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

Abstract

BackgroundEvolutionary 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 ResultsDaily 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.DiscussionWe 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.

Primate energy expenditure and life history

“…24). An FQ of 0.90 was used for diademed sifakas following values for other strepsirrhines (17). See SI Text, section 1 for additional details.…”

Energy (Im-)Balance in Frugivorous Lemurs in Southern Madagascar: A Preliminary Study in Lemur catta and Eulemur rufifrons × collaris

“…There is no significant sex difference in body mass across the populations studied in the forest areas investigated here (ring-tailed lemurs: 2.3 ± 0.3 kg; brown lemurs: 1.9 ± 0.2 kg; [Simmen et al, 2010]). Ring-tailed lemurs at Berenty defend relatively small, well-defined home ranges whereas groups of brown lemurs forage over comparatively larger areas and are less territorial Pinkus et al, 2006;Tanaka, 2007;Simmen, pers.…”

“…The seasonal increase in body fat was reported for the first time in semi-free ranging and wild male squirrel monkeys in relation to rainfall cycles and sexual selection [Du Mond and Hutchinson, 1967]. A high body fat content following periods of high food supply has been reported in Bornean orangutans (Pongo pygmaeus pygmaeus) living in unpredictable habitats and some strepsirrhine species, especially among the small heterotherm cheirogaleids that enter torpid states during the dry season of Madagascar [Knott, 1998;Fietz and Dausmann, 2006;Génin, 2008;Simmen et al, 2010]. Humans also accumulate fat, a characteristic that was undoubtedly present in early hominins exposed to highly seasonal or volatile environments [Wells, 2012].…”

“…On an evolutionary time scale, it would therefore make sense that a range of lemurs has evolved a combination of energy-saving mechanisms, behavioral flexibility, and opportunistic feed-ing strategies. In this respect, a study of body composition and metabolism in sympatric ring-tailed lemurs (Lemur catta) and "brown lemurs" (Eulemur rufifrons × collaris) living in the subarid south of Madagascar (Berenty Reserve) showed that these seasonal breeding species had large amounts of body fat following the period of greatest food abundance [Simmen et al, 2010], consistent with the hypothesis of a well-defined fattening period just prior to the mating season and the long dry season [see also LaFleur, 2012].…”

“…In particular, we analyze whether energy consumption varies according to the timing of the reproductive cycle and is compatible with a fattening process. In order to identify possible periods of positive and negative energy balance, we estimate the metabolizable energy intake in different seasons and contrast these estimates with the total energy expenditure (TEE) measured previously with doubly labeled water at the same study site in both species (Berenty Reserve [Simmen et al, 2010]). Finally, we discuss whether the cathemeral behavior (i.e., significant nocturnal and diurnal activity) reported for these lemurs, one characteristic of the so-called "lemur syndrome" [Wright, 1999], may be a consequence of an insufficient energy intake during daytime or the low ability of these species to digest plant fibers [Engqvist and Richard, 1991;Donati et al, 2007Donati et al, , 2009Donati et al, , 2013LaFleur et al, 2014].…”