Vegetation drives assemblages of entomopathogenic nematodes and other soil organisms: Evidence from the Algarve, Portugal

Abstract

Entomopathogenic nematodes (EPNs) are widely distributed in soils throughout the world. Their activity as biological control agents is modulated by abiotic and biotic factors (e.g. soil type, climatic fluctuation and natural enemies). We sought to identify soil properties in a Mediterranean region, which might be managed to enhance biological control agents’ services provided by EPNs. We hypothesized that responses of EPN soil food web assemblages to abiotic factors in such a Mediterranean region would be consistent with previous observations in other biomes in subtropical and temperate regions, in which pH and variables related to water content were main drivers of such association. We also expected that EPN abundance and species composition would differ between stable botanical habitats (citrus groves, palmetto areas, oaks and pines), with EPNs and associated organisms favoured in cultivated sites (citrus). In spring 2016, 50 georeferenced localities, representing four botanical habitats and two soil-ecoregions (calcareous versus non-calcareous), were surveyed. Using published and de novo real time qPCR tools, we evaluated the frequency and abundance of 10 EPN species and 13 organisms associated with EPNs: 6 nematophagous fungi (NF), 5 free-living nematodes (FLN), and 2 ectoparasitic bacteria. EPN activity was also assessed by traditional insect-baiting, allowing the evaluation of FLN-EPN mixed progeny. EPNs were detected by qPCR in 50% of localities, and strongly correlated with EPN activity. Steinernema feltiae was the dominant EPN species measured by both techniques (qPCR and insect-bait), being widespread in all Algarve, while Heterorhabditis bacteriophora was detected mainly in citrus groves. The species S. arenarium and H. indica were detected by qPCR for the first time in continental Portugal. The molecular analysis of insect cadaver progeny revealed novel FLN-EPN associations with Pristionchus maupasi and P. pacificus. EPN, FLN and NF abundance differed among botanical groups, with citrus groves supporting high numbers of all trophic guilds. Oaks also favoured EPNs. Similarly, calcareous soil-ecoregion supported higher NF, FLN and EPN abundance. Two abiotic variables (pH, and clay content) explained the community variation in multivariate analysis, consistent with key abiotic variables described for other subtropical and temperate regions. The results supported the hypothesis that cultivated perennial habitats favour EPNs and soil organisms that can limit EPN activity as biological control agents.