Introduction

The red ruffed lemur, Varecia rubra, is a large-bodied, highly frugivorous lemur that gives birth to litters which are initially nested and then later transported orally to hidden, protected arboreal spots where they are periodically left unattended (e.g., Vasey, in press). A major question arises as to how a primate with such an unusual, costly reproductive pattern, involving simultaneous investment in multiple young, has become adapted to a diet that is seasonally scarce and requires relatively great foraging effort (e.g., in terms of time and/or distance traveled). To address this issue, I examine and compare the ranging patterns of female and

Natalie Vasey • Department of Anthropology, Portland State University, Portland, Oregon 972070751

male red ruffed lemurs according to seasons and reproductive stages. In documenting the geographic patterns of range use in red ruffed lemurs, it has become evident that, like certain anthropoid primates (chimpanzees, spider monkeys), this prosimian species has a fission-fusion social organization.

In proposing that a related species, the black-and-white ruffed lemur (Varecia variegata), has a fission-fusion social organization, Morland (1991a,b) presented data on affiliation patterns and subgroup dynamics in two adjacent communities, establishing that the black-and-white ruffed lemur has a multilevel social organization that includes subgroups, affiliates, core groups, and a community social network, listed in order of increasing stability. Although the social criteria Morland (1991a,b) used to describe this multifaceted fission-fusion social system are undeniably strong, they were largely based upon select months of the year, rather than an annual cycle, and quite limited data were collected on its geographic patterning throughout the course of different seasons and reproductive stages. A subsequent study by Rigamonti (1993) partly addressed this issue by presenting ranging data for Varecia rubra over a 7-month period. However, the latter study did not sample most hot months, when ruffed lemurs are known to be more gregarious (Morland, 1991a,b). In this article, I present data on the social structure and ranging behavior of wild red ruffed lemurs collected over an entire annual cycle to provide a more comprehensive picture of the ruffed lemur's fission-fusion social system . I focus my analysis on how these factors are impacted by reproduction and seasonal differences in climate and food distribution. These data serve to illustrate the complex fission-fusion social organization of this rainforest lemur in northeast Madagascar.

Background

Food distribution, body size, and reproductive pattern may all potentially impact ranging and foraging behavior. In addition to being governed by abiotic climatic factors, tropical plants have evolved many ways of defending themselves against predation such as rapid leaf expansion, synchronous flushing and masting, production of secondary metabolites, and delayed leaf greening, all of which contribute to the patchy distribution of palatable plant parts (e.g., Coley and Barone, 1996). Thus, edible fruit, flowers, and young leaves are the most clumped and ephemeral plant foods available in a rainforest, and are therefore the most spa-tiotemporally patchy resources. Having a spatiotemporally patchy diet indicates that a species is selecting foods to avoid toxic plant secondary compounds and optimize nutrient mix and nutritional value given the constraints of its digestive system (Freeland and Janzen, 1974; Westoby, 1974; Oates et al., 1977; Milton, 1980; Glander, 1982; Waterman, 1984; Richard, 1985; Janson et al., 1986). However, being selective in food choice increases the costs of food procurement (e.g., time spent or distances traveled to locate food). A primary consumer with a spatiotemporally patchy diet needs to work out a compromise between being selective in food choice and minimizing the high costs of food procurement. Therefore, the criterion of benefit to be maximized is not simply energy uptake per unit foraging time, as predicted by optimal foraging theory (e.g., Krebs and Davies, 1993). Rather, primary consumers should have evolved ways to minimize the costs of procuring preferred foods. These foraging adaptations should be most evident in the way food is located (i.e., in ranging behavior) and are unlikely to be uniform throughout the year due to seasonal shifts in climate and food availability. In an extensive review of tropical vertebrate frugivores from various geographic regions of the world, Fleming et al. (1987) hypothesized that high spatiotemporal patchiness of food resources will favor the evolution of relatively mobile species that can efficiently travel long distances in search of food, whereas low spatiotemporal patchiness of food will favor the evolution of relatively sedentary species with less emphasis placed on energetically efficient long-distance travel.

A species' ranging and foraging behavior can be associated with body size. The vast majority of primates feed on fruit, with smaller-bodied ones supplementing their diets with insects and larger-bodied ones supplementing with leaves (Gaulin, 1979). Above 300 g, it is not possible for a primate to obtain all of its food energy from insects, and below 700 g it is not possible for it to obtain all of its food energy from leaves (Kay, 1984). These trends are due to scaling relationships. Small primates have high metabolic demands and protein requirements per unit body weight compared to larger animals. Small species cannot survive on a diet of fruit and leaves alone because they cannot extract nutrients quickly enough to supply their tissues even if large quantities are eaten. Therefore, small-bodied primates supplement their diets with high quality, but less abundant, insects. Larger species can obtain sufficient nutrients from bulkier foods that are of lower quality because of their relatively lower metabolic rates and longer gut passage times. Since large species require absolutely more energy than small ones, their population densities are lower and consequently, their home ranges are larger (e.g., Clutton-Brock and Harvey, 1978). Although these scaling relationships are broadly predictive of diet and ranging in many primates, dietary diversity in lemurs appears to be distributed according to taxonomic lineages, not just body size (Richard and Dewar, 1991).

