Aliza le Roux

Derived vocalizations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates

Primates are intensely social and exhibit extreme variation in social structure, making them particularly well suited for uncovering evolutionary connections between sociality and vocal complexity. Although comparative studies find a correlation between social and vocal complexity, the function of large vocal repertoires in more complex societies remains unclear. We compared the vocal complexity found in primates to both mammals in general and human language in particular and found that non-human primates are not unusual in the complexity of their vocal repertoires. To better understand the function of vocal complexity within primates, we compared two closely related primates (chacma baboons and geladas) that differ in their ecology and social structures. A key difference is that gelada males form long-term bonds with the 2–12 females in their harem-like reproductive unit, while chacma males primarily form temporary consortships with females. We identified homologous and non-homologous calls and related the use of the derived non-homologous calls to specific social situations. We found that the socially complex (but ecologically simple) geladas have larger vocal repertoires. Derived vocalizations of geladas were primarily used by leader males in affiliative interactions with ‘their’ females. The derived calls were frequently used following fights within the unit suggesting that maintaining cross-sex bonds within a reproductive unit contributed to this instance of evolved vocal complexity. Thus, our comparison highlights the utility of using closely related species to better understand the function of vocal complexity.

Female philopatry and dominance patterns in wild geladas

Cercopithecines have a highly conserved social structure with strong female bonds and stable, maternally inherited linear dominance hierarchies. This system has been ascribed to the pervasiveness of female philopatry within the typical multi‐male, multi‐female social groups. We examined the relationship between female philopatry, dominance hierarchies, and reproduction in geladas (Theropithecus gelada), a species with an unusual multi‐leveled society. During a 4‐year field study on a wild population in the Simien Mountains National Park, Ethiopia, we observed 14 units across two bands of geladas that underwent a number of events, such as male takeovers and female deaths, which could potentially disrupt female relationships and unit structure. First, we corroborate earlier reports that gelada females are natally philopatric: we observed no interunit migrations, and the female mortality rate was comparable to that of philopatric baboons (suggesting all female disappearances were indeed deaths). Second, contrary to previous reports, data from this long‐term study show that geladas exhibit the linear and stable dominance hierarchies typical of other Cercopithecines. Moreover, female ranks appear to be maternally inherited. Third, we found no evidence that alpha females aggressively target the lowest ranking individuals, nor did rank confer clear reproductive advantages to dominant females within our 4‐year observation period. As such, geladas fit the allostatic load model [Goymann & Wingfield, Animal Behaviour 67:591–602, 2004]. Our study confirms the importance of female philopatry in the kin‐based Cercopithecine dominance system. Am. J. Primatol. 73:422–430, 2011.

Indirect rival assessment in a social primate, Theropithecus gelada

Identifying the cognitive challenges of sociality can be difficult because similar social interactions may be based on very different cognitive mechanisms. To better understand the cognitive mechanisms associated with a particular interaction, we investigated the social information that gelada, Theropithecus gelada, bachelors use to assess rival males. Gelada bachelors may use a variety of assessment strategies, including attending to simple cues of immanent mating opportunities, vocal quality signals, and monitoring relationships between attached males and females. Our observational data indicate that bachelors preferentially eavesdrop on male–male fights (over copulations) and maintain close proximity to units that have experienced a recent take-over. As such units also experience elevated rates of fighting and extrapair copulations, bachelors appear to attend to cues of mating opportunities. Furthermore, bachelors monitor vocal contests between rival males, suggesting they are able to remember the quality displayed by competitors. Finally, we used playback experiments to simulate copulations between breeding males and ‘their’ females (control) or other females (test) and found no difference in bachelor response, suggesting a lack of knowledge about third-party relationships between males and females. In contrast to other social primates, gelada bachelors appear to use simpler information, such as outcomes of male–male competition, when assessing others. Given the size of gelada communities (>1000 individuals), the costs of monitoring third-party relationships may outweigh the benefits of obtaining this information, particularly when simpler rules of thumb are available.

