Portrait of Dr Brandon Wheeler

Dr Brandon Wheeler

Lecturer in Biological Anthropology
Programme Convenor for BSc in Biological Anthropology and BSc in Anthropology
Deputy Director of Recruitment and Admissions (Biological Anthropology)

About

Dr Brandon Wheeler is a behavioural ecologist broadly interested in the costs and benefits associated with group-living among primates, especially in terms of predation risk, feeding competition and infanticide by males. More specifically, he is interested in the role of communication in moderating these costs and facilitating the benefits. Brandon conducts fieldwork on wild tufted capuchin monkeys in Iguazú National Park, Argentina. His work uses a largely experimental approach, combined with acoustic and hormonal analyses, to understand social behaviour from both ultimate (ie adaptive) and proximate (eg cognitive, emotional and physiological) levels.

Before arriving at Kent, Dr Wheeler received his BA from the University of Arkansas and PhD from Stony Brook University. Following that, he was a postdoc in the Cognitive Ethology Lab at the German Primate Centre. In addition to his work in Argentina, Brandon has conducted fieldwork with primates in Thailand, Costa Rica and Madagascar.

Research interests

Dr Brandon Wheeler is broadly interested in the behavioural ecology of non-human primates. His current work in Iguazú, Argentina aims to test whether capuchins acquire recognition of heterospecific alarm calls through associative and/or social learning. In addition, Brandon is working in collaboration with Dr Barbara Tiddi to investigate aspects of female sexual signalling and mate choice among capuchins. 

Beyond fieldwork, Dr Wheeler is using modelling and phylogenetic comparative analyses to test and refine socioecological models of primate evolution. Brandon's interest in predation on primates has also led him to work on side projects focused on understanding what, if anything, primate alarm calls can tell us about the evolution of human language, as well as understanding the role of predators on the evolution of the primate visual system.

Geographic areas of interest: Anywhere wild primates are found, especially Misiones, Argentina.  

Current research projects

Teaching

Undergraduate

  • SE557: Primate Communication (convenor)
  • SE605: Hormones and Behaviour (convenor)
  • SE302: Foundations of Biological Anthropology
  • SE307: Thinkers and Theories
  • SE308: Skills for Anthropology and Conservation
  • SE567: Quantitative Research Methods
  • SE580: Primate Behaviour and Ecology
  • SE533: Project in Anthropological Science

Postgraduate

  • SE992: Advanced Topics in Evolutionary Anthropology
  • SE993: Advanced Topics in Primate Behaviour 
  • SE855: Research Project (Evolution & Human Behaviour)

Supervision

Current PhD students

  • Juliette Berthier: The role of emotions in the communication of black crested macaques (Macaca nigra)
  • Caroline Howlett: Expression of the 2D:4D digit ratio across the Primate order
  • Adriana Lowe: Maternal strategies in wild Ugandan chimpanzees

Professional

Dr Wheeler has worked with the BBC for the Monkey Planet series and the World Service for segments on deceptive communication in capuchin monkeys. 

Brandon is able to provide commentary and discussion on topics related to capuchin monkeys, primatology, animal deception and animal communication.  

