Root-Lesion Nematodes Suppress Cabbage Aphid Population Development by Reducing Aphid Daily Reproduction

W H G Hol,Ilse Mons,Ciska E Raaijmakers,Katrin M Meyer,Nicole M Van Dam

doi:10.3389/fpls.2016.00111

Abstract

Empirical studies have shown that belowground feeding herbivores can affect the performance of aboveground herbivores in different ways. Often the critical life-history parameters underlying the observed performance effects remain unexplored. In order to better understand the cause for the observed effects on aboveground herbivores, these ecological mechanisms must be better understood. In this study we combined empirical experiments with a modeling approach to analyze the effect of two root feeding endoparasitic nematodes with different feeding strategies on the population growth of the aboveground feeding specialist aphid Brevicoryne brassicae on Brassica nigra. The aim was to test whether emerging differences in life history characteristics (days until reproduction, daily reproduction) would be sufficient to explain observed differences in aphid population development on plants with and without two species of nematodes. Aphid numbers were lower on plants with Pratylenchus penetrans in comparison to aphid numbers on plants with Meloidogyne spp. A dedicated experiment showed that aphid daily reproduction was lower on plants with P. penetrans (3.08 offspring female–1 day–1) in comparison to both uninfested plants and plants with Meloidogyne spp. (3.50 offspring female–1 day–1). The species-specific reduction of aphid reproduction appeared independent of changes in amino acids, soluble sugars or the glucosinolate sinigrin in the phloem. An individual-based model revealed that relatively small differences in reproduction rate per female were sufficient to yield a similar difference in aphid populations as was found in the empirical experiments.

Highlights

Plants are the primary food source on earth for a wide range of aboveground and belowground organisms
Our results showed that the effect of nematodes on B. brassicae population depends on the nematode species; aphids populations developed more slowly on plants infested with the migratory endoparasitic nematode P. penetrans, but were not affected by the inoculation with the sedentary endoparasitic nematode M. incognita
Negative effects of Pratylenchus spp. on aphid numbers have been found before (Wurst and van der Putten, 2007), but the same applies to Meloidogyne spp. (Sell and KuoSell, 1990) and other sedentary endoparasitic nematodes (Kaplan et al, 2011; Hol et al, 2013) on a range of plant species and various aphids

Summary

Introduction

Plants are the primary food source on earth for a wide range of aboveground and belowground organisms. It has been shown that, depending on the feeding type and species of herbivore, different hormonal signaling pathways are activated upon damage by herbivores or pathogens. Cross talk between these pathways eventually will determine the nature of the defense response (Pieterse et al, 2012). Because of the specificity of the induced response to different species of herbivores, the direction of the interaction between aboveground and belowground herbivores strongly depends on the feeding habit of the herbivores involved (van Dam and Heil, 2011). For example, generally have a negative effect on their aboveground counterparts whereas the effects of root herbivores on sap-sucking shoot herbivores, such as aphids may be more diverse (Kaplan et al, 2008; Johnson et al, 2012)

Methods

Results

Conclusion