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Hybridisation and selective breeding for improvement of low temperature activity of the entomopathogenic nematode Steinernema feltiae

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Abstract

Steinernema feltiae is used to control overwintering larvae of the codling moth Cydia pomonella L. Application is in autumn when efficacy can be limited by low temperature. The objective of this study was to screen for low temperature activity among wild type populations of S. feltiae, hybridise most active strains and further improve low temperature activity by subjection of a hybrid strain to selective breeding. Significant variation was recorded among 22 S. feltiae strains. The temperature at which 50 % (AT50) and 10 % (AT10) of the dauer juveniles (DJs) were active ranged between 2.9 to 5.8 °C and 0.95 to 3.5 °C, respectively. The mean AT50 of 22 S. feltiae strains was 3.83 °C. The five most active strains were crossed. The hybrid strain HYB01 was more active at low temperature than parental and other hybrid strains with an AT50 of 0.52 °C and an AT10 of 0.09 °C. The tolerance was lost after few reproductive cycles in the insect Galleria mellonella, but was recovered after seven selection cycles with exposure to lowering temperatures. The heritability for the low temperature activity was calculated at h 2 = 0.45. Negative trade-off effects on virulence against C. pomonella and reproduction on the same insect were not reported. The most virulent strain was a commercial strain with an LD50 of 30.2 at 8 °C and 37.2 DJs per cocooned instar at 15 °C, followed by the selected hybrid with 48.1 and 47.4 DJs, respectively. Offspring production reached 15.000 DJs per instar at 8 °C and was only half at 15 °C. The results well document the potential of a breeding programme for enhancement of the activity of S. feltiae at lower temperature with the objective to improve the control potential of overwintering codling moth C. pomonella.

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References

  • Anbesse S, Strauch O, Ehlers R-U (2012a) Genetic improvement of the biological control nematode Heterorhabditis bacteriophora (Rhabditidomorpha: Heterorhabditidae): heterosis effect enhances desiccation but not heat tolerance through selective breeding and creation of inbred lines in liquid culture. Biocontrol Sci Technol 22:1035–1045

    Article  Google Scholar 

  • Anbesse S, Sumaya NH, Doerfler AV, Strauch O, Ehlers R-U (2012b) Selective breeding for desiccation tolerance in liquid culture provides genetically stable inbred lines of the entomopathogenic nematode Heterorhabditis bacteriophora. Appl Microbiol Biotechnol. doi:10.1007/s00253-012-4227-5

    PubMed  Google Scholar 

  • Anbesse S, Sumaya NH, Doerfler AV, Strauch O, Ehlers R-U (2012c) Stabilisation of heat tolerance traits in Heterorhabditis bacteriophora through selective breeding and creation of inbred lines in liquid culture. BioControl. doi:10.1007/s10526-012-9467-x

    Google Scholar 

  • Asser-Kaiser S, Fritsch E, Undorf-Spahn K, Kienzle J, Eberle KE, Gund NA, Reineke A, Zebitz CPW, Heckel DG, Huber J, Jehle JA (2007) Rapid emergence of baculovirus resistance in codling moth due to dominant sex-linked inheritance. Science 317:1916–1918

    Article  PubMed  CAS  Google Scholar 

  • Barnes MM (1991) Tortricids in pome and stone fruits, codling moth occurrence, host race formation, and damage. In: van der Geest LPS, Evenhuis HH (eds) Tortricid pests, their biology, natural enemies and control. Elsevier, Amsterdam, The Netherlands, pp 313–327

    Google Scholar 

  • Beers EH, Brunner JF, Willett MJ, Warner GM (1993) Orchard pest management: a resource book for the Pacific Northwest Yakima Washington. Good Fruit Grower, Washington, USA

    Google Scholar 

  • Bilgrami A, Gaugler R, Shapiro-Ilan D, Adams B (2006) Source of trait deterioration in entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema carpocapsae during in vivo culture. Nematology 8:397–409

