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Is male rhesus macaque red color ornamentation attractive to females?
Abstract and Figures
Male sexually selected traits can evolve through different mechanisms: conspicuous and colorful ornaments usually evolve through intersexual selection, while weapons usually evolve through intra-sexual selection. Male ornaments are rare among mammals in comparison to birds, leading to the notion that female mate choice generally plays little role in trait evolution in this taxon. Supporting this view, when ornaments are present in mammals, they typically indicate social status and are products of male-male competition. This general mammalian pattern, however, may not apply to rhesus macaques (Macaca mulatta). Males of this species display conspicuous skin coloration, but this expression is not correlated to dominance rank and is therefore unlikely to have evolved due to male-male competition. Here, we investigate whether male color expression influences female proceptivity toward males in the Cayo Santiago free-ranging rhesus macaque population. We collected face images of 24 adult males varying in dominance rank and age at the peak of the mating season and modeled these to rhesus macaque visual perception. We also recorded female sociosexual behaviors toward these males. Results show that dark red males received more sexual solicitations, by more females, than pale pink ones. Together with previous results, our study suggests that male color ornaments are more likely to be a product of inter- rather than intra-sexual selection. This may especially be the case in rhesus macaques due to the particular characteristics of male-male competition in this species.
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... In comparison to more striking groups such as birds, most mammals display relatively little variation in coloration, with the exception of primates (Caro, 2013). Some primate species exhibit unusually bright red skin on the face or anogenital region, traits thought to function in malemale dominance signalling (Setchell & Dixson, 2001;Bergman et al., 2009;Marty et al., 2009), advertising fertility, proceptivity or pregnancy in females (Nunn, 1999;Setchell et al., 2006;Dubuc et al., 2009;Rigaill et al., 2015), or perhaps serving as an indicator of quality in mate choice (Waitt et al., 2006;Dubuc et al., 2014aDubuc et al., , 2014b. Other primates exhibit vivid red-orange pelage coloration, which can be diverse in extent and pattern even among closely related species. ...
... Red skin in primates is produced by increased vascularization of epidermal tissue (Collings, 1926;Mayor et al., 2015), and the intensity of pink-red coloration is modulated via alterations in blood flow which reflect hormone levels (Vandenbergh, 1965;Baulu, 1976;Rhodes et al., 1997;Dixson, 1998;Dubuc et al., 2009). Such skin is therefore well suited to reflecting short-or mediumterm changes in social status, proceptivity, fertility, and possibly haematological health or mate quality (Dubuc et al., 2014a;Mayor et al., 2015; but see Setchell et al., 2009). Indeed, the evolution of red sexual skin in males is probably driven primarily by intrasexual competition and dominance signalling (Setchell & Dixson, 2001;Setchell et al., 2008;Bergman et al., 2009;Marty et al., 2009;Grueter et al., 2015b;Setchell, 2015;Greenberg et al., 2022), while in females, this trait is thought to act as a probabilistic signal of short-or long-term reproductive status which can incite male mating interest (Van Noordwijk, 1985;Nunn, 1999;Domb & Pagel, 2001;Fujita et al., 2004;Setchell et al., 2006;Dubuc et al., 2009;Gerald et al., 2009;Higham et al., 2009Higham et al., , 2010Higham et al., , 2012Moreira et al., 2015;Rigaill et al., 2015;Street et al., 2016). ...
... We would argue that our use of Bayesian phylogenetic methods that are more robust to such scenarios (Gardner & Organ, 2021), coupled with the separate consideration of polymorphic and trichromatic species and the addition of new data on polymorphic strepsirrhines which maximize the number of evolutionary transitions between traits (Gardner & Organ, 2021), paints a more accurate picture of primate macroevolutionary history. We had anticipated that modulated red facial skin in male primates would be associated with male trichromatic visual system, as this trait is thought to have evolved primarily via intrasexual selection as a result of male-male competition in most species (Dubuc et al., 2014a). However, we found no such association across species. ...
