Discussion

Based on now classic ecological studies of rainforest primates (e.g., Milton, 1980; Terborgh, 1983) and, more generally, on a comparative review of frugivorous tropical vertebrates (Fleming et al., 1987), I hypothesized that species with relatively (1) high reproductive costs, (2) large body size, and (3) spatiotemporally patchy food resources would have foraging adaptations to conserve energy and would demonstrate sex differences in these adaptations due to differing female and male reproductive investment. I predicted that V. rubra, which possesses all three of these traits, would conserve energy by minimizing forest area used and distances traveled within a large home range during the resource-scarce cold seasons. I also predicted that V. rubra would show sex differences in these ranging variables that correspond to energetically costly reproductive stages. Ranging data, mainly of females, support the first prediction, while there is only partial support for the second prediction. While there are indeed marked sex differences for most ranging variables when analyzed by season and/or reproductive stage (individual travel patterns and home range areas), in one regard the sexes are alike. Mean daily distances traveled by males fluctuate in tandem with female reproductive stages in a fashion similar to, rather than different from, the pattern shown by females. This result may reflect the investment made by V. rubra males in providing care to infants while lactating mothers are away feeding and engaging in other activities (Vasey, 1997a, in press; see also below).

Ranging Patterns, Social Organization, and Reproduction

Data on social structure and ranging behavior presented here also provide insight into the complex social organization of red ruffed lemurs. Below I summarize these data and integrate them with data on food distribution and reproduction, and with observations made on other populations of ruffed lemur (e.g., Morland, 1991a,b; Rigamonti, 1993).

Communities of V. rubra at Andranobe are territorial, defending exclusive home ranges from other conspecific communities. Territorial battles occur more often in the resource-rich hot months. Morland (1991a) and Rigamonti (1993) describe similar intercommunity battles in Varecia with females as the primary players and males assuming a subsidiary role. Recording dyadic interactions was not a part of the present study, and therefore female-biased home range defense cannot be directly supported for the Andranobe population, though it appeared to be the case. While males scent-marked copiously during these battles, they typically remained on the fringes of the fray; they did not appear to get involved in chases and they often kept silent when other community members were calling.

At Andranobe V. rubra has a multilevel fission-fusion social organization that includes subgroups, affiliates, core groups, and a community social network, much like that found in V. variegata (Morland, 1991a,b). Ranging variables collected over an annual cycle show that their fission-fusion social organization has (1) a daily component and (2) a higher-level component dictated by both extrinsic seasonal factors and intrinsic reproductive factors. This finding substantiates and augments earlier claims based on social criteria and ranging data of select months (Morland, 1991a,b; Rigamonti, 1993). The daily component of fission fusion involves the formation and disbanding of subgroups and occurs throughout the year. The higher-order component involves the dispersion of core groups into core areas during the food-scarce, cold rainy season and gestation.

Communities of V. rubra are composed of core groups each with their own undefended core area. Although core group members affiliate with one another throughout the year, they do not routinely form spatially cohesive groups. Furthermore, the sexes by and large show highly different ranging patterns. The individual ranges of V. rubra males overlap little and are stable year round, effectively corresponding to core areas. In turn, forest area used and daily distances traveled by males differ little between seasons, and they form subgroups only with members of their own core group and with community members who enter their core areas. The only departure from this uniform ranging pattern concerns daily distances traveled during female reproductive stages; males resemble females in traveling farther during lactation than gestation. Concomitantly, food resources used by males are farther apart (i.e., spatially patchier) when females are lactating compared to when they are pregnant (Vasey, 1996, 1997a).

