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Molecular and ecological approaches to study soil food webs for enhancing biological control of insect pests and monitoring disturbances

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Entomopathogenic nematode food webs in an ancient, mining pollution gradient in Spain
Publication . Campos-Herrera, Raquel; Rodríguez Martín, José Antonio; Escuer, Miguel; García-González, María Teresa; Duncan, Larry W.; Gutíerrez, Carmen
Mining activities pollute the environment with by-products that cause unpredictable impacts in surrounding areas. Cartagena-La Union mine (Southeastern-Spain) was active for >2500 years. Despite its closure in 1991, high concentrations of metals and waste residues remain in this area. A previous study using nematodes suggested that high lead content diminished soil biodiversity. However, the effects of mine pollution on specific ecosystem services remain unknown. Entomopathogenic nematodes (EPN) play a major role in the biocontrol of insect pests. Because EPNs are widespread throughout the world, we speculated that EPNs would be present in the mined areas, but at increased incidence with distance from the pollution focus. We predicted that the natural enemies of nematodes would follow a similar spatial pattern. We used qPCR techniques to measure abundance of five EPN species, five nematophagous fungi species, two bacterial ectoparasites of EPNs and one group of free-living nematodes that compete for the insect-cadaver. The study comprised 193 soil samples taken from mining sites, natural areas and agricultural fields. The highest concentrations of iron and zinc were detected in the mined area as was previously described for lead, cadmium and nickel. Molecular tools detected very low numbers of EPNs in samples found to be negative by insect-baiting, demonstrating the importance of the approach. EPNs were detected at low numbers in 13% of the localities, without relationship to heavy-metal concentrations. Only Acrobeloides-group nematodes were inversely related to the pollution gradient. Factors associated with agricultural areas explained 98.35% of the biotic variability, including EPN association with agricultural areas. Our study suggests that EPNs have adapted to polluted habitats that might support arthropod hosts. By contrast, the relationship between abundance of Acrobeloides-group and heavy-metal levels, revealed these taxa as especially well suited bio-indicators of soil mining pollution. (C) 2016 Elsevier B.V. All rights reserved.
Entomopathogenic nematode food web assemblages in Florida natural areas
Publication . Campos-Herrera, Raquel; El-Borai, Fahiem E.; Rodriguez Martin, Jose Antonio; Duncan, Larry W.
In Florida citrus orchards, root weevil herbivory is tempered by four native entomopathogenic nematode (EPN) species whose spatial patterns are associated with soil properties related to water content. Manipulation of these variables could affect the efficacy and conservation of native EPNs for control of root weevils. The diversity of EPNs in non-agricultural areas it is unknown. We speculated that, whereas different species composition may occur in some natural areas by virtue of non-citrus niche adaptations, similar soil properties and environmental conditions should shape the communities in both systems. We characterized EPN food web assemblages during summer-fall 2011 in 91 sites comprising five naturally occurring botanical groups (oak, pine, palm and palmetto, mixed and other) and two ecoregions (central ridge and flatwoods). We used species-specific qPCR probes for 13 EPN species, two species of Paeni-bacillus (ectoparasitically associated with EPNs), seven species of nematophagous fungi (NF), an oomycete pathogen of citrus (Phytophthora nicotianae) and free-living bactivorous nematodes (Acrobeloides-group), some of which compete with EPN5. Seven EPN species were detected at frequencies about 60% of that reported from citrus. Additional species detected were Steinernema glaseri and Heterorhabditis floridensis, whereas citrus inhabitants Steinernema riobrave and Steinernema scapterisci, were absent, suggesting a possible niche adaptation. EPN recovery frequency did not differ between two ecoregions, except for Heterorhabditis indica which was detected at more sites in the flatwoods than on the central ridge and Heterorhabditis zealandica exhibiting the opposite pattern for detection frequency and abundance. Nor did the botanical habitats much affect EPN5 other than H. indica which occurred with greatest frequency and abundance in abandoned citrus orchards. Soil moisture appeared to be important in modulating these subterranean communities, with groundwater depth, organic matter, soil clay and pH explaining significant EPN variability between sites. There was little evidence that regional or habitat differences in natural enemy occurrence affected