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- Scavenging behavior and interspecific competition decrease offspring fitness of the entomopathogenic nematode Steinernema feltiaePublication . PEREZ, RUBEN; Bueno-Pallero, Francisco Angel; Vicente-Diez, Ignacio; Santiago Marco-Mancebon, Vicente; Perez-Moreno, Ignacio; Campos-Herrera, RaquelEntomopathogenic nematodes (EPNs) are well-studied biocontrol agents of soilw-dwelling arthropod pests. The insecticidal efficiency of EPNs is modulated by food web dynamics. EPNs can reproduce in freeze-killed insect larvae, even in competition with free-living bacterivorous nematodes (FLBNs) in the genus Oscheius. The objective of this study was to assess the efficiency of EPNs as scavengers when competing with free-living saprophagous nematodes and fungi, and to determine the possible impact on subsequent EPN offspring fitness. Live and freeze-killed larvae of Galleria mellonella were used to evaluate the reproduction rate and progeny fitness of two EPN species, Heterorhabditis bacteriophora and Steinernema feltiae, applied individually or combined with the FLBN species Oscheius onirici or Pristionchus maupasi, or Aspergillus flavus, an opportunistic saprophytic fungus. We hypothesized that (1) EPN scavenging behaviors previously observed (for H. megidis and S. kraussei) apply to other EPN species, (2) infective juveniles (IJs) emerging from freeze-killed larvae will display reduced pathogenicity and reproduction, and (3) fitness reduction will be amplified by exposure to other organisms competing for the resources. The reproduction rate of S. feltiae was lower in freeze-killed larvae than in larvae infected and killed by the nematode, whereas H. bacteriophora failed to reproduce as a scavenger. The S. feltiae Fl IJs that emerged from freeze-killed larvae exhibited lower pathogenicity rates than Us resulting from entomopathogenic activity, and also lower reproductive rates if they experienced high FLBN competitive pressure during development. This study illustrates that scavenging is a suboptimal alternative pathway for EPNs, especially in the face of scavenger competition, even though it provides a means for some EPN species to complete their life-cycle.
- Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitatsPublication . Ali, Jared G.; Alborn, Hans T.; Campos-Herrera, Raquel; Kaplan, Fatma; Duncan, Larry W.; Rodriguez-Saona, Cesar; Koppenhöfer, Albrecht M.; Stelinski, Lukasz L.While the role of herbivore-induced volatiles in plant-herbivore-natural enemy interactions is well documented aboveground, new evidence suggests that belowground volatile emissions can protect plants by attracting entomopathogenic nematodes (EPNs). However, due to methodological limitations, no study has previously detected belowground herbivore-induced volatiles in the field or quantified their impact on attraction of diverse EPN species. Here we show how a belowground herbivore-induced volatile can enhance mortality of agriculturally significant root pests. First, in real time, we identified pregeijerene (1,5-dimethylcyclodeca-1,5,7-triene) from citrus roots 9-12 hours after initiation of larval Diaprepes abbreviatus feeding. This compound was also detected in the root zone of mature citrus trees in the field. Application of collected volatiles from weevil-damaged citrus roots attracted native EPNs and increased mortality of beetle larvae (D. abbreviatus) compared to controls in a citrus orchard. In addition, field applications of isolated pregeijerene caused similar results. Quantitative real-time PCR revealed that pregeijerene increased pest mortality by attracting four species of naturally occurring EPNs in the field. Finally, we tested the generality of this root-zone signal by application of pregeijerene in blueberry fields; mortality of larvae (Galleria mellonella and Anomala orientalis) again increased by attracting naturally occurring populations of an EPN. Thus, this specific belowground signal attracts natural enemies of widespread root pests in distinct agricultural systems and may have broad potential in biological control of root pests.
- Effects of cover crops on the overwintering success of entomopathogenic nematodes and their antagonistsPublication . Jaffuel, Geoffrey; Blanco-Pérez, Rubén; Büchi, Lucie; Mäder, Paul; Fließbach, Andreas; Charles, Raphaël; Degen, Thomas; Turlings, Ted C.J.; Campos-Herrera, RaquelConservation agriculture is arising as an alternative to conventional agriculture with the aim to have a reduced impact on the environment. This includes the use of cover crops to conserve soil quality by limiting soil erosion, adding organic matter, and enhancing soil nutrient content, as well as water availability, which are all factors that can greatly influence the presence of soil organisms. In the current study, we investigated whether winter cover crops can enhance the persistence of entomopathogenic nematodes (EPN) over the winter season. In a first trial we augmented EPN populations in plots without (bared) and with the cover crops, pea (Pisum sativum) or mustard (Brassica juncea). In late autumn, individual mini-plots in each of the three treatments were supplemented with infective juveniles (IJs) of either Heterorhabditis bacteriophora or Steinernema feltiae. In a second trial we studied naturally occurring EPN in plots without (bared) and with the cover crop pea (Pisum sativum) followed by planting of winter wheat. To identify and quantify EPN, we analyzed soil samples using quantitative real time PCR (qPCR) at three time points over the winter season. We also measured the activity of augmented EPN by baiting the soil with wax moth larvae, Galleria mellonella. In addition, we used the qPCR method to investigate the presence of nematophagous fungi (NF), free-living nematodes (FLN) and ectoparasitic bacteria, all of which can interfere with EPN performance. Numbers of naturally occurring EPN in the investigated fields were very low (< 1 EPN per 100 g of soil). The cover crops only had a significant positive effect on the numbers of augmented S. feltiae found in early winter. No striking effect was found for H. bacteriophora. Yet, augmentation was found to enhance the insect-suppressiveness of the soil, as the recorded EPN infectivity after the winter was slightly higher than what was observed in autumn, one month after application. The numbers of FLN, which compete for insect cadavers, was higher in spring than in early winter. These FLN and other antagonists may be important in reducing EPN numbers. In conclusion, the effect of cover crops on EPN persistence was only evident during early-winter and was only significant in the plots augmented with S. feltiae. Moreover, we found that higher numbers of EPN in agricultural soils do not necessarily translate into high infectivity, which is the key factor determining their effectiveness in controlling soil pests.
