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Comparison of hermaphrodites of hybrid Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH strain and its parents on reproduction capacity

Year 2021, , 185 - 191, 01.06.2021
https://doi.org/10.16970/entoted.858061

Abstract

Entomopathogenic nematodes (EPNs) are microscopic roundworms used in biocontrol. EPNs are obligate insect parasites, they live in soil, and they are especially effective against soilborne insects. They are a good alternative to chemical pesticides thanks to their advantages, such as prolonged longevity, broad host range and mass production suitability. However, EPNs cannot compete with chemical pesticides due to high production costs and short shelf life. The aim of this study was to determine the reproduction capacity of the Turkish hybrid Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH strain and then compare it with its parents to improve its liquid culture yield. In this way, it is aimed to reveal the effects behind the high reproduction potential of the hybrid HBH strain. All experiments were performed at Bursa Uludağ University, Faculty of Agriculture, Department of Plant Protection, in 2020. All cadavers were periodically dissected, hermaphrodites were counted and their body lengths were measured. Compared to its parents, the hybrid HBH strain had greater hermaphrodite counts, with mean 66 individuals within 12 days, and hermaphrodite body length, with mean 3.88 mm. The results obtained from this study should provide information for commercial EPN production development.

Supporting Institution

TUBITAK (The Scientific and Technological Research Council of Turkey)

Project Number

TOVAG 219O370

Thanks

This study was financially supported by the TUBITAK (The Scientific and Technological Research Council of Turkey), Project number: TOVAG 219O370.

