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Long-term storage does not affect the infectivity of entomopathogenic nematodes on insect hosts

  • Environmental Biotechnology
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Abstract

Entomopathogenic nematodes (EPNs) are effective biopesticides used in insect control. There are several formulations of entomopathogenic nematodes which are commercially available, but their popularity is low because the requirement of periodic release of stored entomopathogenic nematodes in field has reduced infectivity and is a constraint in large-scale repeated application of entomopathogenic nematodes in field. So, in order to overcome this impediment, the current study focuses on storage of entomopathogenic nematodes for a longer period of time using encapsulating beads. In this study, three EPNs, namely, Steinernema carpocapsae, Steinernema monticolum, and Rhabditis blumi, were encapsulated with Arabic gum and sodium alginate gel beads at different concentrations. Bio-efficacy of stored EPNs at different concentrations (50, 100, 200, 500, and 1000 infective juveniles (IJs)) in varying time intervals of 3, 6, 9, and 12 weeks were tested against Culex quinquefasciatus larvae. The results show that, after 3 weeks of storage, these entomopathogenic nematode species showed survival up to 96%, and in 12-week storage, survival rate was 50%. The virulence of the progeny that emerged from these stored entomopathogenic nematodes was similar to the fresh infective juveniles. The results of the present study show that Arabic gum–sodium alginate combination is a promising approach toward storing entomopathogenic nematodes. Furthermore, semi-field trials showed 70–90% larval mortality at a concentration of 3000 IJs (encapsulated and stored entomopathogenic nematodes in S. monticolum, S. carpocapsae, and R. blumi) on C. quinquefasciatus larvae.

Key points

• Increased survival of stored EPNs (S. carpocapsae, S. monticolum, and R. blumi) in encapsulated gel using Arabic gum, sodium alginate, and yeast cells was assessed.

• The efficacy was greater in stored EPNs at different concentrations from 3 to 12 weeks.

• Semi-field trials of stored encapsulated EPNs are efficient in mosquito larval control.

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Data availability

The data will be made available on reasonable request.

References

  • Alkenani NA, Al-Ghamdi KHM, Saleh MS, Mahyuob JA (2015) Semi-field evaluation of some slow-release insecticide formulation against the dengue mosquito Aedes aegypti (L). Alex Sci Exch J 36:157–162. https://doi.org/10.1016/j.sjbs.2018.06.006

    Article  CAS  Google Scholar 

  • Castillo JC, Reynolds SE, Eleftherianos I (2011) Insect immune responses to nematode parasites. Trends Parasitol 27:537–547. https://doi.org/10.1016/j.pt.2011.09.001

    Article  CAS  Google Scholar 

  • Chen S, Glazer I (2005) A novel method for long-term storage of the entomopathogenic nematode Steinernema feltiae at room temperature. Biol Control 32:104–110. https://doi.org/10.1016/j.biocontrol.2004.08.006

    Article  CAS  Google Scholar 

  • Cagnolo SR, Almiron WL (2017) Capacity of the terrestrial entomopathogenic nematode Steinernema rarum (Rhabditida: Steinernematidae) to parasite Culex apicinus larvae (Diptera: Culicidae). Rev Soc Entomol Arge 69:1–2

    Google Scholar 

  • Dilipkumar A, Ramalingam KR, Chinnaperumal K, Govindasamy B, Paramasivam D, Dhayalan A, Pachiappan P (2019) Isolation and growth inhibition potential of entomopathogenic nematodes against three public health important mosquito vectors. Exp Parasitol 197:76–84. https://doi.org/10.1016/j.exppara.2018.11.001

    Article  Google Scholar 

  • Devi G (2019) Interaction between entomopathogenic nematodes and entomopathogenic fungi in biocontrol mechanism. J EntomolZool Stud 7:959–964

    Google Scholar 

  • Eivazian Kary N, Chahardoli S, Mohammadi D, Dillon AB (2018) Effects of abiotic factors on the osmotic response of alginate-formulated entomopathogenic nematode, Heterorhabditis bacteriophora (Nematoda: Rhabditida). Biocontrol Sci Technol 28:688–701. https://doi.org/10.1080/09583157.2018.1479731

    Article  Google Scholar 

  • Eleftherianos I, Clarke DJ, Dowling AJ, Reynolds SE (2010) Dissecting the immune response to the entomopathogen Photorhabdus. Trends Microbiol 18:552–560. https://doi.org/10.1016/j.tim.2010.09.006

