Contrasting Effects of Grass - Endophyte Chemotypes on a Tri-Trophic Cascade

Benjamin Fuchs,Eric Kuhnert,Jochen Krauss

doi:10.1007/s10886-020-01163-9

Abstract

Systemic grass-endophytes of the genus Epichloë symbiotically infect the above-ground plant parts of many grass species, where they produce alkaloids in a grass- and endophyte-specific manner that are toxic or deterrent to herbivores. An increasing number of studies show cascading negative effects of endophyte-derived alkaloids that extend to higher trophic levels, harming beneficial insects, including those that control aphid populations. Lacewings are one of the major biological aphid controls, and are especially resistant to insecticides and pollutants, but their susceptibility to endophyte infection in the food chain has never been studied. Our study found variability in aphid population growth depending on the endophyte-grass chemotype, where aphid population growth was lowest on chemotypes known for producing high amounts of loline alkaloids. We also showed that larval and pupal development and mortality of the Common Green Lacewing (Chrysoperla carnea) was, in a non-choice experiment, not affected by endophyte infection in the food chain. This is a first indication that lacewings might be resistant to endophyte-derived alkaloids and could be robust biocontrol agents when applied together with endophyte-infected grass, possibly replacing chemical pesticides.

Highlights

Pest control in agricultural systems has relied for many decades on the application of chemical pesticides to control plant damage caused by insect herbivores
Aphid population growth was slower on Lolium perenne plants compared to FE- and FEM, and did not differ between with and without endophyte infection until weeks 3 and 4, when populations on LE- plants showed a similar development to FE- plants, and aphid populations on LE+ plants were similar to FEM plants (Table 1, Fig. 1)
Aphid populations were negatively affected by endophyte infection in their host grass, independent of the plant species and its associated symbiotic fungus (i.e. Festuca arundinaceae with Epichloë coenophiala; Lolium perenne with Epichloë festucae var. lolii)

Summary

Introduction

Pest control in agricultural systems has relied for many decades on the application of chemical pesticides to control plant damage caused by insect herbivores. Asexual representatives of systemic fungal endophytes (genus Epichloë) infecting cool-season grasses can be plant mutualistic, improving plant traits such as drought tolerance and herbivore resistance (Saikkonen et al 1998, 2013). The latter trait results from production of several alkaloids such as lolitrem B and ergopeptine alkaloids (e.g., ergovaline), which result in severe diseases in livestock, and peramine, lolines, ergopeptine alkaloids and epoxy-janthitrems, which are toxic and/or deterrent to insect pests (Bush et al 1997; Leuchtmann et al 2000; Panaccione et al 2014). Each grass-endophyte symbiosis produces a specific alkaloid profile in which the amount produced can be affected by biotic and abiotic conditions, but aphid herbivory has not been shown to affect alkaloid concentrations in a common garden study (Bultman et al 2004; Fuchs et al 2017b, 2017c; Helander et al 2016)

Methods

Results

Conclusion