The vocal repertoire in a solitary foraging carnivore, Cynictis penicillata , may reflect facultative sociality

We describe the vocal repertoire of a facultatively social carnivore, the yellow mongoose, Cynictis penicillata. Using a combination of close-range observations, recordings and experiments with simulated predators, we were able to obtain clear descriptions of call structure and function for a wide range of calls used by this herpestid. The vocal repertoire of the yellow mongooses comprised ten call types, half of which were used in appeasing or fearful contexts and half in aggressive interactions. Data from this study suggest that the yellow mongoose uses an urgency-based alarm calling system, indicating high and low urgency through two distinct call types. Compared to solitary mongooses, the yellow mongoose has a large proportion of ‘friendly’ vocalisations that enhance group cohesion, but its vocal repertoire is smaller and less context-specific than those of obligate social species. This study of the vocal repertoire of the yellow mongoose is, to our knowledge, the most complete to have been conducted on a facultatively social species in its natural habitat.

Vocal Complexity in Meerkats and Other Mongoose Species

Complex societies are suggested to generate complex communication. However, tests of this hypothesis rarely go beyond a superficial examination of social and communicative complexity. For a systematic approach, we first have to define what we mean by complexity. What defines social complexity, and what defines communicative complexity? What aspects of social complexity correlate with what aspects of communicative complexity? We reviewed the hypotheses put forward for the evolution of the diverse vocal communicative repertoires and variation within meerkats and four other mongoose species. The obligate group living species, meerkats, dwarf mongoose, and banded mongoose, in comparison to the solitary slender mongoose and the facultative social yellow mongoose show a wider variation in signal use. However, group size within the social mongoose species does not correlate to vocal repertoire size and is rather explained by differences in their social organization and also by the ecology of the species. For example, meerkats and dwarf mongoose seem to have evolved vocal systems based on many discrete call types, while banded mongoose show a more graded system with fewer call types, though the amount of information conveyed to receivers may be the same in both cases. The comparison of vocal complexity in the different mongoose species emphasizes the importance of identifying correlations of communicative variation with specific social contexts and taking the ecology of a species into account. Ultimately, the function of signals has to be considered from both the producer and receiver side, and in the natural habitat of a species, if we are ever to understand what explains the variation, complexity, as well as potential limitations in animal communication.

Vigilance behaviour and fitness consequences: comparing a solitary foraging and an obligate group-foraging mammal

Vigilance behaviour in gregarious species has been studied extensively, especially the relationship between individual vigilance and group size, which is often negative. Relatively little is known about the effect of conspecifics on vigilance in non-obligate social species or the influence of sociality itself on antipredator tactics. We investigated predator avoidance behaviour in the yellow mongoose, Cynictis penicillata, a group-living solitary forager, and compared it with a sympatric group-living, group-foraging herpestid, the meerkat, Suricata suricatta. In yellow mongooses, the presence of conspecifics during foraging—an infrequent occurrence—reduced their foraging time and success and increased individual vigilance, contrary to the classical group-size effect. Comparing the two herpestids, sociality did not appear to affect overt vigilance or survival rates but influenced general patterns of predator avoidance. Whereas meerkats relied on communal vigilance, costly vigilance postures, and auditory warnings against danger, yellow mongooses avoided predator detection by remaining close to safe refuges and increasing “low-cost” vigilance, which did not interfere with foraging. We suggest that foraging group size in herpestids is constrained by species-distinct vigilance patterns, in addition to habitat and prey preference.