References

  • Ali, F. & D. A. Wharton, 2013. Cold tolerance abilities of two entomopathogenic nematodes, Steinernema feltiae and Heterorhabditis bacteriophora. Cryobiology, 66 (1): 24-29.
  • Anbesse, S., N. H. Sumaya, A. V. Dörfler, O. Strauch & R. Ehlers, 2013. Stabilization of heat tolerance traits in Heterorhabditis bacteriophora through selective breeding and creation of inbred lines in liquid culture. BioControl, 58 (1): 85-93.
  • Bode, H. B., 2009. Entomopathogenic bacteria as a source of secondary metabolites. Current Opinion in Chemical Biology, 13 (2): 224-230.
  • Boemare, N., C. Laumond & H. Mauleon, 1996. The entomopathogenic nematode-bacterium complex: biology, life cycle and vertebrate safety. Biocontrol Science and Technology, 6 (3): 333-346.
  • De Waal, J. Y., M. Addison & A. Malan, 2018. Potential of Heterorhabditis zealandica (Rhabditida: Heterorhabditidae) for the control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae) in semi-field trials under South African conditions. International Journal of Pest Management, 64 (2): 102-109.
  • Devi, G. & J. George, 2018. Formulation of Insecticidal Nematode. Annual Research & Review in Biology, 24 (5): 1-10.
  • Divya, K. & M. Sankar, 2009. Entomopathogenic nematodes in pest management. Indian Journal of Science and Technology, 2 (7): 53-60.
  • Dunn, M. D., P. D. Belur & A. P. Malan, 2020. In vitro liquid culture and optimization of Steinernema jeffreyense using shake flasks. BioControl, 65 (2): 223-233.
  • Dunn, M. D., P. D. Belur & A. P. Malan, 2021. A review of the in vitro liquid mass culture of entomopathogenic nematodes. Biocontrol Science and Technology, 31(1): 1-21.
  • Ehlers, R., J. Oestergaard, S. Hollmer, M. Wingen & O. Strauch, 2005. Genetic selection for heat tolerance and low temperature activity of the entomopathogenic nematode-bacterium complex Heterorhabditis bacteriophora-Photorhabdus luminescens. BioControl, 50 (5): 699-716.
  • Ferreira, T., M. Addison & A. Malan, 2014. In vitro liquid culture of a South African isolate of Heterorhabditis zealandica for the control of insect pests. African Entomology, 22 (1): 80-92.
  • Ferreira, T., M. Addison & A. Malan, 2016. Development and population dynamics of Steinernema yirgalemense (Rhabditida: Steinernematidae) and growth characteristics of its associated Xenorhabdus indica symbiont in liquid culture. Journal of Helminthology, 90 (3): 364-371.
  • Garcia-del-Pino, F., X. Alabern & A. Morton, 2013. Efficacy of soil treatments of entomopathogenic nematodes against the larvae, pupae and adults of Tuta absoluta and their interaction with the insecticides used against this insect. BioControl, 58 (6): 723-731.
  • Glare, T., J. Caradus, W. Gelernter, T. Jackson, N. Keyhani, J. Köhl, P. Marrone, L. Morin & A. Stewart, 2012. Have biopesticides come of age? Trends in Biotechnology, 30 (5): 250-258.
  • Grewal, P. S., 2000. Enhanced ambient storage stability of an entomopathogenic nematode through anhydrobiosis. Pest Management Science, 56 (5): 401-406.
  • Hirao, A., R. Ehlers & O. Strauch, 2010. Life cycle and population development of the entomopathogenic nematodes Steinernema carpocapsae and S. feltiae (Nematoda, Rhabditida) in monoxenic liquid culture. Nematology, 12 (2): 201-210.
  • James, M., A. P. Malan & P. Addison, 2018. Surveying and screening South African entomopathogenic nematodes for the control of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Crop Protection, 105: 41-48.
  • Johnigk, S., S. Hollmer, O. Strauch, U. Wyss & R. Ehlers, 2002. Heritability of the liquid culture mass production potential of the entomopathogenic nematode Heterorhabditis bacteriophora. Biocontrol Science and Technology, 12 (2): 267-276.
  • Kagimu, N. & A. P. Malan, 2019. Formulation of South African entomopathogenic nematodes using alginate beads and diatomaceous earth. BioControl, 64 (4): 413-422.
  • Kaya, H. K. & R. Gaugler 1993. Entomopathogenic nematodes. Annual Review of Entomology, 38 (125): 181-206.
  • Kongu, Y. & I. A. Susurluk, 2014. Comparison of virulence of hybridized entomopathogenic nematode Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) strains and their parents. Turkish Journal of Entomology, 38 (2): 125-134.
  • Lacey, L. A. & R. Georgis, 2012. Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology, 44 (2): 218-225.
