Measuring personality in the field: An in situ comparison of personality quantification methods in wild Barbary macaques (Macaca sylvanus).

Three popular approaches exist for quantifying personality in animals: behavioral coding in unconstrained and experimental settings and trait assessment. Both behavioral coding in an unconstrained setting and trait assessment aim to identify an overview of personality structure by reducing the behavioral repertoire of a species into broad personality dimensions, whereas experimental assays quantify personality as reactive tendencies to particular stimuli. Criticisms of these methods include that they generate personality dimensions with low levels of cross-study or cross-species comparability (behavioral coding in unconstrained and experimental settings) or that the personality dimensions generated are not ecologically valid, that is, not reflecting naturally occurring behavior (trait assessment and experimental assays). Which method is best for comparative research is currently debated, and there is presently a paucity of personality research conducted in wild subjects. In our study, all three described methods are used to quantify personality in a wild animal subject, the Barbary macaque (Macaca sylvanus). Our results show that the structures generated by unconstrained behavioral coding and trait assessment were not equivalent. Personality dimensions derived from both trait assessments and experimental assays demonstrated low levels of ecological validity, with very limited correlation with behaviors observed in nonmanipulated circumstances. Our results reflect the methodological differences between these quantification methods. Based on these findings and the practical considerations of wild animal research, we suggest future comparative studies of quantification methods within similar methodological frameworks to best identify methods viable for future comparisons of personality structures in wild animals. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

A protocol for training group-housed rhesus macaques (Macaca mulatta) to cooperate with husbandry and research procedures using positive reinforcement.

There has been increased recognition of the 3Rs in laboratory animal management over the last decade, including improvements in animal handling and housing. For example, positive reinforcement is now more widely used to encourage primates to cooperate with husbandry procedures, and improved enclosure design allows housing in social groups with opportunity to escape and avoid other primates and humans. Both practices have become gold standards in captive primate care resulting in improved health and behavioural outcomes. However, training individuals and social housing may be perceived as incompatible, and so it is important to share protocols, their outcomes and suggestions for planning and improvements for future uptake. Here we present a protocol with link to video for training rhesus macaques (Macaca mulatta) housed in single-male - multi-female breeding groups to sit at individual stations in the social enclosure. Our aim was that the monkeys could take part in welfare-related cognitive assessments without the need for removal from the group or interference by group members. To do this we required most individuals in a group to sit by individual stations at the same time. Most of the training was conducted by a single trainer with occasional assistance from a second trainer depending on availability. We successfully trained 61/65 monkeys housed in groups of up to nine adults (plus infants and juveniles) to sit by their individual stationing tools for >30 s. Males successfully trained on average within 30 min (2 training sessions); females trained on average in 1 h 52 min ± 13min (7.44 sessions), with rank (high, mid, low) affecting the number of sessions required. On average, dominant females trained in 1 h 26 min ± 16 min (5.7 sessions), mid ranked females in 1 h 52 min ± 20min (7.45 sessions), and subordinate females took 2 h 44 min ± 36 min (10.9 sessions). Age, group size, reproductive status, temperament, and early maternal separation did not influence the number of sessions a monkey required to reach criterion. We hope this protocol will be useful for facilities worldwide looking to house their animals in naturalistic social groups without impacting on animal husbandry and management.

Implications of Tourist-Macaque Interactions for Disease Transmission.

During wildlife tourism, proximity or actual contact between people and animals may lead to a significant risk of anthropozoonotic disease transmission. In this paper, we use social network analysis, disease simulation modelling and data on animal health and behaviour to investigate such risks at a site in Morocco, where tourists come to see wild Barbary macaques (Macaca sylvanus). Measures of individual macaques' network centrality-an index of the strength and distribution of their social relationships and thus potentially their ability to spread disease-did not show clear and consistent relationships with their time spent in close proximity to, or rate of interacting with, tourists. Disease simulation modelling indicated that while higher-ranked animals had a significantly greater ability to spread disease within the group, in absolute terms there was little difference in the size of outbreaks that different individuals were predicted to cause. We observed a high rate of physical contact and close proximity between humans and macaques, including during three periods when the macaques were coughing and sneezing heavily, highlighting the potential risk of disease transmission. We recommend that general disease prevention strategies, such as those aimed at reducing opportunities for contact between tourists and macaques, should be adopted.

