So near and yet so far: territorial pairs but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer

Among pair-living species, which represent a simple form of gregariousness, the degree of cohesion appears to be highly variable, but the mechanisms responsible for the maintenance of cohesiveness have been poorly studied. We present data from long-term behavioural observations of eight pairs of fork-marked lemurs, including year-round data on their sleeping site use and spatial data from simultaneous focal follows of both pair partners, that characterize its social organization as ‘dispersed pairs’. Although pairs were stable over several years, territories of pair partners overlapped almost perfectly and interactions between them were frequent, the cohesiveness of pairs was extremely low. High rates of conflict relative to frequencies of affiliative interactions indicated that avoidance of the pair partner is the key mechanism responsible for the observed pattern of space use. The repeated use of the same predictable food resources during the night, frequent conflicts over food and patterns of vocal communication imply that avoidance of direct feeding competition, together with incomplete knowledge about the pair partner's position, lead to the observed low cohesiveness. The freedom to forage solitarily and the associated lack of information about the pair partner's position found in fork-marked lemurs are in contrast to most group-living species and qualify dispersed pairs as a focus for future studies of models on animal movement decisions. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission

Many nonhuman primates produce species-typical loud calls used to communicate between and within groups over long distances. Given their observed spacing functions, primate loud calls are likely to show acoustic adaptations to increase their propagation over distance. Here we evaluate the hypothesis that primates emit loud calls at relatively low sound frequencies to minimize their attenuation. We tested this hypothesis within and between species. First, we compared the frequencies of loud calls produced by each species with those of other calls from their vocal repertoires. Second, we investigated the relationship between loud call frequency and home range size across a sample of primate species. Comparisons indicated that primates produce loud calls at lower frequencies than other calls within their vocal repertoires. In addition, a significant negative relationship exists between loud call frequency and home range size among species. The relationship between call frequency and range size holds after controlling for the potentially confounding effects of body size and phylogeny. These results are consistent with the hypothesis that nonhuman primates produce loud calls at relatively low frequencies to facilitate their transmission over long distances.     

Does nonnutritive tree gouging in a rainforest‐dwelling lemur convey resource ownership as does loud calling in a dry forest‐dwelling lemur?

Nonhuman primates may defend crucial resources using acoustic or chemical signals. When essential resources are limited, ownership display for a resource may be enhanced. Defending resources may depend on population density and habitat characteristics. Using the Milne Edwards' sportive lemurs (Lepilemur edwardsi) and weasel sportive lemurs (L. mustelinus) as models, we tested whether two cryptic nocturnal lemur species differing in population density and habitat show differences in their vocal and chemical communication for signaling ownership of resources. L. edwardsi inhabits a western dry deciduous forest in a high‐density population, whereas L. mustelinus is found in an eastern rainforest in low density. We followed ten L. edwardsi (six males and four females) and nine L. mustelinus (four males and five females) for 215 hr during the early evening (06:00–10:00 p.m.) and the early morning (02:00–05:00 a.m.) and recorded their behavior using focal animal sampling. We found that both species differed in their vocal and chemical communication. L. edwardsi was highly vocal and displayed loud calling in the mornings and evenings while feeding or in the vicinity of resting places. In contrast, L. mustelinus never vocalized during observations, but displayed tree‐gouging behavior that was never observed in L. edwardsi. Tree gouging occurred more often during early evening sessions than early morning sessions. Subjects gouged trees after leaving their sleeping hole and before moving around. We suggest that, in weasel sportive lemurs, non‐nutritive tree gouging is used as a scent‐marking behavior in order to display ownership of sleeping sites. Altogether, our findings provide first empirical evidence on the evolution of different communication systems in two cryptic nocturnal primate species contrasting in habitat quality and population density. Further investigations are needed to provide more insight into the underlying mechanisms. Am. J. Primatol. 72:1062–1072, 2010. © 2010 Wiley‐Liss, Inc.     

