Special Report: Communication in animal societies

The University of Zurich’s Marta Manser and Cambridge University’s Tim Clutton-Brock outline the central role of communication in understanding variations in the social behaviour of animals.

Like humans, many animals live in social groups where they interact repeatedly with the same individuals. The nature of animal groups varies widely between species: some groups consist only of a mated pair, while others can include several hundred individuals; some are stable over long periods, others change in membership from hour to hour; some consist of members of both sexes, while in others, the sexes are in separate, segregated groups that break down in the breeding season; and some consist of related individuals that were born in the same group, while, in others, individuals of either or both sexes disperse to breed and groups consist of unrelated immigrants. These differences are associated with contrasts in the behaviour, physiology and morphology of males and females. Where females live in stable groups, for example, males commonly defend breeding access to these groups against rivals, and successful individuals breed polygynously. The intense competition for access to breeding groups generates intense competition between males and in many of these species, males have evolved to grow faster than females and are substantially larger as adults. These differences in growth have ramifying consequences in that, in many polygynous species, the two sexes commonly rely on different food resources, and males often have higher rates of mortality throughout their lifespans, as well as ageing faster and dying earlier than females. Other contrasts in the size and structure of groups have other

far-reaching consequences; for example, studies of primates show that the nature of relationships between individual group members affects their development, health, breeding success and longevity.

Since contrasts in social behaviour within and between species have

far-reaching effects on breeding success and survival, there are few ecological and evolutionary processes that are not affected by the structure of animal societies and the form of relationships between group members. As a result, understanding the causes and consequences of variation in the social behaviour of animals is of central importance in the conservation and management of animal populations as well as in understanding the course of evolution in humans and other animals.

Understanding animal communication

Social processes depend on communication between individuals, so understanding animal communication is required to identify the causes and consequences of variation in social behaviour. Communication plays a central role in attracting and retaining breeding partners, in deterring reproductive rivals, and in establishing and maintaining dominance rank. In many group-living species it is also used to ensure spatial cohesion and to co-ordinate co-operative activities, such as vigilance behaviour to prevent predation. Current research on animal communication focuses on both the mechanisms involved in the production of signals and their information content, and on their function. One body of such research examines the extent to which hormonal mechanisms affect the structure of signals and the frequency of signalling; another explores the information that signals contain – i.e. whether they simply reflect the signaller’s state or whether they incorporate information about the external environment and whether individuals can recognise the identity of signallers from their calls; and a third investigates questions about the benefits and costs of signalling – i.e. to what extent are signallers attempting to benefit receivers, and to what extent are they attempting to manipulate them to their own advantage?

The complexity of signalling systems, such as the production of a number of distinct signals, or the combinations of signals, varies greatly between species, and identifying factors that explain the communicative diversity is still in the early stages. Detailed studies of animal communication are necessary to identify both contrasts and similarities in communication systems between humans and other animals and the unique characteristics of human speech.

Animal vocal communication can be investigated in natural populations using playback experiments. Vocalisations are recorded from identified individuals in their natural habitat and are then played back to either a specific subject or a whole group of receivers to test their response. This makes it possible to explore the information content and the function of vocal signals. Playbacks can be used to investigate the hormonal states of individuals, to determine whether receivers respond differently to calls given by different individuals, to investigate the responses of receivers, and to assess their costs and benefits to both recipients and to signallers. Playback experiments can also be used to assess the knowledge of animals by manipulating the context in which they are given. Studies have thus investigated whether group members are aware of each other’s presence by playing the calls of individuals absent from the groups and determining whether they react more strongly to them than the calls of the individuals present. Similarly, playback experiments are used to prime test subjects with information and, later, to test whether this affects the responses of receivers to subsequent playbacks.

