Ecological Correlates of Primate Metabolic Variation

Although primates do not significantly differ from other mammals in the scaling of body mass and metabolic rate, there is considerable variation within the order. Haplorhines, as a group, have a scaling relationship similar to other mammals. In contrast, strepsirrhines are hypometabolic and have a scaling relationship that markedly deviates from that of haplorhines and other mammals. Indeed, all strepsirrhine species have RMRs lower than those predicted for body mass based on the Kleiber scaling relationship.

A number of ecological factors, such as low-quality diet, arboreality, and nocturnality, have been linked with hypometabolism, both in strepsirrhines and other mammalian groups (Kurland and Pearson, 1986; McNab, 1978, 1980, 1986; Ross, 1992). In these explanations, adaptations to particular ecological factors are postulated to have led to depressed metabolic rates.

Hypometabolism, which slows passage rates to allow increased nutrient extraction, has been linked to low-quality diets associated with the inclusion of large amounts of foliage (McNab, 1978, 1980, 1986). This may be particularly important in the smaller species with folivorous diets. It has also been suggested that depressed metabolic rates allow a species to consume greater quantities of toxic insects without experiencing deleterious effects (CharlesDominique, 1977; McNab, 1980, 1986; Oates, 1984).

Our examination of the role of low-diet quality in hypometabolism produced mixed results. Strepsirrhine species with low-quality diets for body size tended to have depressed metabolic rates, suggesting that hypometabolism in this group is partially influenced by low-diet quality, particularly in the larger species. Depressed metabolic rates also appear to be associated with low-quality diets in haplorhines; species with lower quality diets than predicted for body size have lower metabolic rates than predicted for body size. However, the regressions describing the relationship for each group are parallel, and thus, dietary differences alone cannot explain the metabolic differences between strepsirrhines and haplorhines.

McNab (1978, 1986) also raises the possibility that folivory in the context of an arboreal habitat may differentially depress metabolic rates in certain mammalian groups, including primates. Specifically, the depressed metabolic rates of arboreal folivores may be attributable to a combination of factors, including a low-quality diet, relatively sedentary habits, and the consequent decreases in skeletal muscle mass (McNab, 1978, 1986). Our results suggest that, like diet, habitat does exert a significant influence on metabolic rates, as arboreal species have lower RMRs than terrestrial species. However, among only arboreal species, strepsirrhines have significantly lower metabolic rates than haplorhines. Lemur catta, the strepsirrhine that spends the largest proportion of time on the ground, is also the most hypometabolic of the strep-sirrhines (-69.22% from predicted), though the confounding effects of body mass and diet make it difficult to separate out habitat preference. While there is some support for a model that considers both low-dietary quality and arbo-reality in strepsirrhines, it cannot explain metabolic rates in some species, including some haplorhines. For example, Alouatta palliata, a folivorous and arboreal haplorhine, has a metabolic rate slightly above that predicted by Kleiber scaling relationship (+ 4.28%). Additionally, hominoids, such as Pongo pygmaeus and Hylobates lar have low-quality diets, but have RMRs (+ 0.68 and +8.93%, respectively) at or slightly above that predicted for body size.

The results presented in the current study indicate that there is a relationship between depressed metabolic rates and lower dietary quality in both strepsirrhines and haplorhines, but the metabolic differences between strep-sirrhines and haplorhines cannot be explained by dietary differences alone. In fact, as discussed previously, the regressions that describe the relationships in each of the groups are parallel. These results echo those of Leonard and Robertson (1994), but with an enlarged sample size.

Another ecological variable that has been discussed in reference to hypometabolism is waking cycle, largely because of its importance in the context of thermoregulation. A relatively low RMR has been proposed to be a thermoregulatory adaptation in strepsirrhines (Charles-Dominique, 1974; Müller and Jaksche, 1980) and in certain haplorhine species, such as Aotus trivirgatus (Le Maho et al., 1981). It is suggested that this adaptation would be seen in well-insulated animals living in tropical environments with high-daytime temperatures and low-nighttime temperatures. In this view, nocturnal activity increases heat production during the coldest part of the 24-h cycle, while inactivity during the day reduces heat production during the hottest part of the 24-h cycle. This hypothesis is a continuation of a larger literature that suggests that strepsirrhines use behavioral adjustments, such as reduced activity levels and sunning behavior, in order to efficiently thermoregulate (e.g., Morland, 1993). It has been proposed that the cath-emeral behavior of Eulemur fulvus, which is active at night during the cool dry season, is an adaptation to minimize cold stress and energy costs (Curtis et al., 1999). Thus, the thermoregulatory hypothesis for strepsirrhine hypometabolism predicts that depressed RMRs in well-insulated, nocturnal primates living in hot environments are the result of thermoregulatory adaptations.

Data from the study demonstrate that among strepsirrhines, nocturnal species have relatively higher RMRs than diurnal species, rather than lower as would be predicted by the thermoregulatory model. This difference, however, may be partially an artifact of body size and diet, as the diurnal species are the four largest of the strepsirrhines and additionally are some of the most folivorous. It should be noted that the two nocturnal haplorhine species, Aotus trivirgatus and Tarsius syrichta, have RMRs that fall substantially below those predicted by the Kleiber scaling relationship, but both are also relatively small bodied. Interestingly, Aotus and Tarsius are thought to be secondarily nocturnal (Martin, 1990). While current data do not support the ther-moregulatory hypothesis, a recent colonization of the diurnal niche has been suggested for the diurnal (and cathemeral) strepsirrhines (Ross, 1996; van Schaik and Kappeler, 1996), which could partially explain metabolic rates of these diurnal strepsirrhines.

In summary, none of the ecological arguments entirely explain the level of hypometabolism observed in strepsirrhines. Depressed metabolic rates are exhibited by strepsirrhines of a range of body sizes, with diverse dietary strategies, and different activity patterns and waking cycles. While it is clear that adaptations to proximate ecological factors, such as diet, play a role in structuring metabolic costs, these factors cannot entirely explain hypometabolism in strepsirrhines.

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