Skip to main content
Log in

Differential effects of foliar endophytic fungi on insect herbivores attacking a herbaceous plant

  • Plant-Animal interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Foliar endophytic fungi appear to be ubiquitous in nature, occurring in a very wide range of herbaceous plants. However, their ecological role within forbs is very poorly known and interactions with foliar-feeding insects virtually unexplored. In this study, leaves of Cirsium arvense were infected with different combinations of endophyte fungi that had been previously isolated from this plant species. Two months later, leaf material was fed to larvae of a generalist insect, Mamestra brassicae, and adults of a specialist feeder, Cassida rubiginosa. Endophytes had different effects on the two insects; one species, Chaetomium cochliodes, reduced growth of M. brassicae but increased feeding by C. rubiginosa. Another species, Cladosporium cladosporioides, increased beetle feeding also, but had no effect on M. brassicae. Interactions were also seen between fungal species and dual infection with C. cladosporioides and Trichoderma viride greatly reduced beetle feeding. It is concluded that endophytes have significant effects on foliar feeding insects that differ with degree of specialism of the herbivore. We suggest that these effects are due to chemical changes in the host, brought about by fungal infection. These fungi have received remarkably little attention in the study of insect–plant interactions and yet could be important determinants of insect growth and even population dynamics.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abbas HK, Mulrooney JE (1994) Effect of some phytopathogenic fungi and their metabolites on growth of Heliothis virescens (F) and its host plants. Biocont Sci Technol 4:77–87

    Article  Google Scholar 

  • Arya C (2001) Qualitative changes of phytochemicals in Tecoma stans induced by fungal pathogens. J Med Aromatic Plant Sci 23:648–651

    CAS  Google Scholar 

  • Bacher S, Friedli J, Schär I (2002) Developing in diseased host plants increases survival and fecundity in a stem-boring weevil. Entomol Exp Appl 103:191–195

    Article  Google Scholar 

  • Beena KR, Ananda K, Sridhar KR (2000) Fungal endophytes of three sand dune plant species of west coast of India. Sydowia 52:1–9

    Google Scholar 

  • Clay K (1996) Interactions among fungal endophytes, grasses and herbivores. Res Pop Ecol 38:191–201

    Article  Google Scholar 

  • Devarajan PT, Suryanarayanan TS (2006) Evidence for the role of phytophagous insects in dispersal of non-grass fungal endophytes. Fungal Div 23:111–119

    Google Scholar 

  • Eschen R, Hunt S, Mykura C, Gange AC, Sutton BC (2010) The foliar endophytic fungal community composition in Cirsium arvense is affected by mycorrhizal colonization and soil nutrient content. Fungal Biol 114:991–998

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gange AC, Croft R, Wu W (2002) Gall insect and endophytic fungal co-occurrence in a xeric and mesic site. Ecol Entomol 27:362–365

    Article  Google Scholar 

  • Gange AC, Dey S, Currie AF, Sutton BC (2007) Site- and species-specific differences in endophyte occurrence in two herbaceous plants. J Ecol 95:614–622

    Article  Google Scholar 

  • Ghisalberti WL, Sivasithamparam K (1991) Antifungal antibiotics produced by Trichoderma spp. Soil Biol Biochem 23:1011–1020

    Article  CAS  Google Scholar 

  • Hartley SE, Gange AC (2009) The impacts of symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Ann Rev Entomol 54:323–342

    Article  CAS  Google Scholar 

  • Hodgson S (2010) Foliar fungal endophyte dynamics in herbaceous hosts. PhD thesis. Royal Holloway, University of London, Egham

  • Jaber LR, Vidal S (2010) Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation. Ecol Entomol 35:25–36

    Article  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 

  • Jongebloed PHJ, Elgersma DM, Sabelis MW (1992) Does a vascular fungus of tomato induce a defence response or a change in host plant quality that also affects the oviposition of spider mites? Exp Appl Acarol 16:227–236

    Article  Google Scholar 

  • Jordon-Thaden IE, Louda SM (2003) Chemistry of Cirsium and Carduus: a role in ecological risk assessment for biological control of weeds? Biochem System Ecol 31:1353–1396

    Google Scholar 

  • Kang JG, Kim KK, Kyu Y (1999) Antagonism and structural identification of antifungal compound from Chaetomium cochliodes against phytopathogenic fungi. Agric Chem Biotechnol 42:146–150

    CAS  Google Scholar 

  • Kluth S, Kruess A, Tscharntke T (2001) Interactions between the rust fungus Puccinia punctiformis and ectophagous and endophagous insects on creeping thistle. J Appl Ecol 38:548–556

