Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Leaf shape deters plant processing by an herbivorous weevil

Nature Plants volume 5, pages 959–964 (2019)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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.

References

  1. Givnish, T. J. in Topics in Plant Population Biology (eds Solbrig, O. T. et al.) 375–407 (Macmillan, 1979).

  2. Nicotra, A. B. et al. The evolution and functional significance of leaf shape in the angiosperms. Funct. Plant Biol. 38, 535–552 (2011).

    Article  Google Scholar 

  3. Kidner, C. A. & Umbreen, S. Why is leaf shape so variable? Int. J. Plant Dev. Biol. 4, 64–75 (2010).

    Google Scholar 

  4. Brown, V. K. & Lawton, J. H. Herbivory and the evolution of leaf size and shape. Philos. Trans. R. Soc. Lond. B 333, 265–272 (1991).

    Article  Google Scholar 

  5. Berneys, E. A. & Chapman, R. F. Host-Plant Selection by Phytophagous Insects (Chapman and Hall, 1994).

  6. Prokopy, R. J. & Owens, E. D. Visual detection of plants by herbivorous insects. Annu. Rev. Entomol. 28, 337–364 (1983).

    Article  Google Scholar 

  7. Rausher, M. D. Search image for leaf shape in a butterfly. Science 200, 1071–1073 (1978).

    Article  CAS  Google Scholar 

  8. Gilbert, L. E. The coevolution of a butterfly and a vine. Sci. Am. 247, 110–121 (1982).

    Article  Google Scholar 

  9. Dell’Aglio, D. D., Losada, M. E. & Jiggins, C. D. Butterfly learning and the diversification of plant leaf shape. Front. Ecol. Evol. 4, 1–7 (2016).

    Google Scholar 

  10. Murata, G. & Yamazaki, T. in Flora of Japan vol. IIIa (eds Iwatsuki, K. et al.) 309–314 (Kodansha, 1993).

  11. Uéhara, C. & Suzuki, K. Host plants of the Subfamilies Apoderinae and Attelabinae (Coleoptera, Attelabidae) in the Chûbu District, Central Honshu, Japan. Res. Rep. Toyama Sci. Mus. 21, 77–97 (1998).

    Google Scholar 

  12. Mclellan, T. & Endler, J. A. The relative success of some methods for measuring and describing the shape of complex objects. Syst. Biol. 47, 264–281 (1998).

    Article  Google Scholar 

  13. Sakurai, K. Leaf size recognition and evaluation of some Attelabid weevils (2) Apoderus balteatus. Behaviour 106, 301–317 (1988).

    Article  Google Scholar 

  14. Sisó, S., Camarero, J. J. & Gil-Pelegrín, E. Relationship between hydraulic resistance and leaf morphology in broadleaf Quercus species: a new interpretation of leaf lobation. Trees 15, 341–345 (2001).

    Article  Google Scholar 

  15. Zwieniecki, M. A., Boyce, C. K. & Holbrook, N. M. Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves. Plant Cell Environ. 27, 357–365 (2004).

    Article  Google Scholar 

  16. Vogel, S. Convective cooling at low airspeeds and the shapes of broad leaves. J. Exp. Bot. 21, 91–101 (1970).

    Article  Google Scholar 

  17. Leigh, A., Sevanto, S., Close, J. D. & Nicotra, A. B. The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? Plant Cell Environ. 40, 237–248 (2017).

    Article  CAS  Google Scholar 

  18. Gianoli., E. & Carrasco-Urra, F. Leaf mimicry in a climbing plant protects against herbivory. Curr. Biol. 24, 984–987 (2014).

    Article  CAS  Google Scholar 

  19. Niemelä, P. & Tuomi, J. Does the leaf morphology of some plants mimic caterpillar damage? Oikos 50, 256–257 (1987).

    Article  Google Scholar 

  20. Fukui, A. Indirect interactions mediated by leaf shelter in animal-plant communities. Pop. Ecol. 43, 31–40 (2001).

    Article  Google Scholar 

  21. Vieira, C. & Romero, G. Q. Ecosystem engineers on plants: indirect facilitation of arthropod communities by leaf-rollers at different scales. Ecology 94, 1510–1518 (2013).

    Article  Google Scholar 

  22. Cornelissen, T., Cintra, F. & Santos, J. C. Shelter-building insects and their role as ecosystem engineers. Neotrop. Entomol. 45, 1–12 (2016).

    Article  CAS  Google Scholar 

  23. Harris, M. O. & Miller, J. R. Foliar form influences ovipositional behavior of the onion fly. Physiol. Entomol. 9, 145–155 (1984).

    Article  Google Scholar 

  24. Howlett, B. G. & Clarke, A. R. Role of foliar chemistry versus leaf-tip morphology in egg-batch placement by Chrysophtharta bimaculate (Olivier) (Coleoptera: Chrysomelidae). Aust. J. Entmol. 42, 144–148 (2003).

    Article  Google Scholar 

  25. Abràmoff, M. D., Magalhães, P. J. & Ram, S. J. Image processing with ImageJ. Biophoton. Int. 11, 36–42 (2004).

    Google Scholar 

  26. R Core Development Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).

Download references

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).

Author information

Authors and Affiliations

  1. Center for Ecological Research, Kyoto University, Otsu, Shiga, Japan

    Yumiko Higuchi

  2. The Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan

    Atsushi Kawakita

Authors
  1. Yumiko Higuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Atsushi Kawakita
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to Yumiko Higuchi.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-019-0505-x

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing