Miniature Flower Specialists

Sussman (1991, 1995, 1999) suggested that the key ecological factor leading to the origin of primates was adaptation to the utilization of angiosperm products—fruit and flowers—at the tips of terminal branches. There is still some question as to whether one particular food item was crucial in the evolution of the earliest primates, or whether primate adaptations are better seen as related to a general exploitation of terminal branch resources. The presence in Australasia of several independent lineages of small mammals specially adapted to the use of flowers has obvious relevance to the angiosperm exploitation theory. Are flower specialists among the phalangeroids particularly primate-like in their hand and foot structure, visual systems, brain sizes, or reproductive patterns?

The most widespread flower specialists in Australia are the pygmy-possums of the genus Cercartetus, distributed in the rainforests of New Guinea and Queensland (C. caudatus), rainforest to dry forest of southeastern Australia (C. nanus), a variety of drier forests of southern Australia and Tasmania (C. lepidus), and dry forest, heath, and scrub of southwestern Australia (C. concinnus). These are tiny mammals, with the smallest, C. lepidus, being only 6-9 g, while the largest, C. caudatus, is 25-70 g. In other words, the largest Cercartetus overlaps in size with the smallest living primate, Microcebus, several species of which fall within the range of 26-77 g (Atsalis et al., 1996). Several early Tertiary primates are as small as Cercartetus, including the earliest certain euprimate from the very base of the Eocene, Teilhardina, and a community of tiny primates from the middle Eocene of China, which includes species possibly as small as 12 g (Gebo et al., 2000). Key morphological attributes of Cercartetus include relatively short snout, large eyes, moderate degrees of orbital convergence, prehensile tail, and grasping hands and feet with reduced claws and expanded lobes on the distal pad. Several authors have repeated the observation that in proportions the forefoot looks like a human hand. These animals show a close physical resemblance to Microcebus in their overall shape, in the short soft fur, and in the grayish to reddish brown coloration often with dark spectacles around the eyes (Figure 2). Marsupial biologists have noted the close resemblance

Figure 2. Comparison between the possum Cercartetus (A) and the primate Microcebus (B). Photograph (A) by R. Whitford, reproduced with permission from Nature Focus © Australian Museum; photograph (B) by R. Mittermeier, reproduced with his permission.

Figure 2. Comparison between the possum Cercartetus (A) and the primate Microcebus (B). Photograph (A) by R. Whitford, reproduced with permission from Nature Focus © Australian Museum; photograph (B) by R. Mittermeier, reproduced with his permission.

between pygmy-possums, the didelphid Marmosa, and the cheirogaleid Microcebus (Lee and Cockburn, 1985). Cartmill (1974a) emphasized the relevance of Cercartetus to primate origins because of their reduced claws and convergent orbits, writing "the adaptations of Cercartetus... represent plausible structural antecedents for the traits that distinguish the extant primates." He pointed out that the orbital marginal orientation (a measure of convergence) of Cercartetus caudatus is almost identical to that of Galago, Avahi, and Tarsius.

Species of Cercartetus are arboreal and nocturnal. They have been noted to be agile scramblers and leapers (Atherton and Haffenden, 1983). Cercartetus has been characterized as a flower specialist, with the diet usually including a significant proportion of nectar and pollen (Lee and Cockburn, 1985; Turner, 1984). They also eat blossoms, fruit, and arthropods (Smith, 1986). Individuals apparently forage solitarily at night, but groups of up to four individuals have been found sleeping together in nests, another similarity to some cheirogaleids (Collins, 1973). Physiologically, they also show some interesting parallels with prosimians—towards the end of the summer, the base of the tail in Cercartetus expands as a result of fat storage, as in the primate Cheirogaleus medius, and they undergo seasonal periods of torpor, also as in cheirogaleids (Hladik et al., 1980; Wright and Martin, 1995). Cercartetus diverges from cheirogaleids in its higher rates of reproductive output—females have four nipples but may occasionally produce five or six offspring (Ward, 1992). From an ecomorphological perspective, Cercartetus appears to offer much promise in helping to understand parallel evolution of primate-like attributes in a small, terminal-branch feeding mammal.

