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Soil Agroecology: characterizing multi-trophic interactions to improve biocontrol of insect pests

RYC-2016-19939

•
Nombre agencia financiadora Agencia Estatal de Investigación
Acrónimo agencia financiadora AEI
Programa Programa Estatal de Promoción del Talento y su Empleabilidad en I+D+i
Subprograma Subprograma Estatal de Incorporación
Convocatoria Ramón y Cajal
Año convocatoria 2016
Unidad de gestión Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016
Centro beneficiario AGENCIA ESTATAL CONSEJO SUPERIOR DE INVESTIGACIONES CIENTIFICAS (CSIC)

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Artículo científico (JournalArticle). 2019

Ground cover management in a Mediterranean vineyard: Impact on insect abundance and diversity

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Sáenz-Romo, María Gloria
  • Veas-Bernal, A.
  • Martínez-García, Héctor
  • Campos-Herrera, Raquel
  • Ibáñez Pascual, Sergio
  • Martínez-Villar, Elena
  • Pérez-Moreno, I.
  • Marco Mancebón, Vicente
Sustainable agriculture requires the support of new tools for successful and low-impact management of pests and diseases at global and local scales. The implementation of cover crops is considered a promising alternative ecological structure for sustainable agriculture, because they provide refuge to natural enemies of pests. Specifically, we hypothesised that implementing cover crop vegetation in a vineyard can enhance populations of natural enemies as a measure to support conservation biological control. We analysed insect abundance and diversity on Vitis vinifera var. Tempranillo (clon RJ-26, rootstock “110-Richter”) in a Mediterranean vineyard located in La Rioja, Spain from spring to autumn 2016–2017. Two types of sampling systems (pitfall traps and vacuum sampling) were used in each of the three evaluated ground cover management approaches (n = 3): (i) tillage, (ii) spontaneous cover, and (iii) flower-driven cover. A total of 58 families that belonged to four functional subgroups of insects (predators, parasitoids, phytophagous insects, and pollinators) were found. Overall, differences among the three treatments were only detected for total abundance of insects collected in the ground traps, and the “spontaneous cover” treatment showed significantly higher predator richness and abundance. However, the higher Shannon–Wiener value was recorded for “flower-driven cover” at both the ground and canopy levels. In addition, the abundance of predators, parasitoids and phytophagous insects in the ground traps for both cover crop treatments was more than two times higher than that observed in “tillage” treatment. Several predator taxa, such as ants, ground beetles, earwigs, and vespoid wasps had significantly higher representation under spontaneous cover treatment. Moreover, for parasitoids, the “flower-driven cover” treatment revealed higher Hill numbers values (0D, 1D, and 2D) at the canopy level, although no significant differences were observed. These results indicate that vegetation cover could be used to promote beneficial entomofauna in v, This study was grant supported by the Ministry of Economy andCompetitiveness (AGL2014-53336R). MGSR and AVB were supported by a fellowship from the University of La Rioja (Spain) (FPI-UR 2015and 2018, respectively). RCH is currently supported by a Ramón y Cajalaward (RYC-2016-19939)., Peer reviewed




Artículo científico (JournalArticle). 2019

Molecular detection and quantification of slug parasitic nematodes from the soil and their hosts

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Jaffuel, Geoffrey
  • Puža, Vladimír
  • Hug, A.S.
  • Meuli, R.G.
  • Nermut, Jiří
  • Turlings, Ted C. J.
  • Desurmont, Gaylord A.
  • Campos-Herrera, Raquel
Terrestrial gastropod molluscs are widely distributed and are well known as pests of many types of plants that are notoriously difficult to control. Many species of nematodes are able to parasitize land snails and slugs, but few of them are lethal to their host. Species and/or populations of mollusc-parasitic nematodes (MPNs) that kill their hosts are promising for biological control purposes. The recent discovery of new nematode species of the genus Phasmarhabditis in Europe and the associations between Alloionema spp. and slugs are expanding the possibilities of using MPNs as control agents. However, very little is known about the distribution and ecology of these species. Using molecular techniques based on qPCR methods for quick identification and quantification of various species of MPN isolated directly from the soil or from infected hosts can assist in providing information on their presence and persistence, as well as the composition of natural assemblages. Here, we developed new primers and probes for five species of the genus Phasmarhabditis and one species of the genus Alloionema. We employed these novel molecular techniques and implemented a published molecular set to detect MPN presence in soil samples coming from natural and agricultural areas in Switzerland. We also developed a method that allows the detection and quantification of Phasmarhabditis hermaphrodita directly from the tissues of their slug host in a laboratory experiment. The new molecular approaches were optimized to a satisfactory limit of detection of the species, with only few cross-amplifications with closely related species in late cycles (>32). Using these tools, we detected MPNs in 7.5% of sampled sites, corresponding to forest areas (P. hermaphrodita and Alloionema appendiculatum) and wheat-oriented agricultural areas (Phasmarhabditis bohemica). Moreover, we confirmed that the method can be used to detect the presence of P. hermaphrodita inside slug hosts, with more detections in the susceptible slug Deroceras larvae compared to the resistant Arion vulgaris. These primers/probe sets provide a novel and quick tool to identify MPNs from soil samples and infected slugs without having to culture and retrieve all nematode life stages, as well as a new tool to unravel the ecology of nematode-slug complexes., This work was funded by the Swiss National Science Foundation: Grants NRP68 and SNSF Div. I-III, reference 166632. The Government of Spain supports RCH with a Ramón y Cajal contract award: RYC-2016-19939., Peer reviewed




Artículo científico (JournalArticle). 2019

Soil nematode abundance and functional group composition at a global scale

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Hoogen, Johan van den
  • Geisen, Stefan
  • Routh, Devin
  • Ferris, Howard
  • Traunspurger, Walter
  • Wardle, David A.
  • Goede, Ron G. M. de
  • Adams, Byron J.
  • Ahmad, Wasim
  • Andriuzzi, Walter S.
  • Bardgett, Richard D.
  • Bonkowski, Michael
  • Campos-Herrera, Raquel
  • Cares, Juvenil E.
  • Caruso, Tancredi
  • Brito Caixeta, Larissa de
  • Chen, Xiaoyun
  • Costa, Sofia R.
  • Creamer, Rachel
  • Cunha Castro, José Mauro da
  • Dam, Marie
  • Djigal, Djibril
  • Escuer, Miguel
  • Griffiths, Bryan S.
  • Gutiérrez, Carmen
  • Hohberg, Karin
  • Kalinkina, Daria
  • Kardol, Paul
  • Kergunteuil, Alan
  • Korthals, Gerard
  • Krashevska, Valentyna
  • Kudrin, Alexey A.
  • Li, Qi
  • Liang, Wenju
  • Magilton, Matthew
  • Marais, Mariette
  • Rodríguez Martín, José Antonio
  • Matveeva, Elizaveta
  • Mayad, El Hassan
  • Mulder, Christian
  • Mullin, Peter
  • Neilson, Roy
  • Nguyen, T. A. Duong
  • Nielsen, Uffe N.
  • Okada, Hiroaki
  • Palomares Rius, Juan E.
  • Pan, Kaiwen
  • Peneva, Vlada
  • Pellissier, Loïc
  • Pereira da Silva, Julio Carlos
  • Pitteloud, Camille
  • Powers, Thomas O.
  • Powers, Kirsten
  • Quist, Casper W.
  • Rasmann, Sergio
  • Sánchez-Moreno, Sara
  • Scheu, Stefan
  • Setälä, Heikki
  • Sushchuk, Anna
  • Tiunov, Alexei V.
  • Trap, Jean
  • Putten, Wim H. van der
  • Vestergård, Mette
  • Villenave, Cecile
  • Waeyenberge, Lieven
  • Wall, Diana H.
  • Wilschut, Rutger
  • Wright, Daniel G.
  • Yang, Jiue-in
  • Crowther, Thomas Ward
Soil organisms are a crucial part of the terrestrial biosphere. Despite their importance for ecosystem functioning, few
quantitative, spatially explicit models of the active belowground community currently exist. In particular, nematodes
are the most abundant animals on Earth, filling all trophic levels in the soil food web. Here we use 6,759 georeferenced
samples to generate a mechanistic understanding of the patterns of the global abundance of nematodes in the soil and the
composition of their functional groups. The resulting maps show that 4.4 ± 0.64 × 1020 nematodes (with a total biomass
of approximately 0.3 gigatonnes) inhabit surface soils across the world, with higher abundances in sub-Arctic regions
(38% of total) than in temperate (24%) or tropical (21%) regions. Regional variations in these global trends also provide
insights into local patterns of soil fertility and functioning. These high-resolution models provide the first steps towards
representing soil ecological processes in global biogeochemical models and will enable the prediction of elemental cycling
under current and future climate scenarios., This research was supported by a grant from DOB Ecology to T.W.C., a grant from the Netherlands Organization for Scientific Research (grant 016.Veni.181.078) to S.G., grants from NSF (OPP 1115245, 1341736, 0840979) to B.J.A., by a Ramon y Cajal fellow award (RYC-2016-19939) to R.C.H., a grant from UNEP & Global Environment Facility to J.E.C., a grant from NERC (NE/M017036/1) to T.C., a grant from FAPEMIG/FAPESP/VALE S.A.(CRA-RDP-00136-10) to L.B.C., through the strategic programme UID/BIA/04050/2013 (POCI-01-0145-FEDER-007569) awarded to S.R.C., a grant from CNPq PROTAX (562346/2010-4) to J.M.d.C.C., a grant from DFG (CRC990) to V.K. and S.S., a grant from the MSHE of Russia (AAAA-A17-117112850234-5) to A.A.K., grants from the Chinese Academy of Sciences (XDB15010402) and the National Natural Science Foundation of China (41877047) to Q.L., grants from the National Natural Science Foundation of China (31330011, 31170484) to W.L., grants from NERC (NE/M017036/1) to M.M., grants from the Spanish Ministry of Innovation (CGL2009-14686-C02-01/ 02, CGL2013-43675-P) to J.A.R.M., grants from NSF (DEB-0450537, DEB-1145440) to P.M., T.O.P. and K. Powers, grants from the German Academic Exchange Service (PKZ 91540366) and NAFOSTED (106.05 – 2017.330) to T.A.D.N., by an ARC Discovery project (DP150104199) to U.N.N., by the National Key Research and Development Program of China (2016YFC0502101) and the National Natural Science Foundation of China (31370632) to K. Pan, a grant from the Natural Environment Research Council (NERC) to D.G.W., a grant from BAPHIQ (106AS-9.5.1-BQ-B3) J.-i.Y. The James Hutton Institute receives financial support from the Scottish Government Rural and Environment Science and Analytical Services (RESAS) division. Investigations in northwest Russia were carried out under state order for IB KarRC RAS and are partially supported by the Russian Foundation for Basic Research (18-34-00849). We thank E. Clark and A. Orgiazzi for review of the manuscript; and R. Bouharroud, Z. Ferji, L. Jackson and E. Mzough for providing data., Peer reviewed




