In honor of Science Online, which begins on Thursday night, I will be writing about lemurs this week. Why lemurs? Because on Friday morning, as a part of Science Online, I will be taking a tour of the Duke Lemur Center.

ringtailed lemur.jpgIt is common among animals - especially primates - to orient their gaze preferentially towards other individuals, as well as to follow the gaze of others. Lots of attention has been paid to gaze-following, in part because the ability to recognize and orient to the behavior of others is missing or impaired in various developmental disorders, such as autism. It is well known that, at least in highly-controlled laboratory studies, human and nonhuman primates pay special attention to the faces and eyes of their conspecifics, and evidence has been found for gaze-following in other animals as well, ranging from horses to tortoises. The problem is that different experiments in different laboratories yield inconsistent results, partly as a result of different measurement techniques, and partly as a result of the different ways that researchers have operationalized the term gaze-following itself. In addition, there are contextual variables that need to be taken into account in order to fully understand the way that gaze-following works. For example, gaze-following in rhesus macaques is dependent upon the social status of the observer as well as the observed individual. Some studies of gaze-following in non-human animals have used humans as the attentional cue, which clearly places the animal in a non-natural social context.

ResearchBlogging.orgStephen V. Shepherd and Michael L. Platt of the Departments of Neurobiology and Cognitive Neuroscience, respectively, at Duke University in Durham, North Carolina think that they have a solution to the methodological problems that have riddled the study of gaze-following in animals. They decided to investigate social orienting in ringtailed lemurs (Lemur catta) continuously in a semi-natural enriched environment. Instead of subjecting each of a group of lemurs to a set of experimental tests using human social cues (as would fit well within the established methodology), they simply observed lemurs behaving naturally with each other. But how could they record that kind of data in a non-intrusive way?

Wireless infrared optical gaze-tracking dual-camera backpacks.

Two adult male ringtailed lemurs from the Duke Lemur Center were outfitted with the packs (males were chosen to avoid potential complications with pregnancy and nursing). Despite the fact that the packs were approximately one quarter the body-weight of the lemurs, they allowed them full range of motion and did not adversely impact their locomotion or social interaction. The two lemurs, Licinius and Aracus, lived in quite different social environments. Licinius shared his enclosure with one other male lemur named Maurice. Aracus shared his enclosure with up to twelve other lemurs: three adult females, four juveniles, 4 infants, and one additional adult male.

The wireless infrared optical gaze-tracking dual-camera backpack.

One camera (a) recorded the position of the reflection of the eye in a mirror (b), while a second camera (c) recorded the scene from the point-of-view of the individual. The wireless transmitter (d) was housed in a backpack. The two subjects habituated to the presence of the apparatus during three one-hour sessions each week, for four to six weeks. During the habituation phase, the human experimenters determined that there were no obvious behavioral changes due to the presence of the apparatus. The testing phase consisted of five one-hour recording sessions (2 hours with Licinius and 3 hours with Aracus).

The first important finding is a bit obvious: ringtailed lemurs show a preference for looking at other lemurs. They also prefer looking at humans, food, and stationary environmental features. Moreover, they preferred looking at agents (humans and lemurs), rather than objects (food and other objects), and both social agents and food items were gazed at more often than other objects in the environment.

Lemur orienting preferences to humans, lemurs, food, and environmental features.

Given the preference for looking at other lemurs, the next question Shepherd and Platt addressed was whether the attention of Licinius and Aracus may have actually been forward from the body and heads of the other lemurs. That is, were they following the eye-gaze and/or body orientation of the other lemurs? It was important to use eye-gaze as well as body-orientation since lemurs have relatively low visual acuity, making it unlikely that they could successfully use eye-gaze alone without the cues provided by body orientation as well. They found that the lemurs spent a significant amount of time orienting towards the gaze of other individuals. They ruled out the possibility that both lemurs were independently orienting towards the same external event; instead, it was clear that the second lemur was engaging in social gaze-following.

Taken together, these data convincingly indicate that ringtailed lemurs use social cues to co-orient during social situations, and can use the gaze of other lemurs to become aware of significant items or events in their environment. This is in contrast to previous studies that reported that ringtailed lemurs do not follow gaze. Other studies had theorized that since lemur visual acuity is lower than other primates, they rely primarily or exclusively on olfactory cues. Instead, it appears as if the wireless infrared optical gaze-tracking dual-camera backpacks have provided a better, more reliable method of investigating this question. Lemurs do, indeed, socially co-orient.

In addition, this study provides a tantalizing possibility: since lemurs (along with other prosimians) split from other primates around 60 million years ago, and retain many of their ancestral traits, it is possible that visual co-orientation in social interactions has played a critical role in the evolution of primate social cognition. Further, given evidence of gaze-following in animals as diverse as goats, dolphins, and even some reptiles, either gaze-following emerged extremely early in evolution, or gaze-following is strongly adaptive for social group-living species and has emerged several times independently throughout evolution.

Is gaze-following a case of early emergence or of convergent evolution?

Shepherd, S., & Platt, M. (2007). Spontaneous social orienting and gaze following in ringtailed lemurs (Lemur catta) Animal Cognition, 11 (1), 13-20 DOI: 10.1007/s10071-007-0083-6