Publications

Article

  • Wheeler, B., Fahy, M. and Tiddi, B. (2019). Experimental Evidence for Heterospecific Alarm Signal Recognition via Associative Learning in Wild Capuchin Monkeys. Animal Cognition [Online]. Available at: https://doi.org/10.1007/s10071-019-01264-3.
    Many vertebrate taxa respond to heterospecific alarm calls with anti-predator behaviours. While it is unclear how apparent recognition is achieved, learned associations between the occurrence of the call and the presence of a predator are considered the most likely explanation. Conclusive evidence that this behaviour is indeed underpinned by learning, however, is scarce. This study tested whether wild black capuchin monkeys (Sapajus nigritus) learn to associate novel sounds with predators through a two-phase field experiment. During an initial training phase, three study groups were each presented with a playback of one of the three novel sounds together with a simulated felid predator on four occasions over an 8- to 12-week period. This was followed by a test phase, wherein each of the three sounds was played back to individuals in all three groups, allowing each sound to serve as both a test stimulus for individuals trained with that sound, and a control stimulus for individuals trained with another sound. Antipredator responses were significantly stronger in response to test sounds than to controls. Limited observations suggest that antipredator responses persisted for at least 2 years without reinforcement of the predator–sound link. Additionally, responses to noisier sounds were typically stronger than were those to more tonal sounds, although the effect of sound type cannot be disentangled from potential effects of group. This study provides the strongest evidence to date that learning affects the responses of primates to sounds such as heterospecific alarm calls, and supports the contention that signals provide receivers with information.
  • Bernaldo de Quirós, E. et al. (2018). Do sexual calls in female black capuchin monkeys (Sapajus nigritus) vary with fertility? An acoustic analysis. American Journal of Primatology [Online] 80:e22920. Available at: https://doi.org/10.1002/ajp.22920.
    Females across a range of animal taxa produce vocalizations and signals uniquely associated with periods of mating. While such signals may ultimately function to increase female attractivity to males, conflicting findings challenge the extent to which these signals co-vary in accordance with the probability of conception. Female black capuchin monkeys (Sapajus nigritus) display an elaborate repertoire of both vocal and visual components as part of their socio-sexual behavior, and previous analyses have shown that the rates of production of visual, but not vocal, components provide graded information on female ovulation. It remains possible, however, that the acoustic parameters of these sexual calls, rather than their rate of productions,co-vary with female fertility. To test this, we analyzed structural and temporal call parameters from estrous calls and post-copulatory calls recorded over five consecutive mating seasons in 12 sexually mature females at Iguazú National Park, Argentina. Calls given during the fertile phase of the female ovarian cycle were compared with those given during the non-fertile phase, as determined by profiles of female reproductive hormones. Similarly, within the fertile phase, we tested whether temporal or spectral acoustic parameters of calls gradually change with the approach of ovulation. We did not find any significant relationship between call parameters and the two measures of female fertility in either female estrous calls or post-copulatory calls. However, some differences between pre- and post-copulatory calls were apparent. Overall, our results indicate that sexual calls in black capuchin females do not provide precise information
    about the timing of ovulation, but may allow listeners to make probabilistic inferences about whether copulations have taken place. This, combined with previous findings, suggests that females in our study may use signals in different modalities to convey information about their fertility and sexual behavior with varying degrees of precision.
  • Tiddi, B. et al. (2018). Male resource defense mating system in primates? An experimental test in wild capuchin monkeys. PLOS ONE [Online] 13:e0197020. Available at: https://doi.org/10.1371/journal.pone.0197020.
    Ecological models of mating systems provide a theoretical framework to predict the effect of the defendability of both breeding resources and mating partners on mating patterns. In resource-based mating systems, male control over breeding resources is tightly linked to female mating preference. To date, few field studies have experimentally investigated the relationship between male resource control and female mating preference in mammals due to difficulties in manipulating ecological factors (e.g., food contestability). We tested the within-group male resource defense hypothesis experimentally in a wild population of black capuchin monkeys (Sapajus nigritus) in Iguazú National Park, Argentina. Sapajus spp. represent an ideal study model as, in contrast to most primates, they have been previously argued to be characterized by female mate choice and a resource-based mating system in which within-group resource monopolization by high-ranking males drives female mating preference for those males. Here, we examined whether females (N = 12) showed a weaker preference for alpha males during mating seasons in which food distribution was experimentally manipulated to be less defendable relative to those in which it was highly defendable. Results did not support the within-group male resource defense hypothesis, as female sexual preferences for alpha males did not vary based on food defendability. We discuss possible reasons for our results, including the possibility of other direct and indirect benefits females receive in exercising mate choice, the potential lack of tolerance over food directed towards females by alpha males, and phylogenetic constraints.
