greater flexibility in the joints. Though the fourth finger is the longest finger on the hand, the middle finger achieves exceptional reach because the metacarpal to which it is attached acts as an extension base and the web of skin between the second and fourth fingers has been suppressed (Jouffroy, 1975). A ball and socket joint at the metacarpophalangeal articulation allows for extraordinary flexibility in every direction. The aye-aye's hand has evolved in such a way as to allow for increased reach and flexibility, which are especially useful when the animal reaches into a deep or oddly shaped cavity to extract insect larvae (Milliken et al., 1991).
The aye-aye uses this specialized finger to acquire most of its major food resources, including nectar, seeds, and wood-boring insects (Figure 7). When probing a cavity in wood for insect larvae, the middle finger may bend as much as 30 degrees toward the dorsum of the hand, allowing the curved claw to follow the wall of the cavity. In this way, the claw moves past the larva in the cavity instead of pushing it into a deeper, irretrievable location. The finger's ball and socket joint permits excursions in any direction, and Milliken et al. (1991) found that aye-ayes can reach and extract larvae from acute, obtuse, and right-angle cavity orientations. When the flesh of the fingertip comes in contact with a larva, the distal phalanx and claw move ventrally to encircle and balance it for retrieval. Rather than pulping the larva inside the cavity, or impaling it on the claw, the aye-aye hooks it with the claw and lifts it out, permitting the recovery of the entire larva. Aye-ayes seem to possess a highly developed tactile sense, as they typically lift their finger out of a cavity only if there is a larva on the claw.
Another striking feature of the aye-aye's hand specialization is independent digit control in the middle finger. When the aye-aye moves along a wood surface and taps the wood with its middle finger, the tapping finger moves substantially faster than the other digits. Similarly, videotapes of aye-aye hands probing cavities showed the movement of the middle digit inside the cavity to be substantially greater than that of the hand and fingers external to the cavity. The aye-aye's hand specializations are remarkable in that a single digit has evolved special capabilities for intricate foraging, while the remaining digits have retained their original form (Milliken et al., 1991).
In addition to its manual specializations, the aye-aye has several other morphological features that make these foraging behaviors possible. The facial skeleton is bent forward relative to the cranial base, possibly as an adaptation for generating and dissipating the large forces needed to chisel through wood and hard fruit carapaces (Cartmill, 1974). While the basic morphology of the aye-aye's facial muscles is clearly that of lemuriform primates, the muscle structure of the oral area and the pinnae more closely resembles that of the Lagomorpha and the rodents (Seiler, 1974). These specialized muscles may assist the aye-aye in using its rodentlike upper incisors for gnawing wood, and to swivel its large ears while feeding. Daubentonia also exhibits an unusually high degree of encephalization among primates, comparable only to that of Homo, Pan, and Cebus. Gibson (1986) notes that these genera show a correlation between large brain size, omnivorous extractive foraging, and complex sensorimotor intelligence. Wild aye-ayes have exhibited sophisticated object manipulations while foraging that are indicative of stage five or six of a modified Piagetian scheme of sensorimotor intelligence. However, behavioral studies suggest that aye-ayes may not achieve higher than a level four or five, and that the advanced tool use observed in the field may have been a result of stage five trial-and-error learning or even simpler learning mechanisms (Sterling and Povinelli, 1999).
The apparent lack of advanced sensorimotor intelligence in the aye-aye calls for an examination of other possible explanations for the extreme encephalization of Daubentonia relative to other prosimian species. The areas of the aye-aye's brain that are enlarged compared to those of other prosimians, including the pons-ventral area, cerebral hemispheres, and cerebellum, have all been implicated in fine motor coordination, olfaction, or auditory capacities. Many of these brain areas are involved in regulating voluntary, rapid repetitive motions, such as those used by the aye-ayes when tapping with their attenuated middle digit. Daubentonia's enlarged brain size may have more to do with the evolution of a fairly narrowly focused set of sensory-perceptual mechanics supporting its specialized foraging techniques than the evolution of broad, domain general cognitive structures (Sterling and Povinelli, 1999).
Field studies have shown that aye-ayes spend 5-41% of their feeding time tap-foraging for wood-boring insects, compared to 11-85% searching for and feeding on seeds or hard-coated fruits (Sterling, 1994a), but tap-foraging behavior has attracted special attention from researchers because it involves a fascinating combination of specialized senses and behaviors. Aye-ayes appear to belong to a small group of vertebrates that uses self-generated acoustical cues when foraging. Other members of this group include bats, cetaceans, woodpeckers, and the striped possum (Dactylopsila trivirgata). The aye-aye's large and flexible ears suggest that hearing plays an important role in an individual's ability to find food. Olfactory signals may also be important, given that the animal sniffs along the surface of the wood as it forages. The sense of touch may play a role as well; the tapping of the third finger is unexpectedly gentle, and it is possible that this extremely slender digit provides an unusual detection of and discriminability among surface vibrations (Erickson, 1991).
Auditory cues are believed to be especially important in prey location by foraging aye-ayes. The pinnae of the aye-aye are more mobile and proportionately larger than in any of the other lemuroid prosimians, and rotate forward when an individual is tap-foraging (Figure 8). In a series of studies on captive aye-ayes, Erickson (1991) found that study animals readily opened cavities in wooden logs, regardless of whether the cavities were empty or contained live or dead mealworms. The aye-ayes gnawed in areas where there were cavities, but not where there were only surface holes, implying that visual cues do not play a role in the decision to excavate. Study animals opened cavities that contained active mealworms slightly more often than they opened empty ones, suggesting that they may be able to identify cavities that contain insects. The tapping may stimulate prey to make audible movements, which would make them easier to detect underneath the wood.
The results of a later study (Erickson, 1998) provide further support for the ability of aye-ayes to locate insects inside a cavity. Captive aye-ayes were presented with wood blocks containing long, narrow channels, designed to resemble the mines of wood-boring insects that an aye-aye would encounter in the wild (Erickson, 1995). Portions of the channels were filled at random with frass or grubs, and other sections were left empty. Aye-ayes captured grubs located in the midsections of the mines as often as they captured those located in the end sectors, indicating that they do not pursue a simple strategy of following the mine to its terminus or to a larva. These results are consistent with those of field data showing that excavations are found both at the mine terminus and in the midsection. Overall, study animals found more than 75% of the grubs in the mines.
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