The development of sex differences in ring-tailed lemur feeding ecology

Abstract

Sex differences in feeding ecology may develop in response to fluctuations in physiological costs to females over their reproductive cycles, or to sexual size dimorphism, or function to minimize feeding competition within a group via resource partitioning. For most mammal species, it is unknown how these factors contribute to sex differences in feeding, or how the development of males and females reflects these intraspecific feeding differences. We show changes in dietary composition, diversity, overlap, and foraging behavior throughout development in ring-tailed lemurs (Lemur catta) and test how the development of sex differences in feeding is related to female costs of reproduction and year-round resource partitioning. Sex differences in dietary composition were only present when females were lactating, but sex differences in other aspects of feeding, including dietary diversity, and relative time spent feeding and foraging, developed at or near the time of weaning. Sex difference in juveniles and subadults, when present, were similar to the differences found in adults. The low year-round dietary overlap and early differences in dietary diversity indicate that some resource partitioning may begin with young individuals and fluctuate throughout development. The major differences between males and females in dietary composition suggest that these larger changes in diet are closely tied to female reproductive state when females must shift their diet to meet energetic and nutritional requirements.Keywords Behavioral development . Diet . Juvenile . Female dominance . Reproduction . Resource partitioning . Lemur catta It is often expected that individuals within a population of different ages, sexes, and sizes, will exploit varying aspects of the species' feeding niche (Schoener 1986; Ebenman 1988). As part of this variation, sex differences in vertebrate feeding can range from temporal and spatial separation of males and females (Ruckstuhl and Neuhaus 2002;Ruckstuhl 2007) to differences in the composition and diversity in diet (CluttonBrock 1977a;Holmes 1986;Clarke et al. 1998;Lewis et al. 2002;Beck et al. 2005;Krüger 2005). For most species, however, little is known about when sex differences appear, how they change throughout development, if early sex differences mimic adult patterns, and if these sex differences function to partition resources or are only apparent with physiological differences between males and females, particularly those related to reproduction.The successful development of ecological competence and adult diet is the primary determinant of whether individuals

Ecological Risk Aversion and Juvenile Ring-Tailed Lemur Feeding and Foraging

“…These same limitations were found in juvenile ring-tailed lemurs which were less effective at capturing insects and opening hard and tough fruits, likely due to dental and gape restrictions [Eaglen, 1985;Yamashita, 2002;Sauther and Cuozzo, 2009]. The lower juvenile ingestion rates of flowers and flower buds are likely due to social displacement from this highly prized resource that appears during seasons of low overall food abundance [Sauther, 1998;O'Mara and Hickey, 2014].…”

“…Additionally, at all ages males receive more aggression than females, except during the cold dry season with the lowest food availability [O'Mara and Hickey, 2014]. Rates of aggression, however, may not be an adequate measure of feeding competition [Johnson and Bock, 2004].…”

“…Logistic generalized linear mixed models with a binomial error distribution and logit link identity were fit to proportional data using the lme4 package in R 2.13 [Bolker et al, 2009;R Core Development Team, 2011]. Individual animal identity, sex and reproductive season were included as random effects to control both for the repeated sampling of individuals, previously identified sex differences Hickey, 2012, 2014] and seasonal fluctuations in food availability [Sauther, 1998;O'Mara and Hickey, 2014]. Age effects in the variables of interest were evaluated by comparing nested models differing in the factor of interest with a likelihood Distance to nearest neighbour (mean ± SD) while feeding and foraging for all observations (triangles) and in high predation risk areas (circles).…”

“…Juveniles must focus on what it takes to survive this vulnerable stage [Bezanson and Morbeck, 2013] and show behavioural repertoires unusual for adults. They play, have more diverse diets and use positional behaviour modes that are either rare or absent in adults [Pereira, 1993;O'Mara and Hickey, 2014]. While juvenile ring-tailed lemur feeding behaviour is much like that of adults, they do show some distinct differences and have the most diverse diets in their groups, and they show a moderate degree of overlap with adults in their social groups [O'Mara and Hickey, 2014].…”

“…They play, have more diverse diets and use positional behaviour modes that are either rare or absent in adults [Pereira, 1993;O'Mara and Hickey, 2014]. While juvenile ring-tailed lemur feeding behaviour is much like that of adults, they do show some distinct differences and have the most diverse diets in their groups, and they show a moderate degree of overlap with adults in their social groups [O'Mara and Hickey, 2014]. Many studies now show that juvenile primates do not meet the ERAH's behavioural predictions of being inefficient in executing their own feeding and foraging, and doing so in a particularly predationsensitive way [Fragaszy and Boinski, 1995;Stone, 2006;Bezanson, 2009].…”