Endophyte-Mediated Resistance to Herbivores Depends on Herbivore Identity in the Wild GrassFestuca subverticillata

Abstract

Understanding factors that affect the context dependency of species interactions has been identified as a critical research area in ecology. The presence of symbionts in host plants can be an important factor influencing the outcome of plant-insect interactions. Similarly, herbivore identity can alter the outcome of plant-symbiont interactions. Symbiotic foliar fungal endophytes confer resistance to herbivores in economically important agronomic grasses, in part through the production of alkaloids. Although endophytes are common in nature, relatively little is known about their effects on herbivores of native, wild grass species, and a recent meta-analysis suggested that endophytes are only beneficial in agronomic settings. In this study, we performed choice trials for five insect species and a greenhouse experiment with one species to assess effects of the fungal endophyte Neotyphodium sp. on herbivores of the wild grass Festuca subverticillata. In feeding trials, endophyte presence altered the preference of all five insect species tested. However, the magnitude and direction of preference varied among species, with Pterophylla camellifolia (F.), Spodoptera frugiperda (J. E. Smith), and Rhopalosiphum padi L. preferring endophyte-disinfected plants and Encoptolophus costalis (Scudder) and Romalea guttata (Houttuyn) preferring endophyte-symbiotic plants. Despite reducing insect preference, the endophyte had no significant effect on S. frugiperda performance in a no-choice greenhouse experiment and did not increase plant growth in response to this herbivore. Our results show that endophyte-mediated resistance to herbivory depends strongly on herbivore identity and suggest that the fitness consequences of endophyte symbiosis for host plants will be context dependent on the local composition of insect herbivores.

Variable Effects of Grass-Neotyphodium Associations on Cereal Leaf Beetle (Coleoptera: Chrysomelidae) Feeding, Development and Survival

“…The results herein further document variable effects of E+ grasses on the preference and performance of phytophagous insects (Breen 1994;Clement et al 1994;Saikkonen et al 1999;Afkhami and Rudgers 2009;Clement 2009;Popay 2009) by showing that two graminoid pests responded differently to Neotyphodium infection of wild P. alpinum. In 48 hour preference experiments, R. padi preferred E-over E+ test plants.…”

“…Since the 1980s, much has been learned about factors that influence the outcome of grass-endophyteinsect interactions. For example, the expression and type of insect resistance (antixenosis, antibiosis) may be affected by host grass species/genotype, endophyte strain (including associated alkaloid profile), and insect species/genotype involved in a given interaction (Breen 1994;Clement et al 1994;Clement et al 2005;Afkhami and Rudgers 2009;Bieri et al 2009;Cheplick and Faeth 2009;Popay 2009;Crawford et al 2010). Today, the number of herbivorous insects that have been reported to be negatively affected by endophyte-infected (E+) grasses has grown to over 40 species (Kuldau and Bacon 2008;Popay 2009).…”

Fungal grass endophytes and arthropod communities: lessons from plant defence theory and multitrophic interactions

“…Note that most of these studies used generalist insect pest species, such as the armyworm and bird oat cherry aphid, in bioassay tests. At the other end of the spectrum, native invertebrate herbivores sometimes prefer and perform better (e.g., Saikkonen et al, 1999,Tibbets and Faeth, 1999and Afkhami and Rudgers, 2009 or reached higher abundances Shochat, 2010 andJani et al, 2010) on infected native grasses, in direct contradiction to the predictions of DMH. Thus, support for the DMH hypothesis appears much more equivocal in native grasses than in agronomic grasses, especially when native insect herbivores are considered.…”

“…The outcomes of these studies span the range of negative to neutral to positive effects of endophyte infection. Some studies involving native grasses show reduced herbivory or increased insect deterrence on infected grasses relative to uninfected grasses (Christensen and Latch, 1991, Brem and Leuchtmann, 2001, Gonthier et al, 2008, Clement et al, 1997, Clement et al, 2005, Tintjer and Rudgers, 2006and Afkhami and Rudgers, 2009, whilst other studies showed no difference (Christensen and Latch, 1991, Lopez et al, 1995, Clement et al, 1997, Tintjer and Rudgers, 2006and Afkhami and Rudgers, 2009, depending on herbivore species and endophyte strain. Note that most of these studies used generalist insect pest species, such as the armyworm and bird oat cherry aphid, in bioassay tests.…”

Environmental conditions and host plant origin override endophyte effects on invertebrate communities

“…Breen 1994;Clay et al 1985;Popay and Rowan 1994). However, there are only a few studies that have considered the impact of grass endophytes on arthropod communities or functional groups (e.g., Afkhami and Rudgers 2009;Faeth and Shochat 2010;Jani et al 2010). In this study, we used a whole-invertebrate community survey of a controlled common garden experiment to test how invertebrate diversity and community structure, and the number of individuals in functional invertebrate taxa and guilds differs between (i) endophyte infected (E+), endophyte free (E-), and manipulatively endophyte-free (ME-) tall fescue, (ii) host plants of different origin (wild populations from Åland, Gotland, coastal Sweden and one agronomical cultivar, K-31 from USA), and (iii) host plants growing in different abiotic environments (nutrient and water treatments).…”