  • Malan, A. P. & S. D. Moore, 2016. Evaluation of local entomopathogenic nematodes for the control of false codling moth, Thaumatotibia leucotreta (Meyrick, 1913), in a citrus orchard in South Africa. African Entomology, 24 (2): 489-501.
  • Mokrini, F., S. E. Laasli, Y. Benseddik, A.B. Joutei, A. Blenzar, H. Lakhal, M. Sbaghi, M. Imren, G. Özer, T. Paulitz, R. Lahlali, & A. A. Dababat 2020. Potential of Moroccan entomopathogenic nematodes for the control of the Mediterranean fruit fly Ceratitis capitata Wiedemann (Diptera: Tephritidae). Scientific Reports, 10 (1): 19204.
  • Mukuka, J., O. Strauch, C. Hoppe & R. Ehlers, 2010. Improvement of heat and desiccation tolerance in Heterorhabditis bacteriophora through cross-breeding of tolerant strains and successive genetic selection. BioControl, 55 (4): 511-521.
  • Nimkingrat, P., S. Khanam, O. Strauch & R. Ehlers, 2013a. Hybridisation and selective breeding for improvement of low temperature activity of the entomopathogenic nematode Steinernema feltiae. BioControl, 58 (3): 417-426.
  • Nimkingrat, P., O. Strauch & R. Ehlers, 2013b. Hybridisation and genetic selection for improving desiccation tolerance of the entomopathogenic nematode Steinernema feltiae. Biocontrol Science and Technology, 23 (3): 348-361.
  • Perry, R. N., R. Ehlers & I. Glazer, 2012. A realistic appraisal of methods to enhance desiccation tolerance of entomopathogenic nematodes. Journal of Nematology, 44 (2): 185-190.
  • Ramakuwela, T., J. Hatting, M. D. Laing, S. Hazir & N. Thiebaut, 2016. In vitro solid-state production of Steinernema innovationi with cost analysis. Biocontrol Science and Technology, 26 (6): 792-808.
  • Sabino, P. H. S., A. S. Negrisoli, V. Andaló, C. C. Filgueiras, A. Moino & F. S. Sales, 2019. Combined application of entomopathogenic nematodes and insecticides in the control of leaf-miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on Tomato. Neotropical Entomology, 48 (2): 314-322.
  • Sajnaga, E. & W. Kazimierczak, 2020. Evolution and taxonomy of nematode-associated entomopathogenic bacteria of the genera Xenorhabdus and Photorhabdus: an overview. Symbiosis, 80 (1): 1-13.
  • Salame, L., I. Glazer, M. T. Chubinishvilli & T. Chkhubianishvili, 2010. Genetic improvement of the desiccation tolerance and host-seeking ability of the entomopathogenic nematode Steinernema feltiae. Phytoparasitica, 38 (4): 359-368.
  • Santhi, V. S., D. Ment, L. Salame, V. Soroker & I. Glazer, 2016. Genetic improvement of host-seeking ability in the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis bacteriophora toward the Red Palm Weevil Rhynchophorus ferrugineus. Biological Control, 100 (1): 29-36.
  • Shapiro-Ilan, D., I. Glazer & D. Segal, 1997. Genetic improvement of heat tolerance in Heterorhabditis bacteriophora through hybridization. Biological Control, 8 (2): 153-159.
  • Shapiro-Ilan, D. I., R. Han & C. Dolinksi, 2012. Entomopathogenic nematode production and application technology. Journal of Nematology, 44 (2): 206-217.
  • Susurluk, A., I. Dix, E. Stackebrandt, O. Strauch, U. Wyss & R. U. Ehlers, 2001. Identification and ecological characterisation of three entomopathogenic nematode-bacterium complexes from Turkey. Nematology, 3 (8): 833-841.
  • Susurluk, I. A., T. C. Ulu & Y. Kongu, 2013. Tolerances of hybridized entomopathogenic nematode Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) strains to heat and desiccation. Turkish Journal of Entomology, 37 (2): 221-228.
  • Ulu, T. C. & A. Susurluk, 2018. Effects of several ingredients on in vitro mass production of Heterorhabditis bacteriophora HBH strain. Mediterranean Agricultural Sciences, 31 (3): 209-212.
  • Upadhyay, D. 2015. Lab-scale in vitro mass production of the entomopathogenic nematode Heterorhabditis bacteriophora using liquid culture fermentation technology. American Journal of Bioscience and Bioengineering, 3 (6): 203-207.
  • van Niekerk, S. & A. P. Malan, 2014. Compatibility of biological control agents and agrochemicals to entomopathogenic nematodes, Steinernema yirgalemense and Heterorhabditis zealandica. African Entomology, 22 (1): 49-56.
  • van Zyl, C. & A. Malan, 2014. Optimization of inoculation techniques for in vivo mass culture of entomopathogenic nematodes through nematode and insect host manipulation. African Entomology, 22 (2): 405-416.
  • Wright, D. J., A. Peters, S. Schroer & J. Fife, 2005. "Application Technology, 91-106". In: Nematodes as Biocontrol Agents (Eds. P. S. Grewal, R. U. Ehlers & D. I. Shapiro-Ilan), CABI, Wallingford, UK, 528 pp.

