Total Energy Expenditure and Body Composition in Two Free-Living Sympatric Lemurs

Background

Evolutionary theories that account for the unusual socio-ecological traits and life history features of group-living prosimians, compared with other primates, predict behavioral and physiological mechanisms to conserve energy. Low energy output and possible fattening mechanisms are expected, as either an adaptive response to drastic seasonal fluctuations of food supplies in Madagascar, or persisting traits from previously nocturnal hypometabolic ancestors. Free ranging ring-tailed lemurs (Lemur catta) and brown lemurs (Eulemur sp.) of southern Madagascar have different socio-ecological characteristics which allow a test of these theories: Both gregarious primates have a phytophagous diet but different circadian activity rhythms, degree of arboreality, social systems, and slightly different body size.

Methodology and Results

Daily total energy expenditure and body composition were measured in the field with the doubly labeled water procedure. High body fat content was observed at the end of the rainy season, which supports the notion that individuals need to attain a sufficient physical condition prior to the long dry season. However, ring-tailed lemurs exhibited lower water flux rates and energy expenditure than brown lemurs after controlling for body mass differences. The difference was interpreted to reflect higher efficiency for coping with seasonally low quality foods and water scarcity. Daily energy expenditure of both species was much less than the field metabolic rates predicted by various scaling relationships found across mammals.

Discussion

We argue that low energy output in these species is mainly accounted for by low basal metabolic rate and reflects adaptation to harsh, unpredictable environments. The absence of observed sex differences in body weight, fat content, and daily energy expenditure converge with earlier investigations of physical activity levels in ring-tailed lemurs to suggest the absence of a relationship between energy constraints and the evolution of female dominance over males among lemurs. Nevertheless, additional seasonal data are required to provide a definitive conclusion.     

A scoring system for coat and tail condition in ringtailed lemurs,Lemur catta

Coat condition can be influenced by a wide variety of disorders and thus provides a useful tool for noninvasive health and welfare assessments in wild and captive animals. Using Lemur catta as an exemplar, we offer a 6‐step scoring system for coat and tail condition, ranging from perfectly fluffy to half or more of body and tail being hairless. The categories are described in detail and illustrated with sample pictures from a wild population in Berenty Reserve, Madagascar. Furthermore, we elaborate on intermediate conditions and discoloration of fur. Coat condition scoring allows the comparison between years, seasons, and the effect of toxin, disease or stress. Although this system was developed for wild L. catta, we believe it can also be of value for other species. We recommend scoring coat condition in healthy wild mammal populations to give a baseline on yearly and seasonal variations vs. deteriorating health conditions or pathology. Am. J. Primatol. 71:183–190, 2009. © 2009 Wiley‐Liss, Inc.     

Genetic population structure of endangered ring‐tailed lemurs (Lemur catta) from nine sites in southern Madagascar

Madagascar's ring‐tailed lemurs (Lemur catta) are experiencing rapid population declines due to ongoing habitat loss and fragmentation, as well as increasing exploitation for bushmeat and the illegal pet trade. Despite being the focus of extensive and ongoing behavioral studies, there is comparatively little known about the genetic population structuring of the species. Here, we present the most comprehensive population genetic analysis of ring‐tailed lemurs to date from across their likely remaining geographic range. We assessed levels of genetic diversity and population genetic structure using multilocus genotypes for 106 adult individuals from nine geographically representative localities. Population structure and F_ST analyses revealed moderate genetic differentiation with localities being geographically partitioned into northern, southern, western and also potentially central clusters. Overall genetic diversity, in terms of allelic richness and observed heterozygosity, was high in the species (AR = 4.74, H_O = 0.811). In fact, it is the highest among all published lemur estimates to date. While these results are encouraging, ring‐tailed lemurs are currently affected by ongoing habitat fragmentation and occur at lower densities in poorer quality habitats. The effects of continued isolation and fragmentation, coupled with climate‐driven environmental instability, will therefore likely impede the long‐term viability of the species.     

