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CHAPTER EIGHT
Adaptations in the Aye-aye:
A Review
Eleanor J. Sterling and Erin McCreless
INTRODUCTION
The aye-aye is one of the most unique primates in the world. In 1863, Richard
Owen, foreshadowing contemporary intelligent design arguments, posited that the
aye-aye’s unique qualities provided clear evidence that Darwin’s theory of natural
selection must be wrong (Owen, 1863). Owen, the most eminent British
anatomist of his time, detailed the aye-aye’s distinctive dental and digital mor-
phology, briefly described how naturalists at the time thought the animal uses these
morphological features to acquire food, and concluded that only God could have
created an animal so well adapted to its environment. Indeed, the aye-aye has a
number of morphological traits that set it apart from other primates and allow it
to exploit resources unavailable to most other animals in Madagascar (Figure 1).
It also exhibits behavioral characteristics that distinguish it from most other
lemurs. Recent research on aye-ayes has begun to overcome obstacles to observ-
ing these animals and has started to shed light on the mysterious social habits of
this species. As we learn more about the aye-aye, we find more ways in which it is
similar to other lemur species, as well as the ways in which it is different.
The aye-aye’s unusual morphological characteristics generated a century of
controversy, beginning with its introduction to Western science in the 1780s
(Sonnerat, 1782), on whether to place Daubentonia within the primates, the
rodents, or even the marsupials (Sterling, 1994c). Owen’s definitive study of aye-
aye anatomy (Owen, 1866) finally quelled the debate over the species’ taxonomic
Lemurs: Ecology and Adaptation, edited by Lisa Gould and Michelle L. Sauther
Springer Science+Business Media LLC, New York, 2007.
161
Eleanor J. Sterlin ●Erin McCreless ●Center for Biodiversity and Conservation, American
Museum of Natural History, New York, NY 10024
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position, focusing attention away from the animal’s rodentlike anterior teeth and
towards its primatelike characteristics, such as a postorbital bar, stereoscopic
vision, and an opposable hallux (Figure 2). Although its placement within the
primates is still being debated, Daubentonia is considered a member of the fam-
ily Indridae (Schwartz, 1986); as a sister taxon to the other Malagasy primates
(Pastorini et al., 2002, 2003; Yoder et al., 1996a,b); and as the most basal branch
of the strepsirhines (Delpero et al. 2001; Groves, 1990).
The only living representative of the family Daubentoniidae, the aye-aye is the
only primate to have claws on all digits but the thumb, a nictitating membrane
(“third eyelid”), and abdominal mammary glands. With a length of 80 cm from
nose to tail and a weight of 2.5–3 kg, Daubentonia is the largest nocturnal pri-
mate species in the world. A distinctive dental formula of 1/1 incisors, 0/0
canines, 1/0 premolars, and 3/3 molars includes incisors that grow continuously
like those of a rodent. The aye-aye is probably best known for its slender middle
finger, in which modifications to the metacarpal provide extra flexibility in the
joint and make the finger appear especially long.
DIET
Many of the aye-aye’s adaptations, especially its chisel-like front teeth and pro-
belike middle finger, enable it to gain access to structurally defended food
resources that are unavailable to most of the vertebrates in Madagascar (Table 1).
162 Eleanor J. Sterling and Erin McCreless
Figure 1. Drawing of a female aye-aye, based on an animal living in the Gardens of the
Zoological Society of London, 1862. Drawing by J. Wolf (Owen, 1866).
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The only long-term study of wild aye-ayes to date was undertaken from 1989 to
1991 on the island of Nosy Mangabe, located off the northeastern coast of
Madagascar. This study found the aye-aye’s diet to consist of items from three
main food types: seeds, fungi, and larvae (Sterling, 1994a). Aye-ayes spent over
90% of their feeding time on only four foods: Canarium (Burseraceae) seeds, lar-
vae, cankers from the Intsia bijuga cambial layer, and nectar (Figure 3). In the
wild, aye-ayes have also been seen to consume seeds of other fruits such as the
palm Orania trispatha and the tropical almond, Terminalia catappa; adult ants;
Adaptations in the Aye-aye 163
Figure 2. Detailed anatomical drawings of the aye-aye’s skull and dental characteristics.
Drawings by J. Erxleben (Owen, 1866).
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a spongy fungus growing on the stems of Macaranga cuspidata; and various cul-
tivated crops, including coconuts, litchis, and mangos.
