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Food Availability

Figure 4. Anogenital scent-marking rates by males and females for food availability and food scarcity periods (p = 0.03).

Between Group encounters in results

A total of 18 conspecific interactions (rate 0.01/hr) were observed and rates were ten times higher during food availability (0.03/hr) than food scarcity (0.003/hr). The majority of the encounters (n = 13) occurred between neighboring groups; three of these took place in a shared food tree on the border between territories and the remaining ten occurred along territorial borders while groups traveled parallel to one another. In each case, males would lunge at, cuff, and direct bites toward nongroup males while grinding their teeth and palmar-marking. Females would also charge and chase nongroup females. Encounters lasted between 2 and 55 minutes (mean = 17.1 min, SD = 18.8 min).

The remaining encounters (n =5) occurred between established groups and solitary males (n = 3) or a male-female pair (n = 2) that did not occupy an established home range. In these cases, the nonresident individuals were observed to move slowly and quietly below the study group while they were feeding and were chased by both the resident adult male and female when detected. These encounters were short and lasted 2 min or less.

In comparison, interspecific interactions were observed four times more often (n = 65, rate 0.04/hr) and occurred during travel toward a food source (n = 6) or while groups were feeding (n = 59). Red-bellied lemurs interacted primarily with rufous lemurs (Eulemur fulvus rufus, n = 52, rate = 0.04/hr), and less often with ruffed lemurs (Varecia variegata, n = 9, rate = 0.006/hr) and Milne Edward's sifaka (Propithecus diadema edwardsi, n = 4, rate = 0.003/hr). No interactions with other sympatric species were recorded. Rates of interspecific encounters were twice as high during food availability (0.06/hr) than during food scarcity (rate = 0.03/hr). The majority of encounters (n = 57, 88%) took place during food availability, and in all of these red-bellied lemurs were either displaced or actively chased from a food tree. On the eight occasions when red-bellied lemurs stood their ground (which occurred during food scarcity), both the adult male and female would lunge, chase, or try to bite and/or cuff approaching E. f. rufus (n = 5) or P. d. edwardsi (n = 2). In all eight cases, red-bellied lemurs remained in control of the food tree.

DISCUSSION Pair-Bonded Groups

Two-adult groups were by far the most common configuration. Based on the demographic, affiliative, and agonistic data summarized above, red-bellied lemurs can easily be considered a pair-bonded species. This is consistent with the definition that Fuentes (2002) provided after a thorough review of social pair-bonding in nonhuman primates: ". . . a long-term association between 2 non-kin adults characterized by a set of partner specific affiliative behaviors . . ." (p. 969). Implicit in this definition is the fact that pair-bonds will persist for longer than an annual cycle and do not vary with seasonal changes in food or reproductive patterns. This was the case for red-bellied lemur groups in this study.

Pair-Bond Formation

How red-bellied lemur pair-bonds form is less clear and warrants further study. In some species, pair-bond formation occurs through: (1) territorial shift (Easley and Kinzey, 1986), (2) replacement of a group resident by a previously solitary individual through eviction or death of a resident member, or (3) a solitary male or a newly formed pair creating a home range/territory from existing ranges (Brockelman et al., 1998). Although sample sizes are small, examples of each of these have been observed in red-bellied lemurs.

Territorial shift is the subtle and gradual relocation of a group's territory over time which allows for one or more matured offspring to take over the abandoned area. In this study, a female which left her natal range when she was 2.5 years old in 1990 was rediscovered in 1994 occupying a home range which partially overlapped her former natal range (Overdorff and Strait, unpublished data). Short-distance dispersal has been reported in other pair-bonded primates and may contribute to the high degree of affiliation seen between neighboring groups of gibbons (Brockelman et al., 1998; Bartlett, 2003).

Replacement and eviction of resident females by nongroup females has also been observed. In three cases, once a resident female died or disappeared, a new female who was assumed to be previously solitary joined the male within 3 to 5 weeks. In another case, a previously solitary female actively evicted an older female from her group. Together, these observations offer some tentative support for Fuentes's (2002) prediction that there are more costs to a solitary existence, particularly for females if resource defense drives pair-bonding. A solitary female's reproductive success is likely to be more vulnerable if she is not accompanied by a male on an established territory. Additionally, in species where males actively care for infants, infants are more likely to survive when a male is consistently present (Overdorff, 1996b; Fietz and Dausmann, 2003; Goldizen, 2003). Since females migrate out of their natal groups between 2.5 and 3 years of age when they have reached full adult body size and are reproductive, it would be in the female's reproductive advantage to move as quickly as possible into an established group. On the other hand, solitary males have the potential to implement other reproductive strategies such as extra-pair copulations as observed in other pair-bonded species (Palombit, 1994; Reichard, 1995; Schulke, 2004). However, Merenlender (1993) found no evidence that this strategy was implemented in her survey of paternity in multiple groups of red-bellied lemurs at two sites within the Ranomafana National Park.

