Phylogenetic Influences on Strepsirrhine Hypometabolism Implications for Subfossil Lemurs

The extant lemurs of Madagascar are diverse in species number, morphological adaptation, and ecology, but there is evidence that this diversity was much larger in the recent past (Godfrey and Jungers, 2002; Mittermeier et al., 1994; Simons, 1997). Known primarily from recent paleontological sites (i.e., "subfossils"), there is evidence for at least 17 species representing at least five families of extinct lemurs: Archaeolemuridae, Daubentoniidae, Lemuridae, Megaladapidae, and Palaeopropithecidae (Godfrey and Jungers, 2002). Only two of these, Daubentoniidae and Lemuridae, have living representatives. Humans initially colonized Madagascar only about 2000 years ago and are implicated in the extinction event of numerous lemur species, as well as three species of hippopotamus, two species of bibymalagasy, a medium-sized carnivore, two genera of flightless birds, and a species of giant tortoise (Garbutt, 1999). Human activities, such as hunting, habitat alteration, introduction of nonnative species (e.g., wild cattle), and possibly, the introduction of nonnative diseases, likely played a major role in the extinction. There is also some evidence that Late Holocene climatic changes might have contributed to the extinctions. The range of dates for subfossil lemurs runs from about 26,000 years BP (Megaladapis from Antsiroandoha Cave in northern Madagascar) to about 500 years BP for Palaeopropithecus from Manamby Plateau in southwest Madagascar (Simons, 1997). Additionally, there is a historical report that suggests the presence of a large-bodied lemur in Madagascar in the 17th century (Flacourt, 1658). Ethnographic sources also suggest that a large-bodied lemur might have survived in Madagascar into the 20th century (Burney and Ramilisonina, 1999). By all indication, the subfossil and extant lemurs are part of the same contemporary fauna and the former should not be considered as ancestors of the latter (Mittermeier et al., 1994).

All of the subfossil lemurs, with the exception of Daubentonia robusta (a relative of the aye-aye), are thought to have been diurnal, based on relative orbit size and body size (Simons, 1997). An enormous range of locomotor diversity is seen in the subfossil lemurs, but it seems likely that, based on body size and postcranial morphology, most of the subfossil lemurs likely spent at least some time on the ground (Godfrey et al., 1997). Certain groups, such as Hadropithecus and Archaeolemur, may have spent considerable time on the ground (Godfrey et al., 1997). With the possible exception of D. robusta, all extinct lemur species likely included some leaves in their diet, supplementing this diet with fruit, seeds, and possibly fauna. Many of the larger species are inferred to be highly folivorous on the basis of both body size and morphological adaptations.

Body mass reconstructions, based on regressions of humeral and femoral midshaft circumferences indicate that the subfossil lemurs were all larger than living strepsirrhine primates (Godfrey et al., 1997; Table 4). Some species had body masses slightly greater than the largest living strepsirrhines (Indri indri and Propithecus diadema) (Smith and Jungers, 1997); however, all known species appear to have had body masses of at least 10 kg (Godfrey et al., 1997). Numerous species were considerably larger, including Archaeoindris fontoynontii, which is estimated to have reached an adult body mass of about 200 kg.

The RMR predictions for 16 species of subfossil lemur are presented in Figure 4 and are based on body masses reconstructed for subfossil taxa (Table 4). For a given body mass, we calculated RMR based on the Kleiber scaling relationship (70M0 75) and a strepsirrhine-only regression from this study (36.3M0 56), which assumes that the subfossil lemurs were hypometa-bolic (based on the retention of the primitive condition). Assuming metabolic rates similar to those seen in living strepsirrhines, there would have been considerable energy savings in all species, which would have been amplified at larger body sizes. For example, in the largest of the subfossil lemurs, A. fontoynontii, with an estimated body mass of 200 kg, would have had an RMR (using the strepsirrhine-only regression) of only about 20% of that predicted by Kleiber scaling relationship. This energy savings likely would have been further amplified through low-total energy costs, as is likely based on morphological evidence, which indicates a highly folivorous sloth-like creature that probably spent considerable time on the ground (Simons, 1997). One of the consequences of depressed metabolic rates is that they may have had the effect of limiting competition for resources (McNab, 1980). However, there are also reproductive consequences of depressed metabolic rates as there is some indication that mammalian species with depressed metabolic rates also have low-intrinsic rates of population increase (McNab, 1980, 1986).

Data on cranial capacity for five species of subfossil lemurs (Table 4) demonstrated a similar scaling relationship of brain size and body mass as in


Figure 4. Predicted RMR (kcal/day) for selected subfossil Malagasy lemurs based on reconstructed body weights from Godfrey et al. (1997). Gray bars represent predicted RMRs based on the Kleiber scaling relationship (70M0 75) and black bars represent predicted RMRs based on the strepsirrhine regression (36.3M0 56).

Figure 4. Predicted RMR (kcal/day) for selected subfossil Malagasy lemurs based on reconstructed body weights from Godfrey et al. (1997). Gray bars represent predicted RMRs based on the Kleiber scaling relationship (70M0 75) and black bars represent predicted RMRs based on the strepsirrhine regression (36.3M0 56).

extant strepsirrhines (Figure 2). M. madagascariensis and P. maximus have similar body masses (40 kg and 55 kg, respectively) as common chimpanzees (P. troglodytes) though their brain sizes are only about one-quarter the size. However, there is variation in the subfossil lemurs in relative brain size; data from A. edwardsi indicate that it was relatively encephalized when compared to the larger subfossil lemurs. These results are in general agreement with Jungers (1999), and demonstrate that strepsirrhines have larger brains than similar-sized mammals but considerably smaller brains than haplorhine primates. This may be the result of physiological limitations in supporting brain metabolism (Armstrong, 1983, 1985).

It seems likely that the earliest strepsirrhine colonizers of Madagascar were hypometabolic and small bodied. Purvis (1995) suggests that mouse and dwarf lemurs of the family Cheirogaleidae are the most ancestral of extant lemurs and, on these grounds, it seems likely that the initial colonizers of Madagascar were small-bodied and later diversified in terms of body size. However, this evidence is currently untestable given the dearth of pre-Holocene primate fossils from Madagascar. Depressed metabolic rates and the ability to enter torpor may also have increased chances of survival during a transoceanic rafting to Madagascar from Africa (Kappeler, 2000; Warren and Crompton, 1996). These low-metabolic rates may have had important consequences for the survival and diversification of Malagasy primates.

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