Acoustic and Temporal Variation in Gelada (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>) Loud Calls Advertise Male Quality

Many animals rely on information from vocal signals to assess potential competitors and mates. For example, in primates, males use loud calls to assess rivals when the acoustic properties of the calls reliably indicate the condition or quality of the sender. Here, we investigate whether the loud calls of male geladas (Theropithecus gelada) function as a quality signal. Gelada males produce loud calls during ritualistic chases with rival males. Given the physically taxing nature of these displays, we hypothesize that variation in the acoustic properties of loud calls reliably signal male stamina or competitive ability. To test this hypothesis, we examined whether the acoustic properties of the gelada loud call varied in relation to individual, age, status, and exhaustion. Specifically, we examined 12 call parameters (e.g., fundamental frequency) and 3 bout parameters (e.g., number of calls per bout), that have been previously shown to vary across condition in male primates. We found that several acoustic features varied consistently across age and status such that males deemed higher quality in gelada society (e.g., high status) produced more calls per bout, produced calls that were lower in overall frequency measures, and exhibited a greater vocal range. In addition, we found that similar acoustic features varied with exhaustion; after a long chase event, males produced both fewer calls per bout and calls with higher spectral measures. Results from this study are consistent with the hypothesis that gelada loud calls are quality signals, contributing to the growing evidence that primates may use acoustic information to assess the quality of a rival or a potential mate.     

Cues to Androgens and Quality in Male Gibbon Songs

Animal vocal signals may provide information about senders and mediate important social interactions like sexual competition, territory maintenance and mate selection. Hence, it is important to understand whether vocal signals provide accurate information about animal attributes or status. Gibbons are non-human primates that produce loud, distinctive and melodious vocalizations resembling more those of birds than of other non-human primates. Wild gibbons are characterized by flexibility in social organization (i.e., pairs and multimale units) as well as in mating system (i.e., monogamy and polyandry). Such features make them a suitable model to investigate whether the physiology (hormonal status) and socio-demographic features find their correspondence in the structure of their songs. By combining male solo song recordings, endocrine outputs using non-invasive fecal androgen measures and behavioral observations, we studied 14 groups (10 pair-living, 4 multimale) of wild white-handed gibbons (Hylobates lar) residing at Khao Yai National Park, Thailand. We collected a total of 322 fecal samples and recorded 48 songs from 18 adult animals. Our results confirmed inter-individuality in male gibbon songs, and showed a clear correlation between androgen levels and song structures. Gibbons with higher androgen levels produced calls having higher pitch, and similarly adult individuals produced longer calls than senior males. Thus, it is plausible that gibbon vocalizations provide receivers with information about singers'' attributes.     

Vocal regulation of inter- and intragroup spacing during boundary encounters in the titi monkey,Callicebus moloch

Monogamous primates maintain exclusive use of their ranges by regularly defining and reinforcing the conventional location of boundaries.Callicebus moloch males often call alone during the first morning bout, when groups are near boundaries but usually separated by more than 100m. Depending on the location and proximity of neighboring animals, groups might begin duetting and approaching one another. Duetting requires close vocal and spatial coordination of the mated pair, and stimulates the approach of neighboring pairs. At the boundary, vocalizations which keep the pair together and those associated with withdrawal from the boundary increase in proportion. To determine the effect of different calls, I played back recordings of six different vocalizations during two playback experiments, holding location and proximity constant. The responses supported hypotheses generated in the normalistic study, and suggested that at the boundary aggression is primarily intrasexual. Vocalizations and their effects in specified contexts constitute the mechanisms regulating spacing. The resulting spacing patterns maintain resource availability and exclusive access to a mate.     

Duetting—A mechanism to strengthen pair bonds in a dispersed pair‐living primate (Lepilemur edwardsi)?

Duetting is defined as an interactively organized pair display in which one pair partner coordinates its vocalizations in time with those of the other. It is widespread among tropical birds and cohesive pair‐living primates, in which it is suggested to strengthen pair bonds. We know very little about the presence and function of duetting in dispersed pair‐living mammals. We studied duetting behavior in a solitary foraging, but pair‐sleeping, primate, the Milne Edwards' sportive lemur, in a dry deciduous forest of north‐western Madagascar. We radio‐tracked six pairs throughout 1 year and recorded their sleeping sites and associations, home‐range use, and vocal and behavioral interactions. Three different periods were covered (mating, pregnancy, and offspring care). Sleeping partners form long‐term pair bonds, indicated by an almost exclusive pair‐specific usage of sleeping sites and home‐ranges across periods. We explored three functional hypothesis of duetting: mate reunion, pair reunion, and joint‐territorial defense. Pairs regularly engaged in duet calling. Duetting increased significantly during the offspring care period. Duetting occurred significantly more often at feeding sites than at sleeping sites. Pair partners synchronized behavioral activities after duetting. The activity most often synchronized was locomotion. Pair partners played an equal role in duetting with no difference between sexes in starting or terminating duetting. Altogether, our results provide support for the hypothesis that in dispersed pair‐living primates, duetting evolved as a mechanism to coordinate activities between pair partners dispersed in space, to strengthen pair bonds, and, perhaps, to limit infanticide and nutritional stress in lactating females. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Avoiding predators at night: antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus)