Two species of Canarium grow on Nosy Mangabe, one found at the island’s
higher elevations, from 250 m to 331 m above sea level, and the other found
164 Eleanor J. Sterling and Erin McCreless
1.0
0.7
0.6
0.5
0.4
0.3
0.2
0.0
0.1
0.8
0.9
Percent of time spent feeding
HD89
HW90 CW90 HD90 HW91
Seed
Nectar
Larvae
Other
Canker
Figure 3. Overall percentage of time spent feeding on different dietary items by season
for aye-ayes on Nosy Mangabe from November 1989 to April 1991. Averages of six indi-
viduals were used to calculate seasonal means. Seasons are: hot, wet (HW); cold, wet
(CW); and hot, dry (HD). Seeds = Canarium spp., T. catappa; other = fungus, ants,
unidentified food sources (Sterling, 1994a).
Table 1. Use of morphological characters for food acquisition by aye-ayes for different
food resources (Sterling, 1994a)
Food resource Incisors Middle finger
Seeds Superior incisors are set mid-endocarp Scrapes out cotyledon
and inferior incisors gnaw into endocarp
Canker Superior incisors serve as point of leverage
as the inferior teeth scrape the growth
Nectar Inserts finger into flower and
brings nectar to mouth with
rapid back-and-forth movements
Larvae Pries off cambium on surface of tree Inserts finger in channel and
or liana or gnaws into seed retrieves larva
Adult insect Raises ant with middle finger and
flicks it into open mouth
Fungus Scrapes fungus off stem of inflorescence
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below 250 m above sea level. Aye-ayes eat Canarium seeds by removing the
endocarp with their long anterior teeth and then extracting the cotyledon with
their slender middle finger (Iwano and Iwakawa, 1988). Individual trees of both
species are large-crowned and abundant on the island, and one study showed the
lowland Canarium species to have the third-highest stem density of all the plants
sampled (Sterling, 1994a). Aye-ayes sometimes spent more than 30% of their
feeding time consuming Canarium seeds, and they appeared to prefer fruits of
the lowland species when they were available. Fruit from one species or the other
is available throughout the year, although both are less abundant during the cold-
est of the three seasons. The preferred lowland species is less common during the
wet, hot season, causing aye-ayes to turn to fallen, and to a lesser extent, upland
Canarium.
To gain access to another of their preferred foods, aye-ayes remove cankers from
a leguminous tree, Intsia bijuga, and then scrape a waxy substance from the under-
lying cambium with their anterior teeth. The growths are found most commonly
on secondary branches and on trunks with more exposure to light and air; it is
either a fungus or a gall, but botanists, entomologists, and local forest specialists
have not been able to identify it further. This resource is patchily distributed and
is restricted to lower elevations on Nosy Mangabe (less than 270 m above sea
level). Aye-ayes eat this food most frequently during the cold season, when
Canarium fruits are less abundant.
Nectar from Ravenala madagascariensis (Strelitziaceae) flowers provides a
high-energy food source for foraging aye-ayes. The animals scoop the viscous liq-
uid out of the flowers with rapid back-and-forth movements of their thin middle
finger. Ravenala inflorescenses are few per tree, but the trees are often clumped
together in groups of 3 to 12. On Nosy Mangabe, they tend to be most common
at higher elevations. In addition, aye-ayes open Ravenala fruits to access an
unknown food source inside the fruit. The fruit contains seeds that are about 2 cm
in length and covered with a blue aril, but aye-ayes do not eat these. Aye-ayes
probably open the fruit to reach insects from a diverse array of families
(Bruchidae, Pyralidae, Cerambycidae, and Tenebrionidae) that can be found
inside the fruits in both adult and larval forms. Larvae (Diptera) have also been
found in the Ravenala nectar that aye-ayes exploit.
The aye-aye is well-known for its ability to locate and extract wood-boring lar-
vae from several different families with a characteristic behavior called tap-foraging.
As it moves along wood surfaces, the aye-aye taps the wood with its middle
finger, keeping its nose near the wood and its large ears pointing forward. When
it senses a cavity, the aye-aye anchors its upper incisors in the wood and uses the
scooping action of its lower incisors to gouge a pit. Larvae from a diverse array of
families (Cerambycidae: Lamiinae, Prioninae; Scarabidae: Dynastinae; Passalidae;
Pyralidae: Phycitinae) are retrieved from the cavity and brought to the mouth
with the slender middle finger (Figure 4). Rich sources of larvae include fallen
dead wood, dead branches on a living tree, living trees, dead and living lianas, the
underside of bark on living trees, and the insides of bamboo stalks and parasitized
seeds. Aye-ayes extract larvae from dead trees, lianas, and the bark of live trees
Adaptations in the Aye-aye 165
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more often than from any other host types, and they are known to remove larvae
from at least 29 different tree species (Figure 5). The periodicity of larval
resources is difficult to measure, but large larvae have been found in the bark of
medium- to large-sized Canarium trees during every month of the year. Bark
beetle larvae that live under the first centimeter of bark are also available year-
round. Density of larvae resources appears to be high, as aye-ayes eat larvae from
beneath the bark of several species that have high stem densities in the forest.
