Discussion

No matter the season or location, crowned lemurs and Sanford's lemurs associate daily. Neither species routinely led or followed the other. When associating both species were often their nearest neighbors. Short of grooming, resting, and mating with each other, both species treated each other as members of the same group. Both responded to each other's group vocalizations; neither species was the recipient of agonistic vocalizations targeted at neighboring conspecific groups. The level of association among these species is unlike most other populations of sympatric, congeneric daylight-active lemurs. In most other communities lemurs barely tolerate, displace, or chase one another. When compared with other primate associations, especially those of tamarins and guenons, the lemur associations did not occur as often, they were not permanent, and neither species routinely dominated the other (Gautier-Hion et al., 1983; Buchanan-Smith, 1999; Bicca-Marques and Garber, 2003). As in Porter (2001), associations varied seasonally in frequency; critical aspects of the lemurs' behaviors within associations did not change.

In northern Madagascar, lemurs receive at least three benefits by forming poly-specific associations. First, during the wet season, when resources are least available, both species in Ampamelonabe perhaps gain increased foraging efficiency by forming associations. Specifically, both species partition their habitat, and continue to forage throughout their home range. When resources are nearly exhausted in the middle story, the Sanford's lemurs' preferred forest level, these lemurs actively seek crowned lemurs in the understory while the latter are feeding or foraging there. This may come at some cost to crowned lemurs. They wind up losing some of their food. Yet the Sanford's lemurs never deplete the crowned lemurs' resources, so the extent to which this poses a cost to the crowned lemurs is unclear. Likewise, when resources deplete in the lower story, crowned lemurs seek Sanford's lemurs that are feeding or foraging in the middle story. Although the Sanford's lemurs may displace the crowned lemurs from certain trees, the crowned lemurs eventually get fruit from these resources simply by waiting their turn. Crowned lemurs often returned to feed on these larger, middle-story resources (e.g., Neotina isoneura and Celtisgomphophylla) when Sanford's lemurs were not present. By doing so, crowned lemurs took advantage of the limited time that tall trees bore fruit. Cords (1990) reported a similar relationship between red-tailed guenons and blue guenons. Blue guenons displaced the smaller red-tailed guenons from food trees, but the latter species fed in the food trees when the former species was not in them. For the most part, the lemurs, as do the guenons, readily consume similar food species while associating, without much interspecific agonism. In terms of costs to the Sanford's lemurs, the crowned lemurs never truly depleted the Sanford's resources. By following this pattern, both crowned lemurs and Sanford's lemurs waste little time and energy foraging for food, while not depleting their associates' resources. They continue to devote their energy to monitoring food availability throughout their range, even when resources are not readily available. In this sense, both species gain a measure of feeding and foraging efficiency by forming polyspecific associations during periods of resource scarcity.

One question that arises is whether forest productivity accurately predicts the frequency of polyspecific associations among these lemurs. For example, in Guyana Lehmann (2000) showed that plant productivity was directly related to the frequency of polyspecific associations. Among these lemurs plant productivity does not seem to predict reliably the incidence of polyspecific associations. Associations were found in both humid, highly productive forests (e.g., Ampamelonabe) and drier, smaller, much less productive forests west of Mt. d'Ambre. Temporally, the frequency of associations was inversely related to the availability of resources within the same forest. Further investigation would be needed to address this question.

Researchers have suggested that species associate to improve food acquisition. White-fronted capuchins (Cebus albifrons) and squirrel monkeys (Saimiri sci-ureus) may have associated with brown capuchins (Cebusapella) to find available resources (Terborgh, 1983). Whereas the first two species had large home ranges, brown capuchins had small ranges and were probably more aware of available resources. Blue guenons (Cercopithecus mitis) and gray mangabeys (Cercocebus albigena), species with large home ranges, initiated associations with smaller-ranged, red-tailed guenons (Cercopithecus ascanius) (Struhsaker, 1981). Blue guenons and gray mangabeys probably benefited from the red-tailed guenons' familiarity with resources. Red-tailed guenons probably also benefited, as gray mangabeys made available food that was otherwise too large or hard for the red-tailed guenons. Unlike these cases, the crowned lemurs and Sanford's lemurs have small, highly overlapping home ranges. Neither species has a more detailed knowledge and familiarity with the horizontal range. On the other hand, given the lemurs' year-round differences and resource partitioning, the lemurs, as do other primates, probably have different familiarity of resources in each forest level. Buchanan-Smith (1999) suggested that such vertical segregation may make more stable associations, and may increase an associate species' likelihood of finding new resources.

Both lemur species probably receive some year-round benefit as well by being able to respond to antipredator vocalizations of associates. Fossa predation of lemurs has been suspected or observed at other sites in Madagascar (Wright et al., 1997; Britt et al., 2004). At Ampamelonabe, however, all groups, whether within or outside associations, benefit from the alarm calls of other lemur groups. As soon as one group in the forest gives an alarm vocalization, the warning spreads quickly throughout the forest, within and outside associations, among both species. I observed similar alarm responses in the small forest patches west of

Mt. d'Ambre, where populations of both lemur species often exchange vocalizations at dusk and when potential predators are spotted.