Tamarind tree seed dispersal by ring-tailed lemurs

In Madagascar, the gallery forests of the south are among the most endangered. Tamarind trees (Tamarindus indica) dominate these riverine forests and are a keystone food resource for ring-tailed lemurs (Lemur catta). At Berenty Reserve, the presence of tamarind trees is declining, and there is little recruitment of young trees. Because mature tamarinds inhibit growth under their crowns, seeds must be dispersed away from adult trees if tree recruitment is to occur. Ring-tailed lemurs are likely seed dispersers; however, because they spend much of their feeding, siesta, and sleeping time in tamarinds, they may defecate a majority of the tamarind seeds under tamarind trees. To determine whether they disperse tamarind seeds away from overhanging tamarind tree crowns, we observed two troops for 10 days each, noted the locations of feeding and defecation, and collected seeds from feces and fruit for germination. We also collected additional data on tamarind seedling recruitment under natural conditions, in which seedling germination was abundant after extensive rain, including under the canopy. However, seedling survival to 1 year was lower when growing under mature tamarind tree crowns than when growing away from an overhanging crown. Despite low fruit abundance averaging two fruits/m³ in tamarind crowns, lemurs fed on tamarind fruit for 32% of their feeding samples. Daily path lengths averaged 1,266 m, and lemurs deposited seeds throughout their ranges. Fifty-eight percent of the 417 recorded lemur defecations were on the ground away from overhanging tamarind tree crowns. Tamarind seeds collected from both fruit and feces germinated. Because lemurs deposited viable seeds on the ground away from overhanging mature tamarind tree crowns, we conclude that ring-tailed lemurs provide tamarind tree seed dispersal services.     

Ring-Tailed Lemur Home Ranges Correlate with Food Abundance and Nutritional Content at a Time of Environmental Stress

In order to determine whether ring-tailed lemurs (Lemur catta) adapt their ranging and select an optimal diet at a time of food shortage, we observed two adjacent troops in Berenty Reserve, Madagascar for over 250 h. The troops, created by a recent fission, ranged through closed canopy gallery forest next to a river and open forest away from the river. We conducted the study in September–October, 2000, normally a time of seasonally low resource availability, which was intensified by damage from a previous windstorm and recent drought. To examine the impact of environmental stress, we mapped their ranging patterns, intertroop encounters, feeding patches, siesta trees, and sleeping trees. We then correlated their ranging and feeding behavior with nutritional analyses of leaves and fruit from tamarind trees located in different parts of their ranges. One of the troops, D1A, ranged farther into open forest than previously. However, the range for troop D1B and the closed canopy portion of D1A's range were located in traditional positions for historical troops D and E. Both troops ate significantly more mature leaves from the tamarind trees in the closed canopy forest, where the leaves had significantly higher nutritional content (water and protein) than that of open forest samples. They fed on tamarind fruit significantly more often in the open forest away from the river, where it was more abundant. The lemurs selected a diet that maximized leaf water and protein and ranged where fruit was most abundant but at high energetic costs for troop D1A.     

Demography of Lemur catta at Berenty Reserve,Madagascar: Effects of Troop Size,Habitat and Rainfall

We censused Lemur catta within a 1 km² study area at Berenty Reserve, Madagascar, during the September–October birth season for 19 years between 1963 and 2000, a total of 290 troop counts (266 with age and sex). The non-infant population was 155 in 1972–5, fell to 105 in 1985, and rose to a maximum of 282 in 1997, while troops increased from 12 in 1972–1985 up to 25 in 1998–2000. Local density varies between habitat types from 1 per ha to ca. 6 per ha. Troops fission at ca. 15–25 individuals, or 6–10 females. Adult sex ratio has no apparent correlation with fissions, birth rate or survival. Birth rate falls steeply with number of adult females, from 80–100% in 2-female troops to about 50% in 8–10 female troops. The penalty for large troop size is greater in the dense, rich areas, but nonetheless troops there are also larger. One-year-survival does not vary with troop size, and is lower in the sparse, dry zone. Troop size is too large for optimal birth rate, but fissioning to much lower size might make troops too small for optimal adult survival, given the intense intertroop competition. This reflects Sibley's (1983) conjecture that troop sizes may not reach stable optima. Rainfall per lemur-year (beginning Oct 1) varied from 265 to 894 mm. Drought followed by rain can eliminate >90% of a cohort, especially in the dryest zone. Possibly this results from fruit failure in years following drought. It is unknown whether food supplementation of some Berenty troops is dangerous for the forest, or helpful for an isolated and vulnerable ring-tailed lemur population.