    Article  CAS  Google Scholar 

  • Ehlers RU, Premachandra D, Berndt O, Poehling HM, Borgemeister C (2003) Laboratory bioassays of virulence of entomopathogenic nematodes against soil-inhabiting stages of Frankliniella occidentalis Pergande (Thysanoptera: Thripidae). Nematology 5:539–547

    Article  Google Scholar 

  • Ferreira T, Malan AP (2014) Potential of entomopathogenic nematodes for the control of the banded fruit weevil, Phlyctinus callosus (Schonherr) (Coleoptera: Curculionidae). J Helminthol 88:293–301. https://doi.org/10.1017/S0022149X13000175

    Article  CAS  Google Scholar 

  • Georgis R (1990) Formulation and application technology. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, FL, pp 173–194

    Google Scholar 

  • Grewal PS, Wang X, Taylor RAJ (2002) Dauer juvenile longevity and stress tolerance in natural populations of entomopathogenic nematodes: is there a relationship? Int J Parasitol 32:717–725. https://doi.org/10.1016/S0020-7519(02)00029-2

    Article  CAS  Google Scholar 

  • Gaugler R, Boush GM (1978) Effects of ultraviolet radiation and sunlight on the entomogenous nematode, Neoaplectana carpocapsae. J Invertebr Pathol 32:291–296. https://doi.org/10.1016/0022-2011(78)90191-X

    Article  Google Scholar 

  • Heriberto CM, Jaime RV, Carlos CM, Jesusita RD (2017) Formulation of entomopathogenic nematodes for crop pest control–a review. Plant Protect Sci 53:15–24. https://doi.org/10.17221/35/2016-PPS

    Article  Google Scholar 

  • Hiltpold I, Hibbard BE, French BW, Turlings TC (2012) Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the western corn rootworm. Plant Soil 358:11–25. https://doi.org/10.1007/s11104-012-1253-0

    Article  CAS  Google Scholar 

  • Hussein MA, Abdel-Aty MA (2012) Formulation of two native entomopathogenic nematodes at room temperature. J Biopestici 5:23–27

    CAS  Google Scholar 

  • Jaffuel G, Sbaiti I, Turlings TC (2020) Encapsulated entomopathogenic nematodes can protect maize plants from Diabrotica balteata larvae. Insects 11:27. https://doi.org/10.3390/insects11010027

    Article  Google Scholar 

  • Kapranas A, Sbaiti I, Degen T, Turlings TC (2020) Biological control of cabbage fly Delia radicum with entomopathogenic nematodes: selecting the most effective nematode species and testing a novel application method. Biol Cont 144:104212. https://doi.org/10.1016/j.biocontrol.2020.104212

    Article  CAS  Google Scholar 

  • Kusakabe A, Peterson BF, Orduño BR, Stock SP (2019) Ecological characterization of Heterorhabditis sonorensis (Caborca strain) (Nematoda: Heterorhabditidae), an entomopathogenic nematode from the Sonoran desert. Zoology 135:125689. https://doi.org/10.1016/j.zool.2019.05.001

    Article  Google Scholar 

  • Kim J, Jaffuel G, Turlings TC (2015) Enhanced alginate capsule properties as a formulation of entomopathogenic nematodes. Bio Control 60:527–535. https://doi.org/10.1007/s10526-014-9638-z

    Article  CAS  Google Scholar 

  • Kaya HK, Nelsen CE (1985) Encapsulation of steinernematid and heterorhabditid nematodes with calcium alginate: a new approach for insect control and other applications. Environ Entomol 14:572–574. https://doi.org/10.1093/ee/14.5.572

    Article  Google Scholar 

  • Lang AE, Schmidt G, Sheets JJ, Aktories K (2011) Targeting of the actin cytoskeleton by insecticidal toxins from Photorhabdus luminescens. N-S Arch Pharmacol 383:227–235. https://doi.org/10.1007/s00210-010-0579-5

    Article  CAS  Google Scholar 

  • Lee YW, Zairi J, Yap HH, Adanan CR (2005) Integration of Bacillus thuringiensis H-14 formulations and pyriproxyfen for the control of larvae of Aedes aegypti and Aedes albopictus. J Am Mosquito Contr 21:84–89. https://doi.org/10.2987/8756-971X(2005)21[84:IOBTHF]2.0.CO;2

    Article  CAS  Google Scholar 

  • Mbata GN, Ivey C, Shapiro-Ilan D (2018) The potential for using entomopathogenic nematodes and fungi in the management of the maize weevil, Sitophilus zeamais (Motschulsky) (Coleoptera: Curculionidae). Biol Control 125:39–43. https://doi.org/10.1016/j.biocontrol.2018.06.008

