Earthworm mediated dispersal of baculovirus occlusion bodies: Experimental evidence from a model system

Infante-Rodríguez, Dennis Adrián; Berber, José J.; Mercado, Gabriel; Valenzuela‐González, Jorge E.; Muñoz, Delia; Williams, Trevor

doi:10.1016/j.biocontrol.2016.05.005

Cited by 14 publications

(7 citation statements)

References 41 publications

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“…In the case of the soil-diet bioassay in first instars, the estimated LC 50 was 1.9 × 10 6 OBs/g soil, which compared favorably with values derived from soil-diet bioassays on second instars of 1.4 × 10 6 OBs/g soil [ 20 ] and 2.7 × 10 6 OBs/g soil, albeit with shorter periods (2–4 days) of feeding on the soil–diet mixture [ 19 ]. The reason why the LC 50 values differed by approximately 100-fold between droplet feeding and soil-diet bioassay techniques is likely due to two reasons: (i) the OB-contaminated soil was diluted ten-fold by the addition of the diet prior to the soil-diet bioassay, and (ii) OBs adhere strongly to components of the soil, particularly clay minerals [ 49 ], and so may be less readily solubilized in the insect midgut than purified OBs in water.…”

Section: Discussionmentioning

confidence: 77%

“…A sensitive bioassay technique has been developed involving feeding early instar larvae with mixtures of soil and semi-synthetic diet [ 15 ]. This technique has been used to obtain novel occluded virus isolates [ 16 ] and to study the abundance and genetic composition of soil OB populations [ 17 , 18 ] and their interaction with soil-dwelling invertebrates [ 19 , 20 ].…”

Section: Introductionmentioning

confidence: 99%

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Presence of Spodoptera frugiperda Multiple Nucleopolyhedrovirus (SfMNPV) Occlusion Bodies in Maize Field Soils of Mesoamerica

Williams¹,

Melo-Molina²,

Jiménez-Fernández³

et al. 2023

Insects

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The occlusion bodies (OBs) of lepidopteran nucleopolyhedroviruses can persist in soil for extended periods before being transported back on to the foliage for transmission to the host insect. A sensitive insect bioassay technique was used to detect OBs of Spodoptera frugiperda multiple nucleopolyhedrovirus (SfMNPV) in 186 soil samples collected from maize fields in the southern Mexican states of Chiapas, Tabasco, Campeche, Yucatán, and Quintana Roo, as well Belize and Guatemala. Overall, 35 (18.8%) samples proved positive for SfMNPV OBs. The frequency of OB-positive samples varied significantly among Mexican states and countries (p < 0.05). Between 1.7 and 4.4% of S. frugiperda larvae that consumed OB-positive samples died from polyhedrosis disease. Restriction endonuclease analysis using PstI and HindIII confirmed that the soil-derived isolates were strains of SfMNPV and that genetic diversity was evident among the isolates. The prevalence of OB-positive soil samples did not differ with altitude or extension (area) of the maize field, but it was significantly higher in fields with the presence of living maize plants compared to those containing dead plants or crop residues (p < 0.05). Georeferenced soil samples were used to identify soil types on digitized soil maps. Lithosol and Luvisol soils had a higher than average prevalence of OB-positive samples (42–45% positive) (p = 0.006), as did Andosol, Gleysol, and Vertisol soils (33–60% OB-positive), although the sample sizes were small (<5 samples) for the latter three soils. In contrast, Cambisol soils had a lower than average prevalence of OB-positive samples (5% positive). Bioassays on Acrisol, Fluvisol, Phaeozem, and Rendzina soils resulted in intermediate levels of OB-positive samples. We conclude that certain soil types may favor OB persistence and virus-mediated biological pest control. The soil is also likely to provide a valuable source of genetic diversity for the design of virus-based insecticides against this pest.

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Section: Discussionmentioning

confidence: 77%

Section: Introductionmentioning

confidence: 99%

Presence of Spodoptera frugiperda Multiple Nucleopolyhedrovirus (SfMNPV) Occlusion Bodies in Maize Field Soils of Mesoamerica

Williams¹,

Melo-Molina²,

Jiménez-Fernández³

et al. 2023

Insects

Self Cite

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“…After ingestion by insects, occlusion bodies are dissolved in the alkaline midgut, and the released virions initiate the infestation through epithelial cells before contaminating the entire organism. Soils represent the most important reservoirs of occlusion bodies and are crucial environmental compartments involved in the control of insects completing a part of their life cycle under the soil surface [27]. The high diversity within baculovirus results from a long coevolution with insects and has led to narrow host specificity [28].…”