Artículo científico (JournalArticle). 2019

Protecting maize from rootworm damage with the combined application of arbuscular mycorrhizal fungi, Pseudomonas bacteria and entomopathogenic nematodes

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Jaffuel, Geoffrey
  • Imperiali, Nicola
  • Shelby, Kent
  • Campos-Herrera, Raquel
  • Geisert, Ryan
  • Maurhofer, M.
  • Loper, Joyce
  • Keel, Christoph
  • Turlings, Ted C. J.
  • Hibbard, B.E.
Diabrotica virgifera virgifera LeConte, the western corn rootworm (WCR), is the most destructive pest of maize in North America, and has recently spread across central Europe. Its subterranean larval stages are hard to reach with pesticides and it has evolved resistance to conventional management practices. The application of beneficial soil organisms is being considered as a sustainable and environmental friendly alternative. In a previous study, the combined application in wheat fields of arbuscular mycorrhizal fungi, entomopathogenic Pseudomonas bacteria, and entomopathogenic nematodes was found to promote growth and protection against a natural pest infestation, without negative cross effects. Because of the insect-killing capacity of the bacteria and nematodes, we hypothesized that the application of these organisms would have similar or even greater beneficial effects in WCR-infested maize fields. During three consecutive years (2015–2017), we conducted trials in Missouri (USA) in which we applied the three organisms, alone or in combinations, in plots that were artificially infested with WCR and in non-infested control plots. For two of the three trials, we found that in plots treated with entomopathogenic nematodes and/or entomopathogenic Pseudomonas bacteria, roots were less damaged than the roots of plants in control plots. During one year, WCR survival was significantly lower in plots treated with Pseudomonas than in control plots, and the surviving larvae that were recovered from these plots were lighter. The bacterial and nematodes treatments also enhanced yield, assessed as total grain weight, in one of the trials. The effects of the treatments varied considerable among the three years, but they were always positive for the plants., The project was funded by National Research Program 68 on the “Sustainable Use of Soil as a Resource” from the Swiss National Science Foundation (406840_143065 awarded to TT, 406840_143141 awarded to C.K. and M.M.). G.J. was supported by an assistantship from the University of Neuchâtel, NI was supported by an assistantship from the University of
Lausanne, and RCH is currently supported by the Ramón y Cajal program, Spanish Government (RYC-2016-19939)., Peer reviewed




Artículo científico (JournalArticle). 2019

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

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Campos-Herrera, Raquel
  • Blanco-Pérez, Rubén
  • Bueno-Pallero, Francisco Ángel
  • Duarte, Amílcar
  • Nolasco, Gustavo
  • Sommer, Ralf J.
  • Rodríguez Martín, José Antonio
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., This work was supported by the Government of Portugal, thanks to the “Starting Grant” associate funds (grant number IF/00552/2014/CP1234/CT0007). RCH was awarded with an Investigator Programme contract (grant number IF/00552/2014), and currently is supported by the Ramón y Cajal Programme (Spanish Government, RYC-2016-19939). RBP and FBP were financed by the scientific assistantship fellowships associated to the grant IF/00552/2014/CP1234/CT0007 (two BI calls, UAlg-2016/004 and UAlg-2016/003, respectively)., Peer reviewed




Artículo científico (JournalArticle). 2020

Effects of ground cover management on insect rpedators and pests in a Mediterranean vineyard

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Sáenz-Romo, María Gloria
  • Veas-Bernal, A.
  • Martínez-García, Héctor
  • Ibáñez Pascual, Sergio
  • Martínez-Villar, Elena
  • Campos-Herrera, Raquel
  • Pérez-Moreno, I.
  • Marco Mancebón, Vicente
Conservative techniques, such as ground cover management, could help promote viticulture sustainability, which is a goal of conservation biological control, by providing shelter and food sources for predatory insects. A field experiment was conducted in a Mediterranean vineyard to evaluate ground cover management impacts on predatory insect and potential grapevine pest abundance and diversity, both on the ground and in the grapevine canopy. Three different ground cover management techniques (tillage, spontaneous cover and flower-driven cover) were tested for two years (2016 and 2017). Overall, the ground cover management significantly affected the abundance of important epigeal predators, of which carabids, forficulids and staphylinids were the most captured. The carabid abundances under both the cover crop treatments were found to be approximately three times higher compared with that under the tillage treatment. In contrast, the canopy insect abundance in the vineyard was similar among the treatments for both the predators and the potential grapevine pest species. These results indicate that cover crop vegetation can be used in vineyards to enhance predatory insect abundance and may improve agroecosystem resilience, This research was funded by the Ministry of Economy and Competitiveness (AGL2014-53336R). M.G.S.-R. and A.V.-B. were supported by fellowships from the University of La Rioja (Spain) (FPI-UR 2015 and 2018, respectively). R.C.-H. is currently supported by a Ramón y Cajal award (RYC-2016-19939




Artículo científico (JournalArticle). 2020

Impact of vineyard ground cover management on the occurrence and activity of entomopathogenic nematodes and associated soil organisms

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Blanco-Pérez, Rubén
  • Sáenz-Romo, María Gloria
  • Vicente-Díez, Ignacio
  • Ibáñez Pascual, Sergio
  • Martínez-Villar, Elena
  • Pérez-Moreno, I.
  • Marco Mancebón, Vicente
  • Campos-Herrera, Raquel
Viticulture is a valuable sector worldwide with an extraordinary socio-economic impact in Spain. Numerous
pests and diseases threaten vineyards, and their management primarily relies on the use of conventional
agrochemicals. The current paradigm of sustainability pursues the implementation of ecologically sound strategies
in vineyard ecosystems. The use of cover crops is arising as an alternative with numerous benefits, including
favoring above-belowground biodiversity and the presence of beneficial soil organisms such as the
entomopathogenic nematodes (EPNs). We hypothesized that the use of specific cover crops in vineyards might
enhance the natural occurrence and activity of EPNs by modulating the assemblage with associated organisms.
We performed the experiments in an ongoing experimental vineyard (Vitis vinifera var Tempranillo, clon RJ-26,
rootstock ‘110-Richter’) located in Logroño (Spain), drove with different soil management systems (three replicates
each): conventional tillage practice and the cover crops (i) seeded with Bromus catharticus (Poaceae), (ii)
flower-driven, and (iii) spontaneous. We took four soil composite samples per plot (n = 48 per sampling time)
late spring and early autumn in two consecutive years (2017 and 2018). By using species-specific primers/probes
qPCR sets, we screened for the presence and abundance of eight EPNs species and 12 related soil organisms: six
nematophagous fungi, four free-living nematodes, and two ectoparasitic bacteria. Additionally, we assessed the
EPN activity by the traditional insect-bait method. Overall, we recorded higher EPN numbers or activity rates on
cover crops than on bare soils. However, some of the results were divergent among no-till treatments. We
observed not only higher EPN abundance and activity on spontaneous covers but lower numbers of antagonistic
organisms, particularly endoparasitic nematophagous fungi. Thus, according to our results, the use of spontaneous
covers could be the most promising strategy to support the conservation biological control service provided
by the naturally occurring EPN species in vineyards, plus with a low cost for the sector., This study was grant supported by the Ministry of Economy and Competitiveness,
Goverment of Spain (AGL2014-53336R). The pre-doctoral contracts
CAR-2018 (Department of Economic Development and Innovation of
the Government of La Rioja) and FPI-UR 2015 (University of La Rioja)
support RBP and MGSR, respectively. IVD awarded the ADER I+D+i
(2019) fellowship by the Rioja Agency of Economic Development (La
Rioja, Spain). The Government of Spain currently supports RCH with a
Ramón y Cajal, government of Spain contract award (RYC-2016-
19939)., Peer reviewed