Although aye-ayes eat a wide variety of foods throughout the year, insects may
represent a stable resource during times when the availability of other resources
fluctuates more.
166 Eleanor J. Sterling and Erin McCreless
Figure 4. Drawing of an aye-aye foraging for wood-boring larvae. Drawing by J. Wolf
(Owen, 1866).
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Morphology and Feeding Adaptations
Many of the aye-aye’s preferred foods are highly structurally defended. The ani-
mal’s long anterior teeth and slender middle finger provide access to foods that are
difficult for many of its competitors to reach. Feeding on wood-boring larvae
requires aye-ayes to use both of these special morphological features, as an indi-
vidual must gnaw through live or dead wood and then extend its middle finger
into the cavity to hook larvae. The pericarp surrounding Canarium seeds is harder
than any fruits or seeds that are broken open by primates in South America (Kinzey
and Norconk, 1990), but the aye-aye is able to break it open with its strong inci-
sors. The prevalence of these two foods in the aye-aye’s diet underscores the
species’ specializations for, and ability to reach, structurally defended foods.
While the aye-aye’s morphology provides access to a variety of food sources that
would otherwise be inaccessible, it does not restrict its diet to only structurally
Adaptations in the Aye-aye 167
1.0
1.2
0.6
0.4
0.2
0.0
0.8
Percent of time spent feeding
HD89
HW90 CW90 HD90 HW91
Liana
Live tree/liana
Dead wood
Other
Bark
Season
Figure 5. Overall percentage of time spent feeding on larvae from different sources by
season for aye-ayes on Nosy Mangabe from November 1989 to April 1991. Averages of six
individuals were used to calculate seasonal means. See Figure 3 for sample sizes and abbre-
viations (Sterling, 1994a).
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defended foods. Nectars and cankers have no known structural defense. Ants may
be defended by chitin, but unless the digestive system of the aye-aye contains
chitinase, they have no better access to ants than do other animals. Aye-aye spe-
cializations and foraging patterns demonstrate that although many ecological
specializations may be associated with morphological adaptations, these adapta-
tions are not necessarily associated with ecological specialization. Indeed, in the
case of the aye-aye, morphological specialization may confer ecological generaliza-
tion by allowing the animal to gain access to structurally defended foods in addi-
tion to those that are more easily reached.
Although aye-ayes exploit a wide variety of food types, such as seeds, nectar, and
larvae, the number of species eaten within each food type is quite small (Table 2).
Most primates, including other lemur species, eat a greater variety of species
within food types. The reasons for the aye-aye’s exploitation of so few species
within each food type remain unknown. It is possible that a high dietary diversity
exists among the larvae, but sampling techniques have not been able to measure
larval diversity. Alternatively, since aye-ayes on Nosy Mangabe specialize on
resources that are structurally defended, their choices may be limited if only a few
species of structurally defended species grow on the island. However, Nosy
Mangabe does not appear to be lacking in structurally defended resources: there
are at least five plant species on the island that produce hard-coated seeds, and
wood-boring larvae are quite common throughout the island.
The specific factors contributing to Daubentonia’s dietary patterns have yet
to be fully understood, but there is no question that the aye-aye’s morphologi-
cal adaptations play an important role in its foraging behavior. The aye-aye’s
hand, which extends up to 45% of its trunk length, is proportionately longer
than the hand of almost any other primate — only Tarsius equals Daubentonia
in relative hand length — and exhibits a number of structural modifications that
are used in locating and consuming food (Figure 6). The middle finger of the
hand differs from the other fingers in its relatively gracile construction and
168 Eleanor J. Sterling and Erin McCreless
Table 2. Numbers of species that aye-ayes were observed to feed on, classified by food
type, for all individuals on Nosy Mangabe, 1989–1991 (Sterling, 1994a)
Number of species
Food resource type eaten by Daubentonia Taxonomic Designation
Seed 3 Canarium spp. (2), Burseraceae; Terminalia
catappa, Combretaceae
Nectar 1–2 Ravenala madagascariensis, Strelitziaceae,
and perhaps Labramia costata, Sapotaceae
Larvae 6–9 Cerambycidae: Lamiinae, Prioninae;
Scarabidae: Dynastinae; Passalidae;
Pyralidae: Phycitinae
Adult insect 1 Unidentified ant
Fungus 1–2 Unidentified
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Adaptations in the Aye-aye 169
Figure 6. Drawing of an aye-aye’s hand skeleton. Drawing by J. Erxleben (Owen, 1866).