The case of the burramyids highlights how important it is to obtain precise ecological and behavioral data, even in the presence of solid morphological data, in order to test ideas about primate origins. Cartmill's (1974a) generalization that Cercartetus and Burramys "forage for fruit and insects in the shrub layer of Australian forests and heaths" is no longer a fair characterization of their habits in light of what has been learned recently about these animals in the wild. Burramys, the one member of the group that falls well outside the characterization of "flower specialist," is a divergent taxon adapted to alpine and subalpine habitats, where it lives terrestrially in boulder screes, eats fruit, and stores winter supplies of seeds (Lee and Cockburn, 1985). Burramys shares plagiaulacoid lower premolars (high serrated bladelike teeth) with a very few other mammals, including the extinct, early Tertiary plesiadapiform Carpolestes (Rose, 1975; Simpson, 1933). The interpretation by the paleontologist Rose (1975) that the carpolestid diet may have consisted of tough herbage, fruits, and seeds, along with insects, is buttressed now by initial data on the actual diet of the dentally similar Burramys, which consists of grasses, fruits, seeds and insects (Calaby, 1983; Lee and Cockburn, 1985). The functional use of the plagiaulacoid p4 is illuminated by observations of Burramys: "hard-shelled seeds and insects with hard cuticles are held at the sides of the mouth and broken or cut up with the premolars. Efficient use of these teeth requires that the animal also have highly manipulative forepaws" (Calaby, 1983). In addition, Burramys uses the specialized premolars to slice grasses for storage in nests (Calaby, 1983). Although insects are fed upon by Burramys, we believe that characterization of this genus as a model of a primitive arboreal visual predator (Cartmill, 1974a) was premature given their dental specializations and what is now known of their diet. But as outlined below, its relevance for other models of primate origins may be more relevant given the recent postcranial discoveries about Carpolestes (Bloch and Boyer, 2002).

The adaptations of Cercartetus also differ significantly from Cartmill's (1974a) characterization. The species that has been studied best (C. nanus) is a flower specialist, particularly dependent on pollen and nectar, rather than eating the blossoms themselves; the species also feeds on insects associated with their food flowers (Turner, 1984; Figure 3). Indeed, most of the insects eaten by C. nanus are suspected to have been obtained directly from the flowers of Banksia (Lee and Cockburn, 1985). Less is known of the diet in C. caudatus-, the one specific item of the natural diet listed by Atherton and Haffenden (1983) is nectar from a species of eucalypt (note this is the possum classified in the genus Eudromicia by Cartmill, 1972). The western species, C. concin-nus, lives in a variety of drier forests and heath habitats, and is known to be partly terrestrial in its activity. The tiny species C. lepidus is reported to be primarily insectivorous, in contrast to its congeners (Green, 1983), but it is also poorly studied, with little information available about where and how it finds insects, and how this relates to other food resources. All species of the genus probably eat arthropods, and interestingly, captive C. nanus have been

Figure 3. Flower feeding by the possum Cercartetus (A) and the primate Cheirogaleus, photograph (A) © Kathie Atkinson; photograph (B) by David Baum, reproduced with his permission.

Figure 3. Flower feeding by the possum Cercartetus (A) and the primate Cheirogaleus, photograph (A) © Kathie Atkinson; photograph (B) by David Baum, reproduced with his permission.

seen capturing flying moths by snatching them out of the air with two hands (Atherton and Haffenden, 1983). While the observed behavior associated with insect capture fits well with expectations from Cartmill's visual predation hypothesis, it occurs in an ecological context that matches Sussman's angiosperm exploitation hypothesis. Based on current data, the best-known species of Cercartetus may be characterized as a flower specialist that captures insects opportunistically from the flowers themselves. This is very similar to the ecological pattern observed in the primate-like didelphid (Caluromys), which captures insects flushed while foraging among fruit and flowers at the tips of branches (Rasmussen, 1990; Steiner, 1981). We suggest that both cases offer support for the idea that it is the combined windfall of insects associated with fruit and flowers that provides an ecological stage for the development of primate-like adaptations (Crompton, 1995; Martin, 1986, 1990; Rasmussen, 1990, 2001; Sussman and Raven, 1978; Sussman, 1999).