Artículo científico (JournalArticle). 2020

Patterns of occurrence and activity of Entomopathogenic Fungi in the Algarve (Portugal) using different isolation methods

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Bueno-Pallero, Francisco Ángel
  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Rodríguez Martín, José Antonio
  • Dionísio, Lídia
  • Campos-Herrera, Raquel
Entomopathogenic fungi (EPF) are distributed in natural and agricultural soils
worldwide. To investigate EPF occurrence in different botanical habitats and soil-ecoregions, we
surveyed 50 georeferenced localities in the spring of 2016 across the Algarve region (South
Portugal). Additionally, we compared three EPF isolation methods: insect baiting in untreated or
pre-dried-soil and soil dilution plating on a selective medium. We hypothesized that forest habitats
(oak and pine semi-natural areas) and the acidic soil ecoregion may favor EPF occurrence. Overall,
EPF species were present in 68% of sites, widely distributed throughout the Algarve. The use of
selective media resulted in higher recovery of EPF than did either soil-baiting method. Contrary to
our hypothesis, neither vegetation type nor ecoregion appeared to influence EPF occurrence.
Traditional and molecular methods confirmed the presence of five EPF species. Beauveria bassiana
(34% of sites), was the most frequently detected EPF, using pre-dried soil baiting and soil dilution
methods. However, baiting untreated soil recovered Fusarium solani more frequently (26% of sites),
demonstrating the utility of using multiple isolation methods. We also found Fusarium oxysporum,
Purpureocillium lilacinum and Metarhizium anisopliae in 14%, 8% and 2% of the sites, respectively.
Three abiotic variables (pH, soil organic matter and Mg) explained 96% of the variability of the
entomopathogen community (EPF and entomopathogenic nematodes) in a canonical
correspondence analysis, confirming the congruence of the soil properties that drive the assemblage
of both entomopathogens. This study expands the knowledge of EPF distribution in natural and
cultivated Mediterranean habitats., The Government of Portugal, thanks to the “Starting Grant” associate funds (Grant Number
IF/00552/2014/CP1234/CT0007), supported this work. R.C.-H. was awarded an Investigator Program contract
(Grant Number IF/00552/2014) and currently is supported by the Ramón y Cajal Program (Spanish Government,
RYC-2016-19939). R.B.-P. and F.A.B.-P. were financed by the scientific assistantship fellowships associated with
the grant IF/00552/2014/CP1234/CT0007 (BI calls UAlg-2016/004 and UAlg-2016/003, respectively). R.B.-P. is
currently supported by the Department of Economic Development and Innovation of the Government of La
Rioja (Spain) with a pre-doctoral contract (CAR-2018). I.V.-D. is currently supported by an ADER postgraduate
grant (Government of La Rioja, Spain), Peer reviewed




Artículo científico (JournalArticle). 2020

Activity of Steinernema colombiense in plant-based oils

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Castruita-Esparza, Gabriela
  • Bueno-Pallero, Francisco Ángel
  • Blanco-Pérez, Rubén
  • Dionísio, Lídia
  • Aquino-Bolaños, Teodulfo
  • Campos-Herrera, Raquel
Entomopathogenic nematodes (EPNs) are excellent biological control agents. Although traditionally EPN application targeted belowground insects, their aboveground use can be supported if combined with adjuvants. We hypothesized that EPN infective juveniles (IJs) could be combined with plant-based oils as adjuvants, without decreasing their efficacy against insect larvae under various scenarios. Specifically, our objectives were to evaluate the activity of Steinernema colombiense (Nematoda: Steinernematidae) when mixed with two plant-based oils (coconut and olive oils) and maintained at different temperatures and times, or combined with entomopathogenic fungi. First, we evaluated how these oils affected IJ survival and virulence against last instar Galleria mellonella (Lepidoptera: Pyralidae) larvae when maintained at five different temperatures (4, 8, 14, 20, and 24°C) and five incubation times (1, 3, 7, 14, and 21 days), using water as control treatment. Second, we evaluated virulence when combined with these two oils as well as with water (control) and combined with the entomopathogenic fungi (EPF), Beauveria bassiana (Hypocreales: Clavicipitaceae). Infective juvenile survival was higher in coconut than olive oil and water mixtures up to 7 days at 4°C. Conversely, olive oil supported higher larval mortality than coconut oil at 4 to 20°C and 14 days. Similarly, the number of days needed to kill insect larvae increased at extreme temperatures (4 and 24°C) after 14 days. Finally, the EPN + EPF combination showed an additive effect compared to EPN and EPF single treatments. Our findings indicate that our plant-based oil mixtures maintain viable IJs at moderate temperatures and up to 7 to 14 days, and can be used in single EPN mixtures or combined with EPF., The Government of Portugal, thanks to the ‘Starting Grant’ associate funds (grant number IF/00552/2014/CP1234/CT0007), supported this work. RCH was awarded an Investigator Program contract (grant number IF/00552/2014) and currently is supported by the Ramón y Cajal Program (Spanish Government, RYC-2016-19939). GCE was supported by a Master Fellowship from the government of Mexico (CONACYT CVU 717361). RBP and FBP were financed by the scientific assistantship fellowships associated with the grant IF/00552/2014/CP1234/CT0007 (BI calls UAlg-2016/004 and UAlg-2016/003, respectively). RBP is currently supported by the Department of Economic Development and Innovation of the Government of La Rioja (Spain) with a pre-doctoral contract (CAR-2018)., Peer reviewed




Artículo científico (JournalArticle). 2020

Cutaneous excreta of the earthworm Eisenia fetida (Haplotaxida: Lumbricidae) might hinder the biological control performance of entomopathogenic nematodes

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Chelkha, Maryam
  • Blanco-Pérez, Rubén
  • Bueno-Pallero, Francisco Ángel
  • Amghar, Souad
  • El Harti, Abdellatif
  • Campos-Herrera, Raquel
Earthworms 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/cm2). 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 μm in size (S. feltiae, S. glaseri, and S. khoungi), by affecting their pathogenicity and reproductive success., The Government of Portugal (FCT), thanks to the “Starting Grant” associate funds (grant number IF/00552/2014/CP1234/CT0007), supported this work. RCH was awarded an Investigator Programme contract (grant number IF/00552/2014). Similarly, FABP and RBP were financed by the scientific assistantship fellowships associated with this grant (BI, UAlg-2016/004 and UAlg-2016/003, respectively, Universidade do Algarve, Portugal). MC was supported as visitor student at the Universidade do Algarve (Portugal) thanks to the international mobility program “Mare-Nostrum”. Currently, MC is supported by a Moroccan scholarship for the Ministry of National Education, Vocational Training, Higher Education and Scientific Research, RBP is financed by the Department of Economic Development and Innovation, Government of La Rioja (Spain) with a predoctoral contract (CAR-2018), and RCH is awarded by Ramon y Cajal contract award (RYC-2016-19939) from the Government of Spain. This study is linked to the CSIC i-coop+ 2018 grant (COOPA20231)., Peer reviewed