  • Kean, D. et al. (2017). Feeling anxious? The mechanisms of vocal deception in tufted capuchin monkeys. Animal Behaviour [Online] 130:37-46. Available at: http://dx.doi.org/10.1016/j.anbehav.2017.06.008.
    An ability to deceive conspecifics is thought to have favoured the evolution of large brains in social animals, but evidence that such behaviours require cognitive complexity is lacking. Tufted capuchin monkeys (Sapajus spp.) have been documented to use false alarm calls during feeding in a manner that functions to deceive competitors. However, comparative evidence suggests that the production of vocalizations by nonhuman primates is largely underpinned by emotional mechanisms, calling into question more cognitive interpretations of this behaviour. To determine whether emotional states are plausibly necessary and sufficient to proximately explain deceptive alarm call production, we examined the association between self-directed behaviours (SDBs), as a proxy for anxiety, and the production of spontaneous false alarm calls among tufted capuchins. Specifically, we predicted that if anxiety is necessary for the production of false alarms, then individuals that produce spontaneous false alarms should exhibit more SDBs in those contexts in which they call. If anxiety is also sufficient to explain the false alarm call production, then we predicted that individuals that call more in a given context would show higher rates of SDBs in that context, and that high rates of calling would be temporally associated with high rates of SDBs. Our results support the contention that states of anxiety are necessary for an individual to spontaneously produce false alarms, but that such states are not sufficient to explain patterns of calling. The link between anxiety and deceptive calling thus appears complex, and cognitively based decision-making processes may play some role in call production.
  • Tiddi, B., Wheeler, B. and Heistermann, M. (2015). Female behavioral proceptivity functions as a probabilistic signal of fertility, not female quality, in a New World primate. Hormones and Behavior [Online] 73:148-155. Available at: http://dx.doi.org/10.1016/j.yhbeh.2015.07.011.
    The interests of males and females in mating contexts often conflict, and identifying the information conveyed by sexual signals is central to understanding how signalers manage such conflicts. Research into the information provided by female primate sexual signals has focused on exaggerated anogenital swellings as either reliable-indicators of reproductive quality (reliable-indicator hypothesis) or probabilistic signals of fertility (graded-signal hypothesis). While these morphological signals are mostly confined to catarrhine primates, these hypotheses are potentially widely applicable across primates, but have not been tested in taxa that lack such morphological signals. Here, we tested these hypotheses in wild black capuchins (Sapajus nigritus), a species in which females lack morphological sexual signals but produce conspicuous behavioral estrous displays. Specifically, we examined the proportion of time different females spent producing these signals with respect to measures of female quality (dominance rank, parity, age-related fecundity and cycle type) and in relation to the timing of fertility, as determined by analysis of fecal progesterone. Time spent displaying did not vary across females based on measures of female quality, but increased with the approach of ovulation. Further, male mating effort varied according to the timing of female fertility. Proceptive behaviors in this species thus meet predictions of the graded-signal hypothesis, providing the first support for this hypothesis based solely on behavioral signals.
  • Wheeler, B. (2015). Functions and mechanisms of communicative behaviors in humans and nonhuman primates. Current Anthropology 56:73-74.
  • Fischer, J., Wheeler, B. and Higham, J. (2015). Is there any evidence for vocal learning in chimpanzee food calls? Current Biology [Online] 25:R1-R2. Available at: http://dx.doi.org/10.1016/j.cub.2015.09.010.
    In their study “Vocal Learning in the Functionally Referential Food Grunts of Chimpanzees”, Watson et al. [1] claimed that they “provide the first evidence for vocal learning in a referential call in non-humans”. We challenge this conclusion, on two counts. For one, we are not convinced that the authors controlled for arousal (or at least they did not report such data); furthermore, the vocal characteristics of the two groups largely overlapped already at the beginning of the study. Accordingly, we also question the authors’ claim that their finding “sheds new light on the evolutionary history of human referential words”.
  • Wheeler, B. and Fischer, J. (2015). The blurred boundaries of functional reference: a response to Scarantino & Clay. Animal Behaviour [Online] 100:e9-e13. Available at: http://dx.doi.org/10.1016/j.anbehav.2014.11.007.
  • Wheeler, B., Tiddi, B. and Heistermann, M. (2014). Competition-induced stress does not explain deceptive alarm calling in tufted capuchin monkeys. Animal Behaviour [Online] 93:49-58. Available at: http://dx.doi.org/10.1016/j.anbehav.2014.04.016.