Primates are remarkably colourful in comparison to other mammals. In particular, several species exhibit red-orange pelage or bright red skin, with the latter thought to signal status in intraspecific dominance interactions or to signal fertility. One potential driver of the interspecific diversity in red coloration is the primate visual system, which, uniquely among eutherian mammals, varies interspecifically and even between conspecifics in the ability to distinguish red and green (trichromatic colour vision). Previous comparative studies, however, have produced conflicting results regarding the proposed link between coloration and visual system. We employed an updated, sex-specific dataset of primate coloration and visual systems to reexamine the relationship between colour vision and red coloration across the entire order. With a few exceptions, increased colour visual ability is not significantly associated with the presence of red skin on the face or anogenital region, nor of red-orange pelage. We discuss possible reasons for the lack of colour-vision associations and suggest that dichromatic colour vision still facilitates effective signalling between conspecifics.
... In comparison to more striking groups such as birds, most mammals display relatively little variation in coloration, with the exception of primates (Caro, 2013). Some primate species exhibit unusually bright red skin on the face or anogenital region, traits thought to function in malemale dominance signalling (Setchell & Dixson, 2001;Bergman et al., 2009;Marty et al., 2009), advertising fertility, proceptivity or pregnancy in females (Nunn, 1999;Setchell et al., 2006;Dubuc et al., 2009;Rigaill et al., 2015), or perhaps serving as an indicator of quality in mate choice (Waitt et al., 2006;Dubuc et al., 2014aDubuc et al., , 2014b. Other primates exhibit vivid red-orange pelage coloration, which can be diverse in extent and pattern even among closely related species. ...
... Red skin in primates is produced by increased vascularization of epidermal tissue (Collings, 1926;Mayor et al., 2015), and the intensity of pink-red coloration is modulated via alterations in blood flow which reflect hormone levels (Vandenbergh, 1965;Baulu, 1976;Rhodes et al., 1997;Dixson, 1998;Dubuc et al., 2009). Such skin is therefore well suited to reflecting short-or mediumterm changes in social status, proceptivity, fertility, and possibly haematological health or mate quality (Dubuc et al., 2014a;Mayor et al., 2015; but see Setchell et al., 2009). Indeed, the evolution of red sexual skin in males is probably driven primarily by intrasexual competition and dominance signalling (Setchell & Dixson, 2001;Setchell et al., 2008;Bergman et al., 2009;Marty et al., 2009;Grueter et al., 2015b;Setchell, 2015;Greenberg et al., 2022), while in females, this trait is thought to act as a probabilistic signal of short-or long-term reproductive status which can incite male mating interest (Van Noordwijk, 1985;Nunn, 1999;Domb & Pagel, 2001;Fujita et al., 2004;Setchell et al., 2006;Dubuc et al., 2009;Gerald et al., 2009;Higham et al., 2009Higham et al., , 2010Higham et al., , 2012Moreira et al., 2015;Rigaill et al., 2015;Street et al., 2016). ...
... We would argue that our use of Bayesian phylogenetic methods that are more robust to such scenarios (Gardner & Organ, 2021), coupled with the separate consideration of polymorphic and trichromatic species and the addition of new data on polymorphic strepsirrhines which maximize the number of evolutionary transitions between traits (Gardner & Organ, 2021), paints a more accurate picture of primate macroevolutionary history. We had anticipated that modulated red facial skin in male primates would be associated with male trichromatic visual system, as this trait is thought to have evolved primarily via intrasexual selection as a result of male-male competition in most species (Dubuc et al., 2014a). However, we found no such association across species. ...
Primates are remarkably colourful in comparison to other mammals. In particular, several species exhibit red–orange pelage or bright red skin, with the latter thought to signal status in intraspecific dominance interactions or to signal fertility. One potential driver of the interspecific diversity in red coloration is the primate visual system, which, uniquely among eutherian mammals, varies interspecifically and even between conspecifics in the ability to distinguish red and green (trichromatic colour vision). Previous comparative studies, however, have produced conflicting results regarding the proposed link between coloration and visual system. We employed an updated, sex-specific dataset of primate coloration and visual systems to re-examine the relationship between colour vision and red coloration across the entire order. With a few exceptions, increased colour visual ability is not significantly associated with the presence of red skin on the face or anogenital region, nor of red–orange pelage. We discuss possible reasons for the lack of colour–vision associations and suggest that dichromatic colour vision still facilitates effective signalling between conspecifics.
... whereas female rhesus macaques prefer males with darker redder faces (Dubuc et al., 2014(Dubuc et al., , 2016. To my knowledge, while Higham et al. (2021) separated analyses into "alpha males" and "all males," detailed analyses on the characteristics of the specific males that female crested macaques are more likely to approach and solicit have yet to be undertaken. ...