Ch08.qxd 19/06/06 6:24 PM Page 169
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 cav-
ity 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.
170 Eleanor J. Sterling and Erin McCreless
Figure 7. Photograph of an aye-aye feeding on a seed of Canarium spp. Photograph
taken by Peter Ersts © AMNH-CBC.
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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 morpho-
logical 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 pin-
nae 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 inci-
sors 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 manip-
ulations 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 coor-
dination, 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 evolu-
tion of broad, domain general cognitive structures (Sterling and Povinelli, 1999).
Tap-Foraging
Field studies have shown that aye-ayes spend 5–41% of their feeding time tap-for-
aging for wood-boring insects, compared to 11–85% searching for and feeding on
Adaptations in the Aye-aye 171
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seeds or hard-coated fruits (Sterling, 1994a), but tap-foraging behavior has
attracted special attention from researchers because it involves a fascinating com-
bination 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 pos-
sum (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 vibra-
tions (Erickson, 1991).
Auditory cues are believed to be especially important in prey location by for-
aging 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 meal-
worms. 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 meal-
worms 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 under-
neath 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 sec-
tors, 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 mid-
section. Overall, study animals found more than 75% of the grubs in the mines.
DISTRIBUTION
The majority of the information on how the aye-aye’s middle digit functions within
the cavities formed by wood-boring insects comes from captive studies. Until rela-
tively recently, the aye-aye’s nocturnal and largely solitary lifestyle prevented
researchers from understanding its behavior, not to mention social structure, in the
172 Eleanor J. Sterling and Erin McCreless
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wild. In addition, little was known about its habitat preferences or distribution. In
the 1970s, aye-ayes were thought to be restricted to eastern coastal forests below
200 m (Petter and Peyrieras, 1970). However, more recent surveys based on iden-
tification of secondary signs of feeding or nesting have revealed that aye-ayes seem
to be able to adapt to different habitat types, from eastern humid forests (Ganzhorn
and Rabesoa, 1986a,b) to western dry forests (Iwano et al., 1991), from primary
forest (Andriamasimanana, 1994; Sterling, 1993b) to degraded patchy forests
and plantations (Ancrenaz et al., 1994; Andriamasimanana, 1994; Petter, 1977)
(Figure 9). To date, little is known about the population density of aye-ayes in any
part of Madagascar where the species is found (Sterling, 1994c), mainly because it
is extremely difficult to locate them with traditional survey and census techniques.
Adaptations in the Aye-aye 173
Figure 8. Drawing of an aye-aye tap-foraging, with its large ears pointed forward.
Drawing by J. Wolf (Owen, 1866).
Ch08.qxd 19/06/06 6:24 PM Page 173
174 Eleanor J. Sterling and Erin McCreless
Figure 9. Distributional map of Daubentonia based on verified sight records, interviews
with villagers, signs of feeding and nesting, and museum specimens. Map by Kevin Koy
© AMNH-CBC. Sources: Andriamasimanana et al. (2001); Britt (2002); Britt et al.
(1999), Colquhoun (1998), de Roland, R. (personal communication), Goodman, S., and
Wilmé, L. (personal communication); Hansen et al. (2003), Rahajanirina and Dollar
(2004); Randrianarisoa et al. (1999), Sterling (1998), Tombomiadana and Rakotonravony
(2000).
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SOCIAL SYSTEM
Systematic study of nocturnal primates in general is difficult due to observation
conditions at night and to lack of ability to detect signals that animals may use to
communicate with one another. Nocturnal primates, including aye-ayes, often
communicate with olfactory signals that are temporally deferred in their delivery,
and with vocalizations that researchers cannot always trace to their source
(Sterling and Richard, 1995).