The acrobatids closely resemble Cercartetus in many respects, and were traditionally classified with that genus in the family Burramyidae based on close physical similarity, but molecular studies appear to have eliminated a close phy-logenetic relationship between acrobatids and burramyids (Baverstock, 1984). The most salient physical difference between acrobatids and Cercartetus relates to the tail—both acrobatid genera (Acrobates of Australia, Distoechurus of New Guinea) have a pair of stiff fringes of hair extending laterally from the tail, resembling a feather. In addition, Acrobates possesses a gliding membrane stretching from elbow to knee, and is adept at sailing. Acrobates also has finely serrated distal pads on their hands and feet that allow them to gain purchase on smooth surfaces, including vertical panes of glass (Russell, 1983). Distoechurus has small, sharp, curved claws and no expansion of the distal digital pads. Both genera are tiny, agile, nocturnal animals that apparently rely on flower products and associated insects in a variety of forest types (Goldingay and Kavanagh, 1995; Lee and Cockburn, 1985). Up to forty individuals of Acrobates have been spotted together in a single flowering tree crown. The two acrobatids parallel primates but diverge from Cercartetus in having small litters; the 1-4 offspring produced by them is less than would be predicted from their tiny body masses (Ward, 1990). Like Cercartetus and some cheirogaleids, Acrobates undergoes periods of torpor (Jones and Geiser, 1992). This group offers another evolutionary view of a small-bodied mammalian flower specialist, this time with the trick of gliding added (in Acrobates) as a way to get around among the terminal branches of a tropical flowering tree (Figure 4).

Figure 4. Two genera of miniature flower specialists, Acrobates (A) and Distoechurus (B). Photograph (A) reproduced with permission from Nature Focus © Australian Museum; Photograph (B) Kathie, Atkinson, reproduced with permission from Nature Focus © Australian Museum.

Figure 4. Two genera of miniature flower specialists, Acrobates (A) and Distoechurus (B). Photograph (A) reproduced with permission from Nature Focus © Australian Museum; Photograph (B) Kathie, Atkinson, reproduced with permission from Nature Focus © Australian Museum.

The final miniature flower specialist is the honey possum, Tarsipes rostratus, the genus name being derived from its tarsier-like foot. While Tarsipes does indeed have primate-like hands and feet with reduced claws, capable of fine grasping (Cartmill, 1992; Renfree et al., 1984), the honey possum is much less primate-like in other respects than are Cercartetus and the acrobatids. Compared to all other phalangeroids, it has an elongated snout (even described as "beaklike" by Szalay, 1994), pronounced development of facial vibrissae, and eyes lacking much convergence. Tarsipes has a specialized, bristle-tipped tongue—which can be extended 25 mm beyond the nose—for harvesting nectar and pollen, and the cheek teeth are reduced to peg-like rudiments. Insects are taken infrequently, if ever (Lee and Cockburn, 1985; Renfree et al., 1984; Wiens et al., 1979; but see Wooller et al., 1984). A bristled tongue used in procuring pollen and nectar is also found in the primate Eulemur rubriventer (Overdorff, 1992; Sussman, 1999). The scansorial Tarsipes lives on sandplain heaths in southwestern Australia, where it is often on the ground; e.g., it is found in pitfalls such as fence postholes. The elongated snout is supposed to be an adaptation for probing flowers, but in proportions, it is reminiscent of rostra seen in other small-bodied terrestrial mammals such as tenrecs, shrews and elephant shrews. Tarsipes can be held up as the ultimate nectar specialist among mammals. Unlike Cercartetus, Tarsipes is not highly arboreal nor does it seem to feed on insects attracted to flowers or the fruit that are generated from flowers. Tarsipes therefore represents an excellent evolutionary trial to help tease apart factors that contribute to primate-like hands and feet, but not primate-like faces. In this case, the obvious inference is that prehensile hands and feet are used for fine-branch grasping, not for insect capture.

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