As in other primate polyspecific associations, some antipredator benefit is likely obtained by associating. Unlike other primate associations, potential predators are few. The exact scope of predation pressure in Ampamelonabe is hard to determine, as predator densities are largely unknown, but is suspected to be low. In terms of predator behavior and food preferences, most potential mammalian predators of lemurs are nocturnal and were likely preying on large crested ibis. Avian predators are rare. During the day, the lemurs are rarely exposed to predators as they feed, forage, and travel, as most of these activities occur in dense cover away from any potential predator. Daylight resting perhaps exposes Sanford's lemurs somewhat more to predators, as these lemurs tended to sleep on larger main branches. They did not sleep as often as did crowned lemurs on smaller, more terminal branches. As in Bicca-Marques and Garber (2003), increased exposure to potential predators may have occurred more often during one of the lemur associates' behaviors, but too few predators were observed during the day. Potential predator protection may be a benefit, but it may not be as useful in predicting the occurrence of polyspecific associations among these lemurs. Treves (1999), for example, readily questioned the usefulness of predation as an explanatory tool to predict social systems in arboreal primates.

Both lemur species benefit socially from associations in at least two ways. First, subadults often form playgroups while adults associate during feeding or resting time. In both 1989 and 1990 groups of subadult lemurs played low in the forest for over 45 minutes, while adults rested or fed in upper forest levels. By forming associations, small groups found additional play partners, and more individuals could detect potential predators of young lemurs. Although Burton and Chan (1996) saw cross-species infant care across macaque associates, none of the lemurs ever exhibited such social behavior. A second social benefit may arise rarely when an individual leaves its group. In 1990 one adult female Sanford's lemur was spotted associating with a group of crowned lemurs for two full days after it left its original Sanford's group, and before it rejoined that group. In this case, the individual was neither dominant nor subordinate to its crowned lemur associates, nor did there seem to be any agonism directed to or from the individual.

Another hypothesis is that the groups form associations by chance alone. Given that the two species have highly overlapping home ranges, one might expect that the groups would run into each other and associate at such high levels. Waser (1982, 1984) and Whitesides (1989) derived a formula to predict the expected encounter frequencies and duration of associations. Assuming knowledge of group velocities, group radii, and densities, Whitesides (1989) calculated that Tiwai forest Diana monkeys associated less than would be expected by chance alone. Using the same formulas, Holenweg et al. (1996) found that the same species and red colobus associated more than expected by chance in Tai' forest. Yet in Ampamelonabe, the Waser/Whitesides formula was inappropriate for several reasons: groups of crowned lemurs were variably spatially cohesive and often subgrouped; the breadth or spread of each crowned lemur group could not be determined reliably; and each study group associated with more than one group. I also did not monitor the precise overlap in home ranges with nonstudy groups. Each study group had a home range that overlapped with home ranges of at least seven groups of the other species. Assessments of these groups' home ranges were simply not feasible.

To some extent many of the associations may form by chance alone. In Ampamelonabe, dry season and hot season polyspecific associations seem to differ from those of the wet season in frequency. The dry season and hot season associations seem to be initiated not while lemurs are feeding, and initiators rarely leave their preferred forest level to start these associations. During these seasons, resources are much more superabundant, as Leea spinea is readily available throughout the forest. Perhaps resource abundance reduces the potential benefit of association. Gautier-Hion et al. (1997), for example, observed that seasonal reduction in fruit availability probably contributed to an increase in the number of polyspecific associations in black colobus monkeys.

In contrast, seasonal variation in the incidence and form of association make chance less likely an explanation for wet season associations. During this time the two lemurs associated nearly twice as often and three times as long as in other seasons. Both lemurs formed associations more readily upon meeting one another. Lemurs initiated associations from outside their preferred forest levels, and most often while associates fed or foraged. Within associations, the two lemurs were usually less than 10 m apart. Finally, groups had clear preferences as to the specific groups with which they readily associated.

Sauther (2002) suggested that polyspecific associations may have substantial benefits for species that face severe energetic demands posed by pregnancy and lactation, especially in habitats where food availability changes greatly with seasons. I was unable to test this hypothesis on crowned lemurs and Sanford's lemurs. During periods of pregnancy (the dry season) and for most of lactation (hot season), polyspecific associations formed at a fairly low rate. During these periods food was superabundant, especially the widely available Leea spinea. As the food became less available, both species increased the frequency of associations. Shortly afterwards females ceased lactating. For nearly the next 4 months, prior to the demands of pregnancy, foraging and feeding times increased. I saw little evidence of body size increases at this time. Yet daily path length and time spent traveling also rose during this season. Thus, energy expenditure for all individuals increased during this period.

In conclusion, a combination of these benefits likely helps explain the incidence of polyspecific associations among crowned lemurs and Sanford's lemurs in northern Madagascar. In a highly seasonal habitat, associations seem to confer better foraging and feeding efficiency during periods of resource scarcity, and may provide some subtle advantage in predator protection during certain activities. Occasionally, social benefits occur, perhaps in the formation of play-groups and also when individuals have no same-species group membership. Some associations may occur by chance alone, particularly during periods of resource superabundance. Overall, the evolutionary benefit of these associations is that both primate species flourish in habitats throughout the far northern tip of Madagascar. These habitats include forests that vary in disturbance, resource availability, and structure. By forming these associations, both lemurs can survive temporary shortages of resources, increases in potential predation and hunting, and threats from the islanding of local forests.

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