Nocturnal primates were long believed to have simpler and more homogeneous
social systems than diurnal primates. The vast majority of solitary primate species
are nocturnal, and without the ability to observe interactions between individu-
als, researchers tended to associate a lack of gregariousness with a lack of social
complexity. Nocturnal primates tend to be predominantly nongregarious and
spend much of their time alone, whereas most diurnal primates live in social
groups consisting of individuals that know one another, interact regularly, and
spend most of their time nearer to one another than to nongroup members
(Sterling, 1993b). Nevertheless, nocturnal primates sometimes form social net-
works between animals that recognize one another and interact regularly, but that
may not spend a significant amount of time in proximity to one another. Richard
(1985) suggests that many solitary foragers live in “neighborhoods,” in which
individuals do not live in distinct social units but are most familiar with those indi-
viduals whose home ranges overlap the most with their own home ranges.
Nocturnal primates appear to communicate with each other in a variety of ways
and to develop complex relationships, but our measurement techniques and sensory
capacities remain unable to grasp the majority of these interactions. Nevertheless,
research is showing aye-aye social systems to be much more complex than was
originally thought (Sterling and Richard, 1995).
Communication
Vocal and olfactory signals are particularly important in the social organization of
aye-ayes, as their nocturnal and generally solitary habits preclude the use of visual
signals in many situations. Aye-ayes on Nosy Mangabe communicated primarily
by means of calls and scent-marks (Sterling and Richard, 1995). No research to
date has explored vocal communication between aye-ayes in the wild, but one
study of captive animals (Stanger and Macedonia, 1994) has provided informa-
tion on the number and structural complexity of vocalizations as well as some of
the contexts in which they are used. Captive aye-ayes were found to emit six dif-
ferent vocalizations in a variety of situations, and three additional vocalizations
have been heard from free-ranging animals. The aye-aye’s primary contact call has
enormous acoustic variation and is used in many different contexts, whereas most
other lemurs use several contact calls, often for spacing purposes. At first glance,
this repertoire of nine vocalizations appears to be rather small for a primate, but
Adaptations in the Aye-aye 175
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given that aye-ayes are relatively solitary animals and that other nocturnal lemur
species also have small vocal repertoires in captivity, this situation may not represent
an aberration among primate vocal patterns (Stanger and Macedonia, 1994).
Olfactory signals, which can provide important information about an individ-
ual’s age, sex, reproductive status, and territory, can be an effective mode of
communication between individuals that may not come into direct contact very
often (Kappeler, 1998). Wild aye-ayes on Nosy Mangabe exhibited three kinds of
scent-marking: ano-genital rubbing, head and chest rubbing, and overmarking,
where individuals urinated or dragged their genital region over an area previously
marked by another animal (Sterling and Richard, 1995). Price and Feistner
(1994) found evidence that captive aye-ayes can discriminate between the scents
of conspecifics from different age–sex classes. The structure of the aye-aye’s nasal
cavity is unusual when compared to other lemurs in that the maxilloturbinal is
somewhat stirrup-shaped, with a single inferior scroll (Tattersall, 1982), and as in
many nocturnal species, the olfactory bulb forms a greater percentage of brain
volume than in diurnal species. However, many of the details regarding the role
that olfactory signals play in social and sexual communication between aye-ayes
have yet to be explored.
In addition to communicating across space and time by means of calls and
scent-marking, aye-ayes do sometimes interact directly with other members of
their species. Sterling (1993a) reported that aye-ayes on Nosy Mangabe generally
spent less than 20% of their time within 20 m of another aye-aye of either sex.
Males and females differ in their reactions to conspecifics of the same and the
opposite sex. Females rarely came into proximity with one another, and when they
did, their interactions were usually aggressive and involved fighting or chasing.
Interactions between males and females occurred more frequently than those
between two females, and the nature of these interactions was highly variable.
Tandem foraging, where individuals foraged in the same or adjacent trees and
called to one another prior to moving in tandem from resource to resource, made
up the largest percentage of time that males and females spent in close proximity.
Similarly, affiliative vocalizations between the sexes were heard more frequently
than agonistic ones. Males interacted with each other more often than they inter-
acted with females, and certainly much more often than females interacted with
each other. Relationships between pairs of males ranged from tandem foraging to
avoidance and aggression.
Tandem foraging deserves special attention in a discussion of aye-aye sociality,
as it may demonstrate that the species is not entirely solitary, as has long been
assumed. Aye-ayes do often forage alone, but Sterling (1993b) documented
groups of up to three individuals foraging and traveling together on Nosy
Mangabe. Foraging associations were observed between adult males, adult and
young males, and adult males and females. Aggregations of several aye-ayes have
also occasionally been seen foraging together in Madagascar’s mainland forests
(Ancrenaz, 1991; Sterling, personal observation). The repeated occurrence of
tandem foraging associations suggests that aye-ayes may be more social than was
176 Eleanor J. Sterling and Erin McCreless
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originally thought, and that established relationships may exist between pairs or
groups of individuals.
