Body Composition and Primate Metabolic Variation

Power Efficiency Guide

Ultimate Guide to Power Efficiency

Get Instant Access

Differences in body composition are important in influencing variation in metabolic energy requirements, given marked differences in mass-specific metabolic rates across tissues. Muscle mass, for example, varies from 24 to 61% of total body weight in mammals, with slow-moving arboreal mammals, such as sloths, occupying the low end and terrestrial carnivores, such as lions, occupying the high end (Calder, 1984; Grand, 1977; Muchlinski et al., 2003). McNab (1978) postulates that the depressed RMRs of arboreal mammals are partly the result of low levels of muscularity. Thus, variation in tissue size and concomitant variation in tissue metabolic rates contribute to the structuring of energy costs and provide a mechanism for deviations from predicted metabolic rates.

The relative size of the brain has been linked by a number of researchers to metabolic rate, since both scale to the three-quarters power of body mass (i.e., 0.75) (Armstrong, 1983, 1985; Hoffman, 1983; Martin, 1981, 1996). While some have hypothesized that brain size and its associated high tissue metabolic rates partially structure RMR (e.g., Holliday, 1986), others have taken the opposite approach and hypothesized that metabolic rates influence brain size (e.g., Armstrong, 1983, 1985). The latter relates to a proposed relationship between the size of the brain and the ability of the body to support brain metabolism. Martin's (1981) maternal energy hypothesis is an extension of this reasoning and postulates that brain size is related to maternal metabolic rate. The relatively small brains of strepsirrhines (compared to haplorhines) could be related to depressed metabolic rates in strepsirrhine females and specifically to the transfer of nutrients during pregnancy and lactation. Importantly, the corollary is that the evolution of higher metabolic rates in anthropoids (or possibly in haplorhines, depending on the position of tarsiers) may have allowed these animals to grow and support relatively larger brains. Strepsirrhines invest less in the prenatal development of their offspring than haplorhines, but when controlled for metabolic rate, this difference disappears (Richard and Dewar, 1991; Young et al., 1990). Female feeding priority is also most common in strepsirrhines, especially those with low-metabolic rates, and this has been suggested to help females cope with high maternal energy costs associated with reproduction (Richard and Dewar, 1991).

The study clearly demonstrates that strepsirrhines are less encephalized than haplorhines for any given body size. However, the available primate data also show that the relationship between brain size and RMR is comparable between the two groups. This result suggests that strepsirrhines and haplorhines spend comparable proportions of their RMR on brain metabolism; this supports the conclusions of Armstrong (1985), who used a smaller sample of species. It is possible that the lower levels of encephalization in strepsirrhines relative to haplorhines may be a consequence of metabolic stress (i.e., the low-metabolic rates of strepsirrhines are unable to support relatively large brains). However, this picture is overly simplistic since numerous species deviate from the brain size to RMR relationship. Additionally, as noted by Martin (1996), the range of variation in the relationship between brain size and body mass exceeds that between RMR and body mass. Finally, humans have extraordinarily large brains that account for roughly 20-25% of RMR but do not have elevated RMRs compared to those predicted for body mass (Leonard and Robertson, 1994). How this could have evolved has been the subject of intense debate (e.g., Aiello and Wheeler, 1995; Leonard and Robertson, 1994).

Implications for Models of Primate Origins

The nature and origins of metabolic variation in strepsirrhines and hap-lorhines have important implications for our understanding of the ecology and evolution of the earliest primates. For any given size, primates and other mammals consume considerably more energy than similar-sized reptiles. Mammals have total daily energy costs that average about 17 times that of comparably sized reptiles (Nagy, 1987).

The earliest true primates appeared in the Late Paleocene and Early Eocene and are defined by a suite of cranial and postcranial features not present in the plesiadapiforms or other mammals. While once considered within the primate order (as archaic primates), plesiadapiforms have recently been removed (Fleagle, 1999; Martin, 1990; Rose, 1995). Some authorities place the plesiadapiforms with colugos within the order Dermoptera (Beard, 1993), while others consider them a separate mammalian order (Fleagle, 1999). In fact, all plesiadapiforms with the exception of Purgatorius are too derived dentally to be ancestral to living primates (Rose, 1995). The first true primates (i.e., Euprimates) show a suite of derived cranial characters, such as orbital convergence and frontation, which are associated with increased reliance on vision. They also show derived postcranial features, such as nails instead of claws, and grasping hands and feet, which have been linked to increased manipulative abilities within an arboreal environment. The earliest fossils attributed to primates are highly fragmentary but nonetheless show characters that link them with living primates (Rose, 1995). These species include Altiatlasius koulchii from the Late Paleocene of Morocco and Altanius orlovi from the Early Eocene of Mongolia (Fleagle, 1999; Rose, 1995). Altiatlasius is thought to have had a body size on the order of between 50 and 100 g, while Altanius is thought to have had a body size of about 10 g. These fossils appear to be more primitive and generalized than adapoids or omomy-oids. Early mammalian forms were similarly small bodied and all appear to have been under 500 g. Fossils of Hadrocodium wui from the Early Jurassic of China had an adult body weight estimated to be about 2 g (Luo et al., 2001), while other groups were slightly larger, (e.g., Morganucodon, at 27-89 g and Sinoconodon, at 13-517 g; Luo et al., 2001).