Correlates of androgens in wild male Barbary macaques: Testing the challenge hypothesis.

Investigating causes and consequences of variation in hormonal expression is a key focus in behavioral ecology. Many studies have explored patterns of secretion of the androgen testosterone in male vertebrates, using the challenge hypothesis (Wingfield, Hegner, Dufty, & Ball, 1990; The American Naturalist, 136(6), 829-846) as a theoretical framework. Rather than the classic association of testosterone with male sexual behavior, this hypothesis predicts that high levels of testosterone are associated with male-male reproductive competition but also inhibit paternal care. The hypothesis was originally developed for birds, and subsequently tested in other vertebrate taxa, including primates. Such studies have explored the link between testosterone and reproductive aggression as well as other measures of mating competition, or between testosterone and aspects of male behavior related to the presence of infants. Very few studies have simultaneously investigated the links between testosterone and male aggression, other aspects of mating competition and infant-related behavior. We tested predictions derived from the challenge hypothesis in wild male Barbary macaques (Macaca sylvanus), a species with marked breeding seasonality and high levels of male-infant affiliation, providing a powerful test of this theoretical framework. Over 11 months, 251 hr of behavioral observations and 296 fecal samples were collected from seven adult males in the Middle Atlas Mountains, Morocco. Fecal androgen levels rose before the onset of the mating season, during a period of rank instability, and were positively related to group mating activity across the mating season. Androgen levels were unrelated to rates of male-male aggression in any period, but higher ranked males had higher levels in both the mating season and in the period of rank instability. Lower androgen levels were associated with increased rates of male-infant grooming during the mating and unstable periods. Our results generally support the challenge hypothesis and highlight the importance of considering individual species' behavioral ecology when testing this framework.

Primates' behavioural responses to tourists: evidence for a trade-off between potential risks and benefits.

The presence of, and interactions with tourists can be both risky and beneficial for wild animals. In wildlife tourism settings, animals often experience elevated rates of aggression from conspecifics, and they may also be threatened or physically aggressed by the tourists themselves. However, tourist provisioning of wild animals provides them with highly desirable foods. In situations of conflicting motivations such as this, animals would be expected to respond using behavioural coping mechanisms. In the present study, we investigated how animals respond to tourist pressure, using wild adult Barbary macaques in the Middle Atlas Mountains, Morocco, as a case study. We found evidence that these animals use a range of different behavioural coping mechanisms-physical avoidance, social support, affiliative, aggressive and displacement behaviours-to cope with the stress associated with tourists. The pattern of use of such behaviours appears to depend on a trade-off between perceived risks and potential benefits. We propose a framework to describe how animals respond to conflicting motivational situations, such as the presence of tourists, that present simultaneously risks and benefits.

Assessing the Effects of Tourist Provisioning on the Health of Wild Barbary Macaques in Morocco.

Feeding wildlife is a very popular tourist activity, largely because it facilitates the close observation of animals in their natural habitat. Such provisioning may benefit animals by improving their survival and reproductive success, especially during periods of natural food shortage. However, provisioning by tourists may also have negative impacts on the health of the animals involved; to date such impacts are poorly understood. Here, we investigated the effects of tourist provisioning on the health of wild adult Barbary macaques, Macaca sylvanus, in Morocco. We compared health measures between a heavily provisioned group and a group that received negligible food from tourists and, in the former group, we also assessed health measures in relation to the intensity of provisioning. We used a broad range of non-invasive health measures relating to birth rate and survival, disease and injury risk, body size and condition, and physiological stress. Our findings indicate that feeding by tourists may overall have negative impacts on the health of Barbary macaques, being linked in particular to larger body size, elevated stress levels and more alopecia. Finally, we propose a framework to help consider the potential costs and benefits of provisioning, which may facilitate future research and management decisions on whether-and how much-provisioning is acceptable.

Foraging with finesse: A hard-fruit-eating primate selects the weakest areas as bite sites.