In contrast to males, the ranging patterns of V. rubra females are complex, shifting in tandem with both seasons and reproductive stages. During the cold rainy season and ensuing gestation months, females use smaller forest areas, travel shorter daily distances, and confine themselves entirely to their respective core areas. This dispersion of core females into their respective core areas adds a higher-level component to their fission-fusion social system, and occurs when their food resources are closer together (Vasey, 1996, 1997a). When females lactate, especially during the food-abundant hot rainy season, they use larger forest areas, travel longer daily distances, and enter other core areas, affiliating with members of other core groups in temporary subgroups that vary daily in membership, size, sex composition, and duration. Correspondingly, food resources used by V. rubra females at this time of year are spatially patchier (Vasey, 1996, 1997a).

Pereira et al. (1987) hypothesized that reliance on fruit coevolved with fission-fusion social organization and reproductive traits in Varecia. Results presented here validate and greatly expand on this hypothesis. Ranging patterns observed in V. rubra, in particular those of females, vary in tandem with reproductive stages and reliance on spatiotemporally patchy resources, not fruit per se (see also Vasey, 2002a,b), producing the daily and higher-level components of fission-fusion social organization.

Further examination of ranging in relation to reproduction is warranted. The limited ranging of V. rubra females during many consecutive months of the year (Jun-Oct) appears to be a tactic for conserving (or accumulating) energy not only during the tough winter months when less food is available in the forest, but also as climate improves when females undergo their extremely costly gestations. This low-effort strategy during gestation is in keeping with predictions outlined in the Introduction, but lies in marked contrast to tactics adopted during lactation. Lactation is the most energetically expensive reproductive stage for female primates (e.g., Portman, 1970; Kirkwood and Underwood, 1984; Sauther and Nash, 1987; Dufour and Sauther, 2002). Yet V. rubra females adopt a high-effort strategy to meet lactational costs by ranging widely to dispersed resources. To interpret this high-effort strategy, it is necessary to carefully evaluate factors associated with lactation. Varecia provides relatively concentrated milk (Tilden and Oftedal, 1997) to litters of infants that grow extremely fast (Pereira et al., 1987). Therefore, energy transfer during lactation must be extremely high, and females may travel farther during the first 4 months of lactation to satisfy high nutritional requirements. However, Varecia may save energy during lactation relative to other primates in a variety of ways. First, Varecia mothers do not transport their infants full-time. Instead, they routinely stash them in concealed, protected arboreal spots rather than carrying them around (e.g., Morland, 1990; Vasey, in press). Second, Varecia mothers benefit from alloparenting (Pereira et al., 1987; Morland, 1990; Vasey, in press), and may even breed cooperatively (Vasey, 1997b, in press), which allows them to leave their infants with other community members while they travel and feed in distant parts of the home range. Third, after the very brief nesting season (1-2 weeks, Morland, 1990; Vasey, in press), ruffed lemur infants are suckled on schedule rather than on demand, which may be less energetically expensive since mothers feed their infants less frequently. A clinging primate infant can and does suckle whenever it wishes (i.e., on demand), but a nonclinging infant feeds only when its mother returns to where she has left it (Martin, 1990). Varecia, and other prosimians with absentee parental systems (e.g., Otolemur, Nycticebus, Cheirogaleus), may spend less time nursing by providing milk that is more concentrated in energy and nutrients (Tilden and Oftedal, 1997). Fourth, ruffed lemur infants develop quickly, growing independent in terms of nutrition and locomotion more rapidly than other lemurids (Vasey, in press). Lastly, minimizing forest area used and distances traveled during gestation, in addition to modulating activity budgets at this time of year (Vasey, 2005), allows females to accumulate fat reserves, which may buffer energetic deficits experienced during lactation. Wild V. rubra do in fact appear fatter during the austral winter and ensuing gestation months. Considered together, reproductive costs of Varecia during gestation and lactation are relatively greater than other diurnal primates but they appear to have a variety of behavioral and physiological methods to mitigate them.