The Eocene primates are typically divided into two major groups, the adapoids (superfamily Adapoidea) and the omomyoids (superfamily Omomyoidea) (Fleagle, 1999). The former have been compared to living lemurs in certain aspects of craniodental and postcranial morphology, while the latter have been likened to living tarsiers; however, the exact phylogenetic relationship with living primates remains unclear (Martin, 1990). While both groups exhibit considerable diversity, the earliest members of each are similar in many aspects. Some of the earliest genera include Donrussellia and Cantius of the adapoids and Teilhardina and Steinius of the omomyoids (Rose, 1995). Reconstructed body size of D. provincialis was about 140 g (Rose, 1995), though some of the other species may have been slightly larger (210-730 g; Fleagle, 1999). Cantius is thought to have been considerably larger and had a body mass range on the order of 1-3 kg for nine species (Fleagle, 1999). Teilhardina, like most other omomyoids, was small bodied, with estimates for the genus (four species) ranging from 60 to 135 g in adult body size (Fleagle, 1999; Rose, 1995). Steinius was on the order of about 300-400 g (Fleagle, 1999). Adapoids later diversified and obtained body sizes up to 7-8 kg (Fleagle, 1999). Some exhibited sexual dimorphism, most appear to have been diurnal, and most were likely frugivores or folivores (Rose, 1995).

Omomyoids remained primarily small bodied (<100 g) though a radiation of omomyoids took place in North America and included larger bodied species (exceeding 2 kg) after the extinction of most of the adapoids. Most adapoid and omomyoid species went extinct at the Grande Coupure extinction event, which occurred about 34 MYA at the end of the Eocene and appears to be associated with decreased temperature and humidity in the Northern Hemisphere (Fleagle, 1999; Köhler and Moya-Sola, 1999).

A number of models have been offered to explain the evolution of primates. Early models of primate origins (e.g., Jones, 1916) explained the suite of distinctive primate characters as adaptations to life in an arboreal environment that favored emphasis on the visual system and grasping hands and feet. However, as pointed out by numerous critics (e.g., Cartmill, 1974), this explanation ignores the fact that most nonprimate arboreal animals possess claws rather than nails, do not have grasping hands and feet, have laterally directed eyes, and rely heavily on olfaction. Thus, a generalized adaptation to an arboreal environment is unlikely to account for the evolution of these derived traits in primates. Additionally, it has become evident that the closest living relatives of primates (the archontans) are all at least partly arboreal; suggesting that the adaptive shift in early primates involved something beyond simply colonization of the trees.

More recent models have sought to explain the origin of primates as result of specific adaptive shifts within the arboreal environment. Cartmill's visual predation model (1974, 1992) explains the evolution of primate characteristics as an adaptive suite of features related to visual prey detection and predation (primarily on insects) on terminal branches and in the forest undergrowth. In contrast, Sussman (1991) has argued that it was not visual predation that led to the evolution of the primate traits but instead they are related to terminal branch feeding on the products of flowering plants (e.g., fruit, nectar, etc.), as well as the insects that pollinate these flowering plants. Terminal branch feeding as the impetus for the evolution of prehensile hands and feet, irrespective of diet, has received support in comparative studies of didelphid marsupials (Lemelin, 1999).

Information on primate bioenergetics has important implications for evaluating alternative models of primate origins. In particular, since body size has important energetic consequences and is critical in shaping dietary patterns, information on the size of early primate ancestors provides an important link to energetics and metabolism.

In general, among primate species there is an inverse relationship between body size and DQ (Leonard and Robertson, 1994; Sailer et al., 1985). This relationship (the "Jarman-Bell" relationship; Bell, 1971; Gaulin, 1979; Jarman, 1974) appears to be a consequence of the Kleiber scaling relationship between mass and metabolic rate. Large primates have high total energy needs, but relatively low mass-specific requirement, and are able to meet their energy demands by feeding on resources that are widely abundant but lower in quality (e.g., leaves, other foliage). In contrast, small primates have low total energy needs, but extremely high requirements per unit mass. These species tend to subsist on food items that are limited in their abundance but rich in energy and nutrients (e.g., insects, small vertebrates, saps, and gums).