OBJECTIVES: Fruit husks are rarely uniformly hard, varying in penetrability via sulci and changes in thickness. We tested whether a hard-food specialist primate i) bites randomly on food fruit husk surfaces to access seeds, or ii) selects areas most easily penetrated by canines. We consider this would occur so as to minimize deployed mechanical force, energetic expenditure and risk of dental breakage when feeding. METHODS: A sulcus is the natural line of weakness where a dehiscent fruit breaks open. Using fruits dentally opened for seeds by golden-back uacaris (Cacajao ouakary) we: 1) analysed bite mark distribution on surface of four fruits types (hard-with-sulcus, soft-with-sulcus, hard-no-sulcus, soft-no-sulcus); 2) quantified the force needed to penetrate hard and soft fruits at sulci and elsewhere on fruit surface; 3) measured fruit wall thickness and correlated it with bite-mark distribution in all four categories of fruit. RESULTS: 1) Bite marks were distributed at random only on surfaces of soft fruits. For other fruits types, bite locations were concentrated at the thinnest areas of husk, either over the entire surface (non-sulcate fruits), or at sulci (sulcate fruits). 2) For hard-husked fruits, areas where uacaris concentrated their bites were significantly easier to penetrate than those where they did not. CONCLUSIONS: This hard-fruit feeding specialist primate is not biting at random on the surface of diet fruits. To access seeds they are focusing on those areas requiring less force to penetrate. This may be to save energy, to minimize the risk of breaking teeth used in food processing, or a combination of both. The study shows, for the first time, the subtlety by which these powerfully-jawed animals process their diet items.

Metabolic strategies in wild male Barbary macaques: evidence from faecal measurement of thyroid hormone.

Selection is expected to favour the evolution of flexible metabolic strategies, in response to environmental conditions. Here, we use a non-invasive index of basal metabolic rate (BMR), faecal thyroid hormone (T3) levels, to explore metabolic flexibility in a wild mammal inhabiting a highly seasonal, challenging environment. T3 levels of adult male Barbary macaques in the Atlas Mountains, Morocco, varied markedly over the year; temporal patterns of variation differed between a wild-feeding and a provisioned group. Overall, T3 levels were related to temperature, foraging time (linked to food availability) and intensity of mating activity, and were higher in the provisioned than in the wild-feeding group. In both groups, T3 levels began to increase markedly one month before the start of the mating season, peaking four to six weeks into this period, and at a higher level in the wild-feeding group. Our results suggest that while both groups demonstrate marked metabolic flexibility, responding similarly to ecological and social challenges, such flexibility is affected by food availability. This study provides new insights into the way Barbary macaques respond to the multiple demands of their environment.

Emotion Evaluation and Response Slowing in a Non-Human Primate: New Directions for Cognitive Bias Measures of Animal Emotion?

The cognitive bias model of animal welfare assessment is informed by studies with humans demonstrating that the interaction between emotion and cognition can be detected using laboratory tasks. A limitation of cognitive bias tasks is the amount of training required by animals prior to testing. A potential solution is to use biologically relevant stimuli that trigger innate emotional responses. Here; we develop a new method to assess emotion in rhesus macaques; informed by paradigms used with humans: emotional Stroop; visual cueing and; in particular; response slowing. In humans; performance on a simple cognitive task can become impaired when emotional distractor content is displayed. Importantly; responses become slower in anxious individuals in the presence of mild threat; a pattern not seen in non-anxious individuals; who are able to effectively process and disengage from the distractor. Here; we present a proof-of-concept study; demonstrating that rhesus macaques show slowing of responses in a simple touch-screen task when emotional content is introduced; but only when they had recently experienced a presumably stressful veterinary inspection. Our results indicate the presence of a subtle "cognitive freeze" response; the measurement of which may provide a means of identifying negative shifts in emotion in animals.

Associations between spatial position, stress and anxiety in forest baboons Papio anubis.

