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Host Feeding by an Herbivore Improves the Performance of Offspring

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Abstract

Herbivores have developed diverse strategies to manipulate host plants for their own benefits. The gall induction by the maize orange leafhopper Cicadulina bipunctata is different from that by other gall-inducing insects in that the galls are induced not on feeding sites but appear on distant, newly developing leaves. In addition, adult C. bipunctata are highly mobile and seldom feed on gall tissue that they have induced. These mean that the gall induction by C. bipunctata is unlikely to contribute to the fitness of the inducer itself. The objective of this study was to determine whether manipulation of the host plant by this leafhopper has a subsequent benefit to offspring. Adults feeding on maize seedlings caused a partial change in the glucose content and a remarkable change in the accumulation of free amino acids in the gall tissue. Increases in emergence and developmental rates were observed in nymphs feeding on gall tissue induced by prior adult feeding. Such improvements were not evident in nymphs feeding on a C. bipunctata-resistant variety, which rarely displays galls after C. bipunctata feeding, nor on maize seedlings previously foraged by another leafhopper, Psammotettix striatus. The results indicate that gall tissue induced by adult C. bipunctata contribute to better performance of its offspring through improvement of the nutritional components of host plants.

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References

  • Abrahamson, W. G., & McCrea, K. D. (1986). Nutrient and biomass allocation in Solidago altissima: effects of two stem gallmakers, fertilization, and ramet isolation. Oecologia, 68, 174–180.

    Article  Google Scholar 

  • Awmack, C. S., & Leather, S. R. (2002). Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817–844.

    Article  PubMed  CAS  Google Scholar 

  • Batlle, A., Martínez, M. A., & Amparo, L. (2000). Occurrence, distribution and epidemiology of Grapevine Yellows in Spain. European Journal of Pathology, 106, 811–816.

    Article  Google Scholar 

  • Belliure, B., Janssen, A., Maris, P. C., Peters, D., & Sabelis, M. W. (2005). Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters, 8, 70–79.

    Article  Google Scholar 

  • Fisher, M. (1987). The effect of previously infested spruce needles on the growth of the green spruce aphid, Elatobium abietinum, and the effect of the aphid on the amino acid balance of the host plant. The Annals of Applied Biology, 111, 33–41.

    Article  Google Scholar 

  • Forrest, J. M. S. (1981). The growth of Aphis fabae as an indicator of the nutritional advantage of galling to the apple aphid Dysaphis devecta. Entomological Experimental Application, 14, 477–483.

    Article  Google Scholar 

  • Fukui, A., Murakami, M., Konno, K., Nakamura, M., & Ohgushi, T. (2002). A leaf-rolling caterpillar improves leaf quality. Entomological Science, 5, 263–266.

    Google Scholar 

  • Giron, D., Kaiser, W., Imbault, N., & Casas, J. (2007). Cytokinin-mediated leaf manipulation by a leafminer caterpillar. Biological Letters, 3, 340–343.

    Article  CAS  Google Scholar 

  • Hartley, S. E., & Lawton, J. H. (1992). Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. Journal of Animal Ecology, 61, 113–119.

    Article  Google Scholar 

  • Howe, G. A., & Jander, G. (2008). Plant immunity to insect herbivores. Annual Review of Plant Biology, 59, 41–66.

    Article  PubMed  CAS  Google Scholar 

  • Ikai, N., & Hijii, N. (2007). Manipulation of tannins in oakd by galling cynipids. Journal of Forest Research, 12, 316–319.

    Article  CAS  Google Scholar 

  • Izumi, Y., Anniwaer, K., Yoshida, H., Sonoda, S., Fujisaki, K., & Tsumuki, H. (2005). Comparison of cold hardiness and sugar content between diapausing and nondiapausing pupae of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Physiological Entomology, 30, 36–41.

    Article  CAS  Google Scholar 

  • Kaiser, W., Huguet, E., Casas, J., Commin, C., & Giron, D. (2010). Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proceedings. Biological Sciences , 277, 2311–2319.

    Article  CAS  Google Scholar 

  • Kamitani, S. (1997). Observation on the lateral carinae of the pronotum in paralimnini and its allied tribes (Homoptera, Cicadellidae, Deltocephalinae). ESAKIA, 37, 25–33.

    Google Scholar 

  • Karley, A. J., Douglas, A. E., & Parker, W. E. (2002). Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. Journal of Experimental Biology, 205, 3009–3018.

    PubMed  CAS  Google Scholar 

  • Koyama, Y., Yao, I., & Akimoto, S. (2004). Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall formation. Entomological Experimental Application, 113, 35–44.