Ranging Patterns of Varecia in Comparative Perspective

The ranging pattern of V. rubra males is similar to that of many nongregarious nocturnal prosimians in that male ranges overlap little (Bearder, 1987). However, unlike many nocturnal prosimians, V. rubra males do not appear to defend their core areas against other males, and during many months of the year their home ranges are smaller than those of females. Nor do their ranges overlap those of many females, but rather just those within their own core group. In contrast, ranging patterns of V. rubra females depart substantially from nocturnal prosimi-ans in that individual female home ranges are larger than male home ranges and overlap with those of other females and males. Female ruffed lemurs may be philopatric (Morland, 1991a), as are the females of certain nocturnal prosimian species (Nash, 2004). More pertinent here, however, female ruffed lemurs can be highly gregarious, resembling diurnal primates more in this regard. Morland (1991a,b) found that V. variegata females were the focus of social activity, giving and receiving the highest rates of affiliative interaction with every age-sex class. They also had more affiliates than males, and interacted socially more often than males in hot months. Both sexes were more solitary in cold months, but males spent more time alone throughout the year and rarely interacted with other males. Although the latter social variables were not quantified in this study of V. rubra, nonquantified observations appear concordant with Morland's characterization of V. variegata. One noteworthy difference is that of eight core groups in Morland's study, one contained two adult males. Thus, nonoverlapping male ranges may not be a strict rule in ruffed lemurs. Given the alternately dispersed and gregarious forms of sociality and ranging seen in Varecia, it is perhaps no coincidence that ruffed lemurs share a suite of reproductive traits with many nocturnal prosimians, in particular, absentee parenting.

Behavioral Variation in Wild Studies of Varecia

In previous studies of wild Varecia, researchers have described a wide array of community (or group) sizes, social structures, social organizations, and home range sizes, as well as differences in territorial behavior (Table 5; see also Vasey, 2003). In the present study, yet a new combination of features was found. Minimum community size ranged between 18 and 31 individuals, animals had a multifemale/mul-timale social structure, a fission-fusion social organization, and an exclusive, communally defended home range of 57.7 ha. This home range area falls between estimates from other sites (Table 5). Yet the Andranobe community is larger than any ruffed lemur community known to date, resulting in the highest known population density of Varecia (31.2-53.4 individuals/km2, Vasey, 1997c, 2003).

Previous studies have varied in length, continuity, and in seasons and reproductive stages sampled (Table 5). Some, though not all, of the behavioral variation found among different populations of Varecia is likely due to short-term observations and to a lack of sampling during the hot rainy season, when it is possible to clearly distinguish small groups (i.e., of two to four individuals) clearly as part of a larger community network. If not observed in the hot rainy season, small groups could be misidentified as monogamous, pair-bonded family groups rather than as part of a single, larger community with a multimale/multifemale social structure.

In northeastern Madagascar alone, three long-term field studies of Varecia (including this one) show remarkable variation in community size, home range size, and territorial behavior (Table 5, Morland, 1991a,b; Rigamonti, 1993; Vasey, this study). Yet despite this variation, all three populations have similar seasonal ranging patterns, and concomitantly, a fission-fusion social organization. For example, in all three studies, Varecia communities were formed of core groups with discrete core areas, animals spent more time in their respective core areas in cold months, and individuals traveled shorter daily distances in cold versus hot months. The latter is also evident in a population of V. variegata in southeastern Madagascar (Britt, 1997).

Flexible behavior may provide a means of maintaining ecological similarity. In every population studied to date, Varecia is highly frugivorous, uses the highest forest strata and the largest feeding trees, is active primarily by day, and is limited to eastern rainforests (Vasey, 2000a, 2003). This ecological inflexibility has undoubtedly contributed to Varecias vulnerability when it is faced with habitat alteration and loss. Compared with other extant lemur species, Varecia has fewer dispersal and habitat options. Factors that elicit behavioral flexibility in Varecia

Table 5. Behavioral variation in wild Varecia

Site and study"

Species

Group structure: community size

Group structure'': age/sex composition

Social organization: intragroup spacing

Home range

Territorial

Andranobe

V. rubra

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