Effects of population-related variation in plant primary and secondary metabolites on aboveground and belowground multitrophic interactions.

Moniek Van Geem,Jeffrey A Harvey,Ciska E Raaijmakers,Rieta Gols

doi:10.1007/s00049-016-0222-0

Moniek Van Geem, Jeffrey A Harvey + Show 2 more

Open Access

https://doi.org/10.1007/s00049-016-0222-0

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Abstract

Insects feeding on aboveground and belowground tissues can influence each other through their shared plant and this is often mediated by changes in plant chemistry. We examined the effects of belowground root fly (Delia radicum) herbivory on the performance of an aboveground herbivore (Plutella xylostella) and its endoparasitoid wasp (Cotesia vestalis). Insects were reared on three populations of wild cabbage (Brassica oleracea) plants, exhibiting qualitative and quantitative differences in root and shoot defense chemistry, that had or had not been exposed to root herbivory. In addition, we measured primary (amino acids and sugars) and secondary [glucosinolate (GS)] chemistry in plants exposed to the various plant population-treatment combinations to determine to what extent plant chemistry could explain variation in insect performance variables using multivariate statistics. In general, insect performance was more strongly affected by plant population than by herbivory in the opposite compartment, suggesting that population-related differences in plant quality are larger than those induced by herbivory. Sugar profiles were similar in the three populations and concentrations only changed in damaged tissues. In addition to population-related differences, amino acid concentrations primarily changed locally in response to herbivory. Whether GS concentrations changed in response to herbivory (indole GS) or whether there were only population-related differences (aliphatic GS) depended on GS class. Poor correlations between performance and chemical attributes made biological interpretation of these results difficult. Moreover, trade-offs between life history traits suggest that factors other than food nutritional quality contribute to the expression of life history traits.

Highlights

Plant–insect interactions have long underpinned ecological and evolutionary theory covering vastly different scales, from gene expression to the levels of communities and ecosystems
We examined the effects of belowground root fly (Delia radicum) herbivory on the performance of an aboveground herbivore (Plutella xylostella) and its endoparasitoid wasp (Cotesia vestalis)
Survival and body mass of the root fly D. radicum was affected by plant population, but not by herbivory treatment, whereas development time was affected by herbivory treatment and not by the population on which the insects had been reared (Table 1)

Summary

Introduction

Plant–insect interactions have long underpinned ecological and evolutionary theory covering vastly different scales, from gene expression to the levels of communities and ecosystems (see Hairston et al 1960; Root 1973; Futuyma and Agrawal 2009). Organisms in the AG and BG compartments may indirectly interact with each other through changes in the quality and quantity of the shared plant that are mostly mediated by their feeding on plant tissues (Bardgett et al 1998; van der Putten et al 2001; Soler et al 2012) These biological interactions are to a large extent mediated by plant traits such as the production of phytochemicals. Plants produce primary metabolites such as amino acids and carbohydrates that are essential for growth, development and reproduction (Schoonhoven et al 2005) They produce secondary metabolites that play no apparent role in fundamental physiological processes and have been shown to function as a defense against plant antagonists such as pathogens and herbivores (Fraenkel 1959; Iason et al 2012)

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