Finally, we suggest that not only solitary males and females are at a reproductive disadvantage. Pairs of individuals that have not established a defendable home range appeared to be just as vulnerable as solitary females because they lost consistently in conspecific encounters and have never been observed with infants.

Pair-Bond Maintenance: Nearest Neighbor and Grooming

Once a pair bond is formed, an adult male and female can remain together for at least 6 years (e.g., Group 2, DJO). As expected, strong, stable affiliative bonds were evident between the adult male and female based on nearest neighbor, grooming, scent-marking, and within-group agonistic patterns. Groups were highly cohesive and group members were rarely without a nearest neighbor. Adults were observed with offspring as nearest neighbors slightly (but not significantly) more often than with each other but male-female nearest neighbor patterns were the only category that remained consistent across seasonal changes. Unfortunately, because the nearest neighbor data were collected using scan sampling, we could not examine which individuals were more responsible for initiating proximity.

We were able, however, to examine initiation patterns for social grooming (allo-groom and mutual-groom) and these patterns varied depending on the type of grooming observed. Overall, rates for both kinds of grooming were similar; they did not mutual-groom each other significantly more often than allo-groom. Rates and directionality patterns between age and sex classes within groups did not change across fluctuations in food availability, which is similar to reported patterns in hylobatid species (Tilson and Tenaza, 1982; Mitani, 1984; Bartlett, 2003). Group members were equally likely to initiate mutual-grooming with each other. However, the adult male was significantly more responsible for initiating allo-grooming with the adult female which is the reverse of what is seen typically in larger groups of anthropoid primates (Arnold and Whiten, 2003). One contributing factor to this reversal in directionality may be the type of dominance pattern that has been established within the group. In contrast to anthropoids, many lemurid primates are female dominant (Jolly, 1984; Sauther et al., 1999; Overdorff and Erhart, 2001; Pochron et al., 2003; Curtis, 2004). When clear female dominance exists, males typically direct few, if any, agonistic behaviors towards females, receive more agonism from females, and groom more than they receive (Pollock, 1977, 1979). However, it is difficult to label red-bellied lemurs as a female-dominant species with female feeding priority (see Jolly, 1984; Overdorff and Erhart, 2001) due to the fact that agonism occurred so infrequently between adults and females were only observed to supplant males from feeding sources twice (February when food was scarce). Consequently, further study of which sex is responsible for initiating proximity is needed to better understand whether the male, the female, or both are responsible for maintaining the social pair bond.

Pair-Bond Maintenance: Scent-Marking

Adult males scent-marked more often than adult females and had a wider range of scent-marking behaviors (head-mark and palmar-mark). Scent-marking is generally considered an indirect way for males to advertise mated status and mediates competition with conspecifics, particularly among strepsirhines (Epple, 1986; Fornasieri and Roeder, 1992; Kappeler, 1998; Gould and Overdorff, 2002; Pochron et al., 2005). In many species, rates of scent-marking increase during the mating season and scent-marks may serve as an indirect form of mating competition in multimale and female groups (Gould and Overdorff, 2002; Heymann, 2003). However, although males in this study scent-marked more often, scent-marking rates decreased significantly during the food scarcity period which also corresponded to the mating period. Consequently, we propose that scent-marking in red-bellied lemurs may function as an additional way to sustain the pair-bond year round. Although red-bellied females were not the direct recipients of scent-marking very often (3%), they were within 5 m or less of the objects the male marked in all other cases. Scent-marking during the food availability period may also serve as an indirect way of defining and defending a home range and the resources contained therein (Kappeler, 1998; Heymann, 2003).

Within-Group and Conspecific Agonism

As predicted, within-group agonism was low and occurred only twice in a feeding context. This is consistent with levels of intragroup aggression observed in anthropoid pair-bonded species (Wright, 1986; Bartlett, 2003) and other lemur species (with the exception of Lemur catta, Erhart and Overdorff, in review). The majority of agonism, in fact, appeared to be related to weaning conflict rather than feeding competition. Although males participate actively in carrying the infants (Overdorff, 1996b; Tecot, personal observation), both parents began to actively discourage infants from riding ventrally or dorsally around 5-6 months of age. This also coincided with the months when food was becoming scarce (February-March) and may serve as an energy conservation strategy for both parents (Wright, 1999). As food becomes scarcer, daily travel between and to food patches becomes longer (Overdorff, 1993a), and food is lower in quality (Erhart, in preparation).