    Article  Google Scholar 

  • Burnell AM, Dowds BCA (1996) The genetic improvement of entomopathogenic nematodes and their symbiotic bacteria: phenotypic targets, genetic limitations and an assessment of possible hazards. Biocontrol Sci Technol 6:435–447

    Article  Google Scholar 

  • Calkins CO, Faust RJ (2003) Overview of area wide programs and the program for suppression of codling moth in the western USA directed by the United States Department of Agriculture—Agricultural Research Service. Pest Manag Sci 59:601–604

    Article  PubMed  CAS  Google Scholar 

  • Cardé RT, Minks AK (1995) Control of moth pests by mating disruption: successes and constraints. Annu Rev Entomol 40:559–585

    Article  Google Scholar 

  • Chen S, Li J, Han X, Moens M (2003) Effect of temperature on the pathogenicity of entomopathogenic nematodes (Steinernema and Heterorhabditis spp.) to Delia radicum. Biol Control 48:713–724

    Google Scholar 

  • de Waal JY, Malan AP, Levings J, Addison MF (2010) Key elements in the successful control of diapausing codling moth, Cydia pomonella (Lepidoptera: Tortricidae) in wooden fruit bins with a South African isolate of Heterorhabditis zealandica (Rhabditida: Heterorhabditidae). Biocontrol Sci Technol 20:489–502

    Article  Google Scholar 

  • Eberle KE, Jehle JA (2006) Field resistance of codling moth against Cydia pomonella granulovirus (CpGV) is autosomal and incompletely dominant inherited. J Invertebr Pathol 93:201–206

    Article  PubMed  Google Scholar 

  • Ehlers R-U, Lunau S, Krasomil-Osterfeld K, Osterfeld KH (1998) Liquid culture of the entomopathogenic nematode bacterium complex Heterorhabditis megidis/Photorhabdus luminescens. BioControl 43:77–86

    Article  Google Scholar 

  • Ehlers R-U, Oestergaard J, Hollmer S, Wingen M, Strauch O (2005) Genetic selection for heat tolerance and low temperature activity of the entomopathogenic nematode–bacterium complex Heterorhabditis bacteriophoraPhotorhabdus luminescens. BioControl 50:699–716

    Article  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Quantitative Genetics, 4th edn. Pearson, Harlow, UK

    Google Scholar 

  • Finney DJ (1971) Probit analysis. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Fodor A, Marton P, Szallas E, Vellai T (1994) Prospects for the genetic improvement/analysis of entomopathogenic nematodes. In: Burnell AM, Ehlers R-U, Masson JP (eds) Genetics of entomopathogenic nematode–bacterium complexes. European Commission Publication, Luxembourg, pp 101–119

    Google Scholar 

  • Gaugler R (1987) Entomogenous nematodes and their prospects for genetic improvement. In: Maramorosch K (ed) Biotechnological advances in invertebrate pathology and cell culture. Academic, New York, USA, pp 457–484

    Chapter  Google Scholar 

  • Gaugler R, Campbell JF, Mcguire TR (1989) Selection for host-finding in Steinernema feltiae. J Invertebr Pathol 54:363–372

    Article  Google Scholar 

  • Grewal PS, Selvan S, Gaugler R (1994) Thermal adaptation of entomopathogenic nematodes: niche breadth for infection, establishment, and reproduction. J Thermal Biol 19:245–253

    Article  Google Scholar 

  • Grewal PS, Bornstein-Forst S, Burnell AM, Glazer I (2006) Physiological, genetic, and molecular mechanisms of chemoreception, thermobiosis, and anhydrobiosis in entomopathogenic nematodes. Biol Control 38:54–65

    Article  CAS  Google Scholar 

  • Griffin CT, Downes MJ (1991) Low temperature activity in Heterorhabditis spp. (Nematoda: Heterorhabditidae). Nematologica 37:83–91

