Insectivorous birds can see and smell systemically herbivore‐induced pines

Abstract

Several studies have shown that insectivorous birds are attracted to herbivore‐damaged trees even when they cannot see or smell the actual herbivores or their feces. However, it often remained an open question whether birds are attracted by herbivore‐induced changes in leaf odor or in leaf light reflectance or by both types of changes. Our study addressed this question by investigating the response of great tits (Parus major) and blue tits (Cyanistes caeruleus) to Scots pine (Pinus sylvestris) damaged by pine sawfly larvae (Diprion pini). We released the birds individually to a study booth, where they were simultaneously offered a systemically herbivore‐induced and a noninfested control pine branch. In the first experiment, the birds could see the branches, but could not smell them, because each branch was kept inside a transparent, airtight cylinder. In the second experiment, the birds could smell the branches, but could not see them, because each branch was placed inside a nontransparent cylinder with a mesh lid. The results show that the birds were more attracted to the herbivore‐induced branch in both experiments. Hence, either type of the tested cues, the herbivore‐induced visual plant cue alone as well as the olfactory cues per se, is attractive to the birds.

Great tits (Parus major) flexibly learn that herbivore‐induced plant volatiles indicate prey location: An experimental evidence with two tree species

“…Birds have also been shown to be attracted to trees infested by herbivores, without seeing the insects or physical foliage damage (Mäntylä et al., 2004 , 2008 , 2016 , 2020 ). Yet, only recently we started to disentangle the mechanism underlying the use of olfactory signals by birds searching for prey (Amo et al., 2013 ; Koski et al., 2015 ; but see Koski et al., 2015 ).…”

Attraction to Smelly Food in Birds: Insectivorous Birds Discriminate between the Pheromones of Their Prey and Those of Non-Prey Insects

“…Amo and collaborators [40] isolated the visual and chemical cues of larvae-infested apple trees and found that great tits were attracted to infested trees when they could only smell but not when they could only see the trees. Therefore, it seems that HIPVs can attract insectivorous birds [40,42], although a previous study using artificial mixtures of volatiles has not found such an attraction [61]. The positive correlation found between avian the predation rates of artificial larvae and the quantity of emission of volatiles emitted by trees experimentally infested with caterpillars in natural conditions also suggests that olfaction may be the mechanism underlying bird attraction to caterpillar-infested trees [53], although vision may also play an important role in finding prey [42,52,57].…”

“…Previous evidence also suggests that birds use olfaction in the process of foraging. The use of olfaction during foraging seems to be an ancient trait in birds (e.g., Kiwis (Apteryx australis) [33]; Cathartes vultures [34]), where it is maintained in modern lineages (Procellariiforms [35]); penguins [36,37]; domestic chickens (Gallus gallus) [38]; and passeriformes, such as zebra finches (Taeniopygia guttata) [39], great tits (Parus major), and blue tits (Cyanistes caeruleus) [40][41][42]). The results of a recent comparative study suggest that the olfactory bulb size, a proxy of olfactory capability, varies substantially across bird species in relation to diet type and ecological conditions [43], suggesting that foraging mode has played an important role in the evolution of chemosensory abilities in birds.…”

“…In the sea, Procellariiformes and Sphenisciformes can detect dimethyl sulphide (DMS [36,37]), a chemical compound released by phytoplankton when zooplankton and pelagic fishes graze on phytoplankton, thus signaling areas of high productivity in oceans [35,51]. Chemical communication also plays an important role in plant-herbivory-predator interactions in terrestrial systems, as insectivorous birds exploit the chemical indirect cues emitted by plants (Herbivore Induced Plant Volatiles, HIPVs) in response to caterpillar herbivory ( [40,42,[52][53][54][55][56][57], reviewed in [41]). When attacked by herbivorous predators, plants respond in a defensive manner to face such herbivory, including the emission of HIPVs that attract the predators of herbivores [58].…”

“…Therefore, it seems that HIPVs can attract insectivorous birds [40,42], although a previous study using artificial mixtures of volatiles has not found such an attraction [61]. The positive correlation found between avian the predation rates of artificial larvae and the quantity of emission of volatiles emitted by trees experimentally infested with caterpillars in natural conditions also suggests that olfaction may be the mechanism underlying bird attraction to caterpillar-infested trees [53], although vision may also play an important role in finding prey [42,52,57]. Avian attraction has also been shown in plants treated with methyl jasmonate (MeJA) [41,56], a phytohormone involved in the development of plant defence against herbivory [62][63][64].…”