Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection

Abstract

Complex biotic interactions shape ecological communities of plants, herbivores and their natural enemies. In studies of multi-trophic interactions, the presence of small, invisible micro-organisms associated with plants and those of a fourth above-ground trophic level have often been neglected. Incorporating these neglected factors improves our understanding of the processes within a multi-trophic network. Here, we ask whether the presence of a fungal endosymbiont, which alters plant quality by producing herbivoretoxic substances, trickles up the food chain and affects the performance and host-selection behaviour of aphid secondary parasitoids. We simultaneously offered hosts from endophyte-free and endophyteinfected environments to secondary parasitoids. Older and more experienced parasitoid females discriminated against hosts from the endophyte-infected environment. Developing in lower quality hosts from the endophyte-infected environment reduced the lifespan of secondary parasitoids. This indicates that aphid secondary parasitoids can perceive the disadvantage for their developing offspring in parasitoids from the endophyte environment and can learn to discriminate against them. In the field, this discrimination ability may shift the success of primary parasitoids to endophyte-infected plants, which co-occur with endophyte-free plants. Ultimately, the control of aphids depends on complex interactions between primary and secondary parasitoids and their relative sensitivity to endophytic fungi.

Endophyte-mediated interactions between cauliflower, the herbivore Spodoptera litura, and the ectoparasitoid Bracon hebetor

“…Our results are in agreement with previous studies on parasitoids where mainly negative effects were recorded (Barker and Addison 1996;Bultman et al 1997Bultman et al , 2003de Sassi et al 2006). Similar detrimental effects of endophytes on the reproductive ability of the aphid parasitoid A. ervi and coccinellid predator have been demonstrated (Harri et al 2008;de Sassi et al 2006). This reduction in reproductive success could have been due to parasitoid exposure during larval development to the fungal toxin present in the host insect that weakened the parasitoid females, which laid fewer eggs with reduced viability.…”

“…The adverse effects of E+ plants on the longevity of female wasps subsequently resulted in reduced fecundity and egg hatchability. Our results are in agreement with previous studies on aphids where negative effects were found on endophyte-naive Aphidius ervi (Haliday) females (Harri et al 2008). Although E+ plants did not influence the parasitism rate of female wasps, they negatively affected their longevity and fecundity.…”

“…The capacity of endophytic fungi to repel insects, induce weight loss, growth and development reduction and increased mortality in insects has been correlated with toxin production by the fungi or by the plant due to interaction with the fungi (Clay 1988a, b;Azevedo et al 2000). The effect of such mycotoxins also moves up the food chain and adversely affects the development and reproductive potential of parasitoids (de Sassi et al 2006;Harri et al 2008).…”

“…Understanding of these multitrophic-level interactions is very important in explaining the success or failure of integration of plant resistance and biological control agents. Most of the studies on trophic interactions involving endophyte-infected plants, insect herbivores and their parasitoids have been conducted on grass endophytes (Bultman et al 2003;Harri et al 2008;Bixby-Brosi and Potter 2011). However, the relationship between fungal endophytes of tropical plants and their effect on insect herbivores and their parasitoids has not been previously much described.…”

Water availability alters the tri-trophic consequences of a plant-fungal symbiosis

“…In accordance with previous experimental results for other host grass species (reviewed by Clay 1996; Cheplick and Faeth 2009), we found that endophyte presence strongly reduced the density of aphids attacking the native grass Poa autumnalis. Endophyte-symbiotic plants had both lower densities of live aphids and lower densities of parasitized aphids, indicating a bottom-up, community-level response to endophyte symbiosis, consistent with previous work (Faeth and Bultman 2002;Finkes et al 2006;Härri et al 2008a;Rudgers and Clay 2008). For example, in a similar study on the introduced grass species, Lolium multiflorum, Omacini et al (2001) found a decline in secondary parasitism that led to a less complex arthropod community structure in the presence of an endophyte.…”