Development of a negative plant–soil feedback in the expansion zone of the clonal grass Ammophila arenaria following root formation and nematode colonization

Abstract

Summary 1The feedback between individual plants and their soil communities is a major driver of plant community processes. We analyse the rate at which plant-soil feedback develops in the root zone of the clonal dune grass Ammophila arenaria . 2 Ammophila arenaria grows vigorously when it can form new roots in newly deposited windblown beach sand. The colonization zone is hypothesized to provide an enemy-free space, with root pathogens and parasites possibly contributing to degeneration of A. arenaria when deposition stops. 3 We quantified root biomass and plant parasitic nematode densities in new and 1-year-old root zones, as well as in degenerate stands, in the field at monthly intervals. Each month, we studied the biomass production of Ammophila seedlings in controlled conditions in sterilized and non-sterilized soil from the different sampling sites, with and without nematicides. 4 Colonization of newly deposited sand by the endoparasitic nematodes Heterodera arenaria and Pratylenchus spp. within 1 month of root formation coincided with a negative feedback in the bioassays. Nematicides counteracted growth reduction significantly, but their effectiveness decreased in soil samples collected later in the growing season. 5 In older layers, roots and nematodes were already present before the sampling started. Growth reduction in unsterilized sand was observed at all sampling events, but was not counteracted by nematicides. 6 In the field, root biomass of A. arenaria in the newly colonized sand increased throughout the growing season, despite the development of a negative plant-soil feedback. 7 We conclude that the development of negative plant-soil feedback in the root zone of A. arenaria closely follows the colonization of newly deposited sand by roots and then by the endoparasitic nematode species Heterodera arenaria . There seems to be a shift in organisms causing this feedback during the first growing season, but root biomass nevertheless increases. However, in older root layers and in the degenerate stand, ongoing negative plant-soil feedback may contribute to a gradual decrease in root biomass.

Plant ectoparasitic nematodes prefer roots without their microbial enemies

“…In this case, theoretically, plants could be actively defending the most valuable parts of their root system against ectoparasitic nematodes in a tri-trophic way. Tritrophic indirect defense is commonly known for aboveground plant defense, but such phenomena in soil have received limited attention (thus far focusing exclusively on entomopathogenic nematodes) (Rasmann et al 2005;van Tol et al 2001).…”

“…At each sampling point, 10 kg of soil was collected from the youngest root zone of A. arenaria (van der Putten et al 1988). The soil was sieved (0.5 cm mesh size) to remove plant parts and debris, and stored in plastic bags at 4°C until used (van der Stoel et al 2002).…”

“…when added two or three weeks in advance (de la Peña et al 2006). The plant can control the cyst nematode Heterodera arenaria (van der Stoel et al 2006) and microbial enemies are a major factor in suppressing the ectoparasitic nematode Tylenchorhynchus ventralis (Piśkiewicz et al 2007). Thus far, in the studies mentioned above and other papers on root feeders, very little attention has been given to nematode behavior in relation to their natural enemies.…”

“…They are able to strongly decrease the biomass of A. arenaria (de Rooij van der Goes 1995a), if not controlled by their microbial enemies (Piśkiewicz et al 2007). In the field T. ventralis usually does not reach population levels that can affect plant growth (van der Stoel et al 2002), but numbers vary locally (de Rooij van der Goes et al 1995b). In the present study, we examine if plant ectoparasitic nematodes T. ventralis are able to sense and avoid microbial communities that include their natural antagonists.…”

Range-expanding plant species and their belowground neighbours : digging into novel interactions

“…Because of the assumed negative effects of root-feeding nematodes on natural plant performance (van der Stoel, van der Putten & Duyts 2002;De Deyn et al 2003), it is important to examine whether plantnematode interactions change between original and new plant ranges. Theoretically, there are two possible causes of such changes in plant-nematode interactions ( Fig.…”