Non-invasive measurement of adrenocortical activity in a myrmecophageous mammal, the bat-eared fox

Measuring physiological stress reactions through the quantification of plasma cortisol often involves physical restraint, which acts as a stressor itself. Here, we present the validation of a non-invasive method for assessing adrenocortical activity as an indicator of stress in the bat-eared fox (Otocyon megalotis). By conducting an adrenocorticotropic hormone (ACTH) challenge, we examined the suitability of three enzyme immunoassays (EIAs) detecting 11,17 dioxoandrostanes (11,17-DOA) as well as faecal glucocorticoid metabolites (fGCM) with a 5β-3α-ol-11-one (3α,11oxo-CM), or 11,17,21-trihydroxy-4-ene-20-one structure (cortisol), respectively, for monitoring stress-related physiological responses in male and female bat-eared foxes. Our results suggest that the cortisol EIA seems most suitable for measuring fGCMs in this myrmecophageous mammal. Using the cortisol EIA, we compared fGCM concentrations of three populations of foxes. Only one population experienced a sudden change in social environment and the assay appeared to effectively detect the expected resulting increase in stress hormone levels. Therefore, the identified EIA is effective at detecting intraspecific variation in fGCM levels and hence is a useful tool to evaluate physiological stress responses in this species.

Acoustic and Temporal Variation in Gelada ( Theropithecus gelada ) 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.

From killer to carer: steroid hormones and paternal behaviour

Mammalian parental investment (i.e. care of descendant offspring) is largely biased towards maternal contributions due to the specific feeding needs of mammalian offspring; however, varying degrees of paternal investment have been reported in about 10% of all mammalian species. Within the order Carnivora, paternal contribution to rearing offspring is particularly high: an estimated 32% of all studied carnivore species exhibit direct paternal care. Despite the prominence of paternal investment in carnivores, the endocrine basis of this behaviour is not well understood. This review examines the current — highly constrained — state of knowledge about the endocrine basis of carnivore paternal investment. We attempt to link changes in androgen and glucocorticoid levels with variation in direct and indirect paternal care behaviour making specific predictions regarding the way forward. Well-studied species, such as bat-eared foxes (Otocyon megalotis), dwarf mongoose (Helogale parvula) and meerkats (Suricata suricatta), where social dynamics are relatively well understood, can act as ideal model systems through which we may further investigate the endocrine basis of paternal investment in carnivores.

Testing the Value of Citizen Science for Roadkill Studies: A Case Study from South Africa

Roads impact wildlife through a range of mechanisms from habitat loss and decreased landscape connectivity to direct mortality through wildlife-vehicle collisions (roadkill). These collisions have been rated amongst the highest modern risks to wildlife. With the development of ‘citizen science’ projects, in which members of the public participate in data collection, it is now possible to monitor the impacts of roads over scales far beyond the limit of traditional studies. However, the reliability of data provided by citizen scientists for roadkill studies remains largely untested. This study used a dataset of 2 666 roadkill reports on national and regional roads in South Africa (total length ~170 000 km) over three years. We first compared roadkill data collected from trained road patrols operating on a major highway with data submitted by citizen scientists on the same road section (431 km). We found that despite minor differences, the broad spatial and taxonomic patterns were similar between trained reporters and untrained citizen scientists. We then compared data provided by two groups of citizen scientists across South Africa: 1) those working in the zoology/conservation sector (that we have termed ‘regular observers’, whose reports were considered to be more accurate due to their knowledge and experience), and 2) occasional observers, whose reports required verification by an expert. Again, there were few differences between the type of roadkill report provided by regular and occasional reporters; both types identified the same area (or cluster) where roadkill was reported most frequently. However, occasional observers tended to report charismatic and easily identifiable species more often than road patrols or regular observers. We conclude that citizen scientists can provide reliable data for roadkill studies when it comes to identifying general patterns and high-risk areas. Thus, citizen science has the potential to be a valuable tool for identifying potential roadkill hotspots and at-risk species across large spatial and temporal scales that are otherwise impractical and expensive when using standard data collection methodologies. This tool allows researchers to extract data and focus their efforts on potential areas and species of concern, with the ultimate goal of implementing effective roadkill-reduction measures.