    Article  CAS  Google Scholar 

  • Lu, Z. X., Heong, K. L., Yu, X. P., & Hu, C. (2004). Effect of plant nitrogen on ecological fitness of the brown planthopper, Nilaparvata lugens Stål, in rice. Journal of Asia- Pacific Entomology, 7, 97–104.

    Article  Google Scholar 

  • Maris, P. C., Joosten, N. N., Goldbach, R. W., & Peters, D. (2004). Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology, 94, 706–711.

    Article  PubMed  CAS  Google Scholar 

  • Matsukura, K., & Matsumura, M. (2010). Cultural control of leafhopper-induced maize wallaby-ear symptom in forage maize via early planting dates. Crop Protection, 29, 1401–1405.

    Article  Google Scholar 

  • Matsukura, K., Matsumura, M., & Tokuda, M. (2009). Host manipulation by the orange leafhopper Cicadulina bipunctata: gall induction on distant leaves by dose-dependent stimulation. Naturwissenschaften, 96, 1059–1066.

    Article  PubMed  CAS  Google Scholar 

  • Matsukura, K., Matsumura, M., & Tokuda, M. (2010). Both nymphs and adults of the maize orange leafhopper induce galls on their host plant. Communicative & Integrative Biology, 3, 388–389.

    Article  Google Scholar 

  • Matsumura, M., & Tokuda, M. (2004). A mass rearing method using rice seedlings for the maize orange leafhopper Cicadulina bipunctata (Melichar) (Homoptera: Cicadellidae) and a simple method for evaluating varietal resistance of maize to maize wallaby ear disease. Kyushu Plant Protection Research, 50, 35–39. (in Japanese with English summary).

    Article  Google Scholar 

  • Matsumura, M., Tokuda, M., & Endo, N. (2006). Recent outbreaks of the maize orange leafhopper Cicadulina bipunctata inducing gall-like structures on maize in Japan. In K. Ozaki, J. Yukawa, T. Ohgushi, & P. W. Price (Eds.), Gall arthropods and their associates: ecology and evolution (pp. 149–158). Tokyo: Springer-Verlag.

    Chapter  Google Scholar 

  • Nyman, T., & Julkunen-Tiitto, R. (2000). Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proceedings. Academy of Natural Science, 97, 13184–13187.

    Article  CAS  Google Scholar 

  • Ofori, F. A., & Francki, R. I. B. (1983). Evidence that maize wallaby ear disease is caused by an insect toxin. The Annals of Applied Biology, 103, 185–189.

    Article  Google Scholar 

  • Price, P. W. (1987). Adaptive nature of insect galls. Environmental Entomology, 16, 15–24.

    Google Scholar 

  • Salehi, M., Izadpanah, K., Siampour, M., & Taghizadeh, M. (2009). Molecular characterization and transmission of Bermuda grass white leaf phytoplasma in Iran. Journal of Plant Pathology, 91, 655–661.

    CAS  Google Scholar 

  • Sandström, J., & Pettersson, J. (1994). Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. Journal of Insect Physiology, 40, 947–955.

    Article  Google Scholar 

  • Schoonhoven, L. M., Jermy, T., & van Loon, J. J. A. (1998). Insect-plant biology. London: Chapman & Hall.

    Google Scholar 

  • Tokuda, M., & Matsumura, M. (2005). Effect of temperature on the development and reproduction of the maize orange leafhopper Cicadulina bipunctata (Melichar) (Homoptera: Cicadellidae). Applied Entomology and Zoology, 40, 213–220.

    Article  Google Scholar 

  • Weibull, J., & Melin, G. (1990). Free amino acid content of phloem sap from Brassica plants in relation to performance of Lipaphis erysimi (Hemiptera: Aphididae). The Annals of Applied Biology, 116, 417–423.

    Article  CAS  Google Scholar 

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Acknowledgments

We thank K. Abe and R. Yamada for rearing the insects for experiments, S. Kamitani and T. Mita for information about P. striatus, and M. Matsumoto for advice and assistance in amino acid analysis. This study was supported partly by a Grant-in Aid for Scientific Research on Innovative Areas (21200066) from MEXT, Japan and a grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan.

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Correspondence to Keiichiro Matsukura.

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Matsukura, K., Matsumura, M. & Tokuda, M. Host Feeding by an Herbivore Improves the Performance of Offspring. Evol Biol 39, 341–347 (2012). https://doi.org/10.1007/s11692-011-9150-7

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  • DOI: https://doi.org/10.1007/s11692-011-9150-7

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