Skip to main content
SpringerLink
Log in

Life history of Stenopsylla nigricornis (Hemiptera: Psylloidea: Triozidae) and phytohormones involved in its gall induction

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Many phytophagous insects have an ability to manipulate plant tissue and induce galls, but the mechanism is not yet fully understood. Some insects have multivoltine life cycles, and each generation induces galls on different plant species or different organs in the same host. Such host-use patterns are interesting study subjects to clarify the gall-inducing mechanisms of insects. We focused on a multivoltine and gall-inducing psyllid Stenopsylla nigricornis Kuwayama (Hemiptera: Psylloidea: Triozidae), which is associated with Symplocos lucida Sieb. (Symplocaceae). Based on periodic field surveys in Kyushu, Japan, S. nigricornis is revealed to have a bivoltine life history. Then, we revealed that the spring generation induces galls on leaves, while the autumn generation does so on flower buds and overwintering leaf buds. We also analyzed phytohormones in normal plant tissue, S. nigricornis nymphs, and their galls. As a result, nymphs were discovered to contain much higher concentrations of isopentenyladenosine and its possible precursor, isopentenyladenosine riboside than plant tissues, strongly suggesting that the phytohormone is involved in gall induction by S. nigricornis. Because flower bud galls contained significantly lower concentrations of abscisic acid (ABA) than normal flower bud, the autumn generation nymphs are considered to regulate the ABA level and to promote the earlier opening of host flower buds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Asami T, Sekimata K, Wang JM, Yoneyama K, Takeuchi Y, Yoshida S (1999) Preparation of (±)-[1, 2-13C2] abscisic acid for use as a stable and pure internal standard. J Chem Res, Synop 11:658–659

    Article  Google Scholar 

  • Askew RR (1984) The biology of gall wasps. In: Ananthakrishnan TN (ed) Biology of gall insects. Oxford and IBH Publishing Co., New Delhi, Bombay, Calcutta, pp 223–271

    Google Scholar 

  • Csóka G, Stone GN, Merika G (2005) Biology, ecology, and evolution of gall-inducing Cynipidae. In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers Inc, Enfield, pp 573–642

    Google Scholar 

  • Dawkins R (1982) The extended phenotype. Oxford University Press, Oxford

    Google Scholar 

  • De Bruyn LJ, Vandevyvere J, Jamié D, Prisen E (1998) The effects of gall formation by Lipara lucens (Diptera: Chloropidae) on its host Phragmites australis (Poaceae). In: Csóka G, Mattson WJ, Stone GN, Price PW (eds) The biology of gall-inducing arthropods. General technical report NC-199. USDA Forest Service, St. Paul, pp 173–187

  • Dorchin N, Hoffmann JH, Stirk WA, Novák O, Strnad M, van Staden J (2009) Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasp larvae. Physiol Entomol 34:359–369

    Article  Google Scholar 

  • Kumashiro S, Matsukura K, Kawaura K, Matsumura M, Ogihara Y, Tokuda M (2011) Effect of barley chromosome addition on the susceptibility of wheat to feeding by a gall-inducing leafhopper. Naturwissenschaften 98:983–987

    Article  CAS  PubMed  Google Scholar 

  • Kutsukake M, Meng X, Katayama N, Nikoh N, Shibao H, Fukatsu T (2012) An insect-induced novel plant phenotype for sustaining social life in a closed system. Nature Commun 3:1187

    Article  Google Scholar 

  • Mani MS (1964) Ecology of plant galls. Dr. W Junk Publishers, The Hague

    Book  Google Scholar 

  • Mapes CC, Davies PJ (2001) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurosta solidaginis. New Phytol 151:203–212

    Article  CAS  Google Scholar 

  • Matsukura K, Matsumura M, Tokuda M (2012) Host feeding by an herbivore improves the performance of offspring. Evol Biol 39:341–347

    Article  Google Scholar 

  • Miyatake Y (1976) Psyllidae of Tsushima Island. In: The Nagasaki Biological Society (ed) Creatures of Tsushima. The Nagasaki Biological Society, Nagasaki, pp 487–495 (in Japanese.)

    Google Scholar 

  • Murata G (1989) Symplocaceae. In: Satake Y, Hara H, Watari S, Tominari T (eds) Wild flowers of Japan (Woody Plants II). Heibonsha Ltd., Publishers, Tokyo, pp 170–174

    Google Scholar 

  • Price PW, Fernandes GW, Waring GL (1987) Adaptive nature of insect galls. Environ Entomol 16:15–24

    Article  Google Scholar 

  • Shorthouse JD, Wool D, Raman A (2005) Gall-inducing insects – nature's most sophisticated herbivores. Basic Appl Ecol 6:407–411

    Article  Google Scholar 

  • Stone GN, Schonrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522

    Article  Google Scholar 

  • Straka JR, Hayward AR, Emery NRJ (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones. J Plant Interact 5:197–203

