Review of Didelphid and Cheirogaleid Ecology and Behavior

The family Didelphidae—commonly called the American opossums—is a group of marsupial mammals that is distributed throughout the New World, mainly in Mexico, Central America, and most of South America (Eisenberg, 1989; Nowak, 1999). Only the Virginia opossum (Didelphis virginiana) is found in the United States and parts of Canada (Eisenberg, 1989; McManus, 1974; Nowak, 1999). Traditionally, the family Didelphidae is considered to be a natural group that includes the genus Caluromys, the woolly opossum (Archer, 1984; Kirsch, 1977; Marshall et al., 1990; Reig et al., 1987). However, recent molecular evidence has shown that Caluromys may be more distinct from other didelphids and should be included in its own family Caluromyidae (Kirsch et al., 1997) or subfamily Caluromyinae (Jansa and Voss, 2000). In any event, since Didelphidae and Caluromyidae are sister families, we have retained the term "didelphids" throughout this chapter for practical reasons.

Like primates, didelphids are pentadactyl and show strong differentiation in body size, ecology, and behavior (Charles-Dominique, 1983; CharlesDominique et al., 1981; Collins, 1973; Eisenberg and Wilson, 1981; Hall and Dalquest, 1963; Hunsaker, 1977; Hunsaker and Shupe, 1977; Figure 1). Five genera were considered for this comparative study: Monodelphis, Didelphis, Philander, Marmosa, and Caluromys.

Monodelphis, the short-tailed opossum, is among the smallest didelphids (about 84 g for Monodelphis brevicaudata, Eisenberg, 1989). It is restricted to the ground where it feeds largely on small prey and some fruits (CharlesDominique et al., 1981; Eisenberg, 1989; Hunsaker, 1977; O'Connell, 1979). Cartmill (1972) described Monodelphis as a forest-floor predator that detects prey by smell, hearing, and vibrissal contact and captures them using its mouth; Hershkovitz (1969) characterized it as shrew-like in habits.

At the opposite end of the size spectrum, Didelphis, the large American opossum, weighs between 1 and 2 kg on an average (Eisenberg and Wilson, 1981). Like Monodelphis, Didelphis spends a large amount of its travel and feeding time budget on the ground (Cunha and Vieira, 2002; Eisenberg,

• Fine branches ■ Canopy

Caluromys Marmosa

Vines • Understory Forest floor

■ Large branches • Understory


• Forest floor

Large branches

■ Clearings Forest floor



Forest floor Clearings

Figure 1. Review of didelphid ecology. For each genus, the forest level where it spends most of its time and types of substrates most commonly used are given. The information relative to Marmosa applies for M. robinsoni. Scale differences between animals are accurate. Figures of the opossums are modified after Eisenberg (1989).

Figure 1. Review of didelphid ecology. For each genus, the forest level where it spends most of its time and types of substrates most commonly used are given. The information relative to Marmosa applies for M. robinsoni. Scale differences between animals are accurate. Figures of the opossums are modified after Eisenberg (1989).

1989; Hunsaker, 1977; McManus, 1974). In fact, D. marsupialis spends about 70% of its travel and feeding time on the ground (Charles-Dominique et al., 1981; Rasmussen, 1990). Nonetheless, Didelphis can also climb well, usually on large vertical trunks (Eisenberg, 1989; Hunsaker, 1977; Hunsaker and Shupe, 1977; McManus, 1970, 1974), and branches account for about 25% of the arboreal supports used by D. marsupialis (Charles-Dominique et al., 1981; Rasmussen, 1990). Didelphis feeds on a wide range of prey and fruits (Eisenberg, 1989; Hunsaker, 1977; Liete et al., 1996; McManus, 1974), but consumes more fruits when found in tropical forests compared to other environments (Atramentowicz, 1988; Hall and Dalquest, 1963).

Likewise, Philander, the "four-eyed" opossum, moves primarily on the forest floor (Charles-Dominique, 1983; Charles-Dominique et al., 1981; Cunha and Vieira, 2002; Eisenberg, 1989; Hunsaker, 1977), more often than Didelphis (Atramentowicz, 1988; Enders, 1935; Passamani, 1995). Philander opossum weighs on average between 330 g (Eisenberg, 1989) and 450 g (Atramentowicz, 1986, 1988), and forages almost exclusively on the ground for prey, ripe fruits, fallen off trees, nectars, and flowers (Atramentowicz, 1988; Charles-Dominique, 1983; Charles-Dominique et al., 1981).