    Article  Google Scholar 

  • Kruess A (2002) Indirect interactions between a fungal plant pathogen and a herbivorous beetle of the weed Cirsium arvense. Oecologia 130:563–569

    Article  Google Scholar 

  • McGee PA (2002) Reduced growth and deterrence from feeding of the insect pest Helicoverpa armigera associated with fungal endophytes from cotton. Aust J Exp Agric 42:995–999

    Article  Google Scholar 

  • Newcombe G, Shipunov A, Eigenbrode SD, Raghavendra AKH, Ding H, Anderson CL, Menjivar R, Crawford M, Schwarzländer M (2009) Endophytes influence protection and growth of an invasive plant. Comm Int Biol 2:29–31

    Article  Google Scholar 

  • Newington JE, Setälä H, Bezemer TM, Jones TH (2004) Potential effects of earthworms on leaf chewer performance. Func Ecol 18:746–751

    Article  Google Scholar 

  • Nitao JK, Meyer SLF, Oliver JE, Schmidt WF, Chitwood DJ (2002) Isolation of flavipin, a fungus compound antagonistic to plant–parasitic nematodes. Nematology 4:55–63

    Article  CAS  Google Scholar 

  • Obermaier E, Zwölfer H (1999) Plant quality or quantity? Host exploitation strategies in three Chrysomelidae species associated with Asteraceae host plants. Entomol Exp Appl 92:165–177

    Article  Google Scholar 

  • Osono T (2008) Endophytic and epiphytic phyllosphere fungi of Camellia japonica: seasonal and leaf age-dependent variations. Mycologia 100:387–391

    Article  PubMed  Google Scholar 

  • Raps A, Vidal S (1998) Indirect effects of an unspecialized endophytic fungus on specialized plant–herbivorous insect interactions. Oecologia 114:541–547

    Article  Google Scholar 

  • Redfern M (1983) Insects on thistles. Cambridge University Press, Cambridge

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Saunders M, Glenn AE, Kohn LM (2010) Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol Appl 3:525–537

    Article  Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect–plant biology. Oxford University Press, Oxford

    Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Schulz B, Wanke U, Draeger S, Aust H-J (1993) Endophytes from herbaceous plants and shrubs: effectiveness of surface sterilization methods. Mycol Res 97:1447–1450

    Article  Google Scholar 

  • Scorer AG (1913) The entomologist’s log book and dictionary of the life histories and food plants of the British macrolepidoptera. Routledge, London

    Google Scholar 

  • Scott PM, van Walbeek W (1971) Cladosporin, a new antifungal metabolite from Cladosporium cladosporioides. J Antibiot 24:747–755

    Article  PubMed  CAS  Google Scholar 

  • Stone JK, Bacon CW, White JF (2000) An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker, New York, pp 3–29

    Google Scholar 

  • Stout MJ, Thaler JS, Thomma BPHJ (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–689

    Article  PubMed  CAS  Google Scholar 

  • Tiley GD (2010) Biological flora of the British Isles: Cirsium arvense (L). Scop J Ecol 98:938–983

    Google Scholar 

  • Van Bael SA, Valencia MC, Rojas EI, Gomez N, Windsor DM, Herre EA (2009) Effects of foliar endophytic fungi on the preference and performance of the leaf beetle Chelymorpha alternans in Panama. Biotropica 41:221–225

    Article  Google Scholar 

  • Vega FE, Posada F, Aime MC, Pava-Ripoll M, Infante F, Rehner SA (2008) Entomopathogenic fungal endophytes. Biol Cont 46:72–82

    Article  Google Scholar 

  • Verma VC, Kharwar RN, Strobel GA (2009) Chemical and functional diversity of natural products from plant associated endophytic fungi. Nat Product Commun 4:1511–1532

    CAS  Google Scholar 

  • Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23:753–771

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to the Natural Environment Research Council and the Nuffield Foundation for funding this work. Thanks also to Neil Morley for providing technical assistance and to Tim Carty, Centre for Ecology and Hydrology for providing the eggs of Mamestra brassicae. Iñaki Valcarel assisted with the chemical analyses.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alan C. Gange.

Additional information

Communicated by Roland Brandl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gange, A.C., Eschen, R., Wearn, J.A. et al. Differential effects of foliar endophytic fungi on insect herbivores attacking a herbaceous plant. Oecologia 168, 1023–1031 (2012). https://doi.org/10.1007/s00442-011-2151-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2151-5

Keywords

Navigation