Fungal endophytes of native grasses decrease insect herbivore preference and performance
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Endophytic fungal symbionts of grasses are well known for their protective benefit of herbivory reduction. However, the majority of studies on endophyte–grass symbioses have been conducted on economically important, agricultural species—particularly tall fescue (Lolium arundinaceum) and perennial ryegrass (Lolium perenne)—raising the hypothesis that strong benefits are the product of artificial selection. We examined whether fungal endophytes found in natural populations of native grass species deterred insect herbivores. By testing several native grass–endophyte symbiota, we examined phylogenetic signals in the effects of endophytes on insects and compared the relative importance of herbivore and symbiotum identity in the outcome of the interactions. Preference was assessed using three herbivore species [Spodoptera frugiperda (Lepidoptera), Schistocerca americana (Orthoptera), Rhopalosiphum padi (Hemiptera)] and ten native symbiota, which spanned seven grass genera. We also assessed herbivore performance in a no choice experiment for five native symbiota against S. frugiperda. We compared greenhouse and laboratory trials with natural levels of herbivory measured in experimental field populations. In all cases, we included the agronomic grass species, L. arundinaceum, to compare with results from the native grasses. Both in the field and in experimental trials, herbivores showed a significant preference for endophyte-free plant material for the majority of native grasses, with up to three times lower herbivory for endophyte-symbiotic plants; however, the degree of response depended on the identity of the herbivore species. Endophyte presence also significantly reduced performance of S. frugiperda for the majority of grass species. In contrast, the endophyte in L. arundinaceum had few significant anti-herbivore effects, except for a reduction in herbivory at one of two field sites. Our results demonstrate that the mechanisms by which native symbionts deter herbivores are at least as potent as those in model agricultural systems, despite the absence of artificial selection.
KeywordsPlant–herbivore interactions Herbivore defenses Native grasses Lolium arundinaceum Alkaloids
We would like to thank S. Behmer and his lab for supplying the grasshoppers used in this experiment, and P. Nagabhyru and C. Schardl for providing loline data for our plant accessions. The Rice Undergraduate Honors Research in Ecology and Evolutionary Biology class of 2009 provided useful discussion, and S. Clement, A. Davitt, C. Schardl, and P. Nagabhyru provided insightful comments on the text. K. Clay, C. Rudolf, D. Saenz, and R. Thill provided logistical support at the field sites, and L. Albert, S. Hammer, E. Seifert, and S. Ziegler assisted with field data collection. KMC was supported by a National Science Foundation Graduate Research Fellowship and a Rice University Presidential Fellowship. JAR was supported by the endowed Godwin Professorship at Rice University and National Science Foundation DEB 054278.
- Bacon CW, White JF (1994) Stains, media, and procedures for analyzing endophytes. In: Bacon CW, White JF (eds) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton, pp 47–56Google Scholar
- Ball DM, Pedersen JF, Lacefield GD (1993) The tall fescue endophyte. Am Sci 81:370–379Google Scholar
- Barbosa P, Krischik VA, Jones CG (1991) Microbial mediation of plant–herbivore interactions. Wiley, New YorkGoogle Scholar
- Bultman TL, Conard NJ (1998) Effects of endophytic fungus, nutrient level, and plant damage on performance of fall armyworm (Lepidoptera:Noctuidae). Environ Entomol 27:631–635Google Scholar
- Clement SL, Lester DG, Wilson AD, Pike KS (1992) Behavior and performance of Diuraphis noxia (Homoptera: Aphididae) on fungal endophyte-infected and uninfected perennial ryegrass. J Econ Entomol 85:583–588Google Scholar
- Dugassa-Gobena D, Raps A, Vidal S (1998) Influence of fungal endophytes on allelochemicals of their host plants and the behaviour of insects. Med Fac Landbouw Univ Gent 63:333–337Google Scholar
- Gehring CA, Whitham TG (2002) Mycorrhizae–herbivore interactions: population and community consequences. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, Heidelberg, pp 295–320Google Scholar
- Hardy TN, Clay K, Hammond AM (1985) Fall armyworm (Lepidoptera, Noctuidae)—a laboratory bioassay and larval preference study for the fungal endophyte of perennial ryegrass. J Econ Entomol 78:571–575Google Scholar
- Institute SAS (2009) The SAS system for Windows, release 9.1.3. SAS Institute. Cary, North CarolinaGoogle Scholar
- Lopez JE, Faeth SH, Miller M (1995) Effect of endophytic fungi on herbivory by redlegged grasshoppers (Orthoptera: Acrididae) on Arizona fescue. Environ Entomol 24:1576–1580Google Scholar
- Rasband WS (2009) ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA, http://rsb.info.nih.gov/ij/