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Development and population dynamics of Steinernema yirgalemense (Rhabditida: Steinernematidae) and growth characteristics of its associated Xenorhabdusindica symbiont in liquid culture

Published online by Cambridge University Press:  09 July 2015

T. Ferreira ,
M.F. Addison  and
A.P. Malan
T. Ferreira
Affiliation:
Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Private Bag X1, Matieland7602, Stellenbosch, South Africa
M.F. Addison
Affiliation:
Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Private Bag X1, Matieland7602, Stellenbosch, South Africa
A.P. Malan*
Affiliation:
Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Private Bag X1, Matieland7602, Stellenbosch, South Africa
*
*Fax: +27 21 8084807 E-mail: [email protected]
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Abstract

Entomopathogenic nematodes have become a valuable addition to the range of biological control agents available for insect control. An endemic nematode, Steinernemayirgalemense, has been found to be effective against a wide range of key insect pests. The next step would be the mass production this nematode for commercial application. This requires the establishment of monoxenic cultures of both the nematode and the symbiotic bacterium Xenorhabdus indica. First-stage juveniles of S. yirgalemense were obtained from eggs, while X. indica was isolated from nematode-infected wax moth larvae. The population density of the various life stages of S. yirgalemense during the developmental phase in liquid culture was determined. The recovery of infective juveniles (IJs) to the third-stage feeding juveniles, was 67 ± 10%, reaching a maximum population density of 75,000 IJs ml− 1 on day 13 after inoculation. Adult density increased after 8 days, with the maximum female density being 4600 ml− 1 on day 15, whereas the maximum male density was 4300 ml− 1 on day 12. Growth curves for X. indica showed that the exponential phase was reached 15 h after inoculation to the liquid medium. The stationary phase was reached after 42 h, with an average of 51 × 107 colony-forming units ml− 1. Virulence tests showed a significant difference in insect mortality between in vitro- and in vivo-produced nematodes. The success obtained with the production of S. yirgalemense in liquid culture can serve as the first step in the optimizing and upscaling of the commercial production of nematodes in fermenters.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 3 , May 2016 , pp. 364 - 371
Copyright
Copyright © Cambridge University Press 2015 