Although about one-third of all primate species are nocturnal, their antipredator behavior has rarely been studied directly. Crypsis and a solitary lifestyle have traditionally been considered to be the main adaptive antipredator strategies of nocturnal primates. However, a number of recent studies have revealed that nocturnal primates are not as cryptic and solitary as previously suggested. Thus, the antipredator strategies available for diurnal primates that rely on early detection and warning of approaching predators may also be available to nocturnal species. In order to shed additional light on the antipredator strategies of nocturnal primates, I studied pair-living red-tailed sportive lemurs (Lepilemur ruficaudatus) in Western Madagascar. In an experimental field study I exposed adult sportive lemurs that lived in pairs and had offspring to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own mobbing calls (barks) given in response to disturbances at their tree holes. I documented the subjects' immediate behavioral responses, including alarm calls, during the first minute following a playback. The sportive lemurs did not give alarm calls in response to predator call playbacks or to playbacks with barks. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two classes of predators, suggesting that the corresponding vocalizations were correctly categorized. In response to barks, they scanned the ground and fled. Because barks do not indicate any specific threats, they are presumably general alarm calls. Thus, sportive lemurs do not rely on early warning of acoustically simulated predators; rather, they show adaptive escape strategies and use general alarm calls that are primarily directed toward the predator but may also serve to warn kin and pair-partners.     

Social influences on foraging behaviour of the Red-cheeked Cordon Bleu Uraeginthus bengalus Estrildidae

Red-cheeked Cordon Bleus U. bengalus forage on bare patches of ground for fallen grass seeds and termites in particular home ranges. Foraging is confined to shaded areas in the middle parts of the day but birds exploit places exposed to the full sun in the early mornings and late afternoons. They mostly occur in pairs but often aggregate to form temporary foraging groups. Although birds in groups spend less time vigilant than those foraging alone, they react sooner than them to approaching danger. Birds foraging in pairs peck more rapidly than those in other situations and it is suggested that one advantage of forming permanent pair bonds is that paired birds forage more efficiently than unpaired ones in preparation for the coming breeding season. Flight calls, contact calls and alarm calls are given in specific behavioural contexts. Birds make contact calls when they become separated from their mates and evidently use them to re-locate one another. It is shown experimentally that members of pairs can recognize one another's contact calls.     

Possible audience effect in Thomas langurs (Primates; Presbytis thomasi): an experimental study on male loud calls in response to a tiger model

Recent research indicates that animal vocalizations can refer to objects in the outside world, and that call production may be controlled by the sender depending on the type of audience involved. Our research on wild male Thomas langurs (Primates: Presbytis thomasi) shows that these males call as a response to a tiger model when they are in a group, but do not call when they are solitary. This is the first experimental study on wild primates to demonstrate that the presence or absence of an audience influences calling behavior. Our results indicate that males in mixed-sex groups give more loud calls than solitary males when exposed to a predator model. This suggests that giving loud calls in response to predators is not purely a reflex and may be controlled in some way by the sender.     

Ranging Behavior and Possible Correlates of Pair-Living in Southeastern Avahis (Madagascar)

Researchers have proposed several hypotheses to explain pair-living in primates. In particular, when males are not involved in direct parental care, pair-living may be related to female dispersal, infanticide prevention, or male mate/resource defense. We aimed to evaluate, through a better understanding of the ranging patterns of avahis, which hypotheses may best account for pair-living in these nocturnal lemurs. We collected focal observations over 26 nights, June–September 2004, in a littoral forest (Sainte Luce, southeastern Madagascar) on 4 adult radiocollared avahis [Avahi laniger (Tattersall, I. (1982). The Primates of Madagascar. Columbia University Press, New York.) or Avahi meridionalis (Zaramody in Primate Reports 74:9–22, 2006)]. We followed 2 males and 2 females from 2 groups: B, a male-female couple, and A, comprising the parental pair and 1-yr-old female offspring. The adult females birthed in August. We recorded resting and feeding tree points (via global positioning system) for home range calculation through minimum convex polygon and kernel methods. We provide the first quantitative information on the ranging behavior of 2 male and 2 female avahis. Home range/daily path length values (means) are higher than the ones previously reported for the same and other folivorous pair-living lemur species. On average, the 2 females spent more time feeding and traveled shorter distances than the 2 males did. Male–female cohesion (mean values), possibly enhanced by offspring presence, was higher in A and after births than in B and before births, respectively. Although male avahis may be forced into pair-living owing to energy constraints related to size, locomotion, and diet, females might accept pair-living in exchange for indirect territory defense and mate guarding.     

