Skip to main content
SpringerLink
Log in

Behavioral responses of Thrips tabaci Lindeman to endophyte-inoculated onion plants

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Endophytic fungi colonize healthy plant tissues and can in some cases induce systemic resistance to the host against biotic and abiotic stresses. In our previous study, Hypocrea lixii isolate F3ST1 was able to colonize onion plants endophytically and conferred resistance to them against onion thrips, Thrips tabaci. To further elucidate the mechanism of resistance, we examined the behavioral response of adult and larval stages of T. tabaci to endophyte-inoculated (E+) and endophyte-free (E−) onion plants/sections. In choice experiments, female T. tabaci preferred E− over E+ plants. The number of feeding punctures and eggs was more on E− than on E+ plants. Oviposition was reduced sixfold on E+ plants within a 72-h experimental period. In the Y-tube olfactometer assay, thrips showed a 3.3-fold preference for E− plants. In individual larval choice experiments, significantly more first and second instars were found on the leaf sections of E− as compared to the E+ plants. In the settlement preference assay with groups of second instars, more larvae preferred leaf sections from E− over E+ plants with incremental time. Our findings suggest that endophyte-colonized onion plants may trigger antixenotic repellence of T. tabaci, impacting their biology. This repellence could be exploited in thrips control programs by using endophyte-inoculated plants in the field.

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

Access this article

Log in via an institution

Price includes VAT (Canada)

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

  • Akello J, Dubois T, Coyne D, Kyamanywa S (2008) Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage. Crop Prot 27:1437–1441

    Article  Google Scholar 

  • Akutse KS, Maniania NK, Fiaboe KKM, Van den Berg J, Ekesi S (2013) Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecol 6:293–301

    Article  Google Scholar 

  • Birithia R, Subramanian S, Pappu HR, Sseruwagi P, Muthomi JW, Narla D (2011) First report of Iris yellow spot virus infecting onions in Kenya and Uganda. Plant Dis 95:1195

    Article  Google Scholar 

  • Birithia RK, Subramanian S, Pappu HR, Muthomi JW, Narla RD (2014) Resistance to Iris yellow spot virus and onion thrips among onion varieties grown in Kenya. Int J Trop Insect Sci 34:73–79

    Article  Google Scholar 

  • Bittleston LS, Brockmann F, Wcislo W, Van Bael SA (2011) Endophytic fungi reduce leaf-cutting ant damage to seedlings. Biol Lett 7:30–32

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cardoza YJ, Alborn HT, Tumlinson JH (2002) In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J Chem Ecol 28:161–174

    Article  CAS  PubMed  Google Scholar 

  • Cherry AJ, Banito A, Djegui D, Lomer C (2004) Suppression of the stem-borer Sesamia calamistis (Lepidoptera: Noctuidae) in maize following seed dressing, topical application and stem injection with African isolates of Beauveria bassiana. Int J Pest Manag 50:67–73

    Article  Google Scholar 

  • Childers CC (1997) Feeding and oviposition injuries to plants. In: Lewis T (ed) Thrips as crop pests. CAB International, Wallingford, pp 505–537

    Google Scholar 

  • Clement SL, Hu J, Stewart AV, Wang B, Elberson LR (2011) Detrimental and neutral effects of a wild grass-fungal endophyte symbiotum on insect preference and performance. J Insect Sci 11:1–13

    Article  Google Scholar 

  • Cloyd RA (2009) Western flower thrips (Frankliniella occidentalis) management on ornamental crops grown in greenhouses: have we reached an impasse? Pest Tech 3:1–9

    Google Scholar 

  • Duffey SS, Felton GW (1991) Enzymatic antinutritive defenses of the tomato plants against insects. In: Hedin PA (ed) Naturally occurring pest bioregulators. American Chemical Society, Washington DC, pp 166–197

    Chapter  Google Scholar 

  • Egger B, Koschier EH (2014) Behavioural responses of Frankliniella occidentalis Pergande larvae to methyl jasmonate and cis-jasmone. J Pest Sci 87:53–59