The occurrence and composition of sleeping groups is another major axis
organizing the social diversity of solitary primates (Kappeler, 1997a; Müller and
Thalmann, 2000). Although aye-ayes show a tendency toward solitary resting,
they do sometimes sleep in nests together or near one another. Aye-ayes sleep
during the day in oval-shaped nests located 7–20 m from the ground in the fork
of a tree or in a tangle of lianas, constructed of branches and lianas from con-
tiguous vegetation. A single individual usually occupies a nest for a few days at a
time, frequently refreshing it with new vegetation. Multiple aye-ayes may use the
same nest at different times, as previous occupants vacate the nest and move on
to new areas. Sterling’s field study on Nosy Mangabe (1993b) revealed that
females never slept near other females, whereas males slept near other individuals
(male or female) only during the mating season. Several aye-ayes on Madagascar’s
mainland have been seen to build and use nests in a single tree during the same
day (Ancrenaz et al., 1994), and males and females have been seen to sleep in
nests located only 5 m apart (Andriamasimanana, 1994). Adult males have been
observed to share a nest on mainland Madagascar (Sterling, unpublished data).
Existing data are not sufficient to draw any conclusions regarding the relation-
ships between individuals or groups of aye-ayes based on choice of sleeping site,
but the possibility of social relationships between individuals that sleep near one
another should not be ruled out.
Home Range Patterns
Another important factor in determining social organization in solitary primates
is the extent of home range overlap with members of the same and the opposite
sex (Müller and Thalmann, 2000). Field studies of aye-aye home ranges have pro-
vided insights into Daubentonia’s social system and how it compares with that of
other lemurs. Overviews of nocturnal primate sociality demonstrate that patterns
of home range overlap vary greatly both within and between the sexes in a given
species (Kappeler and van Schaik, 2002; Müller and Thalmann, 2000).
Preliminary data from a 6-month study on a river island near Mananara in north-
eastern Madagascar show three distribution patterns in male home range size
(Lhota et al., 2004). Sterling’s (1993b) study of radio-collared aye-ayes on Nosy
Mangabe showed male home ranges to have an area of 120–215 ha, which was
three to six times the size of females’ home ranges (30–40 ha ). Male home ranges
often overlapped with each other and with female home ranges, whereas females
seemed to maintain exclusive home ranges that did not overlap with each other at
all (Figure 10). More research is needed, however, to determine whether female
home ranges are always fully isolated from one another.
Male and female home range sizes differ primarily because males travel farther
during nightly forays than do females. Males on Nosy Mangabe periodically went
Adaptations in the Aye-aye 177
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178 Eleanor J. Sterling and Erin McCreless
Figure 10. Home range overlap of five Daubentonia study animals on Nosy Mangabe,
1989–1991. Females = solid line, dashed line. Males = dotted line, dot/dash line, dash/tri-
angle line (Sterling, 1993a).
Ch08.qxd 19/06/06 6:24 PM Page 178
on extended forays into outlying areas, often covering between 2.2 and 4.4 km
per night on successive nights, sometimes without feeding much on the longer
trips. Females generally traveled less than half as far as males did. Nevertheless,
female aye-ayes have much larger home ranges than diurnal lemurs of similar body
size in the same habitat (Sterling, 1993b).
Several factors may be responsible, singly or jointly, for the distribution patterns
of male and female aye-ayes and the differences in foraging travel distances.
Resource distribution and defensibility, predation pressure, and the intensity and
nature of interspecific competition all may influence dispersion patterns among
mammals (Emlen and Oring, 1977; Kappeler, 1997a; Sterling, 1993b; Terborgh
and Janson, 1986). These factors influence males and females differently, result-
ing in sex-specific social and reproductive behavior. Some researchers (Charles-
Dominique, 1993; Müller and Thalmann, 2000; Wrangham, 1980) argue that
female behavior is influenced more directly by ecological pressures than male
behavior because food availability is a major limiting factor on female fitness.
Male behavior focuses more on finding mates and achieving mating success, as
predicted from sexual selection theory.
