Lemurs Groom High-Ranking Females In Order To Gain Thermoregulatory Benefits

Among gregarious animals, it is well-established that socially dominant individuals are able to use their status to leverage resources, resulting in better long-term survival relative to others. In other words, socially dominant individuals enjoy rank-related benefits.

Credit: Timothy Eppley

In colder climates, dominant animals benefit from having multiple social partners to huddle with to keep warm. Huddling, also known as social thermoregulation, is when partners maintain physical contact with one another in a curled position in order to conserve energy. This is a common strategy for coping with thermal stress, as it provides higher and more constant body temperatures than resting alone, thus it is used by a variety of bird and mammal species. For example, emperor penguins increase huddling behavior under low ambient temperatures, enabling them to save energy during the harsh Antarctic winter. Behavioral thermoregulation can even prevent death under extremely low temperatures, and so huddling behavior may have evolved among social animals because of its potential fitness benefits.

In primates, rank-related benefit hypotheses have mostly been tested in large and gregarious social species, for example, capuchins, baboons, macaques, and chimpanzees. Among lemurs, studies on social dynamics have also focused on more gregarious species, for example, brown lemurs and ring-tailed lemurs. In these species, individuals have many social partners to choose from. The notion of rank-related benefits, however, has been somewhat overlooked among members of small, family-based social groups, in which there exist fewer social partners to choose among. Because of this, the authors decided to study the southern bamboo lemurs from Madagascar as they fit this atypical description.

Over the course of a year, the authors lived in a fragmented littoral forest-swamp matrix along the southeast coast of Madagascar, collected daily behavioral data on highly cryptic bamboo lemurs. These lemurs are medium-sized strepsirrhine primates (ca. 1.1 kg) that subsist on a mostly leaf-based diet. Members of their small social groups (average 5.6 individuals) are in mostly constant daily contact.

In order to determine whether members of small social groups gain rank-related benefits, the authors first established a dominance hierarchy through a network-based analysis of win-loss interactions. Unlike most mammals, many lemur species are known to be female-dominant, though this is not always the rule and so it was necessary to establish which sex (if any) was dominant. They showed that adult females maintained social dominance within their groups, often by winning agonistic conflicts, initiating travel direction, and by controlling access to preferred resources. Despite this, males were not peripheral within the group.

To address whether dominant individuals gained rank-related benefits, the authors explored how social dynamics may permit access to resting huddles, which provide a physiological benefit, that is, staying warm when temperatures were low. They found that lower temperatures, especially during shorter resting bouts, increased the likelihood of huddling. Grooming between partners with a high discrepancy in rank increased huddling. Additionally, huddling increased during the reproductive season, potentially offering greater opportunity for males to gain favor with sexually receptive females. Huddling also increased when newborns were present, providing essential thermal maintenance and potential antipredator protection to infants. Together, these results suggest that even in small social groups, dominant females gain rank-related benefits by controlling access to huddles, i.e. the intrinsic benefits of social thermoregulation.

Interestingly, affiliative tendency could not explain dyadic huddling choices. Low-ranking individuals were more likely to huddle after grooming a high ranking female; thus, both partners accrued benefits from grooming and huddling. In contrast, when high ranking individuals groomed each other, their likelihood of huddling did not increase. A function of grooming is to increase the loft of the fur, that is, the pelt depth, to improve thermal insulation; therefore, mutual grooming within 60 min preceding or following huddling serves both a functional and a social purpose beneficial to both partners. Thus, grooming appeared to be integral for the occurrence of huddling during a resting bout. These results highlight that the benefits of social living are not enjoyed equally by all members of small social groups: female bamboo lemurs exert social dominance over males to control access to huddles, although further investigation into the costs and benefits of other social behaviors are warranted.

Additionally, the authors tested two predictions related to female reproductive strategies: mate assessment and infant protection. Sexually receptive females, and later those with infants, increased their rates of huddling relative to others. This behavioral adjustment provided not only thermoregulatory benefits to huddling partners and offspring but also protection of the infant from potential predators. Females and their offspring, therefore, gained rank-related benefits from allowing lower-ranked males to participate in thermoregulatory huddles. These results support the hypothesis that females benefit from their higher social dominance and have greater reproductive success because of it.

These findings are described in the article entitled Climatic, social and reproductive influences on behavioural thermoregulation in a female-dominated lemur, recently published in the journal Animal Behaviour. This work was conducted by Timothy Eppley from University of Hamburg and San Diego Zoo Global, Julia Watzek from Georgia State University, Katie Hall from the Chicago Zoological Society, and Giuseppe Donati from Oxford Brookes University.

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