among females. This seasonal increase in their androgen levels was probably not due to a general increase in ovarian hormone production because those females showing the strongest signs of follicular development tended to have low androgen concentrations. At the individual level neither the individual aggression rates nor the proportion of same-sexed individuals dominated were correlated with their androgen levels. We conclude that female dominance in ring-tailed lemurs is neither based on physical superiority nor on high androgen levels and that it is equally important to study male subordination and prenatal brain priming effects for a complete understanding of this phenomenon.     

Endocrine correlates of pregnancy in the ring-tailed lemur (Lemur catta): implications for the masculinization of daughters

Female ring-tailed lemurs (Lemur catta) are Malagasy primates that are size monomorphic with males, socially dominate males, and exhibit a long, pendulous clitoris, channeled by the urethra. These masculine traits evoke certain attributes of female spotted hyenas (Crocuta crocuta) and draw attention to the potential role of androgens in lemur sexual differentiation. Here, hormonal correlates of prenatal development were assessed to explore the possibility that maternal androgens may shape the masculine morphological and behavioral features of developing female lemurs. Maternal serum 17α-hydroxyprogesterone, dehydroepiandrosterone sulphate (DHEA-S), ?⁴ androstenedione (androst-4-ene-3,17,dione), testosterone, and 17β-estradiol were charted throughout the 19 pregnancies of 11 ring-tailed lemurs. As in spotted hyenas, lemur pregnancies were associated with an immediate increase in androgen concentrations (implicating early maternal derivation), followed by continued increases across stages of gestation. Pregnancies that produced singleton males, twin males, or mixed-sex twins were marked by greater androgen and estrogen concentrations than were pregnancies that produced singleton or twin females, especially in the third trimester, implicating the fetal testes in late-term steroid profiles. Concentrations of DHEA-S were mostly below detectable limits, suggesting a minor role for the adrenals in androgen biosynthesis. Androgen concentrations of pregnant lemurs bearing female fetuses, although less than those of pregnant hyenas, exceeded preconception and postpartum values and peaked in the third trimester. Although a maternal (and, on occasion, fraternal) source of androgen may exist for fetal lemurs, further research is required to confirm that these steroids would reach the developing female and contribute to her masculinization.     

Territorial behavior in Southeast Asian langurs: Resource defense or mate defense?

Between-group antagonism or territoriality in primates may serve two different but compatible functions: resource defense or mate defense. Females are expected to be involved more strongly in the first, males in the second. The resource defense hypothesis predicts that home range overlap should decrease as defensibility and population density increase, and that females should be involved in hostile between-group interactions. The mate defense hypothesis predicts that between-group relations should be hostile and that males should take the primary role in antagonistic encounters. In a comparative study of 12 populations of 6 Presbytis species in Southeast Asia, we found support for the mate defense hypothesis; only males produce loud calls, between-group antagonism is entirely a male affair, and neither defensibility nor population density determine spatial exclusivity or the level of antagonism. We discuss the differences between our findings and traditional interpretations of territorial behavior.