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

  • Chelkha, Maryam
  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Bueno-Pallero, Francisco Ángel
  • Amghar, S.
  • El Harti, Abdellatif
  • Campos-Herrera, R.
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



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

  • Campos-Herrera, R.
  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • Chelkha, Maryam
  • González-Trujillo, M.
  • 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).



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

  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • Chelkha, Maryam
  • Puelles, Miguel
  • Pou, Alicia
  • Campos-Herrera, R.
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



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

  • Campos-Herrera, R.
  • Vicente-Díez, Ignacio
  • Galeano, Magda
  • Chelkha, Maryam
  • González-Trujillo, M.
  • 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



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

  • Forgia, Diana
  • Bruno, Pamela
  • Campos-Herrera, R.
  • 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.



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

  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Ramos-Saez De Ojer, José Luis
  • Marco Mancebón, Vicente
  • Pérez-Moreno, I.
  • Campos-Herrera, R.
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



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

  • Campos-Herrera, R.
  • Vicente-Díez, Ignacio
  • Galeano, Magda
  • Chelkha, Maryam
  • González-Trujillo, M.
  • 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



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

  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • González-Trujillo, M.
  • Pou, Alicia
  • Campos-Herrera, R.
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



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]

  • Vicente-Díez, Ignacio
  • Blanco-Pérez, Rubén
  • Chelkha, Maryam
  • Puelles, Miguel
  • Pou, Alicia
  • Campos-Herrera, R.
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



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

  • Chelkha, Maryam
  • Blanco-Pérez, Rubén
  • Vicente-Díez, Ignacio
  • Bueno-Pallero, Francisco Ángel
  • Amghar, S.
  • El Harti, Abdellatif
  • Campos-Herrera, R.
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