Lastly, there is the potential impact of reproduction on foraging. Gestation and lactation increase nutritional requirements in female mammals (e.g., Loudon and Racey, 1987; Gittleman and Thompson, 1988). Using the rhesus macaque as a model, Portman (1970) estimated that pregnancy and lactation increase energetic and protein requirements of females by 25 and 50%, respectively. Controlled captive studies on primates have demonstrated that females require more food energy during lactation than during other reproductive stages (Kirkwood and Underwood, 1984; Sauther and Nash, 1987; Dufour and Sauther, 2002). Recent field studies on lemurs have suggested specific tactics primates use to meet energetic requirements of reproduction. Morland (1990) demonstrated that lactating V. variegata females spent more time feeding than nonlactating females, and Sauther (1998) demonstrated that pregnant Lemur catta ate more energy-rich foods than males and timed their most costly reproductive stages with specific resource availability. Particularly germane here, diet, activity budgets, and activity rhythms are all known to vary in V. rubra females in tandem not only with seasons, but also with reproductive stages (Vasey, 2000a, 2002, 2004, 2005).

Synthesizing these theoretical and empirical studies, it is cogent to hypothesize that species with spatiotemporally patchy food resources, relatively large body size, and high reproductive costs should have evolved foraging tactics to conserve energy, and should demonstrate sex differences in these tactics due to differing female and male reproductive investment. Varecia rubra, the red ruffed lemur, is in all respects a model taxon with which to test this hypothesis.

Body Size, Diet, and Reproduction in Varecia

Varecia has the largest body size (wild weight range = 2.6-4.1 kg, Vasey, 2003), the highest reproductive costs, and quite likely the most spatiotemporally patchy diet among extant lemurids. Varecia relies chiefly on ripe fruit (e.g., Morland, 1991a; Rigamonti, 1993; Vasey, 2000a), which is one of the most clumped and ephemeral food resources in a rainforest. At Andranobe, V. rubra was shown to have a far more spatially and temporally patchy diet than sympatric E. fulvus alb-ifrons (Vasey, 1996, 1997a). A variety of traits increase reproductive costs of Varecia relative to other primates. Despite being the largest lemurid, Varecia has the shortest gestation period (99-106 days, Boskoff, 1977; Foerg, 1982; Shideler and Lindburg, 1982), the highest mean litter sizes (x = 2.1 for V. rubra, Vasey, in press), and relatively altricial young that grow extremely rapidly, attaining 70% of adult weight at 4 months (Pereira et al., 1987). Varecia has the highest prenatal maternal investment rate of any primate (litter weight divided by gestation length relative to maternal body weight and metabolic rate) (Young et al., 1990). Following their costly gestation periods, they begin lactating, the most energetically expensive reproductive stage for mammals (e.g., Oftedal, 1985; Thompson, 1992; Dufour and Sauther, 2002). Moreover, Varecia must produce milk for litters of rapidly growing infants (e.g., Petter-Rousseaux, 1964; Foerg, 1982), whereas other diurnal primates generally nurse singletons. Varecia produces milk that is higher in dry matter, fat, protein, and gross energy (kcal/g) than other lemurids, with protein concentrations similar to those of lorisoids whose milks are more concentrated in nutrients than any other group of primates (Tilden and Oftedal, 1995, 1997). Like various nocturnal prosimians, Varecia bear their young in nests.

Given the relatively large body size and high reproductive costs of Varecia, and the high spatiotemporal patchiness of its diet, predictions that follow are that V. rubra will: (1) conserve energy by minimizing forest area used and distances traveled within a large home range during the food-scarce cold seasons and (2) show sex differences in the above tactics during energetically costly reproductive stages (gestation and lactation).

METHODS Study Site Location and Climate

A study site was established in northeastern Madagascar on the west coast of the Masoala Peninsula in a region of primary lowland coastal rainforest known locally as Andranobe (15° 40.533' S, 49° 57.800' E to 15° 40.275' S, 49° 57.888' E). The site is located within the recently inaugurated Masoala National Park (Kremen, 1998). There are four distinct seasons in this region: (1) hot rainy (Jan-Mar), (2) transitional cold (Apr-May), (3) cold rainy (Jun-Aug), and (4) hot dry (Oct-Dec) (Table 1). The climatic features of September do not fit any of the four distinct seasons. Therefore, data from this transitional month are not included in seasonal analyses. During the course of the study, average annual rainfall was 5110.26 mm, average monthly temperature maxima ranged from 22.5 to 31.6°C, and average monthly temperature minima ranged from 19 to 23.5°C. Andranobe has more rainfall than any other locality in Madagascar. More extensive descriptions of the study site and climate can be found in Vasey (1997a, 2000a).

Seasonal Food Availability and Reproductive Schedules

Table 1 summarizes plant phenology on the island of Nosy Mangabe (Andrianisa, 1989) and on the Masoala Peninsula (Rigamonti, 1993). These two northeastern Malagasy rainforests are within 25 km of Andranobe and provide a representative view of plant food availability in the region. At both sites, fruit, flowers, and young leaves are more abundant in the hot seasons with additional increases in flower and young leaf availability at the end of the cold rainy season. Peaks in fruit and flower availability are similar in other Malagasy rainforests (Table 1 and references therein). Given the similar patterns in fruit and flower availability in northern and southeastern forests, phenological data from Nosy Mangabe and the Masoala Peninsula are considered reliable indicators of resource availability at Andranobe.

Table 1 also shows the correspondence between seasons, food availability, and reproductive stages. Reproduction in the study population was highly synchronized, with mating occurring in early Jul, gestation Jul-Oct, and lactation Nov-Feb (Vasey, in press). A nonreproductive period followed Mar-Jun, during which time adult females were neither pregnant nor lactating. Thus, seasons and reproductive stages span different, though partially overlapping, sets of months allowing two sets of analyses: by season and by reproductive stage.

Table 1. Correspondence between seasons, reproductive stages, and food availability for Varecia in northeastern Madagascar (Phenological data for two other regions are included for comparison. See superscripts. Absence of superscripts indicates that a resource is scarce or unavailable)

Season

Hot rainy

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