    Tactical deception has long attracted interest because it is often assumed to entail complex cognitive mechanisms. However, systematic evidence of tactical deception is rare and no study has attempted to determine whether such behaviours may be underpinned by relatively simple mechanisms. This study examined whether deceptive alarm calling among wild tufted capuchin monkeys, Cebus apella nigritus, feeding on contestable food resources can be potentially explained by a physiological mechanism, namely increased activation in the adrenocortex and the resulting production of glucocorticoids (GCs; ‘stress hormones’). This was tested experimentally in Iguazu? National Park, Argentina, by manipulating the potential for contest competition over food and noninvasively monitoring GC production through analysis of faecal hormone metabolites. If deceptive false alarms are indeed associated with adreno- cortical activity, it was predicted that the patterns of production of these calls would match the patterns of GC output, generally being higher in callers than noncallers in cases in which food is most contestable, and specifically being higher in callers on those occasions when a deceptive false alarm was produced. This hypothesis was not supported, as (1) GC output was significantly lower in association with the experimental introduction of contestable resources than in natural contexts wherein the potential for contest is lower, (2) within experimental contexts, there was a nonsignificant tendency for noncallers to show higher GC output than callers when food was most contestable, and (3) individuals did not show higher GC levels in cases in which they produced deceptive alarms relative to cases in which they did not. A learned association between the production of alarms and increased access to food may be the most likely cognitive explanation for this case of tactical deception, although unexplored physiological mechanisms also remain possible.
  • Wheeler, B. et al. (2013). Methodological considerations in the analysis of fecal glucocorticoid metabolites in tufted capuchins (Cebus apella). International Journal of Primatology [Online] 34:879-898. Available at: http://dx.doi.org/10.1007/s10764-013-9703-y.
    Analysis of fecal glucocorticoid (GC) metabolites has recently become the standard method to monitor adrenocortical activity in primates noninvasively. However, given variation in the production, metabolism, and excretion of GCs across species and even between sexes, there are no standard methods that are universally applicable. In particular, it is important to validate assays intended to measure GC production, test extraction and storage procedures, and consider the time course of GC metabolite excretion relative to the production and circulation of the native hormones. This study examines these four methodological aspects of fecal GC metabolite analysis in tufted capuchins (Cebus apella). Specifically, we conducted an adrenocorticotrophic hormone (ACTH) challenge on one male and one female capuchin to test the validity of four GC enzyme immunoassays (EIAs) and document the time course characterizing GC me- tabolite excretion in this species. In addition, we compare a common field-friendly technique for extracting fecal GC metabolites to an established laboratory extraction methodology and test for effects of storing “field extracts” for up to 1 yr. Results suggest that a corticosterone EIA is most sensitive to changes in GC production, provides reliable measures when extracted according to the field method, and measures GC metabolites which remain highly stable after even 12 mo of storage. Further, the time course of GC metabolite excretion is shorter than that described yet for any primate taxa. These results provide guidelines for studies of GCs in tufted capuchins, and underscore the importance of validating methods for fecal hormone analysis for each species of interest.
  • Koenig, A. et al. (2013). Variation in grouping patterns, mating systems and social structure: what socio-ecological models attempt to explain. Philosophical Transactions of the Royal Society B: Biological Sciences [Online] 368:20120348. Available at: http://dx.doi.org/10.1098/rstb.2012.0348.
    Socio-ecological models aim to predict the variation in social systems based on a limited number of ecological parameters. Since the 1960s, the original model has taken two paths: one relating to grouping patterns and mating systems and one relating to grouping patterns and female social structure. Here, we review the basic ideas specifically with regard to non-human primates, present new results and point to open questions. While most primates live in permanent groups and exhibit female defence polygyny, recent studies indicate more flexibility with cooperative male resource defence occurring repeatedly in all radiations. In contrast to other animals, the potential link between ecology and these mating systems remains, however, largely unexplored. The model of the ecology of female social structure has often been deemed successful, but has recently been criticized. We show that the predicted association of agonistic rates and despotism (directional consistency of relationships) was not supported in a comparative test. The overall variation in despotism is probably due to phylogenetic grade shifts. At the same time, it varies within clades more or less in the direction predicted by the model. This suggests that the model's utility may lie in predicting social variation within but not across clades.
  • Wheeler, B., Scarry, C. and Koenig, A. (2013). Rates of agonism among female primates: a cross-taxon perspective. Behavioral Ecology [Online] 24:1369-1380. Available at: http://dx.doi.org/10.1093/beheco/art076.
