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Leaf shape deters plant processing by an herbivorous weevil

Abstract

The shapes of plant leaves are remarkably diverse, but their ecological functions are largely unknown. Reports on the effects of leaf shape on biotic interactions such as herbivory are especially scarce, partly because herbivorous insects rarely rely on leaf shape for host selection. Here, we show that leaf shape acts as a physical deterrent against a leaf-processing herbivore. Plants in the genus Isodon (Lamiaceae) host a specialized leaf-rolling weevil (Apoderus praecellens) whose ovipositing females process an entire leaf into a leaf roll to serve as larval food and shelter. Among the species of Isodon, I. umbrosus var. hakusanensis is exceptional in that it has deeply lobed leaves. Because leaf processing follows a consistent sequence of complex behaviours, the unusual shape of I. umbrosus leaves may disrupt this process. Under both natural and laboratory conditions, female weevils preferred I. trichocarpus, a close relative with non-lobed leaves, over I. umbrosus. Nutritional properties of the leaves do not explain this preference because weevil larvae developed equally well on both hosts. Modifying the non-lobed I. trichocarpus leaves to mimic the shape of I. umbrosus leaves also discouraged leaf processing. Leaf processing often terminated because weevils failed to complete the inspection routine on I. umbrosus leaves. Leaf shape may be an important but overlooked factor that affects the interactions between plants and leaf-processing herbivores.

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Fig. 1: The leaf-rolling weevil A. praecellens and host Isodon plants.
Fig. 2: Female preference and offspring performance on I. umbrosus var. hakusanensis and I. trichocarpus.
Fig. 3: Effect of leaf lobation on female preference.

Data availability

The data that support the findings of this study are available from the corresponding author on request.

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Acknowledgements

We thank S. Sakai and K. Mochizuki for helpful suggestions throughout the course of the study and W. Toki, R. Nakadai, S. Furukawa, K. Takeda, J. Li and I. Kamata for discussion. K. Mochizuki, S. Furukawa, K. Takeda, J. Li and I. Kamata helped collect materials and data. S. Sakai, K. Koba and T. Muranaka provided comments that improved the manuscript. This work was supported by a Grant-in-Aid for JSPS Fellows (grant no. 18J12748), a grant from the Fujiwara Natural History Foundation to Y.H. and a Grant-in-Aid for Scientific Research (B) to A.K. (grant no. 15H04421).

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Y.H. and A.K. designed the research. Y.H. performed the research and analysed the data. Y.H. and A.K. wrote the paper.

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Correspondence to Yumiko Higuchi.

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The authors declare no competing interests.

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Peer review information: Nature Plants thanks Thomas Givnish and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Fig. 1 and Tables 1–3.

Reporting Summary

Supplementary Video 1

Surveying behaviours of female A. praecellens on leaves of I. trichocarpus.

Supplementary Video 2

Surveying behaviours of female A. praecellens on leaves of I. umbrosus var. hakusanensis.

Supplementary Video 3

Rolling behaviour of a female A. praecellens on a leaf of I. umbrosus var. hakusanensis.

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Higuchi, Y., Kawakita, A. Leaf shape deters plant processing by an herbivorous weevil. Nat. Plants 5, 959–964 (2019). https://doi.org/10.1038/s41477-019-0505-x

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