    Article  Google Scholar 

  • Everitt BS, Hothorn T (2013) HSAUR: a handbook of statistical analyses using R. R package. http://cran.r-project.org/package=HSAUR. Accessed 15 May 2014

  • Faeth SH (2002) Are endophytic fungi defensive plant mutualists? Oikos 98:25–36

    Article  Google Scholar 

  • Gachu SM, Muthomi JW, Narla RD, Nderitu JH, Olubayo FM, Wagacha JM (2012) Management of thrips (Thrips tabaci) in bulb onion by use of vegetable intercrops. Int J Agri Sci 2:393–402

    Google Scholar 

  • Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34–41

    Article  Google Scholar 

  • HCDA (Horticultural Crops Development Authority) (2012) Export statistics volumes. http://www.hcda.or.ke/Statistics/2012/2012%20Horticulture%20Validated%20Report.pdf/. Accessed 16 Jan 2014

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  • Jallow MFA, Dugassa-Gobena D, Vidal S (2004) Indirect interaction between an unspecialized endophytic fungus and a polyphagous moth. Basic Appl Ecol 5:183–191

    Article  Google Scholar 

  • Jallow MFA, Dugassa-Gobena D, Vidal S (2008) Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthropod Plant Interact 2:53–62

    Article  Google Scholar 

  • Kaur HP, Singh B, Kaur A, Kaur S (2013) Antifeedent and toxic activity of endophytic Alternaria alternata against tobacco caterpillar Spodoptera litura. J Pest Sci 86:543–550

    Article  Google Scholar 

  • Leckie BM (2002) Effects of Beauveria bassiana mycelia and metabolites incorporated into synthetic diet and fed to larval Helicoverpa zea, and detection of endophytic Beauveria bassiana in tomato plants using PCR and ITS. PhD Dissertation, The University of Tennessee

  • Martin NA, Workman PJ, Buttler RC (2003) Insecticide resistance in onion thrips (Thrips tabaci) (Thysanoptera: thripidae). N Z J Crop Hortic Sci 31:99–106

    Article  CAS  Google Scholar 

  • Miller JR, Strickler KL (1984) Finding and accepting host plants. In: Bell WJ, Cardé RT (eds) Chemical ecology of insects. Chapman and Hall, London, pp 127–157

    Chapter  Google Scholar 

  • Mucciarelli M, Camusso W, Maffei M, Panicco P, Bicchi C (2007) Volatile terpenoids of endophyte-free and infected peppermint (Mentha piperita L.): chemical partitioning of a symbiosis. Microb Ecol 54:685–696

    Article  CAS  PubMed  Google Scholar 

  • Muvea AM, Meyhöfer R, Subramanian S, Poehling H-M, Ekesi S, Maniania NK (2014) Colonization of onions by endophytic fungi and their impacts on the biology of Thrips tabaci. PLoS ONE 9:e108242

    Article  PubMed Central  PubMed  Google Scholar 

  • Nault BA, Shelton AM (2010) Impact of insecticide efficacy on developing action thresholds for pest management: a case study of onion thrips (Thysanoptera: Thripidae) on onion. J Econ Entomol 103:1315–1326

    Article  PubMed  Google Scholar 

  • Nawrocka B (2003) Economic importance and the control method of Thrips tabaci Lindeman on onion. Bull OILB/SROP 26:321–324

    Google Scholar 

  • Ownley BH, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. BioControl 55:113–128

    Article  Google Scholar 

  • Popay AJ, Bonos SA (2005) Biotic responses in endophytic grasses. In: Roberts CA, West CP, Spiers DE (eds) Neotyphodium in cool-season grasses. Blackwell, Ames, pp 163–185

    Chapter  Google Scholar 

  • Qawasmeh A, Bourke C, Lee S, Gray M, Wheatley W, Sucher N, Raman A (2011) GC-MS analysis of volatile secondary metabolites in Mediterranean and Continental Festuca arundinacea (Poaceae) infected with the fungal endophyte Neotyphodium coenophialum strain AR542. Acta Chromatogr 23:621–628

    Article  CAS  Google Scholar 

  • Rabinowitch HD, Currah L (2002) Allium crop science: recent advances. CAB International, Wallingford

    Book  Google Scholar 

  • Richmond DS (2007) Mediation of herbivore-natural enemy interactions by Neotyphodium endophytes: the role of insect behavioural response. In: Popay AJ, Thom ER (eds) Proceedings of the 6th international symposium on fungal endophytes of grasses, 25–28 March 2007, Christchurch. Grasslands Research and Practice Series No. 13. New Zealand Grasslands Association, Dunedin, pp 313–319

  • Richmond DS, Kunkel BA, Nethi S, Grewal PS (2004) Top-down and bottom-up regulation of herbivores: Spodoptera frugiperda turns tables on endophyte-mediated plant defence and virulence of an entomopathogenic nematode. Ecol Entomol 29:353–360

    Article  Google Scholar 

  • Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  • Schulz B, Boyle C (2005) What are endophytes? In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 1–13

    Google Scholar 

  • Shrivastava G (2011) Production and roles of volatile secondary metabolites in interactions of the host plant tomato (Solanum lycopersicum L.) with other organisms at multi-trophic levels. PhD Dissertation, University of Tennessee

  • Sikora RA, Pocasangre L, Zum Felde A, Niere B, Vu TT, Dababat AA (2008) Mutualistic endophytic fungi and in-planta suppressiveness to plant parasitic nematodes. Biol Control 46:15–23

    Article  Google Scholar 

  • Stökl J, Brodmann J, Dafni A, Ayasse M, Hansson BS (2011) Smells like aphids: orchid flowers mimic aphid alarm pheromones to attract hoverflies for pollination. Proc R Soc B- Biol Sci 278:1216–1222

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. http://www.r-project.org/. Accessed 20 Apr 2014

  • Thakur A, Kaur S, Kaur A, Singh V (2013) Enhanced resistance to Spodoptera litura in endophyte infected cauliflower plants. Environ Entomol 42:240–246

    Article  PubMed  Google Scholar 

  • Trdan S, Vali N, Zezlina I, Bergant K, Znidar D (2005) Light blue sticky boards for mass trapping of onion thrips, Thrips tabaci Lindeman (Thysanoptera: Thripidae), in onion crops. J Plant Dis Prot 12:173–180

    Google Scholar 

  • Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159

    Article  Google Scholar 

  • Venables WN, Ripley B (2002) Modern applied statistics with S, 4th edn. http://cran.r-project.org/package=MASS. Accessed 10 May 2014

  • Webber J (1981) A natural control of Dutch elm disease. Nature 292:449–451

    Article  Google Scholar 

  • Wiesenborn WD, Morse JG (1986) Feeding rate of Scirtothrips citri (Moulton) (Thysanoptera: Thripidae) as influenced by life stage and temperature. Environ Entomol 15:763–766

    Article  Google Scholar 

Download references

Acknowledgments

This study was funded by BMZ (The German Federal Ministry for Economic Cooperation and Development) through GIZ (Deutsche Gesellschaft für Internationale Zusammenarbeit) through a project grant entitled “Implementation of integrated thrips and tospovirus management strategies in small-holder vegetable cropping systems of Eastern Africa” (project no. 11.7860.7-001.00, contract no. 81141840) for which we are grateful. The authors thank the icipe Thrips IPM Project staff for their technical assistance.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Institute of Horticultural Production Systems, Section Phytomedicine, Leibniz Universität Hannover, Hannover, Germany

    A. M. Muvea, R. Meyhöfer & H.-M. Poehling

  2. Plant Health Division, International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya

    A. M. Muvea, N. K. Maniania, S. Ekesi & S. Subramanian

Authors
  1. A. M. Muvea
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Meyhöfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. K. Maniania
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H.-M. Poehling
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Ekesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Subramanian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Meyhöfer.

Additional information

Communicated by M. Traugott.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muvea, A.M., Meyhöfer, R., Maniania, N.K. et al. Behavioral responses of Thrips tabaci Lindeman to endophyte-inoculated onion plants. J Pest Sci 88, 555–562 (2015). https://doi.org/10.1007/s10340-015-0645-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-015-0645-3

Keywords

Search

Navigation