... For example, Japanese and rhesus exhibit a lower degree of body and canine size dimorphism, and large relative testis volume among males, while females exhibit neither sexual swellings nor copulation calls (Japanese macaques, Soltis et al., 1997aSoltis et al., , 1997b; rhesus macaques, . Reproductive skew by male dominance in these species is both low, and variable, with skew even favoring lower ranked males in some years and groups (Dubuc et al., 2014;Soltis et al., 1997b). Other species of macaques, such as Barbary macaques (Macaca sylvanus), and long-tailed macaques, exhibit phenotypes that are intermediate between these two extremes, and/or that exhibit a mix of these traits. ...
Sexual selection explains the evolution of traits that impact mating and reproductive success. Primates are an excellent system for studying sexually-selected traits, because they exhibit marked variation in mating systems, show evidence of intrasexual competition in both sexes, and mutual mate choice. Here, I discuss the sexual selection dynamic of the crested macaque (Macaca nigra) and its overall putative sexually-selected phenotype. Female crested macaque fertile phases are highly asynchronous, which alpha males monopolize, leading to high reproductive skew. Given the reproductive benefits to alpha status, males compete aggressively over dominance, with all observed alpha male replacements occurring via top-entry challenge competition. Infant disappearances increase after the arrival of a new alpha male, indicating potential infanticide from incoming males. Consistent with strong male-male contest competition, crested macaques exhibit marked body and canine size sexual dimorphism, with males being larger. Males exhibit small relative testis volume, indicating that indirect competition via sperm competition is not prevalent. Male-male relationships are mediated by social status signals, including loud calls and colorful genitals, and males largely avoid each other. Female-female relationships are generally affiliative with low levels of aggression. Females exhibit direct mate choice in the form of some consortship maintenance, and also exhibit a number of proceptive behaviors towards males, which increase in frequency markedly during fertile phases. Females exhibit traits that may facilitate indirect mate choice, including copulation calls and large sexual swellings. Our understanding of the species enables us to set the crested macaque into comparative context, and to characterize many of its traits as part of a holistic sexually-selected phenotype.
... In male macaques, sexual skins also darken during the mating season [11,13], but it is unclear precisely what these sexual skins signal. In some primates such as mandrills and drills, males with redder faces tend to be higher ranking [45,48,49]. In these species, the male sexual skin is likely to be 'a badge of status' signalling the competitive ability of the bearer [11]. ...
... In this study, we used a dual-presentation, free-viewing paradigm to reveal a strong preference for male rhesus macaques to visually inspect the AGRs, rather than faces, of both female and male conspecifics. This was somewhat surprising, as faces are highly salient visual stimuli for rhesus macaques [33,34,[68][69][70] that convey a rich array of information including identity, social status and reproductive state [38,39,47,48]. Monkeys value the opportunity to view conspecific faces so highly that they will forego fluid and food rewards in exchange [33,34]. ...
Social stimuli, like faces, and sexual stimuli, like genitalia, spontaneously attract visual attention in both human and non-human primates. Social orienting behaviour is thought to be modulated by neuropeptides as well as sex hormones. Using a free viewing task in which paired images of monkey faces and anogenital regions were presented simultaneously, we found that male rhesus macaques overwhelmingly preferred to view images of anogenital regions over faces. They were more likely to make an initial gaze shift towards, and spent more time viewing, anogenital regions compared with faces, and this preference was accompanied by relatively constricted pupils. On face images, monkeys mostly fixated on the forehead and eyes. These viewing preferences were found for images of both males and females. Both oxytocin (OT), a neuropeptide linked to social bonding and affiliation, and testosterone (TE), a sex hormone implicated in mating and aggression, amplified the pre-existing orienting bias for female genitalia over female faces; neither treatment altered the viewing preference for male anogenital regions over male faces. Testosterone but not OT increased the probability of monkeys making the first gaze shift towards female anogenital rather than face pictures, with the strongest effects on anogenital images of young and unfamiliar females. Finally, both OT and TE promoted viewing of the forehead region of both female and male faces, which display sexual skins, but decreased the relative salience of the eyes of older males. Together, these results invite the hypothesis that both OT and TE regulate reproductive behaviours by acting as a gain control on the visual orienting network to increase attention to mating-relevant signals in the environment.