    Article  Google Scholar 

  • Hazir S, Stock SP, Kaya HK, Koppenhöfer AM, Keskin N (2001) Developmental temperature effects on five geographic isolates of entomopathogenic nematode Steinernema feltiae (Nematoda: Steinernematidae). J Invertebr Pathol 77:243–250

    Article  PubMed  CAS  Google Scholar 

  • Hirao A, Ehlers R-U, Strauch O (2010) Life cycle and population development of entomopathogenic nematodes Steinernema carpocapsae and S. feltiae (Nematoda: Rhabditida) in monoxenic liquid cultures. Nematology 12:201–210

    Article  Google Scholar 

  • Hopper KR, Roush RT, Powell W (1993) Management of genetics of biological-control introductions. Annu Rev Entomol 38:27–51

    Article  Google Scholar 

  • Hoy MA (1985) Recent advances in genetics and genetic improvement of the Phytoseiidae. Annu Rev Entomol 30:345–370

    Article  Google Scholar 

  • Iraki N, Salah N, Sansour MA, Segal D, Glazer I, Johnigk S-A, Hussein MA, Ehlers R-U (2000) Isolation and characterization of two entomopathogenic nematode strains, Heterorhabditis indica, Nematoda, Rhabditida, from the West Bank, Palestinian Territories. J Appl Entomol 124:375–380

    Article  Google Scholar 

  • Johnigk S-A, Ehlers R-U (1999) Juvenile development and life cycle of Heterorhabditis bacteriophora and H. indica. Nematology 1:251–260

    Article  Google Scholar 

  • Kaya HK, Stock SP (1997) Techniques in insect nematology. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic, San Diego, USA, pp 281–325

    Chapter  Google Scholar 

  • Kaya HK, Joos JL, Falcon LA, Berlowitz A (1984) Suppression of the codling moth (Lepidoptera, Olethreutidae) with the entomogenous nematode, Steinernema feltiae (Rhabditida, Steinernematidae). J Econ Entomol 77:1240–1244

    Google Scholar 

  • Lacey LA, Unruh TR (1998) Entomopathogenic nematodes for control of codling moth Cydia pomonella (Lepidoptera: Tortricidae): effect of nematode species, concentration, temperature and humidity. Biol Control 13:190–197

    Article  Google Scholar 

  • Lacey LA, Unruh TR (2001) Control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae), with Steinernema carpocapsae: effects of supplemental wetting and pupation site on infection rate. Biol Control 20:48–56

    Article  Google Scholar 

  • Lacey LA, Arthurs SP, Unruh TR, Headrick H, Fritts R Jr (2006) Entomopathogenic nematodes for control of codling moth (Lepidoptera: Tortricidae) in apple and pear orchards: effect of nematode species and seasonal temperatures, adjuvants, application equipment, and post-application irrigation. Biol Control 37:214–223

    Article  Google Scholar 

  • Molyneux AS (1986) Heterorhabditis spp. and Steinernema (=Neoaplectana) spp.: temperature, and aspect of behavior and infectivity. Exp Parasitol 62:169–180

    Article  PubMed  CAS  Google Scholar 

  • Mota-Sanchez D, Wise JC, Poppen RV, Gut LJ, Hollingworth RM (2008) Resistance of codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), larvae in Michigan to insecticides with different modes of action and the impact on field residual activity. Pest Manag Sci 64:881–890

    Article  PubMed  CAS  Google Scholar 

  • Mukuka J, Strauch O, Al Zainab MH, Ehlers R-U (2010a) Effect of temperature and desiccation stress on infectivity of stress tolerant hybrid strains of Heterorhabditis bacteriophora. Russ J Nematol 18:111–116

    Google Scholar 

  • Mukuka J, Strauch O, Ehlers R-U (2010b) Variability in desiccation tolerance among different strains of the entomopathogenic nematode Heterorhabditis bacteriophora. Nematology 12:711–720

