Great Tits Learn Odors and Colors Equally Well, and Show No Predisposition for Herbivore-Induced Plant Volatiles

Abstract

Ability to efficiently localize productive foraging habitat is crucial for nesting success of insectivorous birds. Some bird species can use olfaction to identify caterpillar-infested trees by detection of herbivore induced plant volatiles (HIPVs), but these cues probably need to be learned. So far, we know very little about the process of olfactory learning in birds, whether insectivorous species have a predisposition for detecting and learning HIPVs, due to the high ecological significance of these odors, and how olfaction is integrated with vision in making foraging decisions. In a standardized setup, we tested whether 35 wild-caught great tits (Parus major) show any preference for widely abundant HIPVs compared to neutral (non-induced) plant odors, how fast they learn to associate olfactory, visual and multimodal foraging cues with food, and whether the olfactory preferences and learning speed were influenced by bird sex or habitat (urban or rural). We also tested how fast birds switch to a new cue of the same modality. Great tits showed no initial preference for HIPVs compared to neutral odors, and they learned all olfactory cues at a similar pace, except for methyl salicylate (MeSA), which they learned more slowly. We also found no differences in learning speeds between visual, olfactory and multimodal foraging cues, but birds learned the second cue they were offered faster than the first one. Bird sex or habitat had no effect on learning speed or olfactory preference, but urban birds tended to learn visual cues more slowly. We conclude that insectivorous birds utilize olfactory and visual cues with similar efficiency in foraging, and that they probably don‘t have any special predisposition toward the tested HIPVs. These results confirm that great tits are flexible foragers with good learning abilities.

Birds differentially prioritize visual and olfactory foraging cues depending on habitat of origin and sex

“…The birds were trained and tested individually in an experimental foraging arena that contained four artificial trees with five foraging holes and perches each ( figure 1 ). Additional details on bird housing, construction of the arena and preparation of visual and olfactory foraging cues are described in electronic supplementary material, appendix S1, and previously reported in [ 28 ].

Figure 1 Foraging arena setup for testing sensory preferences in great tits: the arena consisted of four wooden boards with foraging holes and perches for landing.

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“…The original data and code used in this paper are included in the electronic supplementary material [63].…”

“…In insects, particularly bees, integration of olfactory and visual information via bottom-up processes is relatively well studied (reviewed by [ 8 ]): in summary, multimodal stimuli have higher salience than unimodal stimuli, attract attention more effectively, improve signal detection and increase discrimination accuracy [ 3 , 8 , 24 – 26 ]. There is currently no evidence that this type of multisensory integration occurs in birds [ 27 ], and a previous study from our group suggests that great tits do not learn multimodal forging cues faster than either visual or olfactory cues alone [ 28 ]. In that study, however, we compared learning speed between birds that were trained with only one type of stimulus (visual, olfactory or multimodal) [ 28 ]; it is still possible that because great tits are good learners they may be able to use unimodal and multimodal signals equally well if required.…”

“…There is currently no evidence that this type of multisensory integration occurs in birds [ 27 ], and a previous study from our group suggests that great tits do not learn multimodal forging cues faster than either visual or olfactory cues alone [ 28 ]. In that study, however, we compared learning speed between birds that were trained with only one type of stimulus (visual, olfactory or multimodal) [ 28 ]; it is still possible that because great tits are good learners they may be able to use unimodal and multimodal signals equally well if required. Yet, other aspects of multisensory integration may be uncovered by examining how birds perceive and prioritize components of multimodal cues.…”

“…This makes it a suitable model species for studying urban adaptations. Great tits use both vision and olfaction during foraging [ 29 ], and will quickly learn cues associated with either sense [ 28 ]. In the present study, we asked the following questions: (1) do great tits learn and perceive components of multimodal cues in an integrated way and (2) do urban and forest great tits, or females and males, prioritize vision and olfaction differently during foraging?…”