Chapter Six - Vocal Complexity in Meerkats and Other Mongoose Species

PORCINE MALIGNANT HYPERTHERMIA, OXIDATIVE METABOLISM AND HALOTHANE

Simple SummaryThe social complexity hypothesis (SCH) for communication predicts that species with complex social systems exhibit complex communication systems. Testing the SHC in a broad range of species can contribute to a better understanding of human evolution because a co-evolutionary runaway process between social and vocal complexity may have shaped human language. Here we compare patterns of vocal complexity between the two species of African elephants: the savanna elephant exhibiting a complex social organization and the forest elephant exhibiting a simpler social organization. We review the existing literature and present novel insights into the vocal communication system of the elusive forest elephant, along with a first direct comparison with savanna elephants. Our findings suggest that the African elephants may contradict the SCH, as well as other factors potentially shaping patterns of vocal complexity across species. A better understanding of vocal complexity in the two species of African elephants will depend on continuing advancements in remote data collection technologies to overcome the challenges of observing forest elephants in their dense rainforest habitat, as well as the availability of comparable data quantifying both structural and contextual variability in the vocal production of both species of African elephants.The social complexity hypothesis (SCH) for communication states that the range and frequency of social interactions drive the evolution of complex communication systems. Surprisingly, few studies have empirically tested the SHC for vocal communication systems. Filling this gap is important because a co-evolutionary runaway process between social and vocal complexity may have shaped the most intricate communication system, human language. We here propose the African elephant Loxodonta spec. as an excellent study system to investigate the relationships between social and vocal complexity. We review how the distinct differences in social complexity between the two species of African elephants, the forest elephant L. cyclotis and the savanna elephant L. africana, relate to repertoire size and structure, as well as complex communication skills in the two species, such as call combination or intentional formant modulation including the trunk. Our findings suggest that Loxodonta may contradict the SCH, as well as other factors put forth to explain patterns of vocal complexity across species. We propose that life history traits, a factor that has gained little attention as a driver of vocal complexity, and the extensive parental care associated with a uniquely low and slow reproductive rate, may have led to the emergence of pronounced vocal complexity in the forest elephant despite their less complex social system compared to the savanna elephant. Conclusions must be drawn cautiously, however. A better understanding of vocal complexity in the genus Loxodonta will depend on continuing advancements in remote data collection technologies to overcome the challenges of observing forest elephants in their dense rainforest habitat, as well as the availability of directly comparable data and methods, quantifying both structural and contextual variability in the production of rumbles and other vocalizations in both species of African elephants.

Although communicative complexity is often predicted to correlate with social complexity in animal societies, few studies have employed large-scale comparative analyses to test whether socially complex species have more complex systems of communication. I tested this social complexity hypothesis in birds (Class: Aves) due to the large amount of natural history information available for both vocal and social systems in these species. To do so, I marshalled data from primary and secondary records of avian vocal repertoires ( n = 253), and for each of the species in the dataset I recorded the reported repertoire size and associated species information. Using phylogenetic comparative methods, I found that cooperative breeding was a strong and repeatable predictor of vocal repertoire size, while other social variables, i.e. group size and group stability, had little or no influence on repertoire size. Importantly, repertoire sizes expanded concurrently with the evolution of cooperative breeding, suggesting a direct link between these two traits. Cooperatively breeding species had devoted significantly more of their repertoire to contact calls and alarm calls. Overall, these results therefore lend support to the hypothesis that social complexity via behavioural coordination leads to increases in vocal complexity.

Although communicative complexity is often predicted to correlate with social complexity in animal societies, few studies have employed large-scale comparative analyses to test whether socially complex species have more complex systems of communication. I tested this social complexity hypothesis in birds (Class: Aves) using the large amount of natural history information that describes both vocal repertoire and social system in these species. To do so, I marshalled data from primary and secondary records of avian vocal repertoires (n = 253), and for each of the species in the dataset I recorded the reported repertoire size and associated species information. Using phylogenetic comparative methods, I found that cooperative breeding was a strong and repeatable predictor of vocal repertoire size, while other social variables, e.g. group size and group stability, had little or no influence on repertoire size. Importantly, repertoire sizes expanded concurrently with the evolution of cooperative breeding, suggesting a direct link between these two traits. Cooperatively breeding species devoted significantly more of their repertoire to contact calls and alarm calls. Overall, these results therefore lend support to the hypothesis that social complexity via behavioural coordination leads to increases in vocal complexity.

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.