Research focus: the meerkat

The work of Manser’s research group focuses on vocal communication in the co-operatively breeding meerkat and other closely related species, including the dwarf mongoose and banded mongoose. The study population of meerkats consists of 12-15 separate groups, each with up to 30 or more group members. Groups consist of a single breeding pair that monopolises reproductions and a variable number of non-breeding helpers that have been born in the group and are usually close relatives (often offspring) of the breeding pair. Meerkats live in arid areas where vegetation is scarce and predation rates are high (approximately 25% of all individuals are predated each year). As a result they have an unusually diverse and complex system of calls. The research initially described the range of their vocalisations, identifying more than 30 discrete call types and showing that some are more variable than others.

By subsequently exploring the use of alarm calls, and by presenting the animals with models of different predators, the researchers were able to show that different alarm call types were produced for different types of predators – depending on whether they approach from the air or on the ground. In addition, the study also found that the acoustic structure changes in relation to factors that affect the immediate risk posed by predators, i.e. the distance to the predator and the speed it approaches.

A second line of work has explored the role of calls in maintaining group cohesion. Meerkats regularly give contact calls while foraging in order to maintain contact and avoid becoming separated, as well as to monitor the location of specific group members, such as the dominant female, for example. Ongoing investigations look at how calls are used to control the movements of groups.

A third line investigates the extent to which variation in call structure is heritable and to what extent the development of call structure is influenced by aspects of the ecological and social environment which affect call structure and associated variations in hormone levels. Finally, detailed knowledge on the vocal systems in meerkats is collected and utilised to compare the vocal systems of mongooses to those of other groups of mammals, and to explore the contrasts between vocal communication in animals and humans. This work shows that alarm signals incorporate different elements that provide a separate form of information about sighted predators and that these are flexibly combined in ways thought to be restricted to human language.

Generational studies

To investigate the social behaviour of animals (and of mammals, in particular) it is usually necessary to be able to recognise individuals and to know their sex and age as well as their social and genetic relationships to each other. In addition, it is important that group members are sufficiently used to the presence of observers so that their behaviour is unaffected. For both reasons, most detailed studies of social behaviour involve long-term studies that have habituated large numbers of individuals to close observation and are able to monitor the growth behaviour and survival of individuals throughout their lifespans. As well as providing a basis for research on communication and social behaviour, long-term data of this kind provide opportunities to assess the costs and benefits of contrasts in morphological and physiological traits, and explore a wide range of evolutionary processes.

The study of meerkats upon which this research was based was initiated by Tim Clutton-Brock in 1993 and now extends over five generations of meerkats, providing complete records of the life histories of more than 2,000 animals. As skin and blood samples have been routinely collected from all individuals and subjected to genetic analysis, Clutton-Brock and colleagues have been able to construct a multigenerational pedigree that can be used to measure the influence of genetics on variation in development, behaviour and breeding success. Since they provide detailed records of variation in behaviour, breeding success and survival, long-term studies also provide crucial insights into ecological processes, including the regulation of population size, the effects of climate change, and the consequences of exploitation and management.

The Kalahari Research Trust

While systematic investigations of many evolutionary and ecological processes require long-term individual-based studies, there are many obstacles to research of this kind. Perhaps the most basic need is for security of access to particular sites for relatively long periods. Unfortunately, secure, long-term access is seldom possible either on privately owned land or in national reserves and parks. To provide a secure basis for long-term, individual-based studies in the Kalahari, Clutton-Brock established the Kalahari Research Trust and the Kalahari Research Centre in 2001. The trust owns around 3,250Ha of unimproved rangeland in southern Africa and provides accommodation for up to 50 scientists as well as scientific facilities that are rarely available at field sites. It currently provides a basis for long-term studies of several mammals (including meerkats, ground squirrels and Damaraland mole-rats) as well as several birds (including pied babblers, drongos and hornbills) and involves scientists from multiple universities in South Africa, Europe and the USA.

The Kalahari Research Trust welcomes applications for further studies, especially on invertebrates and plants. Further details of the site and of the research based there are available at http://kalahari-meerkats.com/kmp/.

Department of Evolutionary Biology and Environmental Studies - 21825_V3

Marta Manser
University of Zurich

Tim Clutton-Brock
University of Cambridge
Kalahari Research Centre