Section: Virusesmentioning

confidence: 99%

“…Indeed, earthworms have been shown to provide an ideal alternative prey for Pterostichus melanarius beetles when pest numbers are too low, and set them ready to switch back to feeding on arthropod pests when they become available [119]. Additionally, it was suggested that earthworms might function as a vector of insect pathogenic fungi [91] as well as dispersal agents of baculovirus occlusion bodies in the soil [27]. Therefore, earthworms not only enhance soil nutrient composition and subsequent plant growth [133], but could also indirectly facilitate pest control of root pest by natural enemies.…”

Section: Synergies Between Different Bio-control Agentsmentioning

confidence: 99%

Biological Control beneath the Feet: A Review of Crop Protection against Insect Root Herbivores

Kergunteuil

Bakhtiari

Formenti

et al. 2016

Insects

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Sustainable agriculture is certainly one of the most important challenges at present, considering both human population demography and evidence showing that crop productivity based on chemical control is plateauing. While the environmental and health threats of conventional agriculture are increasing, ecological research is offering promising solutions for crop protection against herbivore pests. While most research has focused on aboveground systems, several major crop pests are uniquely feeding on roots. We here aim at documenting the current and potential use of several biological control agents, including micro-organisms (viruses, bacteria, fungi, and nematodes) and invertebrates included among the macrofauna of soils (arthropods and annelids) that are used against root herbivores. In addition, we discuss the synergistic action of different bio-control agents when co-inoculated in soil and how the induction and priming of plant chemical defense could be synergized with the use of the bio-control agents described above to optimize root pest control. Finally, we highlight the gaps in the research for optimizing a more sustainable management of root pests.

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“…Although baculoviruses are inactivated by sunlight exposure over several days [23] or even several hours [24] (Akhanaev et al, 2017), they can survive as OBs for a long time under shaded conditions [25][26][27][28]. OBs can remain in bark crevices or soil [29] and are carried underground by abiotic factors such as rainfall, or biotic factors such as earthworms [30][31][32][33][34]. Therefore, we hypothesized that LdMNPV in soil protected from sunlight could be an important source of inoculum for L. dispar during the cyclic outbreak at intervals of approximately 10 years.…”

Section: Introductionmentioning

confidence: 99%

Persistence and genetic diversity of Lymantria dispar multiple nucleopolyhedrovirus in soil during an epizootic

Sato

Takashima

Pavlushin

et al. 2022

Preprint

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Lymantria dispar (gypsy moth), one of the most destructive forest pests, causes periodic outbreaks culminating with an epizootic of the baculovirus L. dispar multiple nucleopolyhedrovirus (LdMNPV). However, the source and mode of LdMNPV infection remain unclear. To examine whether LdMNPV in the soil acts as an inoculum source for an epizootic, we performed DNA analyses and bioassays using samples collected in Yamanashi, Japan. In the study area, L. dispar outbreak began in 2019 and an LdMNPV epizootic occurred in 2020. Using purified occlusion bodies (OBs), the LC50 value of the droplet-feeding bioassay was 1.9 × 105 OBs/mL and that of the soil-feeding bioassay was 6.4 × 104 OBs/mL. PCR assay could detect purified OBs dose-dependently but not soil-mixed OBs. Soil-feeding bioassays using field-collected soils and PCR assay revealed that LdMNPV OBs maintained their biological potency and were estimated to be approximately 104 OBs/g soil. Larvae fed soil from after the epizootic showed a significant lower survival rate than ones fed soil from before the epizootic. DNA sequencing showed increased LdMNPV genetic diversity in the same locality and a single host during the epizootic, suggesting the migration of LdMNPV-infected larvae into the study site. Furthermore, a few identical LdMNPV haplotype were dominant during the epizootic, and the pathogenicity such as mortality rate and the OBs yields did not significantly differ between the LdMNPV isolates. These results suggest that LdMNPV in the soil is an important source of inoculum infecting L. dispar.

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Earthworm mediated dispersal of baculovirus occlusion bodies: Experimental evidence from a model system

Cited by 14 publications

References 41 publications

Presence of Spodoptera frugiperda Multiple Nucleopolyhedrovirus (SfMNPV) Occlusion Bodies in Maize Field Soils of Mesoamerica

Presence of Spodoptera frugiperda Multiple Nucleopolyhedrovirus (SfMNPV) Occlusion Bodies in Maize Field Soils of Mesoamerica

Biological Control beneath the Feet: A Review of Crop Protection against Insect Root Herbivores

Persistence and genetic diversity of Lymantria dispar multiple nucleopolyhedrovirus in soil during an epizootic

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