Population biology of entomopathogenic nematodes: Concepts, issues, and models

The effect of soil moisture on entomopathogenic nematode virulence was examined in the laboratory. Objectives were to determine the virulence of several species and isolates of entomopathogenic nematodes at various soil moisture contents and temperatures, and after fluctuations in soil moisture. Studies included up to five isolates of entomopathogenic nematodes: Heterorhabditis bacteriophora Poinar (Oswego and Tuscarora strains), Steinernema glaseri (Steiner) (NC1 strain), S. feltiae (Filipjev) (Biosys 369 strain), and S. carpocapsae (Weiser) (NY001 strain). Nematodes were applied to sandy loam soils ranging in soil moisture content from below the permanent wilting point of plants to near saturation. In all experiments, a rainfall or irrigation event was simulated by adding water to rehydrate soils to high moisture levels (near saturation). Nematode virulence was evaluated periodically by measuring insect mortality in Galleria mellonella (L.) larval bioassays, before and after rehydration. Nematode virulence increased with soil moisture content for all species and isolates tested. Our studies demonstrated that the virulence of entomopathogenic nematodes in low moisture conditions could be restored by rehydrating the soil. Insect mortality was generally low in low-moisture, nematode-infested soils before rehydration, but increased to high levels posthydration. Moisture effects were evident from the onset of each experiment, whereas the effect of soil temperature on nematode-induced insect mortality was delayed and nonsignificant until 14 wk after the initiation of the third experiment.

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Soil Moisture Effects on Entomopathogenic Nematodes

The soil as a reservoir for natural enemies of pest insects and mites with emphasis on fungi and nematodes

Natural entomopathogenic nematode (EPN) populations were surveyed in La Rioja (Northern Spain) during two consecutive years (2003–2005) to study their diversity, occurrence, and life characteristics under different agricultural management representing natural areas and perennial and annual crops from organic and conventional systems. Native EPN species and strains were identified using morphological and molecular characteristics. Virulence, infection cycle length and reproductive potential were assessed using Galleria mellonella larvae. The EPN occurrence was evaluated through abundance, recovery frequency, larval mortality percentage and EPN population density. EPNs were also related to selected soil physical and chemical variables as well as to some soil pollutants such as heavy metals and organochlorine pesticide residues. Only two steinernematids species were identified: Steinernema feltiae was observed throughout all seasons from natural and agricultural areas and Steinernema carpocapsae in summer and autumn of 2004 from perennial crops only. The virulence of native strains was lower than other previously isolated Spanish strain from natural areas or crop field edges. EPN abundance and recovery frequency indicated that habitat type might influence EPNs occurrence stronger than seasonality with the intensity of agricultural management inversely affecting their distribution. Moreover, clay, P 2 O 5 , Zn, Cu and hexachlorobenzene contents negatively correlating with EPN population density. We consider that agricultural management should be taken into account if EPNs are going to be used as biological control agents.

Diversity, occurrence, and life characteristics of natural entomopathogenic nematode populations from La Rioja (Northern Spain) under different agricultural management and their relationships with soil factors

Entomopathogenic nematodes (EPN) are ubiquitous and generalized consumers of insects in soil food webs, occurring widely in natural and agricultural ecosystems on six continents. Augmentative releases of EPN have been used to enhance biological control of pests in agroecosystems. Pest managers strive to achieve a trophic cascade whereby natural-enemy effects permeate down through the food web to suppress host herbivores and increase crop production. Although trophic cascades have been studied in diverse aboveground arthropod-based systems, they are infrequently investigated in soil systems. Moreover, no overall quantitative assessment of the effectiveness of EPN in suppressing hosts with cascading benefits to plants has been made. Toward synthesizing the available but limited information on EPN and their ability to suppress prey and affect plant yield, we surveyed the literature and performed a meta-analysis of 35 published studies. Our analysis found that effect sizes for arthropod hosts as a result of EPN addition were consistently negative and indirect effects on plants were consistently positive. Results held across several different host metrics (abundance, fecundity and survival) and across measures of plant performance (biomass, growth, yield and survival). Moreover, the relationship between plant and host effect sizes was strikingly and significantly negative. That is, the positive impact on plant responses generally increased as the negative effect of EPN on hosts intensified, providing strong support for the mechanism of trophic cascades. We also review the ways in which EPN might interact antagonistically with each other and other predators and pathogens to adversely affect host suppression and dampen trophic cascades. We conclude that the food web implications of multiple-enemy interactions involving EPN are little studied, but, as management techniques that promote the long-term persistence of EPN are improved, antagonistic interactions are more likely to arise. We hope that the likely occurrence of antagonistic interactions in soil food webs should stimulate researchers to conduct field experiments explicitly designed to examine multiple-enemy interactions involving EPN and their cascading effects to hosts and plants.

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Potential for Entomopathogenic Nematodes in Biological Control: A Meta-Analytical Synthesis and Insights from Trophic Cascade Theory

The survival of Heterorhabditis bacteriophora Oswego Poinar, Steinernema carpocapsae NY001 Weiser, and S. glaseri NC1 Steiner varied in relation to the bulk density of a sandy loam soil. Survival of H. bacteriophora decreased linearly with time (4–70 d) and quadratically with increasing bulk density, whereas S. glaseri survival decreased linearly with time, but increased quadratically with increasing bulk density. Survival of S. carpocapsae decreased quadratically with time, but was unaffected by bulk density. H. bacteriophora and S. glaseri infected larvae of the greater wax moth, Galleria mellonella (L.) for up to 10 wk after soil inoculation, and the incidence of infection showed no significant variation in relation to bulk density or time. In contrast, infection rate by S. carpocapsae increased with bulk density and decreased with time. The combined effects of soil texture and bulk density on movement these of nematode species generally decreased as the bulk density of 3 soil textures increased. However, the degree to which soils of high bulk density reduced movement differed among species and soil textures: H. bacteriophora was the least restricted; whereas, S. carpocapsae was the most restricted. All 3 species moved significantly more in sandy loam, than in loam or silty clay loam. Although movement was reduced at relatively high bulk densities, survival of the 3 nematode species was high. Rates of movement and infection by the nematodes were strongly correlated with the amount of soil pore space having dimensions similar to or greater than the diameters of the nematodes. In a sandy loam soil, H. bacteriophora moved at least 18 cm within 4 d of soil inoculation across all bulk densities tested, whereas S. carpocapsae moved only 9 cm at the 3 lower densities and <9 cm at the highest soil density. S. glaseri showed intermediate levels of movement.

Carlos Portillo-Aguilar

Papers

Entomopathogenic Nematode (Rhabditida: Heterorhabditidae and Steinernematidae) Response to Soil Texture and Bulk Density