Spatial position within a group affects the value of group-living benefits such as reduced predation risk and improved foraging. The threat of predation, poor nutrition or increased competition from conspecifics can all cause stress. In many species, central positions are known to be more beneficial than peripheral positions in terms of reduced predation, vigilance and foraging. In this study, we examine whether spatial position within a group is associated with stress and anxiety in a troop of olive baboons (Papio anubis). We predicted that the benefits of occupying central positions would be reflected by a reduction in stress and anxiety for animals who spent the most time in the centre of the group. The study subjects appeared to compete actively for the centre of the group. Physiological stress measures (faecal glucocorticoid concentrations) were positively correlated with time spent in central positions. Time spent in central positions was positively correlated with proximity but negatively correlated with vigilance behaviours (alarm barks). Vigilance rates were positively correlated with measures of anxiety (self-scratch frequency). It is suggested that individuals experience chronic stress due to proximity to conspecifics in central positions, whilst perceived predation risk causes anxiety, with perceived predation risk experienced more by individuals on the periphery.

Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output.

There is growing evidence that behavioral tendencies, or "personalities," in animals are an important aspect of their biology, yet their evolutionary basis is poorly understood. Specifically, how individual variation in personality arises and is subsequently maintained by selection remains unclear. To address this gap, studies of personality require explicit incorporation of genetic information. Here, we explored the genetic basis of personality in rhesus macaques by determining the heritability of personality components and by examining the fitness consequences of those components. We collected observational data for 108 adult females living in three social groups in a free-ranging population via focal animal sampling. We applied principal component analysis to nine spontaneously occurring behaviors and identified six putative personality components, which we named Meek, Bold, Aggressive, Passive, Loner, and Nervous. All components were repeatable and heritable, with heritability estimates ranging from 0.14 to 0.35. We found no evidence of an association with reproductive output, measured either by infant survival or by interbirth interval, for any of the personality components. This finding suggests either that personality does not have fitness-related consequences in this population or that selection has acted to reduce fitness-associated variation in personality.

Seasonal changes in the structure of rhesus macaque social networks.

Social structure emerges from the patterning of interactions between individuals and plays a critical role in shaping some of the main characteristics of animal populations. The topological features of social structure, such as the extent to which individuals interact in clusters, can influence many biologically important factors, including the persistence of cooperation, and the rate of spread of disease. Yet the extent to which social structure topology fluctuates over relatively short periods of time in relation to social, demographic or environmental events remains unclear. Here, we use social network analysis to examine seasonal changes in the topology of social structures that emerge from socio-positive associations in adult female rhesus macaques (Macaca mulatta). Behavioral data for two different association types (grooming, spatial proximity) were collected for females in two free-ranging groups during two seasons: the mating and birth seasons. Stronger dyadic bonds resulted in social structures that were more tightly connected (i.e. of greater density) in the mating season compared to the birth season. Social structures were also more centralized around a subset of individuals, and were more clustered in the mating season than the birth season, although the latter differences were mostly driven by differences in density alone. Our results suggest a degree of temporal variation in the topological features of social structure in this population. Such variation may feed back on interactions, hence affecting the behaviors of individuals, and may therefore be important to take into account in studies of animal behavior.

Terrestrial foraging by Cacajao melanocephalus ouakary (primates) in Amazonian Brazil: is choice of seed patch size and position related to predation risk?

We analyse the behaviour of Cacajao melanocephalus ouakary feeding at patches of germinating seedlings in dried-out flooded forest. Seedlings of Eschweilera tenuifolia (Lecythidaceae) were the most commonly eaten (88.9%). Some seed patches were revisited over several days, while others were consistently ignored. We tested 3 predictions relating uacari terrestrial foraging behaviour to: (1) arboreal escape route proximity, (2) seed patch size choice and (3) temporal patterns of repeat exploitation. Comparison of fed-at and ignored patches revealed significant preferences for larger patches, and for those close to arboreal refuges but distant from dense ground-based vegetation. Support for these predictions is interpreted as evidence for predation risk-sensitive foraging.

Evidence that emotion mediates social attention in rhesus macaques.