Rates of conspecific encounters were similar to within-group agonistic rates (0.01/hr), interactions with extragroup members were never affiliative, and con-specific encounters occurred most often during food scarcity. Both sexes appear to be equally invested in defending the home range given that adult males and females equally participated in fights with conspecific groups. Aggression with other groups also was exchanged between same-sex individuals which is the case in most other pair-bonded species as well (Fuentes, 2002). Additionally, encounter rates with other red-bellied groups or solitary individuals were ten times higher during food scarcity and occurred primarily at home range borders. Times of food scarcity may force more encounters between conspecifics particularly if ranges are small and food is distributed in large, widely spaced patches (Overdorff, 1996b). In fact, two of the more prolonged encounters with a neighboring group occurred within a Chrysophyllum madagascariensis tree that was fruiting out of season and occupied a place where two ranges overlapped.

Between-Group Agonism, Resource Defense, and Energy Conservation

Interspecific encounters differed in two main ways compared with conspecific encounters: they occurred at higher rates overall (0.04/hr) and they occurred more often during higher food availability. Red-bellied lemurs fought more often with groups of Eulemur fulvus rufus, their only sympatric congener which is similar in diet and body size but lives in multimale and female groups of up to 16 individuals (Overdorff, 1996b; Overdorff et al., 1999). Larger group sizes clearly offer some advantage regarding food competition as they usually displace smaller groups during contests over food patches. Squirrel monkeys (Saimiri sciureus), for example, tend to congregate in groups of 35 individuals compared with sympatric night monkeys (Aotus trivirgatus) and titi monkeys (Callicebus moloch)

which are both pair-bonded (Terborgh, 1985; Wright, 1986). Squirrel monkeys range farther, travel farther between food patches, and easily displace the pair-bonded species from fruit trees. However, both titi monkeys and night monkeys are able to more frequently use smaller, more clumped food patches that squirrel monkeys avoid as these patches are not large enough to support all group members. As a result, all three species are able to effectively coexist.

In the New World monkey example above, these three species are similar and are related at the family level but not at the genus level. Sympatric congeners are substantially more similar in morphology, body size, and diet, and are more likely to compete with each other for access to critical food resources. For both to coexist, some form of niche separation or character displacement must occur and divergence between species may be more pronounced during critical food shortages (Birch, 1957, 1979; Schoener, 1974). Interestingly, encounters between congeners occurred more often during food availability. At this time of year, both red-bellied and rufous lemurs ranged shorter distances, rufous lemurs' core home ranges overlapped considerably with red-bellied lemur ranges, and dietary overlap was higher (Overdorff, 1993a,b). As a result, these two species were more likely to come into contact with each other. When this occurred, red-bellied lemurs were always displaced from the food patches, and in some cases the red-bellied group would withdraw as rufous lemurs entered the patch, minimizing the length and intensity of interaction. Red-bellied lemurs would either move on to a different food source or rest in a nearby tree and revisit the patch once the rufous lemur group departed. Food (fruit in particular) may be abundant enough that it was not worth the cost of retaliating. Indeed, the eight times that red-bellied lemurs did stand their ground to remain in control of a food patch were during food scarcity when the potential cost of leaving and finding alternative food sources would likely be higher. Rufous lemurs will range much farther during food scarcity periods, often migrating more than 8 km away from their core area to find alternative sources of food (Overdorff, unpublished data; Mutschler, unpublished data). Therefore, smaller, pair-bonded groups may allow red-bellied lemurs more flexibility when food is scarce to exploit smaller food patches without having to significantly adjust their ranging patterns. In fact, rufous lemurs in the southeast will also fission-fusion into smaller subgroups of three to five individuals when food is most scarce (Overdorff et al., 2003).

Other aspects of red-bellied lemur behavior such as proximity, grooming, and scent-marking also indicate that food scarcity is a time when energy conservation strategies are of utmost importance (Lee, 1986; Wright, 1999). Although the adult male and female maintained a consistent level of proximity to one another throughout the year, both were observed to be without a nearest neighbor more often during food scarcity. This, in part, is due to the fact that they feed farther apart from one another (Overdorff, 1996a) which may serve as an additional way of minimizing within-group competition for food when food is scarcer. Rates of social grooming and scent-marking also decreased significantly during food scarcity. Seasonal reductions in grooming time and other nonsubsistence activities such as play have been observed in other species as well (Freed, 1996; Bartlett, 1999, 2003) and are presumed to be additional strategies to conserve energy at a time when food resources are severely limited.

In summary, red-bellied lemurs are indeed pair-bonded based on the patterns of social behavior and the consistency of those patterns across seasons of food availability. Solitary individuals or pairs of individuals that have yet to establish a defendable home range are likely to be at a reproductive disadvantage. The lack of within-group competition for food, the higher observed rates of intergroup encounters over food, and the mutual role that males and females play in defending their home range indicate that resource defense particularly from congeners may be an important selection pressure favoring pair bonds in this species.

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