    Article  Google Scholar 

  • Mohiddin A, Lasim AM, Zuharah WF (2016) Susceptibility of Aedes albopictus from dengue outbreak areas to temephos and Bacillus thuringiensis subsp israelensis. Asian Pac J Trop Biomed 6:295–300. https://doi.org/10.1016/j.apjtb.2016.01.006

    Article  CAS  Google Scholar 

  • Maiwald M, Ditton HJ, Sonntag HG, von Knebel DM (1994) Characterization of contaminating DNA in Taq polymerase which occurs during amplification with a primer set for Legionella 5S ribosomal RNA. Mol Cell Probe 8:11–14. https://doi.org/10.1006/mcpr.1994.1002

    Article  CAS  Google Scholar 

  • Niknam G, Kary NE, Nikdel M, Griffin C (2010) Diversity of entomopathogenic nematodes (Nematoda: Steinernematidae, Heterorhabditidae) from Arasbaran forests and range lands in north-west Iran. Nematology 12:767773

    Google Scholar 

  • Navon A, Keren S, Salame L, Glazer I (1998) An edible-to-insects calcium alginate gel as a carrier for entomopathogenic nematodes. Biocontrol Sci Technol 8:429–437

    Article  Google Scholar 

  • Orozco RA, Lee MM, Stock SP (2014) Soil sampling and isolation of entomopathogenic nematodes (Steinernematidae, Heterorhabditidae). JoVE- J vis Exp 89:e52083. https://doi.org/10.3791/52083

    Article  Google Scholar 

  • Pour MM, Saberi-Riseh R, Mohammadinejad R, Hosseini A (2019) Investigating the formulation of alginate-gelatin encapsulated Pseudomonas fluorescens (VUPF5 and T17–4 strains) for controlling Fusarium solani on potato. Int J Biol Macromol 133:603–613. https://doi.org/10.1016/j.ijbiomac.2019.04.071

    Article  CAS  Google Scholar 

  • Peschiutta ML, Cagnolo SR, Almiron WR (2014) Susceptibility of larvae of Aedes aegypti (Linnaeus) (Diptera: Culicidae) to entomopathogenic nematode Heterorhabditis bacteriophora (Poinar) (Rhabditida: Heterorhabditidae). Rev Soc Entomol Arge 73:99–108

    Google Scholar 

  • Pandii W, Maharmart S, Boonchuen S, Silapanuntakul S, Somsook V (2008) Efficacy of entomopathogenic nematodes (Nematoda: Rhabditida) against Culex gelidus (Diptera: Culicidae) larvae. J Vector Born Dis 5:24–35

    Google Scholar 

  • Poinar GO Jr, Kaul HN (1982) Parasitism of the mosquito Culex pipiens by the nematode Heterorhabditis bacteriophora. J Invertebr Pathol 39:382–387. https://doi.org/10.1016/0022-2011(82)90063-5

    Article  Google Scholar 

  • Qiu LH, Lacey MJ, Bedding RA (2000) Permeability of the infective juveniles of Steinernema carpocapsae to glycerol during osmotic dehydration and its effect on biochemical adaptation and energy metabolism. Com Biochem Phys B 125:411–419

    Article  CAS  Google Scholar 

  • Shapiro-Ilan DI, Han R, Qiu X (2014) Production of entomopathogenic nematodes. Mass production of beneficial organisms. Academic Press, pp 321–355

    Chapter  Google Scholar 

  • Shapiro-Ilan DI, Han R, Dolinksi C (2012) Entomopathogenic nematode production and application technology. J Nematol 44:206–217

    Google Scholar 

  • Smallegange RC, Schmied WH, van Roey KJ, Verhulst NO, Spitzen J, Mukabana WR, Takken W (2010) Sugar-fermenting yeast as an organic source of carbon dioxide to attract the malaria mosquito Anopheles gambiae. Malar J 9:292

    Article  Google Scholar 

  • Schroer S, Ziermann D, Ehlers RU (2005) Mode of action of a surfactant–polymer formulation to support performance of the entomopathogenic nematode Steinernema carpocapsae for control of diamondback moth larvae (Plutella xylostella). Biocontrol Sci Technol 15:601–613

    Article  Google Scholar 

  • Schroer S, Ehlers RU (2005) Foliar application of the entomopathogenic nematode Steinernema carpocapsae for biological control of diamondback moth larvae (Plutella xylostella). Biol Control 33:81–86