The observed distribution patterns of male and female aye-ayes are consistent
with the models described above. Females had ranges situated across similar ele-
vation gradients, from 0 to 250 m, possibly in an effort to encompass a variety of
both low- and high-elevation food types in their home ranges. Male aye-aye
ranges may have exceeded in size and overlapped those of many females because
males have greater nutritional requirements than females. However, if
Daubentonia females can obtain adequate food in 30–40 ha, then males, which
are of similar size, should not need 120–215 ha in which to gather food resources.
Mating System
The exploratory sojourns of aye-aye males are striking. Travel over Nosy
Mangabe’s steep slopes using both terrestrial and arboreal locomotion requires a
great expenditure of energy, suggesting that there must be strong incentives for
males to travel long distances. The fact that individual male home ranges over-
lapped those of many females may support the prediction that males are distrib-
uting themselves to best take advantage of the distribution of females. Lemurs
typically exhibit a strictly seasonal pattern of breeding, with a limited number of
successive estrous cycles occurring at a particular time of the year, which varies
from species to species. The aye-aye, however, is unique among Malagasy pri-
mates in the unpredictability of its breeding events throughout the year. Evidence
from the wild suggests that aye-ayes do not exhibit reproductive synchrony:
females in close proximity to one another neither cycle nor become pregnant at
the same time (Gibson, D., personal communication; Sterling, 1994b). Estrus
brevity in individual females and asynchrony across females means that a male aye-
aye’s ability to detect when the female is in estrus is very important and very
Adaptations in the Aye-aye 179
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difficult. Long forays by males and consequent large home ranges may reflect
male efforts to locate estrous females. Indeed, male aye-ayes on Nosy Mangabe
did encounter estrous females on a number of their extended foraging excursions.
Resource availability and photoperiod are often cited as important factors in
reproductive timing in animals, but aye-aye breeding behavior does not appear to
be influenced by either variable. Aye-ayes eat all their major food resources across
almost all months of the year, and the timing of peak availability of fruits varies
from year to year. It is unclear whether the availability of food resources is highly
unpredictable, or if there are patterns that existing data cannot detect. Field
observations of aye-aye births occurring throughout the year suggest that pho-
toperiod has little effect on reproductive timing. In addition, aye-ayes maintained
on different light regimes in two different captive institutions mated and gave
birth at approximately the same time, indicating that breeding was not prompted
by changes in the light cycle. It seems that whatever factors contribute to repro-
ductive seasonality in most other lemurs may not affect wild aye-ayes (Sterling,
1994b).
Behavioral signs of reproductive activity become apparent in female aye-ayes
about 10 days prior to the onset of full estrus. Females increase the frequency of
scent-marking and often visit nests occupied by males, a behavior not seen outside
the mating season (Sterling, 1993b). Physiologically, female estrus is marked by
vulvar and labial swelling, and a color change in the labia from gray to pink or red
(Winn, 1994). Prior to and during mating activity, males exhibit testicular swelling
and increase scent-marking frequency. During this time, males cluster around the
female during both day and night and, like the females, increase their scent-marking
frequency. Males generally mate with a female about a week after testicular swelling
is first observed.
During each night of estrus, females exhibit a repetitive pattern of moving
swiftly over 500–1000 m, and then sitting still for about an hour and emitting
long calls that they use only during the mating period. In response to this call,
several males converge on the female from all directions. Males chase and fight
with one another near the female, and the female repels some mating attempts
while accepting others. The accepted male copulates with the female and main-
tains hold of her for about an hour, while other males chase each other in circles
around the pair and try to dislodge whichever male is copulating with the female.
When copulation is complete, the female quickly moves another 500 to 1000 m
and repeats the pattern. A female may mate with one or more males during each
night of estrus, making it impossible to determine which male is the father of the
female’s offspring without genetic analysis (Sterling and Richard, 1995).
The aye-aye’s home range patterns and breeding behavior suggest that the
species exhibits scramble competition polygyny, in which females are solitary and
males range widely in search of estrous females (Clutton-Brock, 1989). The
females’ advertisement calls suggest that they have an interest in attracting more
than one male, possibly to provide themselves with a choice of several males on
each night of estrus. Individual females may benefit by maintaining reproductive
180 Eleanor J. Sterling and Erin McCreless
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asynchrony, because a large number of males are available to respond to any indi-
vidual female’s call on a given night (Kappeler, 1997c). When a female chooses a
mate, the male monopolizes her for a long period, either through single or mul-
tiple intromissions. In this way, the male temporarily prevents other males from
inseminating the female while increasing his chances for fathering the offspring.
