Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments

Close association between an anoestrous female at the time of lactation and adult male(s) is relatively rare in mammals, but common in baboons (Papio hamadryas subsp.). The functional significance of these “friendships” remains unclear, however. In chacma baboons (P. h. griseipes), friendships are a counter-strategy to infanticide by immigrant males. Experimental playback of female distress calls in chacma baboons revealed that male friends are more motivated to protect females and infants than are control males. Olive baboons (P. h. anubis) also exhibit friendships, but infanticide is rare, suggesting that friendships provide females with protection from non-lethal aggression (anti-harassment hypothesis) or serve to promote male–infant bonds that later benefit the maturing juvenile (future male caretaker hypothesis). We replicated these playback experiments on a group of olive baboons to test between these hypotheses and to evaluate if the lower costs of non-lethal harassment lessens male protective responsiveness relative to protection from (more costly) infanticide. Spatial data revealed that most lactating females had one to four friend males. Relative to non-friends, friend dyads were characterized by higher rates of allogrooming and infant handling, but less agonism. Female rank was correlated with the number of male friends. Just as in chacma baboons, playback of female screams elicited stronger responses from male friends than control males in support the anti-harassment hypothesis. Compared to the chacma baboon, male olive baboons appeared to exhibit similarly high levels of protective solicitude for female friends although they protect against non-lethal harassment rather than infanticide.     

Vocal competition in male Xenopus laevis frogs

Male Xenopus laevis frogs produce underwater advertisement calls that attract gravid females and suppress calling by male competitors. Here we explore whether groups of males establish vocal ranks and whether auditory cues alone suffice for vocal suppression. Tests of male–male pairs within assigned groups reveal linear vocal dominance relations, in which each male has a defined rank. Both the duration over which males interact, as well as the number of competitive opportunities, affect linearity. Linear dominance across the group is stable for about 2 weeks; rank is dynamic. Males engage in physical interactions (clasping) while paired but clasping and vocal rank are not correlated. Playbacks of advertisement calls suppress calling and calls from high- and low-ranking males are equally effective. Thus, auditory cues alone suffice to suppress vocal behavior. Playback intensities equivalent to a nearby male advertising effectively suppress calling while low-intensity playbacks are either ineffective or stimulate vocal behavior. X. laevis advertisement calls are biphasic, composed of alternating fast and slow click trills. Approximately half the males tested are more vocally suppressed by all slow than by all fast trills; thus, these males can distinguish between the two phases. The fully aquatic family Pipidae diverged from terrestrial ancestors approximately 170 mya. Vocal suppression in the X. laevis mating system may represent the translation of an ancient anuran social strategy to underwater life.     

Call matching in the quacking frog (Crinia georgiana)

Males of the quacking frog Crinia georgiana produce calls consisting of 1–11 notes. Playback experiments using synthetic calls showed that males tend to match the number of notes in 2-note and 4-note stimuli; however, males tended to produce more than 1 note in response to a 1-note stimulus and fewer than 8 notes in response to an 8-note stimulus. Successive playbacks of two, 4-note calls from separate speakers indicate that males are likely to match the combined number of notes in the calls of two neighbors, even if they are not equidistant from the focal male. The results are compared with the few other studies of matching in anurans, and interpreted in terms of hypotheses developed to explain matching in songbirds. One attractive and testable hypothesis for call matching in C. georgiana is that males are attempting to produce calls that are at least as attractive to females as those of rivals, without wasting energy. Received: 14 February 2000 / Received in revised form: 11 April 2000 / Accepted: 3 May 2000     

Advertisement-call modification,male competition,and female preference in the bird-voiced treefrog <Emphasis Type="Italic">Hyla avivoca</Emphasis>