This article is part of the theme issue ‘Interplays between oxytocin and other neuromodulators in shaping complex social behaviours’.
... The combination of large group sizes and reproductive seasonality leads to females within a population displaying synchrony in their fertility cycles and is thought to be the driver of weak direct male-male competition, such as through physical combat, and strong indirect male-male competition, such as through female mate choice (Gogarten and Koenig, 2013;Kutsukake and Nunn, 2009;Ostner et al., 2008). High female fertile phase synchrony lowers the ability for males to monopolize females, creating a relatively weak competitive environment which leads to relatively low male reproductive skew where reproductive success is not monopolized by only one or a small number of males, and selects for limited body and canine size dimorphism and large relative testis volume (Dubuc et al., 2014b;Harcourt et al., 1981;Dubuc et al., 2014a). ...
... Females prefer to mate with novel males (i.e. those that have recently immigrated to their social group), middle-aged males, and males with darker red faces (Maestripieri and Hoffman, 2012;Dubuc et al., 2014a). Since the highest ranking males in a social group typically have a long tenure within the group and are of an older age class, female choice is likely to be an additional driver of the relatively weak reproductive skew in male rhesus macaques, by increasing the reproductive success of lower ranking males (Bercovitch, 1997). ...
Of all the non-human primate species studied by researchers, the rhesus macaque ( Macaca mulatta ) is likely the most widely used across biological disciplines. Rhesus macaques have thrived during the Anthropocene and now have the largest natural range of any non-human primate. They are highly social, exhibit marked genetic diversity, and display remarkable niche flexibility (which allows them to live in a range of habitats and survive on a variety of diets). These characteristics mean that rhesus macaques are well-suited for understanding the links between sociality, health and fitness, and also for investigating intra-specific variation, adaptation and other topics in evolutionary ecology.
... Due to the start-stop nature of rhesus consort mounting behaviour 66 , repetitive mounting behaviours (occurring within a 5 min interval) between the same participants were collapsed into counts of singular mounting events. This is in convention with previous studies of reproductive behaviour in rhesus macaques 1,67 , and buffers against the extreme skews arising from this characteristic of rhesus courtship. Gathering mounts between same participants within 5 min intervals was performed in R and Python (v.3.9.2). ...
Numerous reports have documented the occurrence of same-sex sociosexual behaviour (SSB) across animal species. However, the distribution of the behaviour within a species needs to be studied to test hypotheses describing its evolution and maintenance, in particular whether the behaviour is heritable and can therefore evolve by natural selection. Here we collected detailed observations across 3 yr of social and mounting behaviour of 236 male semi-wild rhesus macaques, which we combined with a pedigree dating back to 1938, to show that SSB is both repeatable (19.35%) and heritable (6.4%). Demographic factors (age and group structure) explained SSB variation only marginally. Furthermore, we found a positive genetic correlation between same-sex mounter and mountee activities, indicating a common basis to different forms of SSB. Finally, we found no evidence of fitness costs to SSB, but show instead that the behaviour mediated coalitionary partnerships that have been linked to improved reproductive success. Together, our results demonstrate that SSB is frequent in rhesus macaques, can evolve, and is not costly, indicating that SSB may be a common feature of primate reproductive ecology.
... Given that both absolute and relative ECV are heritable [55,66], greater variability in ECV among males may, in theory, reflect selection on cognition and behaviour-specifically, disruptive or balancing selection on male reproductive strategies. Male rhesus macaques are subject to an interesting mix of sexual selection pressures, including direct male-male competition, reflected by intermediate body and canine size dimorphism [67], indirect male-male competition, reflected by large relative testis volume [68] and mechanisms of indirect female mate choice, such as female preference for males with darker red faces [69]. Accordingly, although dominance rank predicts male rhesus macaque reproductive success, male reproductive skew is relatively low and may reflect that males tend to queue for dominance rank instead of fighting directly [48]. ...
