Assessment of Entomopathogenic Nematodes in Oil Emulsions to Control Scyphophorus acupunctatus in Agave under Laboratory Conditions
Abstract
:1. Introduction
2. Materials and Methods
2.1. Survival of Entomopathogenic Nematodes in Oil Emulsions
2.2. Mortality of Scyphophorus acupunctatus Caused by Nematodes in Oil Emulsions
2.3. Statistical Analysis
3. Results and Discussion
3.1. Survival of Entomopathogenic Nematodes Formulated in Oils
3.2. Mortality of Scyphophorus acupunctatus and Emergence of Nematodes Adhered to Oils
3.3. Emergence of Nematodes in Galleria Mellonella Larvae
4. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Servicio de Información Agroalimentario y Pesquera (SIAP). Available online: https://nube.siap.gob.mx/cierreagricola/ (accessed on 26 September 2023).
- Aquino-Bolaños, T.; Ortiz-Hernández, Y.D.; Martiínez-Gutiérrez, G.A. Relationship between Scyphophorus acupunctatus Gyllenhal Damage and Nutrient and Sugar Content of Agave angustifolia Haw. Southwest. Entomol. 2013, 38, 477–486. [Google Scholar] [CrossRef]
- Aquino-Bolaños, T.; Ortiz-Hernández, Y.D.; Bautista-Cruz, A.; Acevedo-Ortiz, M.A. Viability of Entomopathogenic Fungi in Oil Suspensions and Their Effectiveness against the Agave Pest Scyphophorus acupunctatus under Laboratory Conditions. Agronomy 2023, 13, 1468. [Google Scholar] [CrossRef]
- Terán-Vargas, A.P.; Azuara-Domínguez, A.; Vega-Aquino, P.; Zambrano-Gutiérrez, J.; Blanco-Montero, C. Biological Effectivity of Insecticides to Control the Agave Weevil, Scyphophorus acupunctatus Gyllenhal (Coleoptera: Curculionidae), in Mexico. Southwest. Entomol. 2012, 37, 47–53. [Google Scholar] [CrossRef]
- Nurashikin-Khairuddin, W.; Abdul-Hamid, S.N.A.; Mansor, M.S.; Bharudin, I.; Othman, Z.; Jalinas, J. A Review of Entomopathogenic Nematodes as a Biological Control Agent for Red Palm Weevil, Rhynchophorus ferrugineus (Coleoptera: Curculionidae). Insects 2022, 13, 245. [Google Scholar] [CrossRef]
- Miles, C.; Blethen, C.; Gaugler, R.; Shapiro-Ilan, D.; Murray, T. Using Entomopathogenic Nematodes for Crop Insect Pest Control. Available online: https://www.researchgate.net/profile/Randy-Gaugler/publication/263444652_Using_beneficial_nematodes_for_crop_insect_pest_control/links/0046353ad890787049000000/Using-beneficial-nematodes-for-crop-insect-pest-control.pdf (accessed on 10 November 2023).
- Rehman, G.; Mamoon-Ur-Rashid, M. Evaluation of Entomopathogenic Nematodes against Red Palm Weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Insects 2022, 13, 733. [Google Scholar] [CrossRef]
- Klein, M.G. Efficacy Against Soil-Inhabiting Insect Pests. In Entomopathogenic Nematodes in Biological Control; Gaugler, R., Ed.; CRC Press: Boca Raton, FL, USA, 1990; pp. 195–214. ISBN 978-1-351-07174-1. [Google Scholar]
- Poinar, G.O.; Hom, A. Survival and Horizontal Movement of Infective Stage Neoaplectana carpocapsae in the Field. J. Nematol. 1986, 18, 34–36. [Google Scholar]