BACKGROUND: Recent work on non-human primates indicates that the allocation of social attention is mediated by characteristics of the attending animal, such as social status and genotype, as well as by the value of the target to which attention is directed. Studies of humans indicate that an individual's emotion state also plays a crucial role in mediating their social attention; for example, individuals look for longer towards aggressive faces when they are feeling more anxious, and this bias leads to increased negative arousal and distraction from other ongoing tasks. To our knowledge, no studies have tested for an effect of emotion state on allocation of social attention in any non-human species. METHODOLOGY: We presented captive adult male rhesus macaques with pairs of adult male conspecific face images - one with an aggressive expression, one with a neutral expression - and recorded gaze towards these images. Each animal was tested twice, once during a putatively stressful condition (i.e. following a veterinary health check), and once during a neutral (or potentially positive) condition (i.e. a period of environmental enrichment). Initial analyses revealed that behavioural indicators of anxiety and stress were significantly higher after the health check than during enrichment, indicating that the former caused a negative shift in emotional state. PRINCIPLE FINDINGS: The macaques showed initial vigilance for aggressive faces across both conditions, but subsequent responses differed between conditions. Following the health check, initial vigilance was followed by rapid and sustained avoidance of aggressive faces. By contrast, during the period of enrichment, the macaques showed sustained attention towards the same aggressive faces. CONCLUSIONS/SIGNIFICANCE: These data provide, to our knowledge, the first evidence that shifts in emotion state mediate social attention towards and away from facial cues of emotion in a non-human animal. This work provides novel insights into the evolution of emotion-attention interactions in humans, and mechanisms of social behaviour in non-human primates, and may have important implications for understanding animal psychological wellbeing.

Terrestrial activity in pitheciins (Cacajao, Chiropotes, and Pithecia).

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a "local pattern" of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types.

An experimental study of behavioural coping strategies in free-ranging female Barbary macaques (Macaca sylvanus).

A fundamental goal of stress research is to understand how individuals cope with challenges. Studies on a range of vertebrate species suggest that three groups of behaviour--affiliative, aggressive and self-directed behaviours--serve as coping strategies. To date, experimental studies of coping behaviour have tended to be conducted in captive conditions; the limited number of studies in free-ranging or wild settings have been observational in nature. We investigated coping behaviours in free-ranging female Barbary macaques (Macaca sylvanus) at Trentham Monkey Forest, UK, using an experimental playback approach to quantify subjects' responses to mildly aversive threat-grunts. Compared to silent control trials, playbacks of threat-grunts increased aggressive behaviours and one of the two self-directed behaviours examined (self-scratching). No such differences were seen for self-grooming, or for any affiliative behaviour. Elevations in the rate of one measure of aggression, lunging, were positively related to an average measure of adrenocortical activity (median faecal glucocorticoid metabolite levels over the study period). Evidence from females in a variety of Old World monkey species, including Barbary macaques, indicates that affiliative behaviours have an important role in coping with stressful events in the medium to longer term. Our results suggest that, in the short term, female Barbary macaques may use aggressive rather than affiliative behaviours in response to mild stress. These findings highlight the importance of considering how coping mechanisms may vary over time after a stressor, and how coping mechanisms relate to adrenocortical activity. Playback approaches like ours provide a powerful, flexible tool to explore issues such as this in free-ranging and wild animal populations.

Sleeping site selection by golden-backed uacaris, Cacajao melanocephalus ouakary (Pitheciidae), in Amazonian flooded forests.

In Amazonian seasonally flooded forest (igapó), golden-backed uacaris, Cacajao melanocephalus ouakary, show high selectivity for sleeping trees. Of 89 tree species in igapó, only 16 were used for sleeping (18%). Hydrochorea marginata (Fabaceae) and Ormosia paraensis (Fabaceae) were used most frequently (41% of records) despite being uncommon (Ivlev electivity ratios were 0.76, and 0.84, respectively), though the third most commonly used species (11%), Amanoa oblongifolia (Euphorbiaceae), was selected at near parity. All three species have broad, open canopies with large horizontal limbs and uncluttered interiors. Compared with random trees, sleeping trees had above average diameter at breast height (DBH) and height, lacked lianas and wasp nests, and were more frequently within 5 m of open water. Uacaris generally slept one adult per tree or widely separated in the same canopy and on the outer third of the branch. These behaviours are interpreted as maximising detection of both aerial and arboreal predators.