Loud calls of male Nilgiri langurs (Presbytis johnii): Age-, individual-, and population-specific differences

Adult male Nilgiri langurs (Presbytis johnii) utter loud call bouts consisting of one or more phrases. Phrases are made up of several units showing similar or different structural features. The units involved differ with respect to not only their physical structure but also their overall utilization: three vocal patterns are uttered exclusively by mature males living in bisexual groups or all-male bands and, in addition to being part of loud call bouts, are given during encounters with terrestrial predators; two vocal patterns are uttered by males and females, again not just as constituents of loud calls; and one vocal pattern is given exclusively by mature males living in bisexual groups. Within a given bout, phrases differ not only with respect to their composition but also in their temporal organization. In addition to the acoustic components, loud calls are regularly accompanied by stereotyped motoric displays. The motoric and acoustic components of loud call displays appear independently of each other and at different times during ontogeny. The development of the display is characterized by combination of units with different structural features and synchronization of vocal and motoric components. Although more evidence is needed, our observations suggest that the development of loud call displays coincides with the aquisitation of social maturation and competence and requires not only social experience but also a certain amount of motoric training. In spite of the high degree of ritualization, loud call displays are not completely fixed in form, but instead are open to individual- and population-specific variation.     

Use of male blue monkey “Pyow” calls for long-term individual identification

This study examines whether individual adult male blue monkeys (Cercopithecus mitis stuhlmanni) can be identified through acoustic analysis of their “pyow” calls. It is possible to reliably assign the pyow call of the blue monkeys of Kibale Forest, Uganda, to the individual caller based on the acoustic properties of the vocalization. Analysis of pyows made by a recognizable male over a 10-yr period shows that the acoustic properties of one individual's pyow call can remain relatively constant over time. Acoustic analysis of pyow calls may provide a relatively easy and reliable method to document tenure lengths of adult male blue monkeys resident in groups. Similar analyses of the loud calls of other species of primates may, likewise, prove to be useful in documenting long-term membership. © 1992 Wiley-Liss, Inc.     

Do Females Turn Males on and off in Barnacle Goose Social Display?

Male barnacle goose Branta leucopsis display duration is longest when females respond with loud repetitious calls, intermediate when females follow silently and shortest when females call softly. We argue that these encouraging and discouraging vocalizations and the associated posturing is an influential behaviour used during the mate choice, pair maintenance and aggressive interaction processes.     

Geographic variation in loud calls of sportive lemurs (Lepilemur ssp.) and their implications for conservation

Bioacoustical studies in nonhuman primates have shown that loud calls can be reliably used as a noninvasive diagnostic tool for discriminating cryptic taxa, for their monitoring in the field as well as for the reconstruction of their phylogeny. To date, it is unknown, whether loud calls can be used for these purposes in sportive lemurs, for which current genetic studies suggest the existence of at least 24 cryptic species. The aim of this study was to compare the structure of loud calls of populations of sportive lemurs to characterize informative acoustic traits for taxa discrimination and to establish a phylogenetic tree based on acoustic structure. We have based our study on Inter-River-Systems (IRSs) as operational taxonomic units. Samples were collected from nine different localities of four IRSs along a transect from northwestern to northern Madagascar. Two call types, the ouah and the high-pitched call, were present in almost all IRSs. Six temporal and eight spectral parameters were measured in 196 calls of the best quality given by 21 different males. Variation within and between IRSs was assessed by multivariate statistics. Loud calls differed significantly among the different IRSs. The IRSs varied most in spectral parameters, whereas temporal parameters were less variable. Phylogenetic analysis using parsimony yielded 11 out of 17 acoustic characters as phylogenetically informative. The acoustic tree had an average branch support of 78%. Its topology coincided less with geographic distances than with genetic tree topology. Altogether our findings revealed that loud calls separated geographically isolated populations of sportive lemurs specifically. Based on these results, noninvasive tools for diagnosis and monitoring of cryptic species in nature can be developed for conservation management.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Responses to Playback of Local vs. Distant Contact Calls in the Orange-Fronted Conure, Aratinga canicularis

We conducted interactive playback experiments on foraging flocks of orange‐fronted conures, Aratinga canicularis, using loud contact calls that had been recorded at sites ranging from 0 to 30 km from the playback site. Responses were scored on the basis of the proximity of approach to the speaker, the number of different vocalizations produced by the responding flock, and the duration of respondent vocal interactions with the playbacks. Overall response strength decreased significantly as distance between playback and recording sites was increased up to 9 km, and remained at a steady low level for greater distances. As 9 km is the upper limit of conure home ranges measured in this study site, this nonlinear effect of response with distance suggests that response strength is partly determined by familiarity with calls of local birds. An additional and independent amount of the variation in response strength was explained by the structural similarity between respondent and stimulus calls. This correlation could be caused by a preference to interact with known stimulus birds whose calls have converged during prior associations. However, our data suggest that responding birds subtly changed their call structure during longer trials to more closely match the stimulus call. If subsequently verified as a common phenomenon, this finding could provide an important explanation for the remarkable imitative abilities of parrots.     