- Tamez-Guerra, P.; Rodríguez-Padilla, C.; Galán-Wong, L. Solar Radiation (UV) Protectants for Microbial Insecticides. In Semiochemicals in Pest and Weed Control; ACS: Washington, DC, USA, 2005; pp. 127–147. ISBN 978-0-8412-3888-6. [Google Scholar]
- Shapiro-Ilan, D.I.; Han, R.; Dolinksi, C. Entomopathogenic Nematode Production and Application Technology. J. Nematol. 2012, 44, 206–217. [Google Scholar]
- Batta, Y.A. Invert Emulsion: Method of Preparation and Application as Proper Formulation of Entomopathogenic Fungi. MethodsX 2016, 3, 119. [Google Scholar] [CrossRef]
- Shapiro, M.; McLane, W.; Belli, R. Laboratory Evaluation of Selected Chemicals as Antidesiccants for the Protection of the Entomogenous Nematode, Steinernema feltiae (Rhabditidae: Steinernematidae), Against Lymantria dispar (Lepidoptera: Lymantriidae). J. Econ. Entomol. 1985, 78, 1437–1441. [Google Scholar] [CrossRef]
- Castruita-Esparza, G.; Bueno-Pallero, F.Á.; Blanco-Pérez, R.; Dionísio, L.; Aquino-Bolaños, T.; Campos-Herrera, R. Activity of Steinernema colombiense in Plant-Based Oils. J. Nematol. 2020, 52, 1–12. [Google Scholar] [CrossRef]
- Molina-Acevedo, J.P.; López-Nuñez, J. Supervivencia y Parasitismo de Nematodos Entomopatógenos Para El Control de Hypothenemus hampei Ferrari, (Coleoptera: Scolytidae) En Frutos de Café. Bol. Sanid. Veg. Plagas 2003, 29, 523–534. [Google Scholar]
- San-Blas, E.; Campos-Herrera, R.; Dolinski, C.; Monteiro, C.; Andaló, V.; Leite, L.G.; Rodríguez, M.G.; Morales-Montero, P.; Sáenz-Aponte, A.; Cedano, C.; et al. Entomopathogenic Nematology in Latin America: A Brief History, Current Research and Future Prospects. J. Invertebr. Pathol. 2019, 165, 22–45. [Google Scholar] [CrossRef]
- Kaya, H.; Stock, P. Techniques in Insect Nematology. In Manual of Techniques in Insect Pathology; Lacey, L.A., Ed.; Academic Press: Cambridge, CA, USA, 1997; pp. 281–324. ISBN 978-0-12-432555-5. [Google Scholar]
- SAS. SAS/ETS 9.1 User’s Guide; SAS Institute Inc.: Cary, NC, USA, 2004; ISBN 1-59047-244-6. [Google Scholar]
- Krishnayyaand, P.V.; Grewal, P.S. Effect of Neem and Selected Fungicides on Viability and Virulence of the Entomopathogenic Nematode Steinernema feltiae. Biocontrol Sci. Technol. 2002, 12, 259–266. [Google Scholar] [CrossRef]
- Vashisth, S.; Chandel, Y.S.; Sharma, P. Entomopathogenic Nematodes—A Review. Agric. Rev. 2013, 34, 163. [Google Scholar] [CrossRef]
- Gaugler, R. Entomopathogenic Nematodes in Biological Control; CRC Press: Boca Raton, FL, USA, 2017; ISBN 978-1-351-07174-1. [Google Scholar]
- Aquino-Bolaños, T.; Ruiz-Vega, J.; Iparraguirre-Cruz, M. Control Biológico Del Picudo Negro (Scyphophorus interstitialis Gyllenhal) Con Nemátodos y Hongos Entomopatógenos En Agave En Oaxaca, México. Rev. Cient. UDO Agric. 2006, 6, 92–101. [Google Scholar]
- Naranjo, N.; Montero, D.A.; Sáenz-Aponte, A. Primer Reporte de Patogenicidad Por Nemátodos Entomopatógenos Sobre La Chinche de Los Pastos. Entomotropica 2011, 26, 117–125. [Google Scholar]