Rates of self-directed behaviour and faecal glucocorticoid levels are not correlated in female wild olive baboons (Papio hamadryas anubis).

Non-invasive methods to quantify components of stress in non-human animals rely typically on the use of physiological or behavioural measures. At the physiological level, stress is usually measured non-invasively in terms of faecal or urinary glucocorticoid output. A common group of behavioural measures used are self-directed behaviours (SDBs), which have been shown to be linked to anxiety, a subset of stress, although a number of authors have explicitly linked SDBs to stress more generally. Whether increased rates of SDBs are likely to be associated with increased faecal glucocorticoid ouput in wild mammals remains unclear. Here, for wild female olive baboons, we show no association between day-to-day changes in levels of SDB and cortisol metabolite excretion. We also show no relationship between long-term mean levels of these variables. We discuss several possible interpretations of our results, including the possibility that SDBs represent a behavioural coping mechanism, helping to ameliorate the physiological stress response.

Living on the edge: life-history of olive baboons at Gashaka-Gumti National Park, Nigeria.

Baboons are the most successful and ubiquitous African primates, renowned for their behavioral and reproductive flexibility, which enable them to inhabit a wide variety of habitat types. Owing to a number of long-term field studies, comparative behavioral, developmental, demographic, and life-history data are available from several populations, but study sites show a heavy bias toward South and East African savannahs, with little research in West or Central Africa. Life-history data from such areas are important if we are fully to understand the nature of the environmental factors that limit baboon distribution. Here, we present demographic data for olive baboons at Gashaka-Gumti National Park (GGNP), Nigeria, collected from December 2000-February 2006, and use these data to test comparative models of baboon life-history. The GGNP habitat, which includes large areas of rainforest, is an environment in which baboons are little studied, and rainfall is much higher than at previous study sites. GGNP troop size data are presented from censuses, as well as life-history data for two troops, one of which is within the park and wild-feeding (Kwano troop), whereas the other dwells at the park edge, and supplements its diet by crop-raiding (Gamgam troop). Troop sizes at GGNP are small compared with other field sites, but fit within previously suggested ranges for baboons under these climatic conditions. Inter-birth intervals in Kwano troop were long compared with most studied populations, and values were not as predicted by comparative models. Consistent with known effects of food enhancement, Gamgam troop experienced shorter inter-birth intervals and lower infant mortality than Kwano troop. We indicate some possible factors that exclude baboons from true rainforest, and suggest that the clearing of forests in Central and West Africa for agricultural land may allow baboons to extend their range into regions from which they are currently excluded.

Female reproductive signaling, and male mating behavior, in the olive baboon.

Baboon sexual swellings are among the largest and most colorful signals displayed by any mammal, and many baboon studies have shown an association between sexual swellings and both female and male sexual behavior. However, the extent to which female behavior and sexual swellings combine to signal the timing of ovulation and the fertile period to males, and the extent to which males use these and other signals when determining patterns of mating behavior, remain key topics of research. Here we assess the social and sexual behavior of both female and male olive baboons with respect to detailed measures of swelling size made from digital photographs, measures of fecal progestogen and estrogen levels, and estimates of the timing of ovulation and the fertile period based on those levels. Female aggression and grooming behavior were unrelated to fecal progestogen and estrogen levels, but there were some significant relationships between these hormonal measures and presenting behaviors. Measures of female behavior collected during the study did not appear to reveal the timing of ovulation or the fertile period. Male consortship behavior was closely tied to fine-scale changes in sexual swelling size, but copulation behavior was not. Copulation behavior of consorting males was, however, linked to the timing of both ovulation and the fertile period, suggesting that males did have knowledge about these timings. Together these results suggest that males used fine-scale swelling size changes when deciding when to consort, but that consorting males did not use fine-scale swelling size changes in deciding when to copulate. We propose that swelling size may advertise the period during which males should consort with females, with other signals available only from closer inspection then used by consorting males to assess the timing of the fertile period more accurately. An important implication of this interpretation is that different males may have access to different signals of ovulation at any one time. Such a system would allow females to offer different males different information simultaneously, perhaps offering a solution to the 'female dilemma' of how females can simultaneously assure and confuse paternity in multi-male societies.