To make adaptive behavioural decisions, animals must acquire and process information from their natural and social environment. Reducing uncertainty regarding the actions and goals of conspecifics is especially important for group‐living animals.Bats are often highly gregarious and use versatile social vocalizations to mediate social interactions. These social vocalizations encode a substantial amount of ecologically relevant information, such as individual identity, sex and kin. Decoding this information enables receivers to make informed decisions on resource allocation, mate choice, territorial defence and cooperation. Erroneous decisions on such crucial aspects of bats’ social behaviour can be costly due to reduced reproductive success or survival.Increasingly complex social interactions require social vocalizations encoding more information which, in turn, could facilitate the evolution of even more complex social interactions. Evidence for the positive correlation of social and vocal complexity is available for several taxa but is currently very limited for bats.We conducted a phylogenetic comparative analysis to link the information content encoded in bats’ social vocalizations to the complexity of their social lives, that is the level of uncertainty associated with assessing individual identity. We focused on three different vocalization types encoding individual signatures (pup isolation calls, adult contact calls and male‐specific vocalizations). Information content in bit (i.e. the number of binary decisions necessary to discriminate among N individuals) was used as an estimate of vocal complexity; relevant social group size (i.e. the number of conspecifics whose identity a receiver could confuse) was used as an estimate of social complexity.Our phylogenetic comparative analysis detected a positive relationship between the information content of vocalizations and the respective relevant social group size. This relationship suggests a positive feedback loop between social and vocal complexity for bat vocalizations and highlights the importance of vocal information for negotiating fitness‐relevant social decisions of bats.In conclusion, our work suggests that social complexity drives vocal complexity in bats. Future studies on other hitherto understudied taxa are necessary to establish a comprehensive theory on the multi‐faceted co‐evolution of sociality and communication in the animal kingdom.A freePlain Language Summarycan be found within the Supporting Information of this article.

There is considerable variation in systems of vocal communication in animals. One hypothesis to explain this variation is that the complexity of the social group influences the groups vocal complexity. This social complexity hypothesis for communication is also central to recent arguments for human language origins, but experimental tests of the hypothesis are lacking. This study investigated whether group size, a fundamental component of social complexity, influenced the complexity of the chickadee call, a call system functioning in social organization of Carolina chickadees, Poecile carolinensis. This call system has been studied in chickadees and related species, and is structurally and functionally rich in its note composition. Complexity of calls was measured using uncertainty (diversity) related to note composition, based on Shannon’s mathematical theory of communication. In unmanipulated field settings, calls of individuals in larger groups had greater complexity (more information) than calls of individuals in smaller groups. In aviary settings manipulating group size, individuals in larger groups used calls with greater complexity than individuals in smaller groups. These results indicate that social complexity can influence communicative complexity in this species.

There is no doubt that different factors determine the evolutionary trajectory of a species' communication abilities. Beyond habitat, social life is likely a selection pressure. The hypothesis positing that living in a complex social system requires complex communication skills has gained ground. However, the measures used classically to tackle this question (i.e. number of call types and group size) fail to capture some of the subtleties of the evolution of communication systems. Integrative approaches comparing closely related species to highlight the possible relationship between the characteristics of their social systems, their ecological niche and associated vocal communication systems are required to further our understanding of this evolutionary puzzle. We first addressed this topic in two sympatric guenons, Diana monkeys and Campbell’s monkeys. Interspecies competition, and the niche specialisations this creates, appeared to be a key evolutionary driver of their repertoires. While most of their vocal units were shared, we found a diversification of alarm calls and socially meaningful vocal combinations, as well as a differential use of inconspicuous (less detectable) call structures. This was linked to differences in group size and degree of exposition to predators. Secondly, we compared the acoustic structures in macaques belonging to four species with contrasting social styles. We found that tolerant (Tonkean and crested) macaques displayed higher levels of vocal diversity (number of vocal units) and flexibility (degree of gradation) than intolerant (Japanese and rhesus) macaques in agonistic and affiliative (but not neutral) contexts. Lastly, because the core of communication is represented not only by what is expressed by an isolated caller, but also by the way vocal interactions are structured, we explored ‘conversational rules’ in apes. We found no relationship between classical social (group size, interaction rates) and vocal (repertoire size, call rates) complexity metrics. However, close call interaction patterns differed in line with the nature of societies. Orang-utan, the most solitary species, preferentially used repeated and isolated calls apparently outside of any vocal interactions. Chimpanzee, the most competitive species displayed a high proportion of overlapping vocalisations. Vocal turn-taking predominated in the most tolerant species (bonobo and gorilla). Even if primate vocal repertoires change slowly over evolutionary time, making them good phylogenetic indicators, socio-ecological niches may induce considerable local divergence at different levels: vocal repertoire composition, acoustic structure and contextual use of calls, and vocal interaction patterns.