- Monteiro, C.M.O.; Araújo, L.X.; Gomes, G.A.; Senra, T.O.S.; Calmon, F.; Daemon, E.; De Carvalho, M.G.; Bittencourt, V.R.E.P.; Furlong, J.; Prata, M.C.D.A. Entomopathogenic Nematodes Associated with Essential Oil of Lippia Sidoides for Control of Rhipicephalus microplus (Acari: Ixodidae). Parasitol. Res. 2014, 113, 189–195. [Google Scholar] [CrossRef]
- Webster, J.M.; Bronskill, J.F. Use of Gelgard M and an Evaporation Retardant to Facilitate Control of Larch Sawfly by a Nematode-Bacterium Complex1. J. Econ. Entomol. 1968, 61, 1370–1373. [Google Scholar] [CrossRef]
- Koppenhöfer, A.; Grewal, P. Compatibility and Interactions with Agrochemicals and Other Biocontrol Agents. In Nematodes as Biocontrol Agent; CABI Publishing: Wallingford, UK, 2005; pp. 363–381. ISBN 0-85199-017-7. [Google Scholar]
- Kaya, H.; Gaugler, R. Entomopathogenic Nematodes. Annu. Rev. Entomol. 1993, 38, 181–206. [Google Scholar] [CrossRef]
- Dillman, A.R.; Chaston, J.M.; Adams, B.J.; Ciche, T.A.; Goodrich-Blair, H.; Stock, S.P.; Sternberg, P.W. An Entomopathogenic Nematode by Any Other Name. PLOS Pathog. 2012, 8, e1002527. [Google Scholar] [CrossRef]
- Lewis, E.; Clarke, D. Nematode Parasites and Entomopathogens. In Insect Pathology; Vega, F.E., Kaya, H.K., Eds.; Academic Press: Cambridge, CA, USA, 2011; pp. 395–424. ISBN 978-0-12-384984-7. [Google Scholar]
- Grewal, P.S.; Matsuura, M.; Converse, V. Mechanisms of Specificity of Association between the Nematode Steinernema scapterisci and Its Symbiotic Bacterium. Parasitology 1997, 114 Pt 5, 483–488. [Google Scholar] [CrossRef]
- Ehlers, R.U. Mass Production of Entomopathogenic Nematodes for Plant Protection. Appl. Microbiol. Biotechnol. 2001, 56, 623–633. [Google Scholar] [CrossRef] [PubMed]
- Burman, M.; Pye, A.E. Neoaplectana carpocapsae: Respiration of Infective Juveniles. Nematologica 1980, 26, 214–219. [Google Scholar] [CrossRef]
- Friedman, M.J. Commercial Production and Development. In Entomopathogenic Nematodes in Biological Control; CRC Press: Boca Raton, FL, USA, 1990; ISBN 978-1-351-07174-1. [Google Scholar]
- Sáenz-Aponte, A.; Olivares, W. Searching Capacity of the Entomopathogenic Nematode Steinernema Sp. SNIO 198 (Rhabditida: Steinernematidae). Rev. Colomb. Entomol. 2008, 34, 51–56. [Google Scholar] [CrossRef]
- Boff, M.I.C.; Wiegers, G.L.; Gerritsen, L.J.M.; Smits, P.H. Development of the Entomopathogenic Nematode Heterorhabditis megidis Strain NLH-E 87.3 in Galleria Mellonella. Nematology 2000, 2, 303–308. [Google Scholar] [CrossRef]
- Grewal, P.; Georgis, R. Entomopathogenic Nematodes. In Biopesticides: Use and Delivery; Hall, F.R., Menn, J.J., Eds.; Methods in Biotechnology; Humana Press: Totowa, NJ, USA, 1999; pp. 271–299. ISBN 978-1-59259-483-2. [Google Scholar]
Treatment | Concentration (%) | Nematode | Treatment | Concentration (%) | Nematode |
---|---|---|---|---|---|