    Article  Google Scholar 

  • Stock SP, Campbell JF, Nadler SA (2001) Phylogeny of Steinernema Travassos, 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. J Parasitol 87:877–890

    Article  CAS  Google Scholar 

  • Shapiro DI, Lewis EE (1999) Comparison of entomopathogenic nematode infectivity from infected hosts versus aqueous suspension. Environ Entomol 28:907–911

    Article  Google Scholar 

  • Simons WR, Poinar GO Jr (1973) The ability of Neoaplectana carpocapsae (Steinernematidae: Nematodea) to survive extended periods of desiccation. J Invertebr Pathol 22:228–230. https://doi.org/10.1016/0022-2011(73)90138-9

    Article  Google Scholar 

  • Tariq AM (2020) Using Rhabditis blumi Sudhaus as biological agents to control the palm borer, Arabian rhinoceros beetle, Oryctes agamemnon arabicus. Iraqi J Agric Sci 51:657–664. https://doi.org/10.36103/ijas.v51i2.993

    Article  Google Scholar 

  • Turki H, Soltani A (2017) Semi-field and field studies on the efficacy of monomolecular surface film (Agnique®) against immature mosquitoes in the malarious areas of Iran. Asian Pac J Trop Dis 7:472–476. https://doi.org/10.12980/apjtd.7.2017D7-69

    Article  Google Scholar 

  • Tunholi VM, Lorenzoni PO, da Silva YH, Tunholi-Alves VM, Boeloni JN, da Silva MA, Martins F IV (2017) Molluscicidal potential of Heterorhabditis baujardi (Rhabditida: Heterorhabditidae), strain LPP7, on Lymnaea columella (Gastropoda: Pulmonata): an alternative for biological control of fasciolosis. Acta Trop 173:23–29. https://doi.org/10.1016/j.actatropica.2017.05.024

    Article  Google Scholar 

  • Tandina F, Doumbo O, Traoré SF, Robert PP, V, (2018) Mosquitoes (Diptera: Culicidae) and mosquito-borne diseases in Mali, West Africa. Parasit Vector 11:1–12. https://doi.org/10.1186/s13071-018-3045-8

    Article  Google Scholar 

  • Welch HE, Bronskill JF (1962) Parasitism of mosquito larvae by the nematode, DD136 (Nematoda: Neoaplectanidae). Can J Zool 40(7):1263–1268. https://doi.org/10.1139/z62-102

    Article  Google Scholar 

  • White GF (1927) A method for obtaining infective nematode larvae from cultures. Sci (Washington) 66(1709):302. https://doi.org/10.1126/science.66.1709.302.b

    Article  CAS  Google Scholar 

  • Zorrilla CD, Rivera-Vinas JI, De La Vega-Pujols A, Garcia-Garcia I, Rabionet SE, Mosquera AM (2018) The Zika virus infection in pregnancy: review and implications for research and care of women and infants in affected areas. P R Health Sci J 37:66–72

    Google Scholar 

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Acknowledgements

The authors thank Periyar University, Salem for providing University Research Fellowship (Ref. No. PU/AD-3/URF/029836/2020). The authors also thank the Department of Biotechnology, Periyar University, Salem, Tamil Nadu, India for providing the infrastructural facility for carrying out this research work. We also acknowledge the instrument support from DST–FIST (SR/FIST/LSI-673/2016), Department of Biotechnology, Periyar University, Salem.

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Authors and Affiliations

  1. Department of Biotechnology, Molecular Entomology Laboratory, Periyar University, Salem, Tamil Nadu, India

    Kandhasamy Lalitha, Kannan Nithya, Balasubbiramaniyan Guru Bharathi & Muthugounder Subramanian Shivakumar

  2. Department of Environmental Science, School of Life Sciences, Periyar University, Salem, Tamil Nadu, 636 011, India

    Srinivasan Venkatesan

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  1. Kandhasamy Lalitha
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Contributions

KL, BGB, and KN performed laboratory work related to bioassay tests and prepared the encapsulation beads. KL and KN did data analysis. MSS and KL designed the study. MSS, KL, and SV wrote the manuscript. All authors gave approval for publication.

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Correspondence to Muthugounder Subramanian Shivakumar.

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Lalitha, K., Nithya, K., Bharathi, B.G. et al. Long-term storage does not affect the infectivity of entomopathogenic nematodes on insect hosts. Appl Microbiol Biotechnol 107, 419–431 (2023). https://doi.org/10.1007/s00253-022-12309-y

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