    Agonism is common in group-living animals, shaping dominance relationships and ultimately impacting individual tness. Rates of agonism vary considerably among taxa, however, and explaining this variation has been central in ecological models of female social relationships in primates. Early iterations of these models posited a link to diet, with more frequent agonism predicted in frugivorous species due to the presumed greater contestability of fruits relative to other food types. Although some more recent studies have suggested that dietary categories may be poor predictors of contest competition among primates, to date there have been no broad, cross-taxa comparisons of rates of female–female agonism in relation to diet. This study tests whether dietary variables do indeed pre- dict rates of female agonism and further investigates the role of group size (i.e., number of competitors) and substrate use (i.e., degree of arboreality) on the frequency of agonism. Data from 44 wild, unprovisioned groups, including 3 strepsirhine species, 3 platyrrhines, 5 colobines, 10 cercopithecines, and 2 hominoids were analyzed using phylogenetically controlled and uncontrolled methods. Results indicate that diet does not predict agonistic rates, with trends actually being in the opposite direction than predicted for all taxa except cercopithecines. In contrast, agonistic rates are positively associated with group size and possibly degree of terrestriality. Competitor density and perhaps the risk of ghting, thus, appear more important than general diet in predicting agonism among female primates. We discuss the implications of these results for socio-ecological hypotheses.
  • Wheeler, B. and Hammerschmidt, K. (2013). Proximate factors underpinning receiver responses to deceptive false alarm calls in wild tufted capuchin monkeys: is it counterdeception? American Journal of Primatology [Online] 75:715-725. Available at: http://dx.doi.org/10.1002/ajp.22097.
    Previous research demonstrates that tufted capuchin monkeys use terrestrial predator alarm calls in a functionally deceptive manner to distract conspecifics when feeding on contestable resources, although the success of this tactic is limited because listeners frequently ignore these calls when given in such situations. While this decreased response rate is suggestive of a counterstrategy to deception by receivers, the proximate factors underpinning the behavior are unclear. The current study aims to test if the decreased response rate to alarm calls in competitive contexts is better explained by the perception of subtle acoustic differences between predator-elicited and deceptive false alarms, or by receivers varying their responses based on the context in which the signal is received. This was tested by first examining the acoustic structure of predator-elicited and deceptive false alarms for any potentially perceptible acoustic differences, and second by comparing the responses of capuchins to playbacks of each of predator-elicited and false alarms, played back in noncompetitive contexts. The results indicate that deceptive false alarms and predator-elicited alarms show, at best, minimal acoustic differences based on the structural features measured. Likewise, playbacks of deceptive false alarms elicited antipredator reactions at the same rate as did predator-elicited alarms, although there was a nonsignificant tendency for false alarms to be more likely to elicit escape reactions. The lack of robust acoustic differences together with the high response rate to false alarms in noncompetitive contexts suggests that the context in which the signal is received best explains receiver responses. It remains unclear, however, if listeners ascribe different meanings to the calls based on context, or if they generally ignore all signals in competitive contexts. Whether or not the decreased response rate of receivers directly stems from the deceptive use of the calls cannot be determined until these latter possibilities are rigorously tested.
  • Wheeler, B. and Fischer, J. (2012). Functionally referential signals: a promising paradigm whose time has passed. Evolutionary Anthropology: Issues, News, and Reviews [Online] 21:195-205. Available at: http://dx.doi.org/10.1002/evan.21319.
    Finding the evolutionary origins of human language in the communication systems of our closest living relatives has, for the last several decades, been a major goal of many in the field of animal communication generally and primate communication specifically.1–4 The so-called “functionally referential” signals have long been considered promising in this regard, with apparent parallels with the semantic communication that characterizes language. The once-prominent idea that functionally referential signals are word-like, in that they are arbitrary sounds that refer to phenomena external to the caller, has largely been abandoned.5 However, the idea that these signals may offer the strongest link between primate communication and human language remains widespread, primarily due to the fact the behavior of receivers indicates that such signals enable them to make very specific inferences about their physical or social environment. Here we review the concept of functional reference and discuss modern perspectives that indicate that, although the sophistication of receivers provides some continuity between nonhuman primate and human cognition, this continuity is not unique to functionally referential signals. In fact, because functionally referential signals are, by definition, produced only in specific contexts, receivers are less dependent on the integration of contextual cues with signal features to determine an appropriate response. The processing of functionally referential signals is therefore likely to entail simpler cognitive operations than does that of less context-specific signals. While studies of functional reference have been important in highlighting the relatively sophisticated processes that underlie receiver behavior, we believe that the continued focus on context-specific calls detracts from the potentially more complex processes underlying responses to more unspecific calls. In this sense, we argue that the concept of functional reference, while historically important for the field, has outlived its usefulness and become a red herring in the pursuit of the links between primate communication and human language.
  • Wheeler, B., Bradley, B. and Kamilar, J. (2011). Predictors of orbital convergence in primates: A test of the snake detection hypothesis of primate evolution. Journal of Human Evolution [Online] 61:233-242. Available at: http://dx.doi.org/10.1016/j.jhevol.2011.03.007.
