Discussion
Our results show that attraction of great tits to herbivore-induced
defence cues is not innate. Naïve birds with no experience with green
leaves were not attracted to induced, thus potentially insect rich,
saplings. This confirms the previous findings of Amo et al.(2016). In their experiment, naïve birds
neither preferred the caterpillar-infested sapling for the first visit,
nor visited that sapling more frequently that the uninfested sapling
(control). In contrast, in another study, when the great tits gained
some experience with foraging for caterpillars, they exhibited a
preference for caterpillar infested saplings, and visited them more
often than the uninfested saplings (Amoet al. 2013a). In line with these results, we were able to teach
the birds the association between the herbivore-induced volatile
compounds of saplings and a food reward.
In contrast to our expectation, the great tits were able to associate
the volatile compounds of tropical guava with food similarly well (if
not better) as of the volatile compounds of elm, despite the fact that
they did not share any evolutionary history with this plant species.
After the successful teaching period, each group of trained bird
preferred the induced version of the sapling of the plant species they
were trained to, over any other version of the saplings offered to them.
The birds did not seem to be able to generalize the learned bouquets of
volatile compounds to another plant species. This might imply that the
birds are likely to learn the whole bouquets of the volatile compounds
and associate them with food, rather than learning individual volatile
compounds. Alternative explanation might be that the birds are capable
of some generalization for more closely related plant species producing
more similar plant volatile compounds.
In our experimental plants, we detected significantly more chemical
compounds in induced than in noninduced guavas. The volume of produced
compounds was also higher in induced than in noninduced elms, but the
difference was not significant. Compounds found in significantly higher
concentration in induced plants were β-Ocimene, Heptadiene, Cyclohexane,
α-Pinene, Copaene, Caryophyllene, Tetraline, α-Farensene and Tetraline.
Many of these compounds were previously suspected to correlate with
attractivity of the herbivore-damaged plants with bird’s attractivity to
them (Mrazova et al. 2019). Specifically, β-Ocimene and α-Pinene
were discussed as compounds specifically responsible for the
attractivity of birds to herbivore-damaged plants (Mrazova et al.2019). Our experiment showed that birds exposed to two plants with very
different bouquets can distinguish them better than birds exposed to
more similar bouquets. In our experiment, we selected two plant species
which are very different. One tropical plant with strong odour and one
temperate with rather weak odour. Our birds were not able to generalize
between their odours. The questions remain whether the birds would be
capable of generalization between several temperate plant species which
might have more similar odours.
In contrast to previous study (Amo et
al. 2016), our birds took rather long to successfully search for the
mealworms offered to them on induced saplings. The previous study
indicated a fast ability of birds to use HIPVs as a foraging cue, as
they learned to associate the presence of caterpillars with the HIPVs of
infested trees in 5 h (Amo et al.2016). Similarly, in our previous study, naïve birds were able to
locate more than 80% of caterpillars after 5 h of habituation in aviary
with noninduced trees (Mrazova et al. unpublished). In the
current study, the average bird needed at least 20 hours to be able to
associate the food rich sapling with the volatile compounds. The
difference between current and previous training was in the type of the
sapling offered in training phase (two infested saplings in
Amo et al. 2016 or two uninfested
saplings in Mrazova et al. unpublished vs. one infested and one
uninfested sapling in current study) and the training considered to be
successful (i.e. eating from any sapling vs. eating from the induced
sapling only).
A prenatal chemosensory learning was demonstrated in birds
(Sneddon et al. 1998) previously
but it a very different experiment with domestic chickens. With no
exposure to strawberry before hatching, strawberry was highly aversive
to chicks after hatching. However, following exposure to strawberry
before hatching, chicks expressed a greater preference for (or weaker
aversion to) the strawberry stimulus
(Sneddon et al. 1998). Despite no
association of smell and food was tested in this study, it proved that
chicks can learn and prefer a smell. In a similar study, nest
recognitions via olfactory imprinting was learned in few hours after
hatching, and olfactory stimuli is then a sufficient mechanism for nest
recognition (Caspers et al. 2013).
For birds, as generalist predators, prey availability changes during the
year due to differences in phenology of the plant and insect species.
Therefore, adaptive plasticity may be an advantage for foraging of the
birds in response to changes in distribution and abundance of prey
species (e.g. in Murakami 1998). In the
current study, we showed the existence of such plastic association of
different odours with food resources may maximize success of foraging in
birds. We observed that birds are able to learn even novel odours which
they did not have chance to meet during their evolutionary history.
Thus, they are capable of some generalization with respect to volatile
compounds. However, it is important to note that our study was conducted
on a single bird species but the adaptive value of learning is expected
to vary among bird species depending on their diet breadth at both the
herbivore and plant levels (Vet et
al. 1995, Mrazova et al. 2019).
The use of olfaction in foraging can be innate in different bird species
(Bonadonna et al. 2006,
Amo et al. 2013b).
In our study, we also used very phylogenetically distant tree species,
which differed significantly in the diversity of volatile compounds.
However, it is likely that some generalization may work across more
similar and phylogenetically related tree species. While birds might be
able to learn several plant species occurring in their home ranges in
temperate regions, the tropical birds might be facing different
challenges. Tropical insectivorous understory birds have usually home
ranges up to 30 ha large. A hectare of tropical forest typically
contains more than 250 tree species. It would be generally impossible
for a bird to learn all species in a lifetime, so either individual
birds respond to only subset of local plants, or birds learn groups of
plants which are chemically and therefore also phylogenetically
related). It remains unresolved how the learning of volatile compounds
works in species rich tropical areas, and how is the ability to learn
volatile compounds combined with ability to learn the visual signals.