A growing body of evidence suggests the capacity for animals to combine calls into larger communicative structures is more common than previously assumed. Despite its cross-taxa prevalence, little is known regarding the evolutionary pressures driving such combinatorial abilities. One dominant hypothesis posits that social complexity and vocal complexity are linked, with changes in social structuring (e.g., group size) driving the emergence of ever-more complex vocal abilities, such as call sequencing. In this paper, we tested this hypothesis through investigating combinatoriality in the vocal system of the highly social chimpanzee. Specifically, we predicted combinatoriality to be more common in socially-driven contexts and in females and lower-ranked males (socially challenging contexts and socially challenged individuals respectively). Firstly, through applying methods from computational linguistics (i.e., collocation analyses), we built an objective repertoire of combinatorial structures in this species. Second, we investigated what potential factors influenced call combination production. We show that combinatoriality is predominant in 1) social contexts vs. non-social contexts, 2) females vs. males, and 3) negatively correlates with male rank. Together, these results suggest one function of combinatoriality in chimpanzees may be to help individuals navigate their dynamic social world. More generally, we argue these findings provide support for the hypothesized link between social and vocal complexity and can provide insight into the evolution of our own highly combinatorial communication system, language.

The endemic lemurs of Madagascar (Lemuriformes: Primates) exhibit great social and communicative diversity. Given their independent evolutionary history, lemurs provide an excellent opportunity to identify fundamental principles in the coevolution of social and communicative traits. We conducted comparative phylogenetic analyses to examine patterns of interspecific variation among measures of social complexity and repertoire sizes in the vocal, olfactory and visual modality, while controlling for environmental factors such as habitat and number of sympatric species. We also examined potential trade-offs in signal evolution as well as coevolution between body mass or brain size and communicative complexity. Repertoire sizes in the vocal, olfactory and visual modality correlated positively with group size, but not with environmental factors. Evolutionary changes in social complexity presumably antedated corresponding changes in communicative complexity. There was no trade-off in the evolution of signals in different modalities and neither body mass nor brain size correlated with any repertoire size. Hence, communicative complexity coevolved with social complexity across different modalities, possibly to service social relationships flexibly and effectively in pair- and group-living species. Our analyses shed light on the requirements and adaptive possibilities in the coevolution of core elements of social organization and social structure in a basal primate lineage.This article is part of the theme issue ‘Cognition, communication and social bonds in primates’.

Communicative complexity relates to social complexity, as individuals in more complex social systems either use more signals or more complex signals than individuals living in less complex ones. Taking the individual group member's perspective, here we examine communicative complexity in relation to social complexity, which arises from two components of social systems: social structure and social organization. We review the concepts of social relationships and social complexity and evaluate their implications for communicative and cognitive complexity using examples from primate species. We focus on spider monkeys (Ateles geoffroyi), as their social organization is characterized by flexibility in grouping dynamics and they use a variety of communicative signals. We conclude that no simple relationship exists among social complexity, communicative complexity and cognitive complexity, with social complexity not necessarily implying cognitive complexity, and communicative and cognitive complexity being independently linked to social complexity. To better understand the commonly implied link between social complexity and cognitive complexity it is crucial to recognize the complementary role of communicative complexity. A more elaborated communicative toolkit provides the needed flexibility to deal with dynamic and multifaceted social relationships and high variation in fission-fusion dynamics. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Duality of patterning, language’s ability to combine sounds on two levels, phonology and syntax, is considered one of human language’s defining features, yet relatively little is known about its origins. One way to investigate this is to take a comparative approach, contrasting combinatoriality in animal vocal communication systems with phonology and syntax in human language. In my thesis, I took a comparative approach to the evolution of combinatoriality, carrying out both theoretical and empirical research. In the theoretical domain, I identified some prevalent misunderstandings in research on the emergence of combinatoriality that have propagated across disciplines. To address these misconceptions, I re-analysed existing examples of animal call combinations implementing insights from linguistics. Specifically, I showed that syntax-like combinations are more widespread in animal communication than phonology-like sequences, which, combined with the absence of phonology in some human languages, suggested that syntax may have evolved before phonology. Building on this theoretical work, I empirically explored call combinations in two species of social mongooses. I first investigated social call combinations in meerkats (Suricata suricatta), demonstrating that call combinations represented a non-negligible component of the meerkat vocal communication system and could be used flexibly across various social contexts. Furthermore, I discussed a variety of mechanisms by which these combinations could be produced. Second, I considered call combinations in predation contexts. In particular, I investigated dwarf mongoose (Helogale parvula) alarm call combinations. To do so, I documented their alarm call repertoire, showing that they emitted multiple different alarm calls, of which some were risk related and some were more predator specific. The function of the last, rarely produced, alarm calls remained ambiguous. I then demonstrated that the dwarf mongoose “type 3” (hereafter T3) alarm call represented a combination of their predator specific aerial and terrestrial alarm calls. Observational and experimental data suggested that T3 was a general alarm call with a possible meaning akin to “(aerial or terrestrial) predator”. From a linguistic perspective this combination could be interpreted as a rudimentary form of disjunction, with disjunction being a form of syntax that combines two or more units in which at least one of the propositions is true, but not necessarily both (e.g. “he is right or wrong”). To my knowledge, this would represent the first evidence for this type of combination outside of human language. The data obtained in this thesis showed that social mongooses used call combinations in all facets of their communication, from social to anti-predator situations, and indicated that both of these contexts may play a role in the evolution of combinatoriality. Furthermore, some of the combinations described in this thesis seemed to be the result of simple mechanisms far removed from the combinatoriality seen in human language, whereas others appeared to be rudimentary forms of syntax. Nevertheless, studying combinatoriality across several species’ communication systems can help not only identify the similarities and differences between animal call combinations and linguistic forms of combinatoriality but also, ultimately, help elucidate the impact of different factors, both social and environmental, on the evolution of combinatoriality.