Senders and receivers influence dynamic characteristics of the signals used for mate attraction over different time scales. On a moment-to-moment basis, interactions among senders competing for a mate influence dynamic characteristics, whereas the preferences of receivers of the opposite gender exert an influence over evolutionary time. We observed and recorded the calling patterns of the bird-voiced treefrog Hyla avivoca to assess how the dynamic characters of calls vary during interactions among groups of males in a chorus. This question was also addressed using playback experiments with males. Playback experiments with females showed how changes in dynamic call properties are likely to affect male mating success. Frogs calling in pairs, groups, or in response to playbacks produced longer calls than did isolated males. During call overlap, males often increased the duration of the silent interval (gaps) between the pulses of their calls so that the pulses of the calls of two neighbors interdigitated. This change resulted in increased variability of pulse rate, a traditionally static acoustic property; however, males also produced high proportions of non-overlapped calls in which variability in pulse rate was low and had species-typical values. Females preferred long calls to short- and average-duration calls, and non-overlapped calls to overlapped calls. Given a choice between pairs of overlapped calls, females preferred pairs in which the proportion of overlap was low and pairs in which the pulses of such calls interdigitated completely. The observed patterns of vocal competition thus reflect the preferences of conspecific females, which have influenced the evolution of the calling behavior of H. avivoca. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Female mate selection in the natterjack toad: active choice or passive atraction?

Summary Variation in seasonal mating success among male natterjack toads (Bufo calamita) was influenced by the number of nights that males spent at the pond and by male body size. Large males produced louder and lower frequency calls than small males, and maintained larger acoustic territories. After arriving at the pond, one half of all observed females mated with the first male they encountered. The remainder visited several males before initiating amplexus, but no criteria could be identified that females might have used when deciding whether to accept or reject a male. Movements between several males seem to be best explained by low female responsiveness to male advertisement calls on cold nights which were nonoptimal for oviposition. Females attempted to reject non-calling males both before and after amplexus, but this may be a mechanism to avoid mismating with males of the common toad (Bufo bufo), an explosive breeder that utilised the same pond. In two-choice playback experiments using synthetic advertisement calls, females showed no preference for calls based on their frequency. Females preferred calls of intermediate pulse repetition rate equivalent to those produced by a male at the same body temperature. Pulse rate is thus potentially subject to stabilishing selection and may be an important character for species-recognition. Females preferred fast rather than slow call rates, but only when the alternative rates were extreme. They also preferred calls which they perceived at the highest sound pressure level, but did not discriminate between absolute sound pressure levels of alternative stimuli at different distances. Since females that delay mating and oviposition may suffer predation, it is suggested that female preference for loud, rapidly repeated calls may be adaptive in the sense of minimizing the costs of locating conspecific males, rather than maximizing the probability of obtaining a high quality mate. Competition between males to maintain large acoustic territories and produce calls that can be easily detected by females would seem to be a sufficient mechanism to explain the evolution of the striking calls produced by male natterjacks.     

Interspecific acoustic interactions of the neotropical treefrog Hyla ebraccata

Summary Hyla ebraccata, H. microcephala and H. phlebodes commonly occur together in Panama. The three species have calls exhibiting broad frequency overlap and call during the same season and time of day from similar microhabitats, frequently in close proximity. The vocal repertoires of the three species are structurally and functionally similar. All employ multi-part advertisement and aggressive calls which consist of a primary note followed by a variable number of clicks. H. ebraccata males often responded to heterospecific calls with multi-note synchronized responses, and calls with primary notes greater than 150–200 ms were most effective in eliciting synchrony. Playback experiments with synthetic 1-note advertisement calls of different durations and both synthetic 1-note advertisement calls and 200 ms tones of different frequencies demonstrated that H. ebraccata males will synchronize with stimuli which are similar in frequency and duration to conspecific calls. Data from a two-choice experiment with female H. ebraccata demonstrate that calls of individual H. microcephala can reduce the attractiveness of a H. ebraccata male's calls if primary notes overlap. By synchronizing response calls to those of H. microcephala, a H. ebraccata may reduce the chances that his calls are rendered less attractive to potential mates.Aggressive calls of these species are graded and are characterized by higher pulse repetition rates and often longer durations than advertisement calls. H. ebraccata males respond to aggressive calls of H. microcephala and H. phlebodes as they do to their own calls. Heterospecific aggressive interactions probably occur because the species interfere acoustically. Our results demonstrate that H. ebraccata males behave in ways which enhance their ability to communicate in a noisy assemblage of conspecific and heterospecific males.     