- Combined field inoculations of pseudomonas bacteria, arbuscular mycorrhizal fungi, and entomopathogenic nematodes and their effects on wheat performancePublication . Imperiali, Nicola; Chiriboga, Xavier; Schlaeppi, Klaus; Fesselet, Marie; Villacres, Daniela; Jaffuel, Geoffrey; Bender, S. Franz; Dennert, Francesca; Blanco-Perez, Ruben; van der Heijden, Marcel G. A.; Maurhofer, Monika; Mascher, Fabio; Turlings, Ted C. J.; Keel, Christoph J.; Campos-Herrera, RaquelIn agricultural ecosystems, pest insects, pathogens, and reduced soil fertility pose major challenges to crop productivity and are responsible for significant yield losses worldwide. Management of belowground pests and diseases remains particularly challenging due to the complex nature of the soil and the limited reach of conventional agrochemicals. Boosting the presence of beneficial rhizosphere organisms is a potentially sustainable alternative and may help to optimize crop health and productivity. Field application of single beneficial soil organisms has shown satisfactory results under optimal conditions. This might be further enhanced by combining multiple beneficial soil organisms, but this remains poorly investigated. Here, we inoculated wheat plots with combinations of three beneficial soil organisms that have different rhizosphere functions and studied their effects on crop performance. Plant beneficial Pseudomonas bacteria, arbuscular mycorrhizal fungi (AMF), and entomopathogenic nematodes (EPN), were inoculated individually or in combinations at seeding, and their effects on plant performance were evaluated throughout the season. We used traditional and molecular identification tools to monitor their persistence over the cropping season in augmented and control treatments, and to estimate the possible displacement of native populations. In three separate trials, beneficial soil organisms were successfully introduced into the native populations and readily survived the field conditions. Various Pseudornonas, mycorrhiza, and nematode treatments improved plant health and productivity, while their combinations provided no significant additive or synergistic benefits compared to when applied alone. EPN application temporarily displaced some of the native EPN, but had no significant long-term effect on the associated food web. The strongest positive effect on wheat survival was observed for Pseudomonas and AMF during a season with heavy natural infestation by the frit fly, Oscinella frit, a major pest of cereals. Hence, beneficial impacts differed between the beneficial soil organisms and were most evident for plants under biotic stress. Overall, our findings indicate that in wheat production under the test conditions the three beneficial soil organisms can establish nicely and are compatible, but their combined application provides no additional benefits. Further studies are required, also in other cropping systems, to fine-tune the functional interactions among beneficial soil organisms, crops, and the environment.
- Effect of soil properties, heavy metals and emerging contaminants in the soil nematodes diversityPublication . Gutierrez, Carmen; Fernandez, Carlos; Escuer, Miguel; Campos-Herrera, Raquel; Beltran Rodriguez, Ma Eulalia; Carbonell, Gregoria; Rodriguez Martin, Jose AntonioAmong soil organisms, nematodes are seen as the most promising candidates for bioindications of soil health. We hypothesized that the soil nematode community structure would differ in three land use areas (agricultural, forest and industrial soils), be modulated by soil parameters (N, P, K, pH, SOM, CaCO3, granulometric fraction, etc.), and strongly affected by high levels of heavy metals (Cd, Pb, Zn, Cr, Ni, Cu, and Hg) and emerging contaminants (pharmaceuticals and personal care products, PPCPs). Although these pollutants did not significantly affect the total number of free-living nematodes, diversity and structure community indices vastly altered. Our data showed that whereas nematodes with r-strategy were tolerant, genera with k-strategy were negatively affected by the selected pollutants. These effects diminished in soils with high levels of heavy metals given their adaptation to the historical pollution in this area, but not to emerging pollutants like PPCPs. (C) 2016 Elsevier Ltd. All rights reserved.