Because females mate with more than one male during each period of estrus,
Daubentonia has a multi-male – multi-female breeding system (Sterling, 1993b).
The aye-aye was one of the first lemurs noted to exhibit scramble competition
polygyny, but subsequent studies have pointed to other nocturnal lemurs with this
system, such as Coquerel’s dwarf lemur (Mirza coquereli) (Kappeler, 1997c) and
the gray mouse lemur (Microcebus murinus) (Radespiel, 2000). These species also
display similar home range patterns to those found in Daubentonia, providing
further support for the connection between larger male home ranges and scramble
competition polygyny.
Polygynous species often display pronounced sexual dimorphism, with larger,
stronger males able to outcompete other males for available females. Sexual size
dimorphism is characteristic of many solitary primates, including the Lorisidae,
most Galagidae, and Pongo pygmaeus (Kappeler, 1997a). However, Malagasy pri-
mates, including the aye-aye, generally lack sexual size dimorphism, and some
lemur species even show a trend toward larger female size (Jolly, 1998). The wide
variety of mating systems and patterns of sexual dimorphism found in lemurs are
often seen as a challenge to the general predictions of sexual selection theory
(Kappeler, 1997a; Müller and Thalmann, 2000).
In scramble competition polygyny, a male’s primary challenge is to locate sex-
ually receptive females. Male attributes such as mobility, perceptiveness, and spa-
tial memory are likely to aid a male in finding estrous females in these systems
(Schwagmeyer, 1988). These traits may benefit a male more than would large
body size or other defensive traits that are characteristic of males of species that
engage in direct combat for females. Studies of other species that use a scramble
competition polygyny mating system may help to explain the lack of sexual dimor-
phism in aye-ayes and other lemurs. Eberle and Kappeler (2004) found that body
mass was a poor predictor for mating success in male gray mouse lemurs
(Microcebus murinus), whereas a high level of spatial familiarity improved mating
success. Similarly, the mating success of male thirteen-lined ground squirrels is
closely linked to the number of estrous females he finds, while his ability to dom-
inate over his competitors is a poor predictor of mating success (Schwagmeyer,
1988).
Scramble competition polygyny in aye-ayes may correlate with improved spa-
tial ability and mobility in males, as seems to be the case in other species with this
type of mating system. Unlike aye-ayes, however, gray mouse lemurs and thir-
teen-lined ground squirrels tend to exhibit seasonal reproduction, which may
limit direct contest competition between males and alleviate the need for males
to have a large body size. The lack of seasonality in the estrus cycles of female
aye-ayes would be expected to promote direct (contest) competition between
Adaptations in the Aye-aye 181
Ch08.qxd 19/06/06 6:24 PM Page 181
males, presumably leading to sexual size dimorphism in addition to improved
male spatial ability. The prolonged intromissions and enlarged testes observed in
aye-ayes may be a strategy to manage competition. Males of other lemur species
with polygynous mating systems exhibit increased testis size, either permanently
or through testicular swelling during the mating season (Kappeler, 1997b).
Another successful strategy used by males of many polygynous species is the use
of copulatory plugs, although this possibility has not yet been explored in aye-
ayes. All of these may increase a male’s chance of fathering the offspring of a
female that mates with additional males (Kappeler, 1997c; Parga, 2003; Schwab,
2000). Clearly, much remains to be understood about Daubentonia’s mating system
and correlations with male and female morphology and behavior.
CONCLUSION
While great advances have been made in understanding aye-aye ecology and social
behavior over the past several decades, there is still much to learn about these ani-
mals, their perceived similarities and distinctiveness from other lemurs, and the
morphological and behavioral traits that make them unique. In particular, a
greater understanding is needed about resource use and social and behavioral
ecology of aye-ayes in mainland humid forests and in drier habitats of western
Madagascar.
ACKNOWLEDGMENTS
Many thanks to Mary DeJong and the rest of the staff in the library of the
American Museum of Natural History (AMNH) for helping us to find very old
publications, and for trusting us to keep them safe. Ho-Ling Poon and Tony
Alexander of the AMNH Center for Biodiversity and Conservation (CBC) and
the staff of the AMNH Interdepartmental Laboratories assisted with reproduc-
tion of the images used in this chapter. Kimberley Roosenburg and Jennifer
Stenzel provided many helpful comments on the manuscript. Thanks also to Steve
Goodman, Lucienne Wilmé, and Réné de Roland for providing extensive infor-
mation about aye-aye distribution, and to Kevin Koy of the CBC GIS laboratory
for translating these data into distribution maps.
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