Acoustically mediated neighbor recognition in the North American bullfrog,Rana catesbeiana

Summary Playback experiments were conducted to determine whether territorial male bullfrogs (Rana catesbeiana) were capable of discriminating between advertisement calls of neighbors and strangers. Territorial males adjacent to subject males were removed and replaced with a speaker which broadcast calls of a stranger or the removed male. Ten of 11 males responded more strongly to calls of strangers than to calls of neighbors. When advertisement calls of neighbors were broadcast to subject males from positions within the removed neighbor's territory and from positions opposite the subject male, all 9 males tested responded more strongly to calls of a neighbor broadcast from a new position than to playbacks of the same call broadcast within the removed neighbor's territory. Because male bullfrogs recognize familiar calls and associate these calls with a particular direction or location, these data provide the first evidence for acoustically mediated neighbor recognition in frogs.     

Significance of spectral and temporal call parameters in the auditory communication of male grass frogs

Summary During the spawning period, male grass frogs (Rana temporaria L.) frequently produce short and long territorial calls in addition to mating calls. The calls differ in mean pulse number, duration, and pattern of amplitude modulation. Experiments in which recorded natural calls are played back reveal that male grass frogs are capable of discriminating the different conspecific calls. A male frog stimulated by mating calls always responds by producing mating calls in greater numbers (Fig. 3). Territorial calls presented at low intensity also cause an increase in the mating-call rate (Fig. 4), but at high intensity they clicit territorial calls and turning toward the loudspeaker. A combination of short and long territorial calls was especially effective in eliciting the phonotaxis response. As play-back experiments with simulated calls show, the carrier frequency and the pulse repetition rate are particularly important cues for recognition of conspecific calls (Fig. 5). A simulated call with a 400-Hz carrier frequency (the dominant frquency of the mating call) is just as effective as the natural call with the complete frequency spectrum (Fig. 3), whereas a 1100-Hz simulated call is ineffective (Fig. 5). The chief factors in discrimination among the conspecific calls are the call repetition rate and probably the amplitude and frequency modulation. Changes in the duration of the calls had little effect (Fig. 6). The available evidence suggests that the mating call has a reciprocally stimulating action on males in a chorus, whereas the territorial calls experess aggressiveness and give warning to other males.     

Paternal care and egg survival both increase with clutch size in the fathead minnow,Pimephales promelas

Summary In some species of fishes with paternal care, females prefer to spawn with males who are already defeding eggs; moreover, in many species, paternal care increases with the number of eggs that a male is defending. If egg survival depends on the level of paternal care, and is largely independent of egg number, then egg survival should increase with clutch size. This result would provide a potential adaptive mechanism for female preference for males with eggs. I examined the effects of clutch size on paternal care and egg survival in the fathead minnow, Pimephales promelas, and found that both increased with male clutch size.     

Reproductive consequences of maternal care patterns during estrus among free-ranging rhesus monkeys

Summary We examined the hypothesis that among free-ranging rhesus monkeys (Macaca mulatta), maternal care patterns during estrus influence chances of conception independently of variation in the timing of the postpartum resumption of mating. We observed 24 multiparous mothers and their infants before and during the 1990 mating season. When mothers resumed mating, they abruptly sought less contact with their infants. Infants responded by increasing the rates with which they emitted distress calls and attempted to make nipple contact. High levels of maternal rejection and low levels of maternal nipple contact initiation during the mother's first estrus were associated with low suckling frequencies and high chances of conception. Although demanding infants had some success in gaining access to the nipples of reluctant mothers during estrus, mothers' chances of conception were unrelated to measures of infant demand or distress calling. Individual differences in maternal behavior regulating access to the nipple during estrus were unrelated to those shown previously. During estrus, mothers appeared to regulate nipple contact according to their infant's age and perhaps other factors related to its vulnerability. Correspondence to: C.M. Berman     

