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The attraction of insectivorous tit species to herbivore-damaged Scots pines

Abstract

Insectivorous birds are attracted to insect-damaged deciduous trees by plant cues. However, it is unknown whether birds can locate insects on coniferous trees by plant cues induced by insect feeding activity. Feeding damage may induce plant chemical changes even in parts of a tree where no actual infestation is present. In a laboratory set-up, we studied the behavioural responses of Great Tits (Parus major) and Blue Tits (Cyanistes caeruleus) to Scots pine (Pinus sylvestris) that had been systemically herbivore-induced by pine sawfly larvae (Diprion pini). When birds were simultaneously offered an untreated control Scots pine branch and a systemically herbivore-induced test branch (i.e. a branch without actually feeding larvae) in a study booth, they visited the systemically herbivore-induced test branch first significantly more often than the control branch. In order to elucidate whether this discrimination was based on visual and/or olfactory plant cues, we compared the light reflectance and odour of test and control branches in a separate experiment. The control branches tended to show higher light reflectance throughout the avian vision range of 300–700 nm than the test branches, but the discrimination threshold model suggests that birds are not able to detect this difference. The systemically herbivore-induced branches emitted the same 29 volatile compounds as control branches, but 21 of them were released in greater quantities by the test branches. Our study shows that herbivore-induced Scots pine branches emit olfactory cues that may allow the birds to discriminate between uninfested and insect-infested trees, while the role of visual, systemically induced plant cues is less obvious and needs further investigation.

Zusammenfassung

Insektivore Meisen-Arten werden von fraßgeschädigten Waldkiefern angelockt.

Durch Insekten geschädigte Laubbäume produzieren Signale, die für insektivore Vögel attraktiv sind. Ob Vögel auch Insekten an Nadelbäumen durch Signale, die die Pflanze aufgrund der Fraßaktivität der Insekten produziert, wahrnehmen können, ist dagegen unbekannt. Fraßschäden können systemisch chemische Veränderungen selbst in Teilen der Pflanze induzieren, die gar nicht von Schädlingen befallen sind. In einem Experiment unter kontrollierten Bedingungen untersuchten wir die Verhaltensantworten von Kohlmeisen (Parus major) und Blaumeisen (Cyanistes caeruleus) auf Waldkiefern (Pinus sylvestris), die zuvor systemisch durch Befall von Larven der Kiefernbuschhornblattwespe (Diprion pini) induziert wurden. Wenn Vögel in einer Testbox zwischen einem unbehandelten Kontrollast einer Kiefer und einem systemisch fraßinduzierten Ast wählen konnten, besuchten sie signifikant häufiger zuerst den fraßinduzierten Ast. Um zu untersuchen, ob diese Unterscheidung zwischen ungeschädigtem und fraßinduziertem Kiefernast auf visuellen und/oder olfaktorischen Pflanzensignalen basierte, verglichen wir die Lichtreflexion und den Geruch von Kontroll- und induzierten Ästen. Die Kontrolläste hatten tendenziell höhere Lichtreflexionswerte im kompletten Bereich des für Vögel sichtbaren Lichtspektrums (300–700 nm). Ein Diskriminierungsschwellenmodell sagte jedoch vorher, dass diese Unterschiede zu gering sind, um von den Vögeln wahrgenommen zu werden. Die systemisch fraßinduzierten Äste verströmten die gleichen 29 Duftkomponenten wie die Kontrolläste; 21 davon wurden jedoch von den fraßinduzierten Ästen in höheren Mengen abgegeben. Unsere Studie zeigt, dass systemisch fraßinduzierte Kiefernäste olfaktorische Signale produzieren, die es Vögeln ermöglichen, zwischen unbefallenen und von Insekten befallenen Bäumen zu diskriminieren. Die Rolle von visuellen, systemisch induzierten Signalen ist dagegen nicht eindeutig geklärt und bedarf weiterer Untersuchungen.

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Acknowledgements

We thank Ute Braun, Freie Universität Berlin, for her help in rearing the sawflies and collecting pine branches. Many thanks are also due to the Botanical Garden of Freie Universität Berlin for allowing bird catching there. We also want to thank Prof. Dr. Holger Dau and Dr. Ivelina Zaharieva from the Physics Department, Freie Universität Berlin, for assistance with the spectrophotometer analyses. Thank you to Carita Lindstedt-Kareksela for doing the discrimination threshold model and commenting on the manuscript. We want to thank two reviewers for their valuable comments on an earlier version of this manuscript. The work was supported by the Finnish Cultural Foundation (grant to EM).

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Correspondence to Elina Mäntylä.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. The study was conducted with permission of the Landesamt für Gesundheit und Soziales Berlin (no. 0149/12), and ringing of birds was done with permission from Vogelwarte Radolfzell, Germany (no. 1882).

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Communicated by T. Gottschalk.

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Mäntylä, E., Kleier, S., Kipper, S. et al. The attraction of insectivorous tit species to herbivore-damaged Scots pines. J Ornithol 158, 479–491 (2017). https://doi.org/10.1007/s10336-016-1412-9

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Keywords

  • Cyanistes caeruleus
  • Herbivory
  • Olfaction
  • Parus major
  • Systemic induction
  • Vision
  • Volatile organic compounds