Pair-specific usage of sleeping sites and their implications for social organization in a nocturnal Malagasy primate, the Milne Edwards' sportive lemur (Lepilemur edwardsi)

Safe sleeping sites may be a limited resource crucial for survival. In order to investigate their potential significance for social organization in nocturnal primates, we analyzed the spatial distribution of daily sleeping sites, their characteristics, their usage, and sleeping group compositions in the nocturnal Milne Edwards' sportive lemur during a 6-month field study in the dry deciduous forest of northwestern Madagascar. Sexes did not differ either in body size or in body mass. Sleeping sites were used almost exclusively by adult male-female pairs. Individuals showed a high sleeping-site fidelity limited to 2-3 different sleeping sites in close vicinity during the whole study period. Most females showed a higher fidelity to one distinct sleeping site than their male partners. Sleeping groups consisted of one adult male and one adult female and remained stable in composition over the whole study period. Exclusive pair-specific usage of sleeping sites suggests sleeping site related territoriality of male-female pairs, perhaps influenced by inter- and intrasexual resource competition. Results give first insights into the distribution patterns and social organization of this species. They imply dispersed monogamy for the Milne Edwards' sportive lemur, with sleeping sites as a potentially restricted and defendable resource.     

Assortative Pairing Based on Contact Call Similarity in Budgerigars, Melopsittacus undulatus

A trait typical of parrots, but rare in other groups of birds, is the acquisition of new learned calls (acquired by copying conspecifics) throughout an individual's lifetime. The significance of this distinctive psittacid trait is not understood. In budgerigars, females preferentially affiliate with unfamiliar males whose contact calls resemble their own during brief dyadic choice trials; also, in forced‐pair situations, contact call similarity of members of pairs increases as a result of a male tendency to imitate his mate's call type. The functions of budgerigar call imitation and preference for pre‐pairing similarity are currently unknown. Moreover, as budgerigar pair formation occurs over a span of days or weeks, it is important to determine whether birds in breeding colonies assort and proceed to breed on the basis of pre‐pairing contact call similarity, and whether high levels of call similarity are maintained after pair formation is complete. To explore these questions, we recorded contact calls of male and female budgerigars before and after they were placed into an aviary equipped for breeding. As predicted, birds paired assortatively based on pre‐pairing call similarity. Once birds had paired, their calls converged further in acoustic structure, as previous work had led us to expect. However, after eggs were laid and the males began to feed their mates, the calls of mated birds diverged, suggesting that there might be some cost to maintenance of shared calls. Male care‐giving correlated with the degree to which his pre‐pairing calls resembled those of his mate, but not with the similarity achieved through convergence. These results suggest that female budgerigars may use a male's pre‐pairing call similarity as a predictor of paternal investment. The questions of why such similarity predicts male care‐giving, and why calls converge following initial pairing activities, require further work.     

Life-Phase Related Changes in Male Loud Call Characteristics and Testosterone Levels in Wild Thomas Langurs

Males in many primate species give loud calls. Lifetime changes in loud calls may be due to either age or social changes. We examined loud call characteristics, loud call production and levels of fecal testosterone among 4 life-phases of male Thomas langurs (Presbytis thomasi): all-male band (AMB), early, middle, and late life-phase in mixed-sex groups. Discriminant analyses showed that a high percentage of loud calls could be assigned correctly to the proper life-phase. The most significant change in loud call characteristics is an increase in tonal units and duration from the AMB to the early life-phase, accompanied by a decrease in non-tonal units. Since adult AMB males have a similar age to that of early life-phase males, we suggest that social rather than age-related changes underlie the loud call differences between AMB males and early life-phase males. This could also be related to the increase in testosterone levels from the AMB to the early life-phase. In addition, we postulate that females may use loud call characteristics as a cue to choose between young and old males once they decided to leave their current male, and possibly also as a cue to decide to leave their current male as he enters his late life-phase.