Humpback whales (Megaptera novaeangliae) occur in all major oceans. Given this worldwide distribution, and since they tend to migrate along coastlines, they are one of the best known of the baleen whales. Humpbacks are relatively easy to find and easy to observe. This, along with their surface behaviors and attraction to vessels, makes them popular with whale-watching businesses. In the scientific world, their song and behaviors have been studied since the 1970s, producing hundreds of scientific papers. Despite this, there are still many unsolved mysteries. Why do humpbacks sing (Chaps. 8 and 11), how do they locate their prey (Chap. 5), and how do they navigate when migrating (Chap. 4)? In this chapter, we focus on the mysteries of their social communication. Communication and social complexities often go hand in hand. Animals with more complex social structures tend to have more complex vocal repertoires, perhaps peaking, with humans. Within the baleen whales, humpback whales are considered an exception. Present knowledge indicates that humpbacks have a relatively complex acoustic repertoire but work on their breeding social system has considered them to be socially simple. Animals regarded as having a simple social structure tend to have small group sizes and a lack of repeat associations between individuals over time. Humpback whales meet this criteria in that they form temporary associations between a small number of individuals, and these associations are not repeated over time, leading to the conclusion that their social structure is simple and individually based. Why then do humpbacks have what could be considered a complex acoustic repertoire? Is the conclusion that they possess a simple social structure supported by best available scientific evidence? This chapter illustrates that humpbacks may in fact have a complex social structure, with complexity defined differently than traditional definitions of complexity (number in a group, number of repeat associations). Rather than forming large permanent groups with repeated interactions between individuals, humpback whales during the breeding season form networks that encompass multiple groups. These groups are frequently changing membership, and animals are constantly moving into, and out of this network. Whales must therefore continuously assess, and respond to, a changing social environment. Given that humpbacks likely rely on acoustic communication to manage these interactions, this added layer of social complexity may go toward explaining their large and varied vocal repertoire. Perhaps communicative and social complexities do go hand in hand for the humpback whale.KeywordsBaleen whaleBreeding behaviorCommunication repertoireSocial complexitySocial behaviorVocal repertoireVocal complexity

Vocal communication is widespread in animals, with vocal repertoires of varying complexity. The social complexity hypothesis predicts that species may need high vocal complexity to deal with complex social organization (e.g. have a variety of different interindividual relations). We quantified the vocal complexity of two geographically distant captive colonies of rooks, a corvid species with complex social organization and cognitive performances, but understudied vocal abilities. We quantified the diversity and gradation of their repertoire, as well as the inter-individual similarity at the vocal unit level. We found that males produced call units with lower diversity and gradation than females, while song units did not differ between sexes. Surprisingly, while females produced highly similar call repertoires, even between colonies, each individual male produced almost completely different call repertoires from any other individual. These findings question the way male rooks communicate with their social partners. We suggest that each male may actively seek to remain vocally distinct, which could be an asset in their frequently changing social environment. We conclude that inter-individual similarity, an understudied aspect of vocal repertoires, should also be considered as a measure of vocal complexity.

Calling for help: dwarf mongoose recruitment calls inform receivers about context and elicit disparate responses