the EPN spatial patterns. Indeed, numerous significant direct associations between species of nematodes and nematophagous fungi suggested that the local abundance of the r-selected EPN and Acrobeloides-group nematodes is an important resource modulating population growth of these trapping and endoparasitic fungi. Congruent relationships between EPN spatial patterns and soil properties that affect water potential in both natural areas and citrus orchards suggests that soil moisture drives these patterns and modulates the regulation of root herbivores by EPNs in this part of the Florida peninsula. Consequently, management of soil moisture by manipulating these properties has the greatest potential to enhance and conserve EPN services. (C) 2015 Elsevier Ltd. All rights reserved.
Analyzing spatial patterns linked to the ecology of herbivores and their natural enemies in the soil
Publication . Campos-Herrera, Raquel; Ali, J. G.; Diaz, B. M.; Duncan, L. W.
Modern agricultural systems can benefit from the application of concepts and models from applied ecology. When understood, multitrophic interactions among plants, pests, diseases and their natural enemies can be exploited to increase crop production and reduce undesirable environmental impacts. Although the understanding of subterranean ecology is rudimentary compared to the perspective aboveground, technologies today vastly reduce traditional obstacles to studying cryptic communities. Here we emphasize advantages to integrating as much as possible the use of these methods in order to leverage the information gained from studying communities of soil organisms. PCR-based approaches to identify and quantify species (real time qPCR and next generation sequencing) greatly expand the ability to investigate food web interactions because there is less need for wide taxonomic expertise within research programs. Improved methods to capture and measure volatiles in the soil atmosphere in situ make it possible to detect and study chemical cues that are critical to communication across trophic levels. The application of SADIE to directly assess rather than infer spatial patterns in belowground agroecosystems has improved the ability to characterize relationships between organisms in space and time. We review selected methodology and use of these tools and describe some of the ways they were integrated to study soil food webs in Florida citrus orchards with the goal of developing new biocontrol approaches.
Spatial relationships between entomopathogenic nematodes and nematophagous fungi in Florida citrus orchards
Publication . Pathak, Ekta; Campos-Herrera, Raquel; El-Borai, Fahiem E.; Duncan, Larry W.
Relationships between entomopathogenic nematodes (EPNs), nematophagous fungi (NF) and soil physical and chemical properties were studied in a survey of 53 citrus orchards in central ridge and flatwoods ecoregions of Florida. Seven species of NF associated with nematodes were quantified directly using a real time qPCR assay. All nematophagous fungi studied except Arthrobotrys musiformis and Hirsutella rhossiliensis were frequently detected (24-56%) in both regions. Paecilomyces lilacinus and Gamsylella gephyropagum were encountered more frequently in the flatwoods (P = 0.03) and on the ridge (P = 0.02), respectively. Redundancy analysis revealed seven abiotic and biotic factors as significantly related to the NF occurrence. Multiple regression of fungi on these variables explained 78%, 66%, 48%, 36%, 23% and 4% of the variation in Catenaria sp., A. musiformis, A dactyloides, P. lilacinus, A. oligospora and G. gepharopagum, respectively. When the data from citrus were pooled with those reported previously from natural areas and subjected to principle component analysis, the first two principle components explained 43% of the variation in NF communities. The surveys (citrus vs natural areas) were discriminated by PC2 (P < 0.001) and the ecoregion by PC1 (P < 0.002), and all but one NF species were related (P < 0.01) to one or both components. NF communities tended to have more species and greater diversity in the flatwoods, where EPN richness and diversity were the least. However, the strength of associations between individual EPN and NF species as measured by SADIE reflected the associations between each species and ground water depth, suggesting that ecoregion preferences affected the species associations. Within each ecoregion, significant relationships between the individual NF and EPN species measured by stepwise regression tended to be positive. The results did not support the hypothesis that NF modulate the spatial patterns of EPN species between or within these two ecoregions. (C) 2017 Elsevier Inc. All rights reserved.

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European Commission

Funding programme

FP7

Funding Award Number

252980

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