Marmosa, the mouse opossum, is a small-bodied didelphid (Marmosa robin-soni averages 116 g, Eisenberg and Wilson, 1981) found in a wide variety of environments (Eisenberg, 1989; Hunsaker, 1977; Nowak, 1999). M. robinsoni prefers secondary forests and clearings where it spends most of its time on vines and bushes, but also descends to the ground (Eisenberg, 1989; Enders, 1935; Hall and Dalquest, 1963; Hunsaker, 1977; O'Connell, 1983). It feeds primarily on insects and uses its hands extensively to manipulate them (Eisenberg and Leyhausen, 1972; Enders, 1935; Hunsaker, 1977; Hunsaker and Shupe, 1977). Fruits also represent an important dietary component of M. robinsoni (O'Connell, 1983). Cartmill (1972) described Marmosa as a shrub-layer insectivore relying heavily on visual detection for stalking prey among the complex network of fine branches and capturing insects with the hands. Very often, M. robinsoni anchors itself on a thin support using its feet, while the hands are used to restrain and manipulate a food object (Hunsaker and Shupe, 1977).

Finally, Caluromys, the woolly opossum, is among the most arboreal didel-phids. It travels and forages on small, terminal branches high in the canopy and very rarely descends to the ground (less than 1% of the time) (Atramentowicz, 1982; Bucher and Hoffman, 1980; Charles-Dominique et al., 1981; Eisenberg, 1989; Hall and Dalquest, 1963; Hunsaker, 1977; Liete et al., 1996; Malcolm, 1991; O'Connell, 1979; Rasmussen, 1990). Caluromys philander weighs on average 300 g and feeds primarily on ripe fruits, gums, and nectar (75% of the total diet), as well as invertebrates (25% of the total diet) (Atramentowicz, 1982, 1986, 1988; Charles-Dominique et al., 1981; Charles-Dominique, 1983; Julien-Laferriere, 1995, 1999; Liete et al., 1996). The locomotion of

Caluromys involves quick, agile, and acrobatic quadrupedalism on terminal branches by efficient grasping with the extremities; suspension, cantilevering, and short leaps have been also observed (Rasmussen, 1990). When feeding on terminal branches, upside-down postures by the hindlimbs and tail are frequent (Lemelin, 1996, 1999; Rasmussen, 1990), and the hands are used extensively for manipulation when consuming fruits and insects (Hunsaker and Shupe, 1977; Lemelin, 1996, 1999; Rasmussen, 1990).

The didelphid marsupials included in this study are characterized by two broad adaptive strategies: Monodelphis, Didelphis, and Philander spend a large portion of their activity budget on the ground. When venturing arboreally, they tend to be on large diameter supports. In contrast, Marmosa has a strong preference for understory vines despite spending some time on the ground, and Caluromys is fully committed to the canopy where it relies mainly on terminal branches. Both Marmosa and Caluromys use their hands more often to manipulate fruits and prey, especially insects. It is also very important to point out that the more frequent use of thin arboreal supports is not size related among didel-phids. Indeed, there are smaller (Marmosa) and larger (Caluromys) fine-branch arborealist opossums, as well as smaller (Monodelphis) and larger (Philander and Didelphis) more ground-dwelling opossums.

The primates included in this comparative study are all members of the family Cheirogaleidae. Like Marmosa and Caluromys, cheirogaleids are agile quadrupeds moving on arboreal supports in search of fruits, gums, nectar, and insects (Hladik, 1979; Hladik et al., 1980; Martin, 1972a,b, 1973; Tattersall, 1982; Walker, 1979). They range in body mass from about 30 g for Microcebus myoxinus and 60 g for Microcebus murinus to about 400 g for Cheirogaleus major, with Cheirogaleus medius falling somewhere in between (Smith and Jungers, 1997). Of all cheirogaleids, mouse lemurs are the most committed fine-branch arborealists, moving and foraging frequently on small branches, twigs, or vines in the undergrowth and lower forest levels (Martin, 1972a,b, 1973). They are also the most predatory cheirogaleids, with prey accounting for about 40% of their diet (Hladik et al., 1980). Mouse lemurs use swift movements of the hands to capture fast-moving insect prey (Bishop, 1964; Lemelin, 1996). During feeding, cantilevering and upside-down postures are used by all cheirogaleids and the hands are used to hold food objects (Lemelin, 1996, 1999; Martin, 1972a; Gebo, 1987). Cheirogaleids share with Marmosa and Caluromys behavioral and ecological similarities that are believed to represent the primitive condition for the order Primates (Cartmill, 1972, 1974a,b;

Charles-Dominique, 1983; Charles-Dominique and Martin, 1970; Eisenberg and Wilson, 1981; Hershkovitz, 1969; Hunsaker and Shupe, 1977; Lemelin, 1996, 1999; Martin, 1972b; Rasmussen, 1990).

On the basis of this review, it is quite clear that these contrasts among didelphids and similarities between Marmosa, Caluromys, and cheirogaleids in ecology and behavior have potential to elucidate the functional role and adap-tiveness of grasping hands and feet with regard to the problem of primate origins. In the next section, we present a functional model that explains why more prehensile hands and feet should be expected in mammals that travel and forage on thin arboreal supports compared to those that spend more time on the ground or larger arboreal substrates.

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