However, primates are now recognized to possess an excellent sense of smell that
is often on par with that of mammals like dogs and rodents [116], and it becomes
increasingly clear that olfaction plays a major role in the feeding ecology of
primates, primarily for discrimination between ripe and unripe fruits [15, 78].
Until recently, most studies that demonstrated reliance on olfaction for fruit selection
did not consider the chemical properties of fruits [78]. Nevo et al. [46] showed that
spider monkeys (Ateles geoffroyi) can discriminate between synthetic mixtures
mimicking the scent of ripe and unripe fruits of two Neotropical fruit species.
Notably, the monkeys can discriminate between the scents of ripe and unripe fruits
even when individual compounds in the scent of unripe fruits are manipulated to
match the concentration in ripe fruit scent. This indicates that identification of ripe
fruits is not based on individual compounds and thus less sensitive to within-species
variance in fruit VOC content, which has been found in studies that sampled multiple
fruits per species [39, 51].
In the field, two recent studies quantified the relationship between fruit olfactory
conspicuousness, defined as the difference between ripe and unripe fruit scent, and the
tendency of primates to sniff fruits before ingesting or rejecting them. Red-bellied
lemurs (Eulemur rubriventer) are more likely to sniff fruits of species which increase
the amount of scent upon ripeness or change the chemical composition of ripe fruits
[51]. In the neotropics, white-faced capuchins (Cebus capucinus imitator) increase the
rate of sniffing when feeding on fruits of species in which the amount of scent emitted
by ripe fruits is larger [117]. Another study found no relationship between sniffing
behavior in brown lemurs (Eulemur fulvus) and the overall amount of scent emitted by
ripe fruits [118], indicating that the determining factor is not scent per se but the
olfactory conspicuousness of the fruit, i.e., how different it is from conspecific unripe
fruits [15, 39]. However, scent in this study [118] was corrected for the surface area of
the fruit. Thus, the variable analyzed was not the amount of scent available for the
lemurs but the amount emitted by a unit of surface area. This procedure is meaningful
when studying, for example, the costs of scent emission. But from an ecological
perspective, in fruit selection, the animal is exposed to the scent emitted by a single
fruit, which is therefore a more appropriate measurement.
Primate-consumed fruits tend to emit common VOCs: terpenoids, aromatic
compounds, and fatty acid derivatives [15, 39, 51]. Lemur-consumed fruits in
Madagascar – especially those which attract more olfactory investigation by lemurs –
tend to be rich in aliphatic esters [51]. Some fruits also emit nitrogen- and sulfurcontaining compounds [15, 16, 51].
3.1.3 Birds
Frugivorous birds are important seed dispersers across the tropics and are probably
the most important animal seed disperser in temperate regions [119]. The most
dominant group of frugivorous birds are the passerines, although frugivory is also
present in non-negligible numbers among woodpeckers, parrots, and pigeons [120].
Birds possess an excellent color vision. Most species are tetrachromatic, i.e., possess
one more pigment type than the best color-discriminating primates, among them
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O. Nevo and M. Ayasse
is often on par with that of mammals like dogs and rodents [116], and it becomes
increasingly clear that olfaction plays a major role in the feeding ecology of
primates, primarily for discrimination between ripe and unripe fruits [15, 78].
Until recently, most studies that demonstrated reliance on olfaction for fruit selection
did not consider the chemical properties of fruits [78]. Nevo et al. [46] showed that
spider monkeys (Ateles geoffroyi) can discriminate between synthetic mixtures
mimicking the scent of ripe and unripe fruits of two Neotropical fruit species.
Notably, the monkeys can discriminate between the scents of ripe and unripe fruits
even when individual compounds in the scent of unripe fruits are manipulated to
match the concentration in ripe fruit scent. This indicates that identification of ripe
fruits is not based on individual compounds and thus less sensitive to within-species
variance in fruit VOC content, which has been found in studies that sampled multiple
fruits per species [39, 51].
In the field, two recent studies quantified the relationship between fruit olfactory
conspicuousness, defined as the difference between ripe and unripe fruit scent, and the
tendency of primates to sniff fruits before ingesting or rejecting them. Red-bellied
lemurs (Eulemur rubriventer) are more likely to sniff fruits of species which increase
the amount of scent upon ripeness or change the chemical composition of ripe fruits
[51]. In the neotropics, white-faced capuchins (Cebus capucinus imitator) increase the
rate of sniffing when feeding on fruits of species in which the amount of scent emitted
by ripe fruits is larger [117]. Another study found no relationship between sniffing
behavior in brown lemurs (Eulemur fulvus) and the overall amount of scent emitted by
ripe fruits [118], indicating that the determining factor is not scent per se but the
olfactory conspicuousness of the fruit, i.e., how different it is from conspecific unripe
fruits [15, 39]. However, scent in this study [118] was corrected for the surface area of
the fruit. Thus, the variable analyzed was not the amount of scent available for the
lemurs but the amount emitted by a unit of surface area. This procedure is meaningful
when studying, for example, the costs of scent emission. But from an ecological
perspective, in fruit selection, the animal is exposed to the scent emitted by a single
fruit, which is therefore a more appropriate measurement.
Primate-consumed fruits tend to emit common VOCs: terpenoids, aromatic
compounds, and fatty acid derivatives [15, 39, 51]. Lemur-consumed fruits in
Madagascar – especially those which attract more olfactory investigation by lemurs –
tend to be rich in aliphatic esters [51]. Some fruits also emit nitrogen- and sulfurcontaining compounds [15, 16, 51].
3.1.3 Birds
Frugivorous birds are important seed dispersers across the tropics and are probably
the most important animal seed disperser in temperate regions [119]. The most
dominant group of frugivorous birds are the passerines, although frugivory is also
present in non-negligible numbers among woodpeckers, parrots, and pigeons [120].
Birds possess an excellent color vision. Most species are tetrachromatic, i.e., possess
one more pigment type than the best color-discriminating primates, among them
412
O. Nevo and M. Ayasse