Male bill colour and age are associated with parental abilities and breeding performance in blackbirds

In monogamous bird species, male parental investment may influence offspring fitness and females may gain advantages through mating with males providing extensive paternal care. However, paternal care is a benefit that can only be assessed indirectly because mate choice precedes paternal activities. Individual quality and age, both signalled by morphological characteristics, may reflect parental abilities. Because they may reflect individual foraging abilities, carotenoid-based colorations have been proposed to honestly signal parental quality. The blackbird (Turdus merula), a socially monogamous species, exhibits biparental care and males show bills that vary from pale yellow to orange due to carotenoid pigments. In this study, we investigated whether male bill colour and age are associated with parental ability. Our results suggest that males with more orange bills and older males are better fathers. Indeed, male visit rate increased with their bill colour index independently of age, and brood condition was higher for adult males, compared to yearlings, independently of bill colour. Overall, the number of fledglings produced was positively influenced by both the age of males and the colour intensity of their bills. Males with more orange bills and adults had a greater number of fledglings and these males also had higher levels of prolactin, a hormone known to promote parental care. This latter finding suggests that prolactin may be the link between carotenoid based colorations and the intensity of paternal effort. Thus, male bill colour seems to honestly reveal male physiological adjustment to paternal activities.     

Female preferences for male calling bout duration in a field cricket

Summary The calls of male field crickets attract sexually receptive females. In Gryllus integer, males differ from one another in their durations of uninterrupted calling (calling bout lengths). Tape recordings of the calls of 50 wild-caught males revealed that 14 males spent most of their calling time in short bouts (Fig. 1A), 18 in both short and long bouts (Fig. 1B), and 18 in long bouts (Fig. 1C). Re-recordings of 32 males after 3 weeks showed that calling bout lengths of individual males are stable with time (age) (Fig. 2). Three phonotaxis experiments investigated whether calling bout lengths of males affect female preferences. They demonstrated that (1) females can discriminate among conspecific males on the basis of calls alone; (2) females are preferentially attracted to males with long calling bout lengths; and (3) calling bout length is the specific factor responsible for preferential attraction. These results precisely identify a criterion that females use to discriminate among potential mates of their own species.     

Calling energetics of a neotropical treefrog,Hyla microcephala

Summary We investigated the calling energetics of Hyla microcephala, a neotropical treefrog with an unusually complex vocal repertoire. Males respond to the calls of other individuals by adding secondary click notes to their calls, thereby increasing the total number of notes given per minute. Rates of oxygen consumption of males calling in metabolic chambers were 0.41–2.80 ml O₂/(g·h), corresponding to calling rates of 205–6330 notes/h. Note rate explained 95% of the variance in meta-bolic rate; the effect of variation in body size and temperature was small. Data from playback experiments with males in the field showed that note rate increased as as the number of notes in a stimulus call increased, and this resulted in substantial increases in the cost of calling. Average metabolic rates for males in the field were about 1.7 ml O₂/(g·h), for a net cost of calling of about 20 J/h for an average-size male. However, estimated metabolic rates varied by more than 300% and were strongly influenced by the proximity and calling activity of other males in the chorus. Male H. microcephala appear to conserve energy by reducing calling rates when only a few males are active and increasing calling efforts only when vocal competition among males is intense.     

