Did extinct lemurs exploit fibrous food sources

Evidence for folivory in many of the extinct lemurs also supports the inference of energy-conserving lifestyles. In general, herbivores consuming low-calorie, fiber-rich foods have lower basal and field metabolic rates than those consuming higher "quality" foods, and certainly than carnivorous or omnivorous species (Anderson and Jetz, 2005; Calder and Dawson, 1978; Cruz-Neto and Bozinovic, 2004; McNab, 1974, 1983, 1986). This applies to large as well as small-bodied animals (e.g., Christiansen, 2004). Among extant lemurs, folivorous species have very low total energy budgets (Nash, 1998; Warren and Crompton, 1997, 1998). It is likely that the same applied to the large-bodied, folivorous subfossil lemurs.

Trophic adaptations are registered in the teeth as well as aspects of cranial architecture of extinct species. The second molar shearing quotients and ratios, calculated on the basis of shearing crest and molar lengths for Megaladapis spp., Palaeopropithecusspp., and Babakotia radofilai, are all extremely high, suggesting strong folivory (Jungers et al., 2002; see also Kay, 1984). The sharp edges formed as the molars wear bear further testimony to folivory (Figure 2). Microwear data also support folivory in many species—particularly the largest of the subfossil lemurs, Archaeoindris fontoynontii and all members of the genus Megaladapis (Godfrey et al., 2004a; Rafferty et al., 2002).

The most speciose family to have succumbed to extinction was the Palaeopropithecidae (sloth lemurs: Palaeopropithecus spp., Archaeoindris, Babakotia, and Mesopropithecus spp.)—the sister clade to the extant Indriidae.

Figure 2. Maxillary first and second molars of a young Megaladapis edwardsi. This individual has unreplaced deciduous premolars and its third molar is in its crypt. The M2 is not quite in occlusion. Note the long shearing crests, which form sharp edges as they begin to wear (e.g., M1).

About 40% of all known extinct lemur species are sloth lemurs. Not merely do their teeth bear long shearing crests but their microwear signatures are very like those of indriids (Godfrey et al., 2004a). Palaeopropithecus is known to have shared with indriids a highly unusual dental developmental trajectory signalling early acquisition of ecological adulthood (Schwartz et al., 2002; see below). Indeed, the entire suite of digestive specializations that distinguish indriids from lemurids and other extant lemurs may have been present in the common ancestor of the Indriidae and Palaeopropithecidae. Like all lemurids (except the highly derived bamboo lemurs), indriids consume varying amounts of fruit and foliage, but they differ from the former in their lower dependence on ripe fruit, higher dependence on seeds, and adaptations for processing and digesting fiber-rich foods (Campbell et al., 2000, 2004; Hemingway, 1996; Meyers and Wright, 1993; Overdorff and Strait, 1998; Yamashita, 2003). In effect, the indriids are (and most probably, the palaeopropithecids were) physiological folivores, adapted to maximize the potential utilization of resources rich in structural carbohydrates.

Not all of the extinct lemurs were folivorous. There is compelling evidence (in the form of macrowear signalling heavy chemical erosion, presumably due to the consumption of highly acidic foods, as well as microwear) that Pachylemur, the sole extinct member of the family Lemuridae, preferred fruit (Godfrey et al., 2004a; Vasey et al., 2005). The Archaeolemuridae appear to have had extremely coarse and probably diverse diets most similar to those of tufted capuchins, pitheciins, and aye-ayes (Godfrey et al., 2004a, 2005a). Indeed, not merely is the microwear signature of Archaeolemur remarkably like that of Cebus apella (omnivore, seed predator, hard-object processor; Anapol and Lee, 1994; Peres, 1994;

Phillips et al., 2004; Port-Carvahlo et al., 2004; Sampaio and Ferrari, 2005; Simmen and Sabatier, 1996), but fecal pellets found associated with a young individual in a cave in northwest Madagascar demonstrate that Archaeolemur consumed small vertebrates and gastropods as well as plants (Burney et al., 1997). The occlusal relief characteristics of the molars of Archaeolemur are also more similar to C. apella than to papionins (King et al., 2005). Cranial architecture and molar microstructure (heavy enamel prism decussation, extraordinarily thick enamel; Godfrey et al., 2005a) also support hard-object processing in Archaeolemur. Hadropithecus may have included some C4 grasses in its diet (see the discussion above of its stable isotope signature) but its coarse microwear and cranial architecture suggest some hard-object processing (Godfrey et al., 2004a, 2005a). A diverse, omnivorous diet somewhat similar to that inferred here for Archaeolemur as well as to that attributed to Paranthropus robustus or Australopithecus africanus (Peters and Vogel, 2005) is also consistent with its stable isotope signature. There are no known molars of the giant aye-aye (Daubentonia robusta), but postcranial adaptations (an elongate, filiform third digit of the hand) confirm a pattern of exploitation of structurally-defended resources very like that of its much smaller congener, D. madagascariensis (Simons, 1994). Fruits, seeds, and animal matter were likely staples for the Archaeolemuridae as well as the giant extinct aye-aye.

In summary, leaves were likely staples or important fallback foods in the diets of most subfossil lemurs (certainly the sloth and koala lemurs), but alternative special diets (e.g., exploitation of hard or structurally-defended resources) characterized other clades (the Archaeolemuridae and Daubentoniidae). Pachylemur was highly frugivorous.

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