Browsing by Author "Campos-Herrera, Raquel"
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- Analyzing spatial patterns linked to the ecology of herbivores and their natural enemies in the soilPublication . 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.
- 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.
- Cutaneous excreta of the earthworm Eisenia fetida (Haplotaxida: Lumbricidae) might hinder the biological control performance of entomopathogenic nematodesPublication . Chelkha, Maryam; Blanco-Perez, Ruben; Bueno-Pallero, Francisco Angel; Amghar, Souad; El Harti, Abdellatif; Campos-Herrera, RaquelEarthworms enhance soil structure, the decomposition of organic matter and the dissemination of beneficial soil organisms such as the entomopathogenic nematodes (EPNs). Nevertheless, the effects of earthworm feeding behavior or cutaneous excreta (CEx) on the performance of EPNs as biological control agents is poorly understood. We hypothesized that the presence of earthworms or their excreta reduces EPN fitness, measured in terms of pathogenicity and reproductive success. In laboratory experiments we first evaluated the killing ability of EPNs against Galleria mellonella (Lepidoptera: Pyralidae) larvae when inoculated in autoclaved soil alone or in combination with the earthworm Eisenia fetida (Haplotaxida: Lumbricidae) or their excreta. We also evaluated EPN efficacy and reproduction when exposed to CEx derived from E. fetida at two nematode concentrations (1.5 and 10 IJs/cm(2)). For both experiments, we tested four steinernematids (Steinernema carpocapsae, S. feltiae, S. glaseri, and S. khuongi) and two heterorhabditids (Heterorhabditis bacteriophora and H. zealandica). The presence of earthworms or their excreta resulted in significant reduction of the larval mortality caused by some of the steinernematids at certain timings depending of the species (P < 0.015), while heterorhabditids were mainly not affected. Both S. feltiae and H. zealandica progeny production was significantly reduced (P < 0.01) when exposed to CEx. Hence, we showed that the presence of CEx might alter the biocontrol performance of certain EPN species, especially steinernematids bigger than 600 mu m in size (S. feltiae, S. glaseri, and S. khoungi), by affecting their pathogenicity and reproductive success.
- Earthworms and their cutaneous excreta can modify the virulence and reproductive capability of entomopathogenic nematodes and fungiPublication . Chelkha, Maryam; Blanco-Pérez, Rubén; Vicente-Díez, Ignacio; Bueno-Pallero, Francisco; Amghar, Souad; El Harti, Abdellatif; Campos-Herrera, RaquelEarthworms are ecological engineers that can contribute to the displacement of biological control agents such as the entomopathogenic nematodes (EPNs) and fungi (EPF). However, a previous study showed that the presence of cutaneous excreta (CEx) and feeding behavior of the earthworm species Eisenia fetida (Haplotaxida: Lumbricidae) compromise the biocontrol efficacy of certain EPN species by reducing, for example, their reproductive capability. Whether this phenomenon is a general pattern for the interaction of earthworms-entomopathogens is still unknown. We hypothesized that diverse earthworm species might differentially affect EPN and EPF infectivity and reproductive capability. Here we investigated the interaction of different earthworm species (Eisenia fetida, Lumbricus terrestris, and Perionyx excavatus) (Haplotaxida) and EPN species (Steinernema feltiae, S. riojaense, and Heterorhabditis bacteriophora) (Rhabditida) or EPF species (Beauveria bassiana and Metarhizium anisopliae) (Hypocreales), in two independent experiments. First, we evaluated the application of each entomopathogen combined with earthworms or their CEx in autoclaved soil. Hereafter, we studied the impact of the earthworms’ CEx on entomopathogens applied at two different concentrations in autoclaved sand. Overall, we found that the effect of earthworms on entomopathogens was species-specific. For example, E. fetida reduced the virulence of S. feltiae, resulted in neutral effects for S. riojaense, and increased H. bacteriophora virulence. However, the earthworm P. excavates increased the virulence of S. feltiae, reduced the activity of H. bacteriophora, at least at specific timings, while S. riojaense remained unaffected. Finally, none of the EPN species were affected by the presence of L. terrestris. Also, the exposure to earthworm CEx resulted in a positive, negative or neutral effect on the virulence and reproduction capability depending on the earthworm-EPN species interaction. Concerning EPF, the impact of earthworms was also differential among species. Thus, E. fetida was detrimental to M. anisopliae and B. bassiana after eight days post-exposure, whereas Lumbricus terrestris resulted only detrimental to B. bassiana. In addition, most of the CEx treatments of both earthworm species decreased B. bassiana virulence and growth. However, the EPF M. anisopliae was unaffected when exposed to L. terrestris CEx, while the exposure to E. fetida CEx produced contrasting results. We conclude that earthworms and their CEx can have positive, deleterious, or neutral impacts on entomopathogens that often coinhabit soils, and that we must consider the species specificity of these interactions for mutual uses in biological control programs. Additional studies are needed to verify these interactions under natural conditions.
- 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.
- 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.
- Entomopathogenic nematode food web assemblages in Florida natural areasPublication . 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.
- 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.