Male baboon responses to experimental manipulations of loud “wahoo calls”: testing an honest signal of fighting ability

Among male chacma baboons (Papio hamadryas ursinus), rank positions in the dominance hierarchy are fiercely contested. Physical fighting is costly but relatively rare in this species. Instead, disputes are frequently resolved using displays that include loud, repetitive “wahoo” (two-syllable bark) vocalizations. We previously found that males of all ranks adjust their contest behavior based on the relative fighting ability of opponents and that length of the second syllable (“hoo” duration), calling rate, and fundamental frequency reliably indicate fighting ability. To test whether males indeed attend to hoo duration when assessing opponents, we designed two sets of playback experiments in which call sequence pairs were identical except for this single modified feature. In experiment 1, we used calls recorded from high-ranking males unfamiliar to all subjects. In experiment 2, callers were familiar rivals that ranked one position below subjects in the dominance hierarchy. In paired analyses, subjects in both experiments responded more strongly to sequences with more intense signal features (most commonly associated with high-quality males) compared to sequences with relatively less exaggerated features (most often associated with low-quality males). Results suggest that males can use acoustic features to both indirectly evaluate strangers and to monitor the changing condition of those rivals that present the biggest intragroup threat to their position in the dominance hierarchy. Taken together with our previous research, baboons appear to follow a classic assessor strategy—signal features related to rank and condition are salient to males and directly affect their propensity to respond to rivals.     

Clinal variation in anuran advertisement calls: basis for acoustic isolation?

Summary The calls of male treefrogs (Eleutherodactylus coqui) were studied along an altitudinal gradient in the Luquillo Mountains in eastern Puerto Rico. The fundamental frequency of each note in the advertisement call was highly negatively correlated with altitude. Although males responded vigorously to playbacks of calls of other males recorded at their own altitude, males at high altitudes responded less frequently to recorded calls of males from low altitudes, and males at low altitudes responded less frequently to recorded calls of males from high altitudes. These results are discussed in relation to potential isolation in contiguous populations of E. coqui.     

Evolution of male mating behavior: male spadefoot toads preferentially associate with conspecific males

The evolution of male breeding aggregations is difficult to explain because males may reduce their reproductive success by associating with their closest competitors. We examined aggregative behavior by male New Mexico spadefoot toads, Spea multiplicata, which form breeding choruses in rain-filled pools. We specifically asked whether males are attracted to conspecific calls and, if so, whether they preferentially associate with those male calls that are also attractive to females. Field observations revealed that males showed significant clustering with conspecifics within breeding ponds, whereas laboratory phonotaxis experiments revealed that males preferentially associated with conspecific male calls. Moreover, when males were presented with conspecific calls that differed in call rate, smaller males associated with the stimulus preferred by females (average call rate). Thus, males appear to evaluate the attractiveness of competitors using the same trait employed by females to assess potential mates, and males adjust their positions relative to competitors depending on their size. We discuss these results in the light of several current hypotheses on the adaptive significance of male breeding aggregations. Received: 20 December 1999 / Accepted: 18 March 2000     

Female and male behavioral response to advertisement calls of graded complexity in túngara frogs, <Emphasis Type="Italic">Physalaemus pustulosus</Emphasis>

We investigated the natural dynamics in a sexual signal that combines different call components and explored the role of call complexity in sexual selection using a neotropical frog. Male túngara frogs, Physalaemus pustulosus, facultatively add up to seven short, multi-harmonic components (chucks) to the simple form of their calls (whines). Female túngara frogs are preferentially attracted to whines with chucks over whines without chucks, and males also call more in response to calls containing chucks. Because acoustic predators prefer complex calls, in the context of simple (no chucks) versus complex (any number of chucks) calls, the variably complex call appears to have evolved in response to the opposing selective forces of natural and sexual selection. There is no evidence, however, for the function of increasing the number of chucks within complex calls. We tested two aspects of increasing call complexity: natural patterns of use of call types in males and how both sexes respond to variation in multi-chuck calls. Males incrementally change call complexity by the addition or subtraction of a single chuck and usually do not produce more than two chucks. Variation in call complexity, for calls with at least one chuck, does not influence response calling in males or phonotaxis in females. Our results suggest that one reason for not increasing call complexity beyond a single chuck is the diminishing effectiveness on the responses of both sexes. This is a posthumous publication for A. Stanley Rand     