Artículo científico (JournalArticle). 2021

A global database of soil nematode abundance and functional group composition

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Hoogen, Johan van den
  • Geisen, Stefan
  • Wall, Diana H.
  • Wardle, David A.
  • Traunspurger, Walter
  • Goede, Ron G. M. de
  • Adams, Byron J.
  • Ahmad, Wasim
  • Ferris, Howard
  • Bardgett, Richard D.
  • Bonkowski, Michael
  • Campos-Herrera, Raquel
  • Cares, Juvenil E.
  • Caruso, Tancredi
  • Brito Caixeta, Larissa de
  • Chen, Xiaoyun
  • Costa, Sofia R.
  • Creamer, Rachel
  • Cunha Castro, José Mauro da
  • Dam, Marie
  • Djigal, Djibril
  • Escuer, Miguel
  • Griffiths, Bryan S.
  • Gutiérrez, Carmen
  • Hohberg, Karin
  • Kalinkina, Daria
  • Kardol, Paul
  • Kergunteuil, Alan
  • Korthals, Gerard
  • Krashevska, Valentyna
  • Kudrin, Alexey A.
  • Li, Qi
  • Liang, Wenju
  • Magilton, Matthew
  • Marais, Mariette
  • Rodríguez Martín, José Antonio
  • Matveeva, Elizaveta
  • Mayad, El Hassan
  • Mzough, E.
  • Mulder, Christian
  • Mullin, Peter
  • Neilson, Roy
  • Nguyen, T. A. Duong
  • Nielsen, Uffe N.
  • Okada, Hiroaki
  • Palomares Rius, Juan E.
  • Pan, Kaiwen
  • Peneva, Vlada
  • Pellissier, Loïc
  • Pereira da Silva, Julio Carlos
  • Pitteloud, Camille
  • Powers, Thomas O.
  • Powers, Kirsten
  • Quist, Casper W.
  • Rasmann, Sergio
  • Sánchez-Moreno, Sara
  • Scheu, Stefan
  • Setälä, Heikki
  • Sushchuk, Anna
  • Tiunov, Alexei V.
  • Trap, Jean
  • Vestergård, Mette
  • Villenave, Cecile
  • Waeyenberge, Lieven
  • Wilschut, Rutger
  • Wright, Daniel G.
  • Keith, Aidan M.
  • Yang, Jiue-in
  • Schmidt, Olaf
  • Bouharroud, R.
  • Ferji, Z.
  • Putten, Wim H. van der
  • Routh, Devin
  • Crowther, Thomas Ward
As the most abundant animals on earth, nematodes are a dominant component of the soil community. They play critical roles in regulating biogeochemical cycles and vegetation dynamics within and across landscapes and are an indicator of soil biological activity. Here, we present a comprehensive global dataset of soil nematode abundance and functional group composition. This dataset includes 6,825 georeferenced soil samples from all continents and biomes. For geospatial mapping purposes these samples are aggregated into 1,933 unique 1-km pixels, each of which is linked to 73 global environmental covariate data layers. Altogether, this dataset can help to gain insight into the spatial distribution patterns of soil nematode abundance and community composition, and the environmental drivers shaping these patterns., This research was supported by a grant from DOB Ecology to T.W.C., a grant from the
Netherlands Organization for Scientific Research (grant 016.Veni.181.078) to S.G., grants from NSF (OPP
1115245, 1341736, 0840979) to B.J.A., by a Ramon y Cajal fellow award (RYC-2016-19939) to R.C.H., a grant
from UNEP & Global Environment Facility to J.E.C., grants from NERC’s Soil Security Programme to R.D.B.
(NE/M017028/1) T.C. (NE/M017036/1), a grant from FAPEMIG/FAPESP/VALE S.A.(CRA-RDP-00136-10) to
L.B.C., through the strategic programme UID/BIA/04050/2013 (POCI-01-0145-FEDER-007569) awarded to
S.R.C., a grant from CNPq PROTAX (562346/2010-4) to J.M.d.C.C., a grant from DFG (CRC990) to V.K. and S.S.,
a grant from the MSHE of Russia (AAAA-A17-117112850234-5) to A.A.K., grants from the Chinese Academy
of Sciences (XDB15010402) and the National Natural Science Foundation of China (41877047) to Q.L., grants
from the National Natural Science Foundation of China (31330011, 31170484) to W.L., grants from NERC (NE/
M017036/1) to M.M., grants from the Spanish Ministry of Innovation (CGL2009-14686-C02-01/02, CGL2013-
43675-P) to J.A.R.M., grant from the Spanish Ministry of Innovation (RYC-2016-19939) to R.C.H., grants from
NSF (DEB-0450537, DEB-1145440) to P.M., T.O.P. and K. Powers, grants from the German Academic Exchange
Service (PKZ 91540366) and NAFOSTED (106.05–2017.330) to T.A.D.N., by an ARC Discovery project
(DP150104199) to U.N.N., by the National Key Research and Development Program of China (2016YFC0502101)
and the National Natural Science Foundation of China (31370632) to K. Pan, a ERC Research Council Advanced
grant (ERC-Adv 323020 SPECIALS) to W.H.v.d.P, a grant from the Natural Environment Research Council
(NERC) to D.G.W., a grant from BAPHIQ (106AS-9.5.1-BQ-B3) to J.-i.Y., a grant from the Russian Foundation
for Basic Research (18-29-05076) to A.V.T. The James Hutton Institute receives financial support from the
Scottish Government Rural and Environment Science and Analytical Services (RESAS) division. Investigations in
Northwest Russia were carried out under state order for IB KarRC RAS and are partially supported by the Russian
Foundation for Basic Research (18-34-00849).




Contribución de congreso (ConferenceOutput). 2021

Efficiency of an attract-and-kill system with entomopathogenic nematodes against wireworms (Coleoptera: Elateridae)

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Forgia, Diana
  • Jaffuel, Geoffrey
  • Campos-Herrera, Raquel
  • Verheggen, F.
  • Turlings, Ted C. J.
Trabajo presentado en el 52nd Annual Meeting of the Society for Invertebrate Pathology y 17th Meeting of the IOBC‐WPRS Working Group “Microbial and Nematode Control of Invertebrate Pests”, celebrado en Valencia (España), del 28 de julio al 1 de agosto de 2019, This study aimed at contributing to the development of an attract-and-kill strategy combining plant natural extracts with entomopathogenic nematodes (EPNs). We first compared the efficiency of two EPN strains through classical screening laboratory assays (contact application of EPNs) and found 8.3 and 16.7% of mortality after 10 days for Steinernema carpocapsae B14 and Heterorhabditis bacteriophora, respectively. Then, we encapsulated EPNs with potato extracts (acting as attractant and feeding stimulant) in alginate beads and the results showed higher mortality rates: 16.7% and 41.7% for S. carpocapsae and H. bacteriophora, respectively. In absence of attractants in the beads, the mortality dropped to 0% (S. carpocapsae) and 8.3% (H. bacteriophora). We conclude that the ingestion of EPN lead to increased mortality, compared to contact application of EPNs. The association of volatiles organic compounds as attractants and EPNs as biological agents represent a promising alternative to pesticides that remains to be evaluated in the field., D. la Forgia is supported by a PhD grant from Coordinated Integrated Pest Management in
Europe (C-IPM), project ElatPro and a FNRS mobility grant. R. Campos-Herrera is awarded
with a Ramón y Cajal contract (RYC-2016-19939)




Artículo científico (JournalArticle). 2021

Insecticidal Effect of Entomopathogenic Nematodes and the Cell-Free Supernatant from Their Symbiotic Bacteria against Philaenus spumarius (Hemiptera: Aphrophoridae) Nymphs

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • González-Trujillo, María del Mar
  • Pou, Alicia
  • Campos-Herrera, Raquel
This article belongs to the Special Issue Entomopathogenic Nematodes: Lethal Parasites of Insects., [Simple Summary] The disease caused by Xylella fastidiosa affects economically relevant crops such as olives, almonds, and grapevine. Since curative means are not available, its current management principally consists of broad-spectrum pesticide applications to control vectors like the meadow spittlebug Philaenus spumarius, the most important one in Europe. Exploring environmentally sound alternatives is a primary challenge for sustainable agriculture. Entomopathogenic nematodes (EPNs) are well-known biocontrol agents of soil-dwelling arthropods. Recent technological advances for field applications, including improvements in obtaining cell-free supernatants from EPN symbiotic bacteria, allow their successful implementation against aerial pests. Here, we investigated the impact of four EPN species and their cell-free supernatants on nymphs of the meadow spittlebug. First, we observed that the exposure to the foam produced by this insect does not affect the nematode virulence. Indeed, direct applications of certain EPN species reached up to 90–78% nymphal mortality rates after five days of exposure, while specific cell-free supernatants produced 64% mortality rates. Overall, we demonstrated the great potential of EPN and cell-free supernatant of their symbiont bacteria applications against this vector, opening new venues to develop novel biopesticides for integrated management practices and organic productions., The meadow spittlebug Philaenus spumarius (Hemiptera: Aphrophoridae) is the primary vector of Xylella fastidiosa (Proteobacteria: Xanthomonadaceae) in Europe, a pest–disease complex of economically relevant crops such as olives, almonds, and grapevine, managed mainly through the use of broad-spectrum pesticides. Providing environmentally sound alternatives to reduce the reliance on chemical control is a primary challenge in the control of P. spumarius and, hence, in the protection of crops against the expansion of its associated bacterial pathogen. Entomopathogenic nematodes (EPNs) are well-known biocontrol agents of soil-dwelling arthropods. Recent technological advances in field applications, including improvements in obtaining cell-free supernatant from their symbiotic bacteria, allow their successful implementation against aerial pests. Thus, this study aimed to evaluate, for the first time, the efficacy of EPN applications against nymphal instars of P. spumarius. We tested four EPN species and the cell-free supernatant of their corresponding symbiotic bacteria: Steinernema feltiae–Xenorhabdus bovienii, S. carpocapsae–X. nematophila, S. riojaense–X. kozodoii, and Heterorhabditis bacteriophora–Photorhabdus laumondii subsp. laumondii. First, we showed that 24 and 72 h exposure to the foam produced by P. spumarius nymphs did not affect S. feltiae virulence. The direct application of steinernematid EPNs provided promising results, reaching 90, 78, and 53% nymphal mortality rates after five days of exposure for S. carpocapsae, S. feltiae, and S. riojaense, respectively. Conversely, the application of the cell-free supernatant from P. laumondii resulted in nymphal mortalities of 64%, significantly higher than observed for Xenorhabdus species after five days of exposure. Overall, we demonstrated the great potential of the application of specific EPNs and cell-free supernatant of their symbiont bacteria against P. spumarius nymphs, introducing new opportunities to develop them as biopesticides for integrated management practices or organic vineyard production., This study was funding by a grant from the Ministry of Science and Innovation (PID2019-104112RB-I00). The researchers were funded by the following agencies and grants:

-
I.V.-D. funded by ADER I + D + i (2019) fellowship by the Rioja Agency of Economic Development (La Rioja, Spain) and currently is supported by an FPU-UR-2020 fellowship.
-
R.B.-P. was supported by the pre-doctoral contracts CAR-2018 (Department of Economic Development and Innovation of the Government of La Rioja).
-
M.d.M.G.-T. is supported by Program JAE-Intro CSIC call 2020 (JAEINT20_EX_0939).
-
R.C.-H. is supported by Ramón y Cajal contract award from the Government of Spain (RYC-2016-19939)., Peer reviewed




Artículo científico (JournalArticle). 2022

Earthworms and their cutaneous excreta can modify the virulence and reproductive capability of entomopathogenic nematodes and fungi

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Chelkha, Maryam
  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Bueno-Pallero, Francisco Ángel
  • Amghar, Souad
  • El Harti, Abdellatif
  • Campos-Herrera, Raquel
Earthworms 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., MC is supported by a Moroccan scholarship of the Ministry of National Education, Vocational Training, Higher Education and Scientific
Research, and the travel assistance associated with the grant CSIC ICOOP + 2018 grant (COOPA20231). RBP is financed with an FPI contract (CAR-2018) by the Department of Economic Development and
Innovation of The Government of La Rioja (Spain). IVD is supported
with an FPI-UR fellowship by the Universidad de La Rioja (Spain). RCH
is awarded by Ramon y Cajal contract award (RYC-2016-19939) of the
Government of Spain. This study is supported by CSIC I-COOP + 2018
grant (COOPA20231)., Peer reviewed




Artículo científico (JournalArticle). 2022

Positioning entomopathogenic nematodes for the future viticulture: Exploring their use against biotic threats and as bioindicators of soil health

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Campos-Herrera, Raquel
  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • Chelkha, Maryam
  • González-Trujillo, María del Mar
  • Puelles, Miguel
  • Čepulité, Rasa
  • Pou, Alicia
Vineyards face several biotic threats that compromise the grape quality and quantity. Among those that cause relevant economic impact and have worldwide distribution are the oomycete Plasmopara vitícola, the fungi Erysiphe necator and Botrytis cinerea, and the arthropods Lobesia botrana, Tetranychus urticae, and Phylaenus spumarius (principal vector of the bacterial disease Xylella fastidiosa in Europe). Their management relies primarily on agrochemicals with short persistence; widespread use of these chemicals causes environmental and human health problems. The challenge of sustainable viticulture is to provide ecologically sound alternatives. In this regard, the application of entomopathogenic nematodes (EPNs) and natural products derived from their symbionts can be an alternative. EPNs are well-known biocontrol agents for soil-dwelling insects. However, current research demonstrates the great potential of both EPN and their derivates as direct bio-tools against some of the key fungal and arthropods pests present aboveground. In addition, recent evidence shows that detecting EPN presence and activity and their relation with other soil organisms associated with them can help us to understand the impact of different agricultural practices on vineyard management. Altogether, this review illustrates the great potential of EPN to enhance pest and disease management in the next generation of viticulture., This review is produced in the context of the grant
awarded from Ministry of Science and Innovation
(PID2019-104112RB-I00). Also, some of the studies
presented were conducted in the framework of the
Interdisciplinar Thematic Platform PTI-SolXyl on Xylella
fastidiosa from CSIC (Spain). RCH is awarded by Ramon
y Cajal contract award (RYC-2016-19939) from the
Government of Spain. IVD is supported with a FPI-UR
(2021) fellowship (Universidad de La Rioja, Spain). RBP
is financed by the Department of Economic Development
and Innovation, Government of La Rioja (Spain) with an
FPI contract (CAR-2018). MC is supported by a Moroccan
scholarship for the Ministry of National Education,
Vocational Training, Higher Education and Scientific
Research, and the travel assistance associated with the
grant CSIC I-COOP+ 2018 grant (COOPA20231).
MMGT is funded by the Programme JAE-Intro CSIC
call 2020 (JAEINT20_EX_0939). MP is funded by an
introduction to research fellowship from Government
of La Rioja (CAR 2020). RC is funded by a postdoctoral
internship from Lituania Goverment supported by EU
funds (LMT-K-712-21-0098).




Artículo científico (JournalArticle). 2022

Exploring the use of entomopathogenic nematodes and the natural products derived from their symbiotic bacteria to control the grapevine moth, Lobesia botrana (lepidoptera: tortricidae)

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • Chelkha, Maryam
  • Puelles, Miguel
  • Pou, Alicia
  • Campos-Herrera, Raquel
The European grapevine moth (EGVM) Lobesia botrana (Lepidoptera: Tortricidae) is a relevant pest in the Palearctic region vineyards and is present in the Americas. Their management using biological control agents and environmentally friendly biotechnical tools would reduce intensive pesticide use. The entomopathogenic nematodes (EPNs) in the families Steinernematidae and Heterorhabditidae are well-known virulent agents against arthropod pests thanks to symbiotic bacteria in the genera Xenorhabdus and Photorhabdus (respectively) that produce natural products with insecticidal potential. Novel technological advances allow field applications of EPNs and those bioactive compounds as powerful bio-tools against aerial insect pests. This study aimed to determine the viability of four EPN species (Steinernema feltiae, S. carpocapsae, S. riojaense, and Heterorhabditis bacteriophora) as biological control agents against EGVM larval instars (L1, L3, and L5) and pupae. Additionally, the bioactive compounds from their four symbiotic bacteria (Xenorhabdus bovienii, X. nematophila, X. kozodoii, and Photorhabdus laumondii subsp. laumondii, respectively) were tested as unfiltered ferment (UF) and cell-free supernatant (CFS) against the EGVM larval instars L1 and L3. All of the EPN species showed the capability of killing EGVM during the larval and pupal stages, particularly S. carpocapsae (mortalities of ~50% for L1 and >75% for L3 and L5 in only two days), followed by efficacy by S. feltiae. Similarly, the bacterial bioactive compounds produced higher larval mortality at three days against L1 (>90%) than L3 (~50%), making the application of UF more virulent than the application of CFS. Our findings indicate that both steinernematid species and their symbiotic bacterial bioactive compounds could be considered for a novel agro-technological approach to control L. botrana in vineyards. Further research into co-formulation with adjuvants is required to expand their viability when implemented for aboveground grapevine application., This research was funded by the following institutions (name: reference), MCIN/AEI/
10.13039/501100011033: Grant PID2019-104112RB-I00, University of La Rioja: FPI-UR-2020, Department
of Economic Development and Innovation of the Government of La Rioja: FPI-CAR-2018,
Rioja Agency of Economic Development: ADER I+D+i (2019), CSIC I-COOP+ 2018: COOPA20231,
Government of La Rioja: Intro-CAR 2020, MCIN/AEI/10.13039/501100011033 and by “ESF Investing
in your future”: Grant RYC-2016-19939., Peer reviewed




Artículo científico (JournalArticle). 2022

Intraspecific virulence of entomopathogenic nematodes against the pests Frankliniella occidentalis (Thysanoptera: Thripidae) and Tuta absoluta (Lepidoptera: Gelechiidae)