- The abundance, diversity, and metabolic footprint of soil nematodes is highest in high elevation alpine grasslandsPublication . Kergunteuil, Alan; Campos-Herrera, Raquel; Sánchez-Moreno, Sara; Vittoz, Pascal; Rasmann, SergioNematodes are key components of soil biodiversity and represent valuable bio-indicators of soil food webs. Numerous community indices have been developed in order to track variations in nematode-mediate soil ecosystem processes, but their use is mainly restricted to anthropogenic stresses. In this study, we propose to expand the use of nematodes' derived ecological indices in order to shed light on variations of soil food webs in natural systems distributed along elevation gradients. For this purpose, we aimed at determining how elevation affects the community structure and the trophic diversity by studying the abundance, the composition and the functional diversity of nematode communities.
- Entomopathogenic nematode food webs in an ancient, mining pollution gradient in SpainPublication . Campos-Herrera, Raquel; Rodríguez Martín, José Antonio; Escuer, Miguel; García-González, María Teresa; Duncan, Larry W.; Gutíerrez, CarmenMining 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.
- Prevalence and activity of entomopathogenic nematodes and their antagonists in soils that are subject to different agricultural practicesPublication . Jaffuel, Geoffrey; Mader, Paul; Blanco-Perez, Ruben; Chiriboga, Xavier; Fliessbach, Andreas; Turlings, Ted C. J.; Campos-Herrera, RaquelAgricultural management practices can modify soil properties in ways that may disrupt the abundance and activity of beneficial organisms in the soil. We assessed the impact of different soil management practices on entomopathogenic nematodes (EPN), which have great potential as biological control agents against root-feeding insects. Soils were sampled during spring and autumn 2013 in all 96 plots of a long-term Swiss field trial (DOK experiment). By combining a traditional insect-baiting technique and real-time qPCR analyses, we identified and quantified over 20 soil-dwelling species (or genera). This allowed us to investigate how communities of natural EPN populations and their associated natural enemies and competitors are affected by (i) three crop types (wheat, maize and grass-clover ley) and (ii) farming systems, i.e. conventional, organic and biodynamic, which differed in fertilization, and pesticide use. We also determined the effects on soils' microbial biomass in terms of carbon (C-mic) and nitrogen (N-mic) and applied spatial distribution analysis (SADIE) to uncover patterns of aggregations and associations of the study organisms. Although manure based farming systems increased microbial biomass, the systems did not influence the presence of EPN or their antagonists. EPN was more abundant in winter-wheat plots than in maize and grass-clover ley plots. Overall, very low numbers of EPN were recorded, implying that their natural presence would not be sufficient to have a satisfactory suppressive effect on root-feeding pests and the application of EPN would therefore be an appropriate measure to protect yields in case of root pest outbreaks. (C) 2016 Elsevier B.V. All rights reserved.
- Reproductive efficiency of entomopathogenic nematodes as scavengers. Are they able to fight for insect’s cadavers?Publication . Blanco-Pérez, Rubén; Bueno-Pallero, Francisco Ángel; Neto, Luis; Campos-Herrera, RaquelEntomopathogenic nematodes (EPNs) and their bacterial partners are well-studied insect pathogens, and their persistence in soils is one of the key parameters for successful use as biological control agents in agroecosystems. Free-living bacteriophagous nematodes (FLBNs) in the genus Oscheius, often found in soils, can interfere in EPN reproduction when exposed to live insect larvae. Both groups of nematodes can act as facultative scavengers as a survival strategy. Our hypothesis was that EPNs will reproduce in insect cadavers under FLBN presence, but their reproductive capacity will be severely limited when competing with other scavengers for the same niche. We explored the outcome of EPN - Oscheius interaction by using freeze-killed larvae of Galleria mellonella. The differential reproduction ability of two EPN species (Steinernema kraussei and Heterorhabditis megidis), single applied or combined with two FLBNs (Oscheius onirici or Oscheius tipulae), was evaluated under two different infective juvenile (IJ) pressure: low (3IJs/host) and high (20IJs/host). EPNs were able to reproduce in insect cadavers even in the presence of potential scavenger competitors, although EPN progeny was lower than that recorded in live larvae. Hence, when a highly susceptible host is available, exploiting cadavers by EPN might limit the adaptive advantage conferred by the bacteria partner, and might result in an important trade-off on long-term persistence. Contrary to our hypothesis, for most of the combinations, there were not evidences of competitive relationship between both groups of nematodes in freeze-killed larvae, probably because their interactions are subject to interference by the microbial growth inside the dead host. Indeed, evidences of possible beneficial effect of FLBN presence were observed in certain EPN-FLBN treatments compared with single EPN exposure, highlighting the species-specific and context dependency of these multitrophic interactions occurring in the soil.
- Vegetation drives assemblages of entomopathogenic nematodes and other soil organisms: evidence from the Algarve, PortugalPublication . Campos-Herrera, Raquel; Blanco-Pérez, Rubén; Bueno-Pallero, Francisco Ángel; Duarte, Amílcar; Nolasco, Gustavo; Sommer, Ralf J.; Rodríguez Martín, José AntonioEntomopathogenic 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 fi rst 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.