T1 DW (absolute control) | 0 | H. bacteriophora | T12 T. vulgare | 20 | S. glaseri |
T2 DW (absolute control) | 0 | S. carpocapsae | T13 T. vulgare | 40 | H. bacteriophora |
T3 DW (absolute control) | 0 | S. glaseri | T14 T. vulgare | 40 | S. carpocapsae |
T4 S. hispanica | 20 | H. bacteriophora | T15 T. vulgare | 40 | S. glaseri |
T5 S. hispanica | 20 | S. carpocapsae | T16 O. europea | 20 | H. bacteriophora |
T6 S. hispanica | 20 | S. glaseri | T17 O. europea | 20 | S. carpocapsae |
T7 S. hispanica | 40 | H. bacteriophora | T18 O. europea | 20 | S. glaseri |
T8 S. hispanica | 40 | S. carpocapsae | T19 O. europea | 40 | H. bacteriophora |
T9 S. hispanica | 40 | S. glaseri | T20 O. europea | 40 | S. carpocapsae |
T10 T. vulgare | 20 | H. bacteriophora | T21 O. europea | 40 | S. glaseri |
T11 T. vulgare | 20 | S. carpocapsae |
Treatment | Concentration (%) | Nematode | Time (h) | ||||
---|---|---|---|---|---|---|---|
24 | 48 | 72 | 96 | 120 | |||
T1 DW (absolute control) | 0 | H. bacteriophora | 100.0 ± 0.0 a | 71.2 ± 2.0 bc | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 d |
T2 DW (absolute control) | 0 | S. carpocapsae | 100.0 ± 0.0 a | 81.6 ± 1.7 b | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 d |
T3 DW (absolute control) | 0 | S. glaseri | 100.0 ± 0.0 a | 70.8 ± 2.0 c | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 d |
T4 S. hispanica | 20 | H. bacteriophora | 56.4 ± 1.5 c | 26.8 ± 2.8 e | 12.6 ± 1.0 e | 9.6 ±0.9 e | 3.2 ± 0.2 d |
T5 S. hispanica | 20 | S. carpocapsae | 47.6 ± 2.0 e | 17.6 ± 1.3 e | 14 ± 1.2 e | 12.8 ± 1.0 e | 0.0 ± 0.0 d |
T6 S. hispanica | 20 | S. glaseri | 88.4 ± 3.3 b | 78.6 ± 2.3 b | 47.8 ± 3.7 c | 46.2 ±3.3 b | 41.2 ± 3.0 bc |
T7 S. hispanica | 40 | H. bacteriophora | 67.6 ± 2.8 c | 57.4 ± 1.5 c | 44.4 ± 3.4 c | 32 ± 3.2 bc | 14 ± 1.2 d |
T8 S. hispanica | 40 | S. carpocapsae | 82.4 ± 1.7 b | 78.8 ± 2.3 b | 58.8 ± 1.5 b | 42.4 ± 3.2 b | 32.4 ±3.1 c |
T9 S. hispanica | 40 | S. glaseri | 88.8 ± 3.3 b | 79.6 ± 2.4 b | 49.6 ± 3.9 c | 35.6 ± 3.6 bc | 30 ± 3.1 c |
T10 T. vulgare | 20 | H. bacteriophora | 84.8 ± 1.8 b | 74.6 ± 2.2 b | 46.2 ± 3.6 c | 29.4 ± 1.8 bc | 15.4 ± 1.2 d |
T11 T. vulgare | 20 | S. carpocapsae | 88.4 ± 3.3 b | 73.2 ± 2.2 b | 63.4 ± 2.5 ab | 55 ± 1.5 ab | 38 ± 3.7 c |
T12 T. vulgare | 20 | S. glaseri | 74.4 ± 2.2 bc | 64.6 ± 2.5 bc | 31.8 ± 3.2 cd | 20.8 ± 2.0 c | 10 ± 0.9 e |
T13 T. vulgare | 40 | H. bacteriophora | 90.6 ± 2.6 a | 80.2 ± 1.6 b | 73.8 ± 2.2 b | 50.8 ± 1.7 ab | 35.2 ± 3.6 d |
T14 T. vulgare | 40 | S. carpocapsae | 82.4 ± 1.7 b | 72.4 ± 2.1 bc | 54 ± 1.5 b | 42 ± 3.2 b | 30.8 ± 3.1 c |
T15 T. vulgare | 40 | S. glaseri | 82.8 ± 1.7 b | 72.8 ± 2.1 b | 66.8 ± 2.8 ab | 54 ±1.4 ab | 41.2 ± 3.0 bc |
T16 O. europea | 20 | H. bacteriophora | 96.2 ± 2.6 a | 86.2 ± 1.9 ab | 44.8 ± 3.2 c | 20.4 ± 2.0 c | 12.8 ± 1.0 e |
T17 O. europea | 20 | S. carpocapsae | 90.8 ± 2.6 a | 80.8 ± 1.6 ab | 35.6 ± 3.6 cd | 33.2 ± 3.2 e | 30 ± 3.1 c |