    Article  CAS  Google Scholar 

  • Suzuki H, Yokokura J, Ito T, Arai R, Yokoyama C, Toshima H, Nagata S, Asami T, Suzuki Y (2014) Biosynthetic pathway of the phytohormone auxin in insects and screening of its inhibitors. Insect Biochem Mol Biol 53:66–72

    Article  CAS  PubMed  Google Scholar 

  • Tanaka Y, Okada K, Asami T, Suzuki Y (2013) Phytohormones in Japanese mugwort gall induction by a gall-inducing gall midge. Biosci Biotechnol Biochem 77:1942–1948

    Article  CAS  PubMed  Google Scholar 

  • Tokuda M (2012) Biology of Asphondyliini (Diptera: Cecidomyiidae). Entomological Science 15:361–383

    Article  Google Scholar 

  • Tokuda M, Jikumaru Y, Matsukura K, Takebayashi Y, Kumashiro S, Matsukura M, Kamiya Y (2013) Phytohormones related to host plant manipulation by a gall-inducing leafhopper. PLoS ONE 8:e62350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tooker JF, De Moraes CM (2011) Feeding by a gall-inducing caterpillar species increases levels of indole-3-acetic and decreases abscisic acid in Solidago altissima stems. Arthropod-Plant Interact 5:115–124

    Article  Google Scholar 

  • Tooker JF, Helms AM (2014) Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. J Chem Ecol 40:742–753

    Article  CAS  PubMed  Google Scholar 

  • Uematsu K, Shibao H (2014) Formation of long-lasting galls by overwintered nymphs in the Japanese aphid Quadrartus yoshinomiyai (Hemiptera: Aphididae: Hormaphidinae) Entomological. Science 17:118–121

    Google Scholar 

  • Wood BW, Payne JA (1988) Growth regulators in chestnut shoot galls infected with oriental chestnut wasp (Hymenoptera, Cynipidae). Environ Entomol 17:915–920

    Article  CAS  Google Scholar 

  • Yamaguchi H, Tanaka H, Hasegawa M, Tokuda M, Asami T, Suzuki Y (2012) Phytohormones and willow gall induction by a gall-inducing sawfly. New Phytol 196:586–595

    Article  CAS  PubMed  Google Scholar 

  • Yukawa J, Masuda H (1996) Insect and mite galls of Japan in colors. Zenkoku Nôson Kyôiku Kyôkai, Tokyo (In Japanese with English explanations for color plates)

    Google Scholar 

  • Zheng C, Halaly T, Acheampong AK, Takebayashi Y, Jikumaru K, Kamiya Y, Or E (2015) Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. J Exp Bot 66:1527–1542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Dr. K. M. Harris for his critical reading of an early draft and Dr. H. Inoue for his kind advice to observe psyllid ovaries.

Author information

Authors and Affiliations

  1. Laboratory of Systems Ecology, Faculty of Agriculture, Saga University, Saga, 840-8502, Japan

    Shinya Kai, Shun Kumashiro, Yoshihisa Shiomi & Makoto Tokuda

  2. The United Graduate School of Agricultural Sciences, Kagoshima University, Kagoshima, 890-0065, Japan

    Shuhei Adachi & Makoto Tokuda

  3. Department of Bioresource Science, Ibaraki University, Inashiki-gun, Ibaraki, 300-0393, Japan

    Yoshihito Suzuki

  4. Hikarigaoka, Chikushino, Fukuoka, 818-0036, Japan

    Kiyoko Matsunaga

  5. Yamakawa, Kurume, Fukuoka, 839-0817, Japan

    Naohisa Gyoutoku

  6. Department of Applied Biological Chemistry, The University of Tokyo, Bunkyo-ku, Tokyo, 113-8657, Japan

    Tadao Asami

Authors
  1. Shinya Kai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shun Kumashiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shuhei Adachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoshihito Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshihisa Shiomi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kiyoko Matsunaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Naohisa Gyoutoku
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tadao Asami
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Makoto Tokuda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Makoto Tokuda.

Additional information

Handling Editor: John F Tooker.

Appendices

Appendix 1: Seasonal changes in the bud status on Symplocos lucida and density of galls induced by Stenopsylla nigricornis at the census site from April 2013 to March 2014

figure a

Appendix 2: Seasonal changes in the bud status on Symplocos lucida and density of galls induced by Stenopsylla nigricornis at the census site from April to December 2014

figure b

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kai, S., Kumashiro, S., Adachi, S. et al. Life history of Stenopsylla nigricornis (Hemiptera: Psylloidea: Triozidae) and phytohormones involved in its gall induction. Arthropod-Plant Interactions 11, 99–108 (2017). https://doi.org/10.1007/s11829-016-9470-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-016-9470-8

Keywords

Search

Navigation