The greater male variability (GMV) hypothesis proposes that traits are more variable among males than females, and is supported by numerous empirical studies. Interestingly, GMV is also observed for human brain size and internal brain structure, a pattern which may have implications for sex-biased neurological and psychiatric conditions. A better understanding of neuroanatomical variability in non-human primates may illuminate whether certain species are appropriate models for these conditions. Here, we tested for sex differences in the variability of endocranial volume (ECV, a proxy for brain size) in a sample of 542 rhesus macaques ( Macaca mulatta ) from a large pedigreed free-ranging population. We also examined the components of phenotypic variance (additive genetic and residual variance) to tease apart the potential drivers of sex differences in variability. Our results suggest that males exhibit more variable ECVs, and that this pattern reflects either balancing/disruptive selection on male behaviour (associated with alternative male mating strategies) or sex chromosome effects (associated with mosaic patterns of X chromosome gene expression in females), rather than extended neurodevelopment among males. This represents evidence of GMV for brain size in a non-human primate species and highlights the potential of rhesus macaques as a model for sex-biased brain-based disorders.
When looking at others, primates primarily focus on the face – detecting the face first and looking at it longer than other parts of the body. This is because primate faces, even without expression, convey trait information crucial for navigating social relationships. Recent studies on primates, including humans, have linked facial features, specifically facial width-to-height ratio (fWHR), to rank and Dominance-related personality traits, suggesting these links’ potential role in social decisions. However, studies on the association between dominance and fWHR report contradictory results in humans and variable patterns in nonhuman primates. It is also not clear whether and how nonhuman primates perceive different facial cues to personality traits and whether these may have evolved as social signals. This review summarises the variable facial-personality links, their underlying proximate and evolutionary mechanisms and their perception across primates. We emphasise the importance of employing comparative research, including various primate species and human populations, to disentangle phylogeny from socio-ecological drivers and to understand the selection pressures driving the facial-personality links in humans. Finally, we encourage researchers to move away from single facial measures and towards holistic measures and to complement perception studies using neuroscientific methods.
Vitiligo affects a significant portion of human and animal populations. The disease causes irregular and multifocal progressive loss of fur, skin, and mucous membrane pigmentation due to the loss or absence of melanocytes. While etiopathogenesis is not completely understood, autoimmunity, environmental, and genetic factors are implicated We present a case report on a 16-y-old female rhesus macaque ( Macaca mulatta ) with depigmented areas that are progressively increasing on the skin and coat and are distributed on the head and back. Histopathology revealed alterations compatible with vitiligo characterized by the absence of melanocytes in the epidermis and dermis. The clinical history and complementary exams support this diagnosis.
Speciation can be caused by divergent adaptation in allopatry as a result of ecological or reproductive character displacement in sympatry or parapatry. The latter can result as a means of preventing hybridization, a process known as reinforcement speciation. Though this has been described in a variety of taxonomic systems though the prevalence throughout nature is still unknown. In this study, we use whole-genome sequencing (WGS) of two primate species that have experienced introgression in their history, the rhesus (Macaca mulatta) and cynomolgus (M. fascicularis) macaques, to identify genes exhibiting a pattern of reproductive character displacement consistent with reinforcement speciation. Using windowed scans of various population genetic statistics to identify reproductive character displacement, we find candidate genes associated with a variety of functions, including an overrepresentation of multiple neurological functions and some genes involved in sexual development and gametogenesis. This suggests a variety of genes acting at multiple stages of a reinforcement process between these species. We also find signatures of introgression of the Y-chromosome that confirm previous studies suggesting male-driven introgression of M. mulatta into M. fascicularis populations. This study is among the first to utilize whole-genome sequencing to analyze the phenomenon of reinforcement and among the first to find evidence of this phenomenon in primates, particularly ones that have medical relevance.
The degree of polygyny is predicted to influence the strength of direct male–male competition, leading to a high variance in male lifetime reproductive success and to reproduction limited to the prime period of adulthood. Here, we explore the variance in male lifetime reproductive success and reproductive time in an anthropoid primate forming multimale–multifemale groups. Males of this species form dominance hierarchies, which are expected to skew reproduction toward few high-ranking males. At the same time, however, females mate with multiple males (polygynandry), which should limit the degree of polygyny. Using 20 years of genetic and demographic data, we calculated lifetime reproductive success for the free-ranging rhesus macaque (Macaca mulatta) population of Cayo Santiago for subjects that died naturally or reached senescence. Our results show that 1) male lifetime reproductive success was significantly skewed (range: 0–47 offspring; males reproducing below average: 62.8%; nonbreeders: 17.4%), 2) variance in male lifetime
reproductive success was 5 times larger than in females, and 3) male lifetime reproductive success was more influenced by variation in fecundity (60%) than longevity (25%), suggesting that some direct male–male competition takes place. However, the opportunity for selection (i.e., standardized variance in male lifetime reproductive success) is low compared with that in other large mammal species characterized by a high degree of polygyny. Moreover, male reproductive life extended much beyond the prime period, showing that physical strength was not required to acquire mates. We conclude that rhesus macaques exhibit a moderate degree of polygyny and, therefore, low levels of direct male–male competition for fertile females, despite the fact that males form linear dominance hierarchies.