    Traditional explanations for the evolution of high orbital convergence and stereoscopic vision in primates have focused on how stereopsis might have aided early primates in foraging or locomoting in an arboreal environment. It has recently been suggested that predation risk by constricting snakes was the selective force that favored the evolution of orbital convergence in early primates, and that later exposure to venomous snakes favored further degrees of convergence in anthropoid primates. Our study tests this snake detection hypothesis (SDH) by examining whether orbital convergence among extant primates is indeed associated with the shared evolutionary history with snakes or the risk that snakes pose for a given species. We predicted that orbital convergence would be higher in species that: 1) have a longer history of sympatry with venomous snakes, 2) are likely to encounter snakes more frequently, 3) are less able to detect or deter snakes due to group size effects, and 4) are more likely to be preyed upon by snakes. Results based on phylogenetically independent contrasts do not support the SDH. Orbital convergence shows no relationship to the shared history with venomous snakes, likelihood of encountering snakes, or group size. Moreover, those species less likely to be targeted as prey by snakes show significantly higher values of orbital convergence. Although an improved ability to detect camouflaged snakes, along with other cryptic stimuli, is likely a consequence of increased orbital convergence, this was unlikely to have been the primary selective force favoring the evolution of stereoscopic vision in primates.
  • Wheeler, B. (2010). Decrease in alarm call response among tufted capuchins in competitive feeding contexts: possible evidence for counterdeception. International Journal of Primatology [Online] 31:665-675. Available at: http://dx.doi.org/10.1007/s10764-010-9419-1.
    Animal signals function to elicit behaviors in receivers that ultimately benefit the signaler, while receivers should respond in a way that maximizes their own fitness. However, the best response may be difficult for receivers to determine when unreliable signaling is common. “Deceptive” alarm calling is common among tufted capuchins (Cebus apella nigritus) in competitive feeding contexts, and responding to these calls is costly. Receivers should thus vary their responses based on whether a call is likely to be reliable. If capuchins are indeed able to assess reliability, I predicted that receivers will be less likely to respond to alarms that are given during competitive feeding contexts than in noncompetitive contexts, and, within feeding contexts, that individuals inside or adjacent to a food patch will be less likely to respond to alarms than those further from the resource. I tested these predictions in a group of wild capuchins by observing the reactions of focal animals to alarm calls in both noncompetitive contexts and experimental feeding contexts. Antipredator escape reactions, but not vigilance reactions, occurred significantly less often in competitive feeding contexts than in noncompetitive contexts and individuals adjacent to food patches were more likely to respond to alarm calls than were those inside or further from food patches. Although not all predictions were fully supported, the findings demonstrate that receivers vary their behavior in a way that minimizes the costs associated with “deceptive” alarms, but further research is needed to determine whether or not this can be attributed to counterdeception.
  • Wheeler, B. (2010). Community ecology of the Middle Miocene primates of La Venta, Colombia: the relationship between ecological diversity, divergence time, and phylogenetic richness. Primates [Online] 51:131-138. Available at: http://dx.doi.org/10.1007/s10329-009-0181-y.
    It has been suggested that the degree of ecological diversity that characterizes a primate community correlates positively with both its phylogenetic richness and the time since the members of that community diverged (Fleagle and Reed in Primate communities. Cambridge University Press, New York, pp 92–115, 1999). It is therefore questionable whether or not a community with a relatively recent divergence time but high phylogenetic richness would be as ecologically variable as a community with similar phylogenetic richness but a more distant divergence time. To address this question, the ecological diversity of a fossil primate community from La Venta, Colombia, a Middle Miocene platyrrhine community with phylogenetic diversity comparable with extant platyrrhine communities but a relatively short time since divergence, was compared with that of modern Neotropical primate communities. Shearing quotients and molar lengths, which together are reliable indicators of diet, for both fossil and extant species were plotted against each other to describe the dietary “ecospace” occupied by each community. Community diversity was calculated as the area of the minimum convex polygon encompassing all community members. The diversity of the fossil community was then compared with that of extant communities to test whether the fossil community was less diverse than extant communities while taking phylogenetic richness into account. Results indicate that the La Ventan community was not significantly less ecologically diverse than modern communities, supporting the idea that ecological diversification occurred along with phylogenetic diversification early in platyrrhine evolution.
  • Wheeler, B. (2010). Production and perception of situationally variable alarm calls in wild tufted capuchin monkeys (Cebus apella nigritus). Behavioral Ecology and Sociobiology [Online] 64:989-1000. Available at: http://dx.doi.org/10.1249/10.1007/s00265-010-0914-3.