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References

Akhurst, R.J. (1980) Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. Journal of General Microbiology 121, 303–309.Google Scholar
Alsaiyah, M.A.M., Ebsa, L., Zenner, A., O'Callaghan, K.M. & Griffin, C.T. (2009) Sex ratios and sex-biased infection behaviour in the entomopathogenic nematode genus Steinernema . International Journal of Parasitolology 39, 725–734.Google Scholar
Atlas, R.M. (1988) Microbiology: Fundamentals and applications. 807 pp . New York, Macmillan.Google Scholar
Aumann, J. & Ehlers, R.-U. (2001) Physico-chemical properties and mode of action of a signal from the symbiotic bacterium Photorhabdus luminescens inducing dauer juvenile recovery in the entomopathogenic nematode Heterorhabditis bacteriophora . Nematology 3, 849–853.Google Scholar
Boemare, N.E. & Akhurst, R.J. (1988) Biochemical and physiological characterization of colony from variants in Xenorhabdus (Enterobacteriaceae). Journal of General Microbiology 134, 751–756.Google Scholar
Chavarría-Hernández, N., Maciel-Vergara, G., Chavarría-Hernández, J.-C., Castro-Rosas, J., Rodríguez-Pastrana, B.-R., De la Torre-Martínez, M. & Rodríques-Hernández, A. (2011) Mass production of the entomopathogenic nematode. Steinernema carpocapsae CABA01, through the submerged monoxenic culture in two internal-loop airlift bioreactors with some geometric differences. Biochemical Engineering Journal 55, 145–153.Google Scholar
De Waal, J.Y., Malan, A.P. & Addison, M.F. (2011) Efficacy of entomopathogenic nematodes (Rhabditida: Heterorhabditidae and Steinernematidae) against codling moth, Cydia pomonella (Lepidoptera: Tortricidae) in temperate regions. Biocontrol Science and Technology 20, 489–502.Google Scholar
Efron, B. & Tibshirani, R. (1993) An introduction to the bootstrap. 456 pp . London, UK, Chapman & Hall.Google Scholar
Ehlers, R.-U. (2001) Mass production of entomopathogenic nematodes for plant protection. Applied Microbiology and Biotechnology 56, 623–633.Google Scholar
Ehlers, R.-U. & Hokkanen, H.M.T. (1996) Insect biocontrol with non-endemic entomopathogenic nematodes Steinernema and Heterorhabditis spp.: conclusions and recommendations of a combined OECD and COST workshop on scientific and regulatory policy issues. Biocontrol Science and Technology 6, 295–302.Google Scholar
Ehlers, R.-U., Lunau, S., Krasomile-Osterfeld, K. & Osterfeld, K.H. (1998) Liquid culture of the entomopathogenic nematode–bacterium-complex Heterorhabditis megidis/Photorhabdus luminescens . Biocontrol 43, 77–86.Google Scholar
Ferreira, T. & Malan, A.P. (2014) Xenorhabdus and Photorhabdus, bacterial symbionts of the entomopathogenic nematodes Steinernema and Heterorhabditis and their in vitro liquid mass culture: a review. African Entomology 22, 1–14.Google Scholar
Ferreira, T., Addison, M.F. & Malan, A.P. (2014a) In vitro liquid culture of a South African isolate of Heterorhabditis zealandica for the control of insect pests. African Entomology 22, 80–92.Google Scholar
Ferreira, T., Van Reenen, C.A., Tailliez, P., Pagé, S., Malan, A.P. & Dicks, L.M.T. (2014b) First report of the symbiotic bacterium Xenorhabdus indica associated with the entomopathogenic nematode Steinernema yirgalemense . Journal of Helminthology doi:10.1017/S0022149X14000583.Google ScholarPubMed
Frost, S. & Clarke, D. (2002) Bacteria–nematode symbiosis. pp. 57–77 in Gaugler, R. (Ed.) Entomopathogenic nematology. Wallingford, UK, CABI Publishing.Google Scholar
Gaugler, R. & Georgis, R. (1991) Culture method and efficacy of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae). Biological Control 1, 269–274.Google Scholar
Grewal, P.S., Ehlers, R.-U. & Shapiro-Ilan, D.I. (2005) Nematodes as biological control agents. 528 pp . Wallingford, UK, CABI.Google Scholar
Han, R. & Ehlers, R.-U. (1998) Cultivation of axenic Heterorhabditis spp. dauer juveniles and their response to non-specific Photorhabdus luminescens food signals. Nematologica 44, 425–435.Google Scholar
Han, R. & Ehlers, R.-U. (2000) Pathogenicity, development, and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. Journal of Invertebrate Pathology 75, 55–58.CrossRefGoogle ScholarPubMed
Hirao, A. & Ehlers, R.-U. (2009a) Influence of cell density and phase variants of bacterial symbionts (Xenorhabdus spp.) on dauer juvenile recovery and development of biocontrol nematodes Steinernema carpocapsae and S. feltiae (Rhabditida: Nematoda). Applied Microbiology and Biotechnology 84, 77–85.Google Scholar
Hirao, A. & Ehlers, R.-U. (2009b) Population dynamics of Steinernema carpocapsae and S. feltiae in liquid culture. Insect Pathogens and Insect Parasitic Nematodes 45, 353–356.Google Scholar
Hirao, A. & Ehlers, R.-U. (2010) Influence of inoculum density on population dynamics and dauer juvenile yields in liquid culture of biocontrol nematodes Steinernema carpocapsae and S. feltiae (Nematoda: Rhabditida). Applied Microbiology and Biotechnology 85, 507–515.CrossRefGoogle ScholarPubMed
Hirao, A., Ehlers, R.-U. & Strauch, O. (2010) Life cycle and population development of the entomopathogenic nematodes Steinernema carpocapsae and S. feltiae (Nematoda, Rhabditida) in monoxenic liquid culture. Nematology 12, 201–210.CrossRefGoogle Scholar