A combination of field and laboratory investigations has revealed that the temporal patterns of testosterone (T) levels in blood can vary markedly among populations and individuals, and even within individuals from one year to the next. Although T is known to regulate reproductive behavior (both sexual and aggressive) and thus could be expected to correlate with mating systems, it is clear that the absolute levels of T in blood are not always indicative of reproductive state. Rather, the pattern and amplitude of change in T levels are far more useful in making predictions about the hormonal basis of mating systems and breeding strategies. In these contexts we present a model that compares the amplitude of change in T level with the degree of parental care shown by individual males. On the basis of data collected from male birds breeding in natural or captive conditions, polygynous males appear less responsive to social environmental cues than are monogamous males. This model indicates that there may be widely different hormonal responses to male-male and male-female interactions and presumably equally plastic neural mechanisms for the transduction of these signals into endocrine secretions. Furthermore, evidence from other vertebrate taxa suggests strongly that the model is applicable to other classes
Two semifree-ranging mandrill groups, inhabiting large, naturally rainforested enclosures in Gabon, were studied to measure morphological, endocrine, and behavioral changes that occurred when adult males rose, or fell, in dominance rank. Gaining alpha rank (N = 4 males) resulted in increased testicular size and circulating testosterone, reddening of the sexual skin on the face and genitalia, and heightened secretion from the sternal cutaneous gland. Blue sexual skin coloration was unaffected. New alpha males increased in rump "fattedness," but not in body mass, and spent more time associated with other group members, rather than ranging alone. Loss of alpha position (N = 4 males) resulted in less pronounced effects than those that occurred after males had risen to alpha positions. Deposed alpha males showed decreased testicular volume, decreased body mass, a reduction in the extent of red (but not blue) sexual skin coloration, and decreased sternal gland activity. Deposed males did not decrease in the brightness of sex skin coloration. These results demonstrate that male-male competition and rank reversals have remarkable effects upon testicular function, secondary sexual traits, and behavior in the adult male mandrill. Secondary sexual traits respond to changes in male social status and therefore may be important as intrasexual signals of dominance rank. (C) 2001 Academic Press.
Sexual Selection in Primates provides an account of all aspects of sexual selection in primates, combining theoretical insights, comprehensive reviews of the primate literature and comparative perspectives from relevant work on other mammals, birds and humans. Topics include sex roles, sexual dimorphism in weapons, ornaments and armaments, sex ratios, sex differences in behaviour and development, mate choice, sexual conflict, sex-specific life history strategies, sperm competition and infanticide. The outcome of the evolutionary struggle between the sexes, the flexibility of roles and the leverage of females are discussed and emphasised throughout. Sexual Selection in Primates is aimed at graduates and researchers in primatology, animal behaviour, evolutionary biology and comparative psychology.
Whether animal vocalizations have the potential to communicate information regarding ongoing external events or objects has received considerable attention over the last four decades. Such ‘functionally referential signals’ (Macedonia & Evans 1993) have been shown to occur in a range of mammals and bird species and as a consequence have helped us understand the complexities that underlie animal communication, particularly how animals process and perceive their socio‐ecological worlds. Here, we review the existing evidence for functionally referential signals in mammals according to the framework put forward in the seminal Macedonia and Evans review paper. Furthermore, we elucidate the ambiguities regarding the functionally referential framework that have become obvious over the last years. Finally, we highlight new potential areas for investigation within referential signalling. We conclude the functionally referential framework is still informative when interpreting the meaning of animal vocalizations but, based on emerging research, requires further integration with other approaches investigating animal vocal complexity to broaden its applicability.