The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor)

Summary The vocal behavior of Hyla versicolor was studied in the field by means of behavioral observations and playback experiments, and these data were coupled with measurements of oxygen consumption in calling frogs to estimate the effect of social interactions on calling energetics. Male gray treefrogs have intense calls (median peak SPL=109 dB, fast RMS SPL=100 dB at 50 cm). At an air temperature of 23° C, males produced an average of 1,200–1,300 calls/h for 2–4 h per night. Calling rates and call durations differed among individuals, but were relatively constant for each male during periods of sustained calling. Males in dense choruses gave calls about twice as long as isolated males, but produced calls at about half the rate. Consequently, total calling effort and estimated aerobic costs were largely independent of chorus density. Playbacks of recorded calls to males in the field elicited increases in call duration and decreases in calling rate, regardless of the rate or duration of the stimulus. Males gave longer calls in response to long calls or to stimuli presented at high rates, but they did not precisely match either stimulus rate or duration. Calling effort and estimated oxygen consumption changed only slightly during stimulus playbacks. These results indicate that male-male competition elicits pro-found changes in the vocal behavior of calling males, but these changes have little effect on energy expenditure. We estimated that most calling males had metabolic rates of about 1.7–1.8 ml O₂/(g\h), or about 280 J/h for an average size (8.6 g) male at 20° C. Although changes in call duration and calling rate did not affect aerobic costs of calling, males producing long calls at slow rates called for fewer hours per night than males producing shorter calls at higher rates. This suggests that calling time may be limited by the rate at which muscle glycogen reserves are depleted.     

Individual differences in the mechanisms underlying the onset and maintenance of paternal behavior and the inhibition of infanticide in the monogamous biparental California mouse,Peromyscus californicus

Virgin male Peromyscus californicus tend to behave infanticidally or nonparentally towards pups, whereas virtually all males exhibit parental behavior following birth of their own young. Most males (65–75%) living with their pregnant partner attacked or ignored unfamiliar pups and did not become parental (behave parentally) prior to birth of their young. However, a significant minority of males (34%) living with their partner became parental after just 24 h of postcopulatory cohabitation with the female and remained parental throughout their mate's pregnancy. Males that were infanticidal before the birth of their young became parental only after their young were born. The presence of the mother was necessary for the postpartum maintenance of paternal behavior and the inhibition of infanticide in males that were infanticidal prepartum. In contrast, males that were paternal prior to birth of their young continued to be paternal after birth, even in the absence of postpartum contact with the mother. Thus, different mechanisms are involved in the inhibition of infanticide and the onset and maintenance of paternal behavior. Correspondence to: D.J. Gubernick     

Loud calls as indicators of dominance in male baboons (Papio cynocephalus ursinus)

Adult male baboons (Papio cynocephalus) give loud two-syllable 'wahoo' calls during dawn choruses, interactions between groups, when chasing females, and in aggressive interactions with other males. These 'contest' wahoos are acoustically different from 'alarm' wahoos given to predators. In a study of free-ranging baboons in the Okavango Delta, Botswana, we found no significant correlations between the acoustic features of wahoos and adult male size; however, acoustic features were correlated with male dominance rank, age, and calling bout length. Here we show that other measures of calling behavior also appear to function as honest indicators of stamina and competitive ability. High-ranking males were more likely than middle- or low-ranking males to participate in wahoo bouts. They called at significantly higher rates, and their bouts were longer and contained more calls. All males were significantly more likely to participate in wahoo bouts with another male if their opponent's rank was similar to their own. Bouts involving males of similar ranks were longer, contained more wahoos, and involved calling at higher rates, than other bouts. In contests between males of similar ranks, the subordinate and dominant were equally likely to end the bout, whereas in contests involving males of disparate ranks, subordinates were significantly more likely to end the bout. Bouts involving males of similar rank were significantly more likely than others to escalate and result in physical fighting.