    Many mammalian and avian species produce conspicuous vocalizations upon encountering a predator, but vary their calling based on risk urgency and/or predator type. Calls falling into the latter category are termed “functionally referential” if they also elicit predator-appropriate reactions in listeners. Functionally referential alarm calling has been well documented in a number of Old World monkeys and lemurs, but evidence among Neotropical primates is limited. This study investigates the alarm call system of tufted capuchin monkeys (Cebus apella nigritus) by examining responses to predator and snake decoys encountered at various distances (reflecting differences in risk urgency). Observations in natural situations were conducted to determine if predator-associated calls were given in additional contexts. Results indicate the use of three call types. “Barks” are elicited exclusively by aerial threats, but the call most commonly given to terrestrial threats (the “hiccup”) is given in nonpredatory contexts. The rate in which this latter call is produced reflects risk urgency. Playbacks of these two call types indicate that each elicits appropriate antipredator behaviors. The third call type, the “peep,” seems to be specific to terrestrial threats, but it is unknown if the call elicits predator-specific responses. “Barks” are thus functionally referential aerial predator calls, while “hiccups” are better seen as generalized disturbance calls which reflect risk urgency. Further evidence is needed to draw conclusions regarding the “peep.” These results add to the evidence that functionally referential aerial predator alarm calls are ubiquitous in primates, but that noncatarrhine primates use generalized disturbance calls in response to terrestrial threats.
  • Wheeler, B. (2010). Snakes! The Unified Theory of Everything about Primates? Evolutionary Anthropology [Online] 19:37-38. Available at: http://dx.doi.org/10.1002/evan.20244.
  • Wheeler, B., Pokempner, A. and Tiddi, B. (2009). Post-golden age primatology in Edinburgh. Evolutionary Anthropology [Online] 18:44-45. Available at: https://doi.org/10.1002/evan.20204.
  • Wheeler, B. (2009). Monkeys crying wolf? Tufted capuchin monkeys use anti-predator calls to usurp resources from conspecifics. Proceedings of the Royal Society B: Biological Sciences [Online] 276:3013-3018. Available at: http://dx.doi.org/10.1098/rspb.2009.0544.
    The use of ‘tactical deception’ is argued to have been important in the cognitive evolution of the order Primates, but systematic studies of active deception in wild non-human primates are scant. This study tests whether wild tufted capuchin monkeys (Cebus apella nigritus) use alarm calls in a functionally deceptive manner to usurp food resources. If capuchins use alarm calls ‘deceptively’, it was predicted that false alarms should be: (i) given by subordinates more than by dominants, (ii) more frequent when food is most contestable, (iii) more frequent when less food is available, and (iv) given when the caller is in a spatial position in which it could increase its feeding success if conspecifics react to the call. These predictions were tested by observing subjects in experimental contexts, in which the amount and distribution of a high-value resource (banana pieces) were manipulated using wooden platforms suspended from tree branches. While false alarms were non-significantly more common when more food was available, the three remaining predictions were supported. These results generally support the hypothesis that alarm calls are used by capuchins to reduce the effects of feeding competition. Whether this is intentional on the part of the caller requires further investigation.
  • Wheeler, B. (2008). Selfish or altruistic? An analysis of alarm call function in wild capuchin monkeys, Cebus apella nigritus. Animal Behaviour [Online] 76:1465-1475. Available at: http://dx.doi.org/10.1016/j.anbehav.2008.06.023.
    Alarm calls facilitate some antipredatory benefits of group living but may endanger the caller by attracting the predator's attention. A number of hypotheses invoking kin selection and individual selection have been proposed to explain how such behaviour could evolve. This study tests eight hypotheses for alarm call evolution by examining the responses of tufted capuchin monkeys to models of felids, perched raptors and vipers. Specifically, this study examines: (1) differences between individuals in their propensity to call in response to different threat types, (2) whether there is an audience effect for alarm calling and (3) the response of conspecifics to alarms. Results indicate that the benefits likely to be afforded to the caller vary with stimulus type. Alarm calling in response to felids is most likely selfish, with calls apparently directed towards both the predator and potential conspecific mobbers. Alarm calling in response to vipers attracts additional mobbers as well, but also appears to be driven by kin selection in the case of males and parental care benefits in the case of females. Alarm responses to perched raptors are rare, but seem to be selfish, with callers benefiting by recruiting additional mobbers.
  • Wheeler, B. and Ungar, P. (2001). Congruence of tail use behaviors between male and female mantled howling monkeys (Alouatta palliata). Folia Primatologica [Online] 72:292-297. Available at: http://dx.doi.org/1159/000049950.
    Differences between males and females in locomotor and positional behaviors have been documented for several primate species [1, 2]. In Alouatta palliata for example, females climb and use smaller substrates more than males [3–5]. Such sex differences are usually related to body size. Indeed, interspecific studies have repeatedly demonstrated relationships between body size and locomotor and positional behaviors. It is easier, for example, for a large primate to suspend beneath a branch than to balance on top of it [6, 7]. This is particularly true for primates that feed near the periphery of the crown, where branches tend to be smaller.