Johnigk, S.A. & Ehlers, R.-U. (1999) Juvenile development and life cycle of Heterorhabditis bacteriophora and H. indica (Nematoda: Heterorhabditidae). Nematology 1, 251–260.Google Scholar
Kaya, H.K. & Stock, S.P. (1997) Techniques in insect nematology. pp. 281–324 in Lacey, L.A. (Ed.) Manual of techniques in insect pathology. London, Academic Press.Google Scholar
Le Vieux, P.D. & Malan, A.P. (2013) The potential use of entomopathogenic nematodes to control Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). South African Journal of Enology and Viticulture 34, 296–306.Google Scholar
Lewis, E.E. (2002) Behavioural ecology. pp. 205–223 in Gaugler, R. (Ed.) Entomopathogenic nematology. Wallingford, UK, CABI.Google Scholar
Lunau, S., Stoessel, S., Schmidt-Peisker, A.J. & Ehlers, R.-U. (1993) Establishment of monoxenic inocula for scaling up in vitro cultures of the entomopathogenic nematodes Steinernema spp. and Heterorhabditis spp. Nematologica 39, 385–399.Google Scholar
Malan, A.P., Knoetze, R. & Moore, S.D. (2011) Isolation and identification of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) in citrus orchards in South Africa and their biocontrol potential against false codling moth. Journal of Invertebrate Pathology 108, 115–125.Google Scholar
Martens, E.C., Vivas, E.I., Heungens, K., Cowles, C.E. & Goodrich-Blair, H. (2004) Investigating mutualism between entomopathogenic bacteria and nematodes. Nematology monographs and perspectives (2). Proceedings of the Fourth International Conference in Nematology 2, 447–462.Google Scholar
Mekete, T., Gaugler, R., Nguyen, K.B., Mandefro, W. & Tessera, T. (2005) Biogeography of entomopathogenic nematodes in Ethiopia. Nematropica 35, 31–35.Google Scholar
Molyneux, A.S. (1985) Survival of infective juveniles of Heterorhabditis spp. and Steinernema spp. (Nematoda: Rhabditida) at various temperatures and their subsequent infectivity for insects. Revue de Nematologie 8, 165–170.Google Scholar
Mwaniki, S.W., Nderitu, J.H., Olubayo, F., Kimenju, J.W. & Nguyen, K. (2008) Factors influencing the occurrence of entomopathogenic nematodes in the Central Rift Valley Region of Kenya. African Journal of Ecology 46, 79–84.Google Scholar
Nguyen, K.B., Tesfamariam, M., Gozel, U., Gaugler, R. & Adams, B.J. (2004) Steinernema yirgalemense n. sp. (Rhabditida: Steinernematidae) from Ethiopia. Nematology 6, 839–856.Google Scholar
Poinar, G.O. & Thomas, G.M. (1966) Significance of Achromobacter nematophilus Poinar and Thomas (Achromobacteriaceae: Eubacteriales) in the development of the nematode DD-136 (Neoplectana sp. Steinernematidae). Parasitology 56, 385–390.CrossRefGoogle Scholar
Poinar, G.O. Jr, Thomas, G.M. & Hess, R. (1977) Characteristics of the specific bacterium associated with Heterorhabditis bacteriophora (Heterorhabditidae: Rhabditida). Nematologica 23, 97–102.Google Scholar
San-Blas, E., Gowen, S.R. & Pembroke, B. (2008) Steinernema feltiae: ammonia triggers the emergence of their infective juveniles. Experimental Parasitology 119, 180–185.Google Scholar
Selvan, S., Campbell, F. & Gaugler, R. (1993) Density-dependent effects on entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) within an insect host. Journal of Invertebrate Pathology 62, 278–284.Google Scholar
Statsoft Inc. (2011) STATISTICA (data analysis software system). Version 10. Available at http://www.statsoft.com (accessed accessed 14 May 2015).Google Scholar
Strauch, O. & Ehlers, R.-U. (1998) Food signal production of Photorhabdus luminescens inducing the recovery of entomopathogenic nematodes Heterorhabditis spp. in liquid culture. Applied Microbiology Biotechnology 50, 369–374.CrossRefGoogle Scholar
Strauch, O., Stoessel, S. & Ehlers, R.-U. (1994) Culture conditions define automictic or amphimictic reproduction in entomopathogenic rhabditid nematodes of the genus Heterorhabditis . Fundamental and Applied Nematology 17, 575–582.Google Scholar
Torr, P., Heritage, S. & Wilson, M.J. (2004) Vibrations as novel signal for host location by parasitic nematodes. International Journal Parasitology 34, 997–999.Google Scholar
Van Niekerk, S. & Malan, A.P. (2012) Potential of South African entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) for control of the citrus mealybug, Planococcus citri (Pseudococcidae). Journal of Invertebrate Pathology 111, 166–176.Google Scholar
Vanninen, I. (1990) Depletion of endogenous lipid reserves in Steinernema feltiae and Heterorhabditis bacteriophora and effect on infectivity. Proceedings of the 5th International Colloquium on Invertebrate Pathology and Microbial Control, Adelaide, Australia.Google Scholar
Woodring, J.L. & Kaya, H.K. (1988) Steinernematid and Heterorhabditid nematodes: A handbook of techniques. Southern Cooperative Series Bulletin 331. 30 pp. Fayetteville, Arkansas, Arkansas Agricultural Experiment Station.Google Scholar
Wouts, W.M. (1981) Mass production of the entomogenous nematode Heterorhabditis heliothidis (Nematoda: Heterorhabditidae) on artificial media. Journal of Nematology 13, 467–469.Google ScholarPubMed