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Campos-Herrera, Raquel
  • Vicente-Díez, Ignacio
  • Galeano, Magda
  • Chelkha, Maryam
  • González-Trujillo, María del Mar
  • Puelles, Miguel
  • Labarga, David
  • Pou, Alicia
  • Calvo-Garrido, Javier
  • Belda, J. E.
Entomopathogenic nematodes (EPN) are excellent biocontrol agents against various insect pests. Novel biotechnological approaches can enhance their utility against insects above-ground, opening a new venue for selecting superior EPN against certain insects. We hypothesize that different populations of the same species but from different origins (habitat, ecoregion) will differ in their virulence. This study aimed to evaluate the virulence of various EPN populations against two pests of worldwide incidence and damage to high value crops: Frankliniella occidentalis (Thysanoptera: Thripidae) and Tuta absoluta (Lepidoptera: Gelechiidae). We tested 10 EPN populations belonging to three EPN species: Heterorhabditis bacteriophora (Koppert, MG-618b, AM-203, RM-102), Steinernema feltiae (Koppert, RS-5, AM-25, RM-107), and Steinernema carpocapsae (Koppert, MG-596a). Each EPN population was tested at two concentrations. Frankliniella occidentalis was tested at 160 and 80 IJs/cm2 and T. absoluta at 21 and 4 IJs/cm2. Control treatments followed the same experimental procedure but only adding distilled water. Overall, whenever different, higher IJs concentration resulted in lower adult emergence, higher larval mortality, and shorter time to kill the insects. Considering the low concentration, S. feltiae provided the best results for both insects and instars investigated, while H. bacteriophora and S. carpocapsae required a high concentration to reach similar or slightly better results. Differences among populations of each of the species were detected, but only the native populations of H. bacteriophora populations showed consistently higher control values against both insects/instar compared with the commercial one. Differences among S. feltiae and S. carpocapsae populations depended on the IJs concentration, insect, and instar. We consider S. feltiae a very promising species for their application against F. occidentalis and T. absoluta, with the Koppert population as the most consistent among the populations tested. Specific EPN-populations of S. carpocapsae and H. bacteriophora were good candidates against certain instar/insects at high concentrations. This study emphasized the importance of intraspecific variability for EPN virulence., RCH is awarded by Ramon y Cajal contract award
MCIN/AEI/10.13039/501100011033 and by “ESF
Investing in your future”: Grant RYC-2016-19939 from
the Government of Spain. IVD is supported with a
FPI-UR (2021) fellowship (Universidad de La Rioja,
Spain). MC is supported by a Moroccan scholarship
for the Ministry of National Education, Vocational
Training, Higher Education and Scientific Research,
and the travel assistance associated with the grant
CSIC I-COOP + 2018 grant (COOPA20231). MMGT
is funded by the Program JAE-Intro CSIC call 2020
(JAEINT20_EX_0939). MP and DL are funded by an
introduction to research fellowship from Government
of La Rioja (CAR 2020). The study was performed
under the Research and Innovation grant at CSIC ref.
20200154 and 20194898., Peer reviewed




Artículo científico (JournalArticle). 2022

The lure of hidden death: Development of an attract-and-kill strategy againsagriotes obscurus (coleoptera: Elateridae) combining semiochemicals and entomopathogenic nematodes

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Forgia, Diana
  • Bruno, Pamela
  • Campos-Herrera, Raquel
  • Turlings, Ted C. J.
  • Verheggen, F.
Wireworms are polyphagous soil-dwelling pests that are hard to control. Attract-and-kill strategies, combining attractive semiochemicals with biocontrol agents, have great promise to control insect pests. We hypothesized that the combination of plant semiochemicals and entomopathogenic nematodes (EPNs) in an attract-and-kill system could greatly enhance the nematodes’ efficiency against wireworms. We evaluated the potential of alginate beads loaded with plant extracts and EPNs to control Agriotes obscurus. We tested the efficiency to kill wireworms or to reduce their feeding activity when combining potato tuber extracts as attractants with any of seven different EPN populations. While a direct application of EPNs on wireworms did not reduce the feeding activity nor increased their mortality, the combination of attractants and EPNs encapsulated in alginate beads resulted in attraction and consumption of the EPNs and caused up to 50% wireworm mortality with the EPN species Steinernema carpocapsae. Beads with EPNs caused a significant reduction of the wireworms’ feeding activity. This study shows that wireworms feeding on EPN-containing beads have their feeding activity and survival negatively affected. Considering their long developmental time and the survival capability of EPNs in the soil, implementing this attract-and-kill system in the field might be a suitable strategy for the long-term management of wireworms., The authors thank Ricardo Machado from the University
of Bern (Switzerland), Selcuk Hazir from the Aydın Adnan
Menderes University (Turkey) and Fernando García del Pino
from the Universidad Autónoma de Barcelona (Spain) for
providing the nematodes populations that were used in the
experiments. The authors also thank to Mickaël Gaillard for
the statistical help. The results presented in this study are
part of the PhD thesis by the first author DLF, supported by a
Ph.D. grant from Coordinated Integrated Pest Management
in Europe (C-IPM), project ElatPro. RCH is awarded by
Ramon y Cajal contract award (RYC-2016-19939) from the
Government of Spain.




Artículo científico (JournalArticle). 2022

Organic viticulture enhanced the activity of native entomopathogenic nematodes in DOCa Rioja soils (North of Spain)

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Ramos-Saez De Ojer, José Luis
  • Marco Mancebón, Vicente
  • Pérez-Moreno, I.
  • Campos-Herrera, Raquel
Vineyards and their associated socio-economic activities are relevant sectors worldwide. Still, this agroecosystem is one of the most intensely managed crops and erosion-prone land areas. The conventional viticulture practices to control pests, diseases, and weeds, like tillage and agrochemical applications, accelerate the loss of soil biodiversity and compromise the presence of beneficial soil organisms such as the entomopathogenic nematodes (EPNs). Such human disturbances in the agroecosystems can strongly affect abiotic (e.g., soil texture and properties) and biotic factors (natural enemies and potential competitors) that modulate the EPN activity as biological control agents. For the first time in viticulture, this study aimed to investigate the impact of differentiating management on the EPN community and associated soil organisms and if their assemblage will provide indicators of better practices for sustainable farming. We hypothesized that organic pest management and alternative strategies to tillage might enhance the abundance and activity of the native EPN community in vineyard soils. In autumn 2019, we collected two composite soil samples from 80 vineyards distributed across the Guaranteed Designation of Origin (denominated DOCa) Rioja region. The sites belonged to one category of each of the two factors: pest management (integrated vs. organic, 40 plots each) and soil managing (tillage vs. cover cropping, 48 and 32 vineyards, respectively). Isolated through sucrose-gradient centrifugation and employing species-specific primers/probe qPCR sets, we investigated the presence of ten EPN species and associated soil organisms: four free-living nematodes (FLNs), six nematophagous fungi (NF), and two ectoparasitic bacteria (EcPB). Besides, we estimated the EPN activity using the traditional insect-bait method. We included in the analysis twenty soil variables to characterize the evaluated treatments and assess their impact on soil organism distribution. Our results provide evidence on the support of organic viticulture to beneficial soil organisms, notably the activity of native EPNs. We also reported a higher abundance of S. feltiae (the predominant steinernematid species in Europe) and FLNs for organic farming than IMP, while the presence of NF and EcPB resulted in unaffected. Contrarily, the soil management practices considered did not differ in their impact on EPNs or their natural enemies/competitors, even if contrasted for several soil properties. Future research may expand the screened soil-dwelling species using novel molecular technics to unravel their complex interactions and determine the best farming practices to preserve soil health., The authors thank to all the DOCa Rioja wineries and winegrowers involved in this study for sharing their vineyards. We appreciate the help offered by Esperanza López Ubis (Government of La Rioja, Spain) for her support in the search of organic farmers. We also thank Dr. David Gramaje Pérez and members of Biovitis Lab (ICVV-CSIC, Spain) for kindly sharing their equipment. The pre-doctoral contracts CAR-2018 (Department of Economic Development and Innovation of the Government of La Rioja, Spain) and FPI-UR 2021 (University of La Rioja, Spain) support RBP and IVD, respectively. Similarly, RCH received the grant RYC-2016-19939 funded by MCIN/AEI/ 10.13039/501100011033 and “ESF Investing in your future”. This study was also funded by the Instituto de Estudios Riojanos (IER, Government of La Rioja, Spain, ref. 21/2021)., Peer reviewed




Set de datos (Dataset). 2022

Intraspecific virulence of entomopathogenic nematodes against the pests Frankliniella occidentalis (Thysanoptera: Thripidae) and Tuta absoluta (Lepidoptera: Gelechiidae) [Dataset]