Book section

  • Wheeler, B. (2017). Deceptive Alarm Calls. in: Shackelford, T. K. and Weekes-Shackelford, V. eds. Encyclopedia of Evolutionary Psychological Science. Springer.
  • Di Bitetti, M. and Wheeler, B. (2017). The vocal repertoire of the black horned capuchin monkey (Cebus [Sapajus] nigritus): an acoustic and contextual analysis. in: Kowalewski, M. M. and Oklander, L. I. eds. Primatology in Argentina. Sociedad Argentina para el Estudio de los Mamíferos. Available at: https://www.sarem.org.ar/en/products/primatology-in-argentina-en/.
  • Zinner, D. and Wheeler, B. (2012). Violence among our closest relatives--aggression in nonhuman primate societies. in: Kortüm, H. -H. and Heinze, J. eds. Aggression in humans and other primates: biology, psychology, sociology. Berlin: De Gruyter, pp. 41-86. Available at: https://www.degruyter.com/view/product/183617.
  • Wheeler, B. et al. (2011). Communication. in: Menzel, R. and Fischer, J. eds. Animal thinking: contemporary issues in comparative cognition. MIT Press, pp. 187-205. Available at: https://doi.org/10.7551/mitpress/9780262016636.001.0001.

Conference or workshop item

  • Wheeler, B., Fahy, M. and Tiddi, B. (2017). Experimental evidence of associative learning of heterospecific alarms in wild black capuchin monkeys.
  • Wheeler, B., Fahy, M. and Tiddi, B. (2016). Experimental evidence of associative learning of heterospecific alarms in wild black capuchin monkeys.
  • Koenig, A. et al. (2015). Rate of agonism may be the only useful predictor of despotic dominance hierarchies. in: AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY. pp. 192-192.
  • Tiddi, B., Wheeler, B. and Heistermann, M. (2015). Mating patterns in relation to the timing of ovulation in Argentine black capuchins. in: 6th European Federation for Primatology Meeting. Karger, pp. 371-372. Available at: http://dx.doi.org/10.1159/000435825.
    Tufted capuchin ( Sapajus spp.) females have been shown to strongly prefer the alpha male and direct most of their solicitations to this individual. The strength of this preference, however, varies across populations of tufted capuchins and copulations with other males occur in all stud-ied populations. Females thus mate promiscuously, and a focus on the timing of mating with alpha versus other males is crucial to understand female mating strategies better and, in turn, their potential influence on male reproductive skew. However, these questions have been largely unaddressed due to the lack of data matching the timing of ovulation with timing of copulations in wild populations. Here, we examined female mating preference with a specific focus on the distribution pattern of copulations with different males in relation to the timing of ovulation. During four mating seasons, we observed 150 copulations with 17 females belonging to three groups of black capuchins (Sapajus nigritus) in Iguazú National Park, Argentina. Although fe-males showed high preference for the alpha male, 12 out of 17 females also mated with other group males (n = 55 copulations). When considering the timing of ovulation as assessed by faecal progestogen measurements, copulations were highly synchronized with the female fertile phase and copulations with alpha males tended to occur significantly closer to ovulation compared to other males. In addition, Hinde index values showed that females were actively responsible for maintaining proximity to the target male during their proceptive periods. However, Hinde index values did not increase with the approach of ovulation, suggesting that females’ contribution to proximity maintenance was not strictly linked to the timing of ovulation. Overall, females in our study groups seem to show a combination of strategies that aim at both biasing paternity to the alpha male and confusing paternity among group males. Our research complied with the Euro-pean Directive 2010/63/EU.
  • Wheeler, B. and Janson, C. (2015). Ambush predators may select for small group size in rainforest primate prey. in: 6th European Federation for Primatology Meeting, XXII Italian Association of Primatology Congress. pp. 381-381. Available at: http://dx.doi.org/10.1159/000435825.
    Classic ecological models of social groups suggest that increasing group size typically leads to a decrease in both individual predation risk and net food intake, with optimal group size being a compromise between these benefits and costs. Among rainforest primates, the main antipreda-tor benefits of sociality are thought to result from the dilution effect and collective detection of predators. However, recent research suggests that vegetation density in rainforest habitats limits the benefits of collective detection against ambush predators such as raptors, felids and snakes. Further, while larger groups are acknowledged to be more conspicuous to predators, it is widely assumed that this cost is unlikely to outweigh dilution benefits. Here we show in a simple model that per-individual rates of both encounters with predators and successful ambush attacks per encounter can increase with group size, under conditions likely to hold for many primate groups (when increases in group size lead to increases in group spread, conspicuousness and daily trav-el distance). Consequently, individual risk against ambush predators that employ a sit-and-wait strategy to search for prey, such as many snakes and some raptors, is lowest in small to medium-sized groups. In contrast, individuals in relatively large groups are favoured against ambush pred-ators like felids that employ a cruising strategy to search for prey, although even in this case in-creasing group size above some threshold increases individual risk. These results suggest that maximum group size among primates can be limited by increasing predation risk. Research fo-cused on primate predators is needed to determine the extent to which the model accurately re-flects their behaviour.
  • Wheeler, B. and Janson, C. (2014). Ambush predators may select for small group size in rainforest primate prey.
  • Wheeler, B. (2003). Community ecology of the middle Miocene primates of La Venta, Columbia: The relationship between divergence time and ecological diversity. in: 72rd Annual Meeting of the American Association of Physical Anthropologists. WILEY-LISS, DIV JOHN WILEY & SONS INC, pp. 223-223.
  • Wheeler. C, B. (2003). Community ecology of the middle Miocene primates of La Venta, Columbia: The relationship between divergence time and ecological diversity. in: AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY. WILEY, pp. 223-223. Available at: 10.1007/s10329-009-0181-y.
    It has been suggested that the degree of ecological diversity that characterizes a primate community correlates positively with both its phylogenetic diversity and the time since the members of that community diverged (Fleagle & Reed, 1999). Therefore, it is questionable whether or not a community with a relatively recent divergence time but high phylogenetic diversity would be as ecologically variable as a community with similar phylogenetic diversity but a more distant divergence time. To address this question, the ecological diversity of a middle Miocene platyrrhine primate community with high phylogenetic diversity but a relatively recent divergence time (members of the Honda Group from La Venta, Columbia) was compared with that of modern neotropical primate communities.
    Shearing quotients and molar lengths (which together are reliable indicators of diet) for both fossil and extant species were plotted against each other to describe the dietary ecospace each community occupies. Community diversity was calculated using three measure: the area of the minimum convex polygon encompassing all community members, the average distance from the centroid of the polygon to each community member, and the average distance between taxa on the bivariate plot. By these measures, the La Venta community was as diverse as most modern communities with similar phylogenetic diversity, indicating that neotropical communities have not become more diverse as the time since the common ancestor of the members of these communities increased.
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