according to which fruit characteristics have evolved in response to the traits of their
primary seed disperser [29, 83, 84]. Yet empirical tests of the hypothesis that fruit
scent has evolved as a signal for seed dispersers have until recently been absent,
possibly due to the predominance of the view that fruit traits are not strongly selected
by frugivores in the last 15 years of the last century [21, 22, 85, 86] – a timeframe in
which the understanding of floral scent evolution has exploded [30, 32, 47]. Another
factor has been that chemical communication between fruits and frugivores is more
common in tropical regions, in which chemical sampling and analysis tend to be
more challenging. Yet the growing support for the dispersal syndrome hypothesis
[24, 26, 87] and increasing availability of techniques allowing chemical sampling
and analysis [27, 28] have led to a renewed interest in the question. We first examine
this question from the animal side, asking how and whether animals may use fruit
scent to find and identify ripe fruits, i.e., whether fruit scent is a useful cue for
frugivores. We then move on to examine whether in cases in which it is used by
animals, fruit scent can be considered an evolved signal which is selected to fulfill
this function.
3.1
Fruits Scent as a Cue
3.1.1 Bats
With 1200 known species, bats are the second-most diverse group of mammals
[88]. Frugivory has evolved independently in the Old and New Worlds, and in both
systems bats are important seed dispersers, contributing to early succession and,
in the Old World, recruitment of canopy species [89]. As nocturnal animals, bats
can rely on their vision less than diurnal species, although many retain dichromatic
vision and may rely on vision more than previously considered [90]. Some bats
lineages have evolved to use sonar [91] and can echolocate flowers and fruits
which have presumably evolved specialized structures that reflect back their calls
[20, 92–95]. But echolocation is not present in most Old World frugivorous bats
[91], and thus a major sensory trajectory for frugivorous bats is olfaction [96].
Olfaction also plays a role in bat pollination, a relationship which is primarily
facilitated by chemical communication [32] or a combination of olfaction and
echolocation [97].
Reliance on olfaction has been demonstrated in behavioral tests that focused
primarily on New World frugivorous bats. New World bats have been reported to be
attracted to fig scent [98, 99], and early experiments showed attraction to the scent of
bananas, which are consumed by local bats but are not wild and thus possibly not
representative [100]. Thies et al. [101] showed that New World Carollia
perspicillata and C. castanea use the scent of Piper fruits to identify ripe fruits.
In a series of experiments, they showed that unripe fruits are rejected and that
artificial fruits are approached only when impregnated with the scent of ripe fruits.
C. perspicillata were also shown to possess high olfactory sensitivity to a series of
esters, alcohols, and carboxylic acids common in fruits [102]. Similarly, in an
experimental setting, New World Artibeus watsoni and Vampyressa pusilla showed
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O. Nevo and M. Ayasse
primary seed disperser [29, 83, 84]. Yet empirical tests of the hypothesis that fruit
scent has evolved as a signal for seed dispersers have until recently been absent,
possibly due to the predominance of the view that fruit traits are not strongly selected
by frugivores in the last 15 years of the last century [21, 22, 85, 86] – a timeframe in
which the understanding of floral scent evolution has exploded [30, 32, 47]. Another
factor has been that chemical communication between fruits and frugivores is more
common in tropical regions, in which chemical sampling and analysis tend to be
more challenging. Yet the growing support for the dispersal syndrome hypothesis
[24, 26, 87] and increasing availability of techniques allowing chemical sampling
and analysis [27, 28] have led to a renewed interest in the question. We first examine
this question from the animal side, asking how and whether animals may use fruit
scent to find and identify ripe fruits, i.e., whether fruit scent is a useful cue for
frugivores. We then move on to examine whether in cases in which it is used by
animals, fruit scent can be considered an evolved signal which is selected to fulfill
this function.
3.1
Fruits Scent as a Cue
3.1.1 Bats
With 1200 known species, bats are the second-most diverse group of mammals
[88]. Frugivory has evolved independently in the Old and New Worlds, and in both
systems bats are important seed dispersers, contributing to early succession and,
in the Old World, recruitment of canopy species [89]. As nocturnal animals, bats
can rely on their vision less than diurnal species, although many retain dichromatic
vision and may rely on vision more than previously considered [90]. Some bats
lineages have evolved to use sonar [91] and can echolocate flowers and fruits
which have presumably evolved specialized structures that reflect back their calls
[20, 92–95]. But echolocation is not present in most Old World frugivorous bats
[91], and thus a major sensory trajectory for frugivorous bats is olfaction [96].
Olfaction also plays a role in bat pollination, a relationship which is primarily
facilitated by chemical communication [32] or a combination of olfaction and
echolocation [97].
Reliance on olfaction has been demonstrated in behavioral tests that focused
primarily on New World frugivorous bats. New World bats have been reported to be
attracted to fig scent [98, 99], and early experiments showed attraction to the scent of
bananas, which are consumed by local bats but are not wild and thus possibly not
representative [100]. Thies et al. [101] showed that New World Carollia
perspicillata and C. castanea use the scent of Piper fruits to identify ripe fruits.
In a series of experiments, they showed that unripe fruits are rejected and that
artificial fruits are approached only when impregnated with the scent of ripe fruits.
C. perspicillata were also shown to possess high olfactory sensitivity to a series of
esters, alcohols, and carboxylic acids common in fruits [102]. Similarly, in an
experimental setting, New World Artibeus watsoni and Vampyressa pusilla showed
410
O. Nevo and M. Ayasse