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Campos-Herrera, Raquel
  • Vicente-Díez, Ignacio
  • Galeano, Magda
  • Chelkha, Maryam
  • González-Trujillo, María del Mar
  • Puelles, Miguel
  • Labarga, David
  • Pou, Alicia
  • Calvo-Garrido, Javier
  • Belda, J. E.
The data were generated by the authors in independent experiments, all performed in the same conditions and installations. All the experiments were performed twice and the data corresponding with trials 1 and 2 of the same set was compared to allow combination in the statistical analysis. Each trial was performed with new and fresh nematodes and insects, Entomopathogenic nematodes (EPN) are excellent biocontrol agents against various insect pests. Novel biotechnological approaches can enhance their utility against insects above-ground, opening a new venue for selecting superior EPN against certain insects. We hypothesize that different populations of the same species but from different origins (habitat, ecoregion) will differ in their virulence. This study aimed to evaluate the virulence of various EPN populations against two pests of worldwide incidence and damage to high value crops: Frankliniella occidentalis (Thysanoptera: Thripidae) and Tuta absoluta (Lepidoptera: Gelechiidae). We tested 10 EPN populations belonging to three EPN species: Heterorhabditis bacteriophora (Koppert, MG-618b, AM-203, RM-102), Steinernema feltiae (Koppert, RS-5, AM-25, RM-107), and Steinernema carpocapsae (Koppert, MG-596a). Each EPN population was tested at two concentrations. Frankliniella occidentalis was tested at 160 and 80 IJs/cm2 and T. absoluta at 21 and 4 IJs/cm2. Control treatments followed the same experimental procedure but only adding distilled water. Overall, whenever different, higher IJs concentration resulted in lower adult emergence, higher larval mortality, and shorter time to kill the insects. Considering the low concentration, S. feltiae provided the best results for both insects and instars investigated, while H. bacteriophora and S. carpocapsae required a high concentration to reach similar or slightly better results. Differences among populations of each of the species were detected, but only the native populations of H. bacteriophora populations showed consistently higher control values against both insects/instar compared with the commercial one. Differences among S. feltiae and S. carpocapsae populations depended on the IJs concentration, insect, and instar. We consider S. feltiae a very promising species for their application against F. occidentalis and T. absoluta, with the Koppert population as the most consistent among the populations tested. Specific EPN-populations of S. carpocapsae and H. bacteriophora were good candidates against certain instar/insects at high concentrations. This study emphasized the importance of intraspecific variability for EPN virulence., Grants ICVV-CSIC and Koppert with the following references:
1) ref. 20194898 (ID CSIC 201912)
2) ref. 20200154 (ID CSIC 205137)
3) ref. 20202349 (ID CSIC 210825), 1) RCH is awarded by Ramon y Cajal contract award MCIN/AEI/10.13039/501100011033 and by “ESF Investing in your future”: Grant RYC-2016-19939 from the Government of Spain
2) IVD is supported with a FPI-UR (2021) fellowship (Universidad de La Rioja, Spain).
3) MC is supported by a Moroccan scholarship for the Ministry of National Education, Vocational Training, Higher Education and Scientific Research, and the travel assistance associated with the grant
CSIC I-COOP + 2018 grant (COOPA20231).
4) MMGT is funded by the Program JAE-Intro CSIC call 2020 (JAEINT20_EX_0939).
5) MP and DL are funded by an introduction to research fellowship from Government of La Rioja (CAR 2020)., Peer reviewed




Set de datos (Dataset). 2022

Insecticidal Effect of Entomopathogenic Nematodes and the Cell-Free Supernatant from Their Symbiotic Bacteria against Philaenus spumarius (Hemiptera: Aphrophoridae) Nymphs [Dataset]

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • González-Trujillo, María del Mar
  • Pou, Alicia
  • Campos-Herrera, Raquel
Experiment performed in the lab, following details described in the publication (http://hdl.handle.net/10261/240920 / https://doi.org/10.3390/insects12050448), Grants ICVV-CSIC:

Ministry of Science and Innovation (PID2019-104112RB-I00) funded by MCIN/AEI/10.13039/501100011033.

Support for researchers:

1) RCH is awarded by Ramon y Cajal contract award MCIN/AEI/10.13039/501100011033 and by “ESF Investing in your future”: Grant RYC-2016-19939 from the Government of Spain
2) IVD is I.V.-D. funded by ADER I + D + i (2019) fellowship by the Rioja Agency of Economic Development
(La Rioja, Spain) and by FPI-UR (2021) fellowship (Universidad de La Rioja, Spain).
4) MMGT is funded by the Program JAE-Intro CSIC call 2020 (JAEINT20_EX_0939).
5) R.B.-P. was supported by the pre-doctoral contracts CAR-2018 (Department of Economic Development and Innovation of the Government of La Rioja)., Peer reviewed




Set de datos (Dataset). 2022

Exploring the Use of Entomopathogenic Nematodes and the Natural Products Derived from Their Symbiotic Bacteria to Control the Grapevine Moth, Lobesia botrana (Lepidoptera: Tortricidae) [Dataset]

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • Chelkha, Maryam
  • Puelles, Miguel
  • Pou, Alicia
  • Campos-Herrera, Raquel
Experiment performed in the lab, following details described in the publication: https://doi.org/10.3390/insects12111033 / http://hdl.handle.net/10261/262517, Grants ICVV-CSIC:

Ministry of Science and Innovation (PID2019-104112RB-I00) funded by MCIN/AEI/10.13039/501100011033.

Support for researchers:

1) RCH is awarded by Ramon y Cajal contract award MCIN/AEI/10.13039/501100011033 and by “ESF Investing in your future”: Grant RYC-2016-19939 from the Government of Spain
2) IVD is I.V.-D. funded by ADER I + D + i (2019) fellowship by the Rioja Agency of Economic Development (La Rioja, Spain) and by FPI-UR (2021) fellowship (Universidad de La Rioja, Spain).
3) MP is funded by an introduction to research fellowship from the Government of La Rioja (CAR 2020).
4) MC was supported by the travel assistance is associated with the CSIC I-COOP+ 2018 grant (COOPA20231) and a Moroccan scholarship for the Ministry of National Education, Vocational Training, Higher Education, and Scientific Research
5) RBP was supported by the pre-doctoral contracts CAR-2018 (Department of Economic Development and Innovation of the Government of La Rioja)., Peer reviewed




Set de datos (Dataset). 2022

Earthworms and their cutaneous excreta can modify the virulence and reproductive capability of entomopathogenic nematodes and fungi [Dataset]

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Chelkha, Maryam
  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Bueno-Pallero, Francisco Ángel
  • Amghar, Souad
  • El Harti, Abdellatif
  • Campos-Herrera, Raquel
Experiment performed in the lab, following details described in the publication: http://dx.doi.org/10.1016/j.jip.2021.107620 / http://hdl.handle.net/10261/261936, Grants ICVV-CSIC:

1) CSIC I-COOP + 2018 grant (COOPA20231)

2) Associated funds of Ramon y Cajal contract award MCIN/AEI/10.13039/501100011033 and by “ESF Investing in your future”: Grant RYC-2016-19939 from the Government of Spain

Support for researchers:

1) MC was supported by the travel assistance is associated with the CSIC I-COOP+ 2018 grant (COOPA20231) and a Moroccan scholarship for the Ministry of National Education, Vocational Training, Higher Education, and Scientific Research
2) RBP was supported by the pre-doctoral contracts CAR-2018 (Department of Economic Development and Innovation of the Government of La Rioja).
3) IVD was funded by ADER I + D + i (2019) fellowship by the Rioja Agency of Economic Development (La Rioja, Spain) and by FPI-UR (2021) fellowship (Universidad de La Rioja, Spain).
4) RCH was awarded by Ramon y Cajal contract award MCIN/AEI/10.13039/501100011033 and by “ESF Investing in your future”: Grant RYC-2016-19939 from the Government of Spain, Peer reviewed




Artículo científico (JournalArticle). 2023

Organic mulching modulated native populations of entomopathogenic nematode in vineyard soils differently depending on its potential to control outgrowth of their natural enemies

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Pou, Alicia
  • Pérez-Moreno, I.
  • Marco Mancebón, Vicente
  • Campos-Herrera, Raquel
The entomopathogenic nematodes (EPNs) are biological control agents that are widespread in crop soils. However, traditional agricultural management practices such as cultivation and agrochemical usage can alter the soil balance that enables their occurrence and activity. Alternative strategies like mulching are commonly employed to prevent weed growth, enhance below-ground biodiversity by improving soil, organic matter content, fertility, and moisture. We hypothesized that organic mulches would favor biotic conditions for nematofauna development in crop soil, including EPNs, compared to herbicide application or tillage. Traditional (insect baits) and molecular (qPCR analysis) tools were used in this study to assess the abundance and activity of native EPNs, and the abundance of potential natural enemies, such as free-living nematode (FLN) competitors, nematophagous fungi (NF), and ectoparasitic bacteria, in soils managed with different organic mulches or traditional practices. As a model agroecosystem, we selected the vineyard, one of the most intensively managed crop systems. We compared mulches of grape pruning debris (GPD-M), straw (Str-M), and spent mushroom compost (SMC-M) in two commercial vineyards, which employed either integrated or organic pest and disease management. Following a completely randomized design, we retrieved two composite samples per plot (n = 3 per treatment in each vineyard) in April, June, and October 2020. Numbers of EPNs and selected members of their soil food web were higher in the organic than the integrated managed vineyard. Supporting our hypothesis, organic mulching overall favored nematode occurrence in both vineyards. We found higher NF abundance for Str-M, and GPD-M in the organic vineyard, which plausibly explained the lower EPN activity and occurrence compared to SMC-M in both vineyards. We conclude that the organic mulches can provide appropriate conditions for increasing nematofauna numbers but, depending on the mulch type, may also adversely affect EPNs by increasing their natural enemies. Our findings highlight the need to explore alternative farming practices to unravel complex biotic interactions that affect beneficial soil organisms in agroecosystems., The pre-doctoral contracts CAR-2018 (Department of Economic Development and Innovation of the Government of La Rioja) and FPI-UR 2021 (University of La Rioja) support RBP and IVD, respectively. Similarly, RCH received the grant RYC-2016-19939 funded by MCIN/AEI/ 10.13039/501100011033 and “ESF Investing in your future”. This study was also funded by the FEDER-Government of La Rioja Funds (P.R.-05-20) and MCIN/AEI/ 10.13039/501100011033 (RTI2018-095748-R-I00 Project).