Thus, as data on extant species show, body size greatly shapes and constrains the types of foods on which a primate can subsist. For example, insectivorous diets can only be sustained in very small animals and folivorous diets can only be sustained in considerably larger animals (Kay, 1984). Insects are excellent energy and protein sources for small animals, given their high relative energy demands. Conversely, leaves can provide an ample source of energy for larger bodied animals because of relatively lower energy requirements and longer gut passage times that allow for more nutrient extraction. However, animals smaller than about 700 g have a difficult time sustaining themselves energetically on a diet largely based on leaves. Fruits typically provide an ample source of available carbohydrates but are limited in terms of available protein. Frugivorous animals must supplement their diet with other sources of protein such as insects, leaves, or vertebrates.

Fossil and comparative studies of living animals suggests that the earliest primates were small bodied, with body sizes considerably smaller than 500 g and likely under 100 g. These early primates were likely primarily arboreal, nocturnal, inhabited tropical forests, and were adapted for climbing, grasping, and leaping in a fine-branch niche (Rose, 1995; Martin, 1990). As noted by Martin (1990), this ancestor was similar in many respects to living mouse lemurs and dwarf bushbabies, and contrasts markedly with the tree shrews, which are commonly used as early-primate analogs.

Considering the metabolic data on two strepsirrhines under 100 g (Galagoides demidoff and Microcebus murinus), we find that both are hypometabolic, with deviations from predicted RMR of -23.85 and -37.51%, respectively. While no haplorhines in the sample are below 100 g, the 105 g Cebuella pygmaea and the 113 g Tarsius syrichta are both also hypometabolic, with deviations of -21.78 and -34.80%, respectively. These species all have relatively high-quality diets and all obtain considerable energy from insects. While tarsiers are the only living primates to subsist on 100% animal prey (primarily insects), the living strepsirrhines under 100 g, G. demidoff and members of the genus Microcebus (including M. murinus and M. rufus), consume high-quality diets with varying amounts of insects and vertebrates (Atsalis, 1999; Charles-Dominique, 1977; Mittermeier et al., 1994). Galagoides demidoffconsumes roughly 70% insects and supplements these primarily with fruit and gums (Charles-Dominique, 1977). Microcebus murinus has an omnivorous diet that includes insects, fruits, flowers, small vertebrates, insect secretions, gums, nectars, and other plant products (Corbin and Schmid, 1995; Hladik et al., 1980; Martin, 1973). Microcebus rufus appears to be heavily reliant on both fruit and insects, and has been described as a frugivore-faunivore (Atsalis, 1999). Interestingly, while M. rufus consumes a variety of plant species, it is heavily reliant upon several varieties of Bakerella (a type of mistletoe) known to have a very high fat content. Both M. murinus and M. rufus show seasonal shifts in diet (Atsalis, 1999; Hladik et al., 1980).

The ancestral primate most likely relied heavily on insects, especially during certain seasons, and supplemented its diet with high-quality plant parts, such as fruits, as well as small vertebrates. As pointed out by Martin (1990) it is in the terminal branches of tropical trees and shrubs that insects and fruit resources would have been most readily available to the earliest primates. Terminal branch feeding and its associated anatomical features in primates may have evolved to exploit changing patterns of insect and fruit availability that resulted from radiation of angiosperms during the Early Cenozoic. Low maintenance and total energy costs may have enhanced survival in early primates, especially in environments with low overall productivity and/or marked seasonality.

While hypometabolism can enhance survival in certain environments, there are important reproductive consequences of hypometabolism. Mammalian species with relatively low-metabolic rates also tend to have low-intrinsic rates of population growth (McNab, 1980, 1986). However, while population growth may be slower in hypometabolic species, there are environments where this would clearly be favored. The depressed metabolic rates of some mammal and bird species from isolated oceanic islands appear to be the result of selection for resource minimization in an environment with limited resources (McNab, 1994). It has been suggested that hypometabolic insectivores are better able to deal with seasonal fluctuations in food abundance (McNab, 1980). There is also evidence from bats that indicates that low-metabolic rates are important for coping with variation in food availability (i.e., avoiding starvation during periods of low-insect availability) (Audet and Thomas, 1997). Additionally, nonseasonal torpor and hibernation can confer considerable energy savings to small-bodied mammals (Wang and Wolowyk, 1988).

Thus, the physiological ecology of extant small-bodied strepsirrhines strongly suggests that the earliest primates were hypometabolic and heavily reliant on insects. The specific explanations for why hypometabolism is so common among small-bodied primates remain unclear; however, the patchy and seasonally variable nature of key food resources for these species may have played an important role. Further, it appears that the low-metabolic rates common among all extant strepsirrhines may have a deep evolutionary history. Such an interpretation implies that increased rates of metabolic turnover (and greater encephalization) occurred with the evolution of larger-bodied primates that were reliant on a different suite of food resources.

Was this article helpful?

0 0

Post a comment