    Article  Google Scholar 

  • Mukuka J, Strauch O, Hoppe C, Ehlers R-U (2010c) Improvement of heat and desiccation tolerance in Heterorhabditis bacteriophora through cross-breeding of tolerant strains and successive genetic selection. BioControl 55:511–521

    Article  Google Scholar 

  • Mukuka J, Strauch O, Hoppe C, Ehlers R-U (2010d) Fitness of heat and desiccation tolerant hybrid strains of Heterorhabditis bacteriophora (Rhabditidomorpha: Heterorhabditidae). J Pest Sci 83:281–287

    Article  Google Scholar 

  • Mukuka J, Strauch O, Waeyenberge L, Viaene N, Moens M, Ehlers R-U (2010e) Heat tolerance among different strains of the entomopathogenic nematode Heterorhabditis bacteriophora. BioControl 55:423–434

    Article  Google Scholar 

  • Navaneethan T, Strauch O, Besse S, Bonhomme A, Ehlers R-U (2010) Influence of humidity and a surfactant–polymer-formulation on the control potential of the entomopathogenic nematode Steinernema feltiae against diapausing codling moth larvae (Cydia pomonella L.) (Lepidoptera: Tortricidae). BioControl 55:777–788

    Article  CAS  Google Scholar 

  • Reyes M, Franck P, Charmillot PJ, Ioriatti C, Olivares J, Pasqualin E, Sauphanor B (2007) Diversity of insecticide resistance mechanisms and spectrum in European populations of the Codling moth, Cydia pomonella. Pest Manag Sci 63:890–902

    Article  PubMed  CAS  Google Scholar 

  • Roush RT (1990) Genetic considerations in the propagation of entomophagous species. In: Baker RR, Dunn PE (eds) Critical issues in biological control. Liss, New York, USA, pp 373–387

    Google Scholar 

  • Shapiro-Ilan DI, Duncan LW, Lacey LA, Han R (2005) Orchard applications. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI Publishing, Wallingford, UK, pp 65–78

    Google Scholar 

  • Stara J, Kocourek F (2007) Insecticidal resistance and crossresistance in populations of Cydia pomonella (Lepidoptera: Tortricidae) in Central Europe. J Econ Entomol 100:1587–1595

    Article  PubMed  CAS  Google Scholar 

  • Strauch O, Oestergaard J, Hollmer S, Ehlers R-U (2004) Genetic improvement of the desiccation tolerance of the entomopathogenic nematode Heterorhabditis bacteriophora through selective breeding. Biol Control 31:218–226

    Article  Google Scholar 

  • Unruh TR, Lacey LA (2001) Control of codling moth Cydia pomonella (Lepidoptera: Tortricidae) with Steinernema carpocapsae: effects of supplemental wetting and pupation site on infection rate. Biol Control 20:48–56

    Article  Google Scholar 

  • Wang X, Grewal PS (2002) Rapid genetic deterioration of environmental tolerance and reproductive potential of an entomopathogenic nematode during laboratory maintenance. Biol Control 23:71–78

    Article  CAS  Google Scholar 

  • Wouts WM (1981) Mass production of the entomogenous nematode, Heterorhabditis heliothidis (Nematoda: Heterorhabditidae) on artificial media. J Nematol 13:467–469

    PubMed  CAS  Google Scholar 

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Acknowledgments

Thanks to all colleagues for supply with nematode strains. The scholarship to the first author by the German Academic Exchange Service (http://www.daad.de) is gratefully acknowledged as well as a scholarship granted to the second author by the Flemish Interuniversity Council, University Development Cooperation (VLIR-UOS) for participation in the Postgraduate International Nematology Course (http://www.pinc.ugent.be).

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Correspondence to Ralf-Udo Ehlers.

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Nimkingrat, P., Khanam, S., Strauch, O. et al. Hybridisation and selective breeding for improvement of low temperature activity of the entomopathogenic nematode Steinernema feltiae . BioControl 58, 417–426 (2013). https://doi.org/10.1007/s10526-012-9497-4

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