Artículo científico (JournalArticle). 2023

New insights on the impact of earthworm extract on the growth of beneficial soil fungi: species-specific alteration of the nematophagous fungal growth and limitation of an entomopathogenic fungus

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Chelkha, Maryam
  • Yakkou, Lamia
  • Houida, Sofia
  • Raouane, Mohamed
  • Amghar, Souad
  • Campos-Herrera, Raquel
  • El Harti, Abdellatif
Earthworms influence soil ecosystem functions such as decomposition and regulation of nutrient cycles by burrowing, feeding,
or secreting their cutaneous excreta. Earthworms can also modulate soil biodiversity and their interactions. Recent research has revealed
that earthworm feeding activity or excretions can alter the performance of entomopathogenic nematodes (EPNs) and entomopathogenic
fungi (EPFs), known biological control agents. Still, the impact of earthworm cadavers on the growth and reproduction of other biological
control agents such as nematophagous fungus (NFs) and EPFs has been poorly explored. We suggest that earthworm body tissue could
be used as a food supply by certain fungal species. We hypothesize that fungi with a high adaptive capacity as pathobionts such as NF will
use earthworm cadavers to a certain extent, while the growth and reproduction of fungi with limited or specific nutrition needs, such
as EPFs, will be restricted. In this study, we evaluated two NF species: a nematode-trapping fungus Arthrobotrys musiformis Drechsler
(Orbiliales: Orbiliaceae) and a nematode egg or cyst parasite Purpureocillium lilacinum (Thom) (Hypocreales: Ophiocordycipitaceae),
and one EPF species: Beauveria bassiana (Balsamo). We exposed each fungus to two different Aporrectodea molleri extract media at six
concentrations in agar medium (n = 3 per treatment) and liquid medium (n = 5): (i) earthworms devoid of intestinal contents (EDG)
(C1...C6), and (ii) fresh earthworms (FE) (C1...C6). The use of FE and EDG was designed to discriminate the effect of earthworms’
intestinal content on fungal growth. These treatments were also compared to alternative conventional media potato dextrose agar (PDA)
and brain heart infusion (BHI) as the positive controls. We evaluated the vegetative growth capacity daily for 18 days, registering the
reproduction at the end of the experiment. We observed that EPF B. bassiana did not grow in FE and EDG solid medium but showed
germination in their liquid media. However, both NF species could grow and reproduce in both media but following a species-specific
pattern. In all cases, FE and EDG reduced fungal growth compared to PDA and BHI. Our results suggest that the use of earthworm as a
resource in natural conditions might depend on the expected specialization, with EPF B. bassiana with the lowest use, NF A. musiformis
moderately, and P. lilacinum widely used. The study illustrates the complexity of the soil organisms’ interactions and highlights the
necessity to advance the understanding of the contribution of all the beneficial soil organisms in a comprehensive manner., MC is supported by a Moroccan scholarship of the
Ministry of National Education, Vocational Training,
Higher Education and Scientific Research. RCH received
the grant RYC-2016-19939 funded by MCIN/AEI/
10.13039/501100011033 and “ESF Investing in your
future”.




Artículo científico (JournalArticle). 2023

Control of post-harvest gray mold (Botrytis cinerea) on grape (Vitis vinifera) and tomato (Solanum lycopersicum) using volatile organic compounds produced by Xenorhabdus nematophila and Photorhabdus laumondii subsp. laumondii

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Vicente-Díez, Ignacio
  • Moreira Tomé, Xoaquín
  • Pastor, Victoria
  • Vilanova de la Torre, María del Mar
  • Pou, Alicia
  • Campos-Herrera, Raquel
Post-harvest fruit and vegetable rot produced by Botrytis cinerea (Helotiales: Sclerotiniaceae) causes significant reductions in food availability and drastically increases economic losses. The use of microbial-based tools for pathogen management holds promise. In particular, volatile organic compounds (VOCs) emitted by microbes (e.g., bacterial compounds) are becoming increasingly more frequent as an alternative to chemical and physical treatments. In this study, we performed three laboratory experiments to investigate the effects of VOCs emitted by two gram-negative entomopathogenic bacteria, Xenorhabdus nematophila, and Photorhabdus laumondii subsp. laumondii, on the infection and growth of the pathogenic mold B. cinerea on post-harvest red grapes and tomatoes. In addition, we evaluated the preventive effects of these bacterial VOCs against pathogens in post-harvest wounded and intact grapes. Overall, VOCs emitted by X. nematophila and P. laumondii limited the lesion area of B. cinerea to 0.5% and 2.2%, respectively, on the grapes. Similarly, VOCs emitted by X. nematophila and P. laumondii limited the lesion area of B. cinerea to 0.5% and 0.02%, respectively, in tomatoes. In addition, the emission of VOCs by both bacteria showed strong preventive fungal effects. In particular, VOCs emitted by P. laumondii reduced to 13% B. cinerea incidence in damaged grapes exposed to VOCs. Moreover, intact grapes exposed to VOCs emitted by X. nematophila and P. laumondii decreased B. cinerea incidence by 33%. This study provides insightful information about a potential novel bacteria-based tool that can be used as an alternative in the integrated control of post-harvest diseases., The authors thank Elisabet Vaquero Jiménez for her invaluable assistance in the laboratory, and members of Biovitis Lab and VitisGen (ICVV) for kindly sharing their equipment. The pre-doctoral contract FPI-UR 2021 (University of La Rioja) support IVD. Similarly, RCH received the Grant RYC-2016-19939 funded by MCIN/AEI/ 10.13039/501100011033 and “ESF Investing in your future”. This study was also funded by the Ministry of Science and Innovation, Grant PID2019-104112RB-I00 (MCIN/AEI/10.13039/50110001103)., Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature., Peer reviewed




Set de datos (Dataset). 2023

Control of post-harvest gray mold (Botrytis cinerea) on grape (Vitis vinifera) and tomato (Solanum lycopersicum) using volatile organic compounds produced by Xenorhabdus nematophila and Photorhabdus laumondii subsp. laumondii [Dataset]

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Vicente-Díez, Ignacio
  • Moreira Tomé, Xoaquín
  • Pastor, Victoria
  • Vilanova de la Torre, María del Mar
  • Pou, Alicia
  • Campos-Herrera, Raquel
Experiment performed in the lab, following details described in the publication https://doi.org/10.1007/s10526-023-10212-7, Grant PID2019-104112RB I00 from Ministry of Science and Innovation (MCIN/AEI/10.13039/50110001103).

Grant RYC-2016-19939 funded by Ministry of Science and Innovation (MCIN/
AEI/ 10.13039/501100011033) and “ESF Investing in your future”.
The predoctoral contract FPI-UR 2021 (University of La Rioja) support IVD, Peer reviewed




Set de datos (Dataset). 2026

Organic viticulture enhanced the activity of native entomopathogenic nematodes in DOCa Rioja soils (North of Spain) [Dataset]

DIGITAL.CSIC. Repositorio Institucional del CSIC
  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Ramos-Saez De Ojer, José Lui
  • Marco Mancebón, Vicente
  • Pérez-Moreno, I.
  • Campos-Herrera, Raquel
Experiment performed in the laboratory, following details described in the publication, The MCIN/AEI/ 10.13039/501100011033 and “ESF Investing in your future” supported the grant RYC-2016-19939

The Instituto de Estudios Riojanos (IER, Government of La Rioja, Spain, ref.21/2021).

Support for researchers:

RBP was supported by a FPI-CSIC-CAR grant Department of Economic Development and Innovation of the Government of La Rioja, Spain

IVD was supported by a FPI-UR grant (UR, 2020)

RCH was supported by the RYC-2016-19939 funded by MCIN/AEI/ 10.13039/501100011033 and “ESF Investing in your future”., Peer reviewed