T18 O. europea | 20 | S. glaseri | 96 ± 2.0 a | 86 ± 1.8 ab | 63.6 ± 2.5 ab | 50.8 ± 2.1 ab | 42.4 ± 3.1 bc |
T19 O. europea | 40 | H. bacteriophora | 90.4 ± 2.6 a | 80 ± 1.6 ab | 42 ± 3.0 c | 29.6 ± 2.6 c | 17.2 ± 1.3 d |
T20 O. europea | 40 | S. carpocapsae | 96 ± 2.0 a | 86.4 ± 1.9 ab | 76.4 ± 2.3 a | 68.4 ±2.8 a | 62.2 ± 2.4 a |
T21 O. europea | 40 | S. glaseri | 95.2 ± 1.9 a | 85.8 ± 1.8 ab | 40.8 ± 3.0 c | 20.8 ± 2.0 c | 12.7 ± 1.0 c |
Treatment (40%) | Time (h) | |||||
---|---|---|---|---|---|---|
48 | 72 | 96 | 120 | 144 | 168 | |
T1 S. glaseri 50 ± 5 nematodes + T. vulgare | 20 ± 2.4 b | 30 ± 3.8 bc | 50 ± 1.6 b | 80 ± 1.5 ab | 80 ± 1.5 b | 90 ± 2.7 a |
T2 S. glaseri 100 ± 10 nematodes + T. vulgare | 30 ± 3.8 ab | 50 ± 1.6 b | 70 ± 2.4 bc | 70 ± 2.4 b | 90 ± 2.7 a | 90 ± 2.7 a |
T3 S. glaseri 50 ± 5 nematodes + O. europea | 50 ± 1.6 a | 70 ± 2.4 ab | 80 ± 1.5 ab | 80 ± 1.5 ab | 90 ± 2.7 a | 100.0 ± 0.0 a |
T4 S. glaseri 100 ± 10 nematodes + O. europea | 50 ± 1.6 a | 90 ± 2.7 a | 90 ± 2.7 a | 100.0 ± 0.0 a | 100.0 ± 0.0 a | 100.0 ± 0.0 a |
T5 H. bacteriophora 50 ± 5 nematodes + T. vulgare | 20 ± 2.4 b | 50 ± 1.6 b | 70 ± 2.4 ab | 80 ± 1.5 a | 90 ± 2.7 a | 90 ± 2.7 a |
T6 H. bacteriophora 100 ± 10 nematodes + T. vulgare | 20 ± 2.4 b | 40 ± 3.9 bc | 70 ± 2.4 bc | 70 ± 2.4 b | 70 ± 2.4 bc | 80 ± 1.5 b |
T7 H. bacteriophora 50 ± 5 nematodes + O. europea | 50 ± 1.6 a | 70 ± 2.4 ab | 70 ± 2.4 bc | 90 ± 2.7 a | 100.0 ± 0.0 a | 100.0 ± 0.0 a |
T8 H. bacteriophora 100 ± 10 nematodes + O. europea | 50 ± 1.6 a | 70 ± 2.4 ab | 90 ± 2.7 a | 100 ± 0.0 a | 100.0 ± 0.0 a | 100.0 ± 0.0 a |
T9 DW (absolute control) | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 c | 0.0 ± 0.0 c | 0.0 ± 0.0 c |
T10 Triticum vulgare (positive control) | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 c | 0.0 ± 0.0 c | 0.0 ± 0.0 c |
T11 Olea europea (positive control) | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 d | 0.0 ± 0.0 c | 0.0 ± 0.0 c | 0.0 ± 0.0 c |
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Ahedo-Quero, H.O.; Ortiz-Hernández, Y.D.; Aquino-Bolaños, T.; Acevedo-Ortiz, M.A. Assessment of Entomopathogenic Nematodes in Oil Emulsions to Control Scyphophorus acupunctatus in Agave under Laboratory Conditions. Agronomy 2023, 13, 2946. https://doi.org/10.3390/agronomy13122946
Ahedo-Quero HO, Ortiz-Hernández YD, Aquino-Bolaños T, Acevedo-Ortiz MA. Assessment of Entomopathogenic Nematodes in Oil Emulsions to Control Scyphophorus acupunctatus in Agave under Laboratory Conditions. Agronomy. 2023; 13(12):2946. https://doi.org/10.3390/agronomy13122946
Chicago/Turabian StyleAhedo-Quero, Hector Osvaldo, Yolanda Donají Ortiz-Hernández, Teodulfo Aquino-Bolaños, and Marco Aurelio Acevedo-Ortiz. 2023. "Assessment of Entomopathogenic Nematodes in Oil Emulsions to Control Scyphophorus acupunctatus in Agave under Laboratory Conditions" Agronomy 13, no. 12: 2946. https://doi.org/10.3390/agronomy13122946