Hibrit Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH ırkı ve ebeveynlerinin hermafroditlerinin üreme kapasitelerinin karşılaştırılması

Year 2021, , 185 - 191, 01.06.2021
https://doi.org/10.16970/entoted.858061

Abstract

Entomopatojen nematodlar (EPN) biyolojik mücadelede kullanılan mikroskobik ölçülerdeki yuvarlak solucanlardır. EPN’ler zorunlu böcek parazitleri olup, toprak altında yaşamakta ve toprak kökenli böceklere karşı etkili olmaktadırlar. Uygulamalarının kolay olması, uzun sürekli etkinliği, geniş konukçu aralığı ve kitle üretimi yapılabilmesi gibi avantajları sayesinde kimyasal ilaçlara iyi bir alternatif olmaktadırlar. Bununla beraber, yüksek üretim maliyetleri ve kısa raf ömrü nedeniyle EPN’ler kimyasal ilaçlar ile rekabet edememektedir. Bu çalışma, sıvı kültürdeki üretim verimini artırmak amacıyla Türk hibriti Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH ırkının üreme kapasitesini belirlemek ve ebeveynleri ile karşılaştırmak amacıyla yapılmıştır. Bu sayede hibrit HBH ırkının yüksek üreme potansiyelinin arkasında yatan etkilerin ortaya çıkarılması hedeflenmiştir. Tüm denemeler Bursa Uludağ Üniversitesi Ziraat Fakültesi Bitki Koruma Bölümü’nde 2020 yılında gerçekleştirilmiştir. Bütün kadavralar periyodik olarak disekte edilmiş, hermafroditler sayılmış ve vücut uzunlukları ölçülmüştür. Ebeveynleri ile karşılaştırıldığında, hibrit HBH ırkı, 12 günde ortalama 66 hermafrodit birey ile hermafrodit sayısında ve ortalama 3.88 mm ile hermafrodit vücut uzunluğu açısından daha yüksek değerlere sahip olmuştur. Bu çalışma ile elde edilen sonuçlar, ticari EPN üretim çalışmalarına bilgi sağlayacaktır.

Project Number

TOVAG 219O370

References

  • Ali, F. & D. A. Wharton, 2013. Cold tolerance abilities of two entomopathogenic nematodes, Steinernema feltiae and Heterorhabditis bacteriophora. Cryobiology, 66 (1): 24-29.
  • Anbesse, S., N. H. Sumaya, A. V. Dörfler, O. Strauch & R. Ehlers, 2013. Stabilization of heat tolerance traits in Heterorhabditis bacteriophora through selective breeding and creation of inbred lines in liquid culture. BioControl, 58 (1): 85-93.
  • Bode, H. B., 2009. Entomopathogenic bacteria as a source of secondary metabolites. Current Opinion in Chemical Biology, 13 (2): 224-230.
  • Boemare, N., C. Laumond & H. Mauleon, 1996. The entomopathogenic nematode-bacterium complex: biology, life cycle and vertebrate safety. Biocontrol Science and Technology, 6 (3): 333-346.
  • De Waal, J. Y., M. Addison & A. Malan, 2018. Potential of Heterorhabditis zealandica (Rhabditida: Heterorhabditidae) for the control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae) in semi-field trials under South African conditions. International Journal of Pest Management, 64 (2): 102-109.
  • Devi, G. & J. George, 2018. Formulation of Insecticidal Nematode. Annual Research & Review in Biology, 24 (5): 1-10.
  • Divya, K. & M. Sankar, 2009. Entomopathogenic nematodes in pest management. Indian Journal of Science and Technology, 2 (7): 53-60.
  • Dunn, M. D., P. D. Belur & A. P. Malan, 2020. In vitro liquid culture and optimization of Steinernema jeffreyense using shake flasks. BioControl, 65 (2): 223-233.
  • Dunn, M. D., P. D. Belur & A. P. Malan, 2021. A review of the in vitro liquid mass culture of entomopathogenic nematodes. Biocontrol Science and Technology, 31(1): 1-21.
  • Ehlers, R., J. Oestergaard, S. Hollmer, M. Wingen & O. Strauch, 2005. Genetic selection for heat tolerance and low temperature activity of the entomopathogenic nematode-bacterium complex Heterorhabditis bacteriophora-Photorhabdus luminescens. BioControl, 50 (5): 699-716.
  • Ferreira, T., M. Addison & A. Malan, 2014. In vitro liquid culture of a South African isolate of Heterorhabditis zealandica for the control of insect pests. African Entomology, 22 (1): 80-92.
  • Ferreira, T., M. Addison & A. Malan, 2016. Development and population dynamics of Steinernema yirgalemense (Rhabditida: Steinernematidae) and growth characteristics of its associated Xenorhabdus indica symbiont in liquid culture. Journal of Helminthology, 90 (3): 364-371.
  • Garcia-del-Pino, F., X. Alabern & A. Morton, 2013. Efficacy of soil treatments of entomopathogenic nematodes against the larvae, pupae and adults of Tuta absoluta and their interaction with the insecticides used against this insect. BioControl, 58 (6): 723-731.
  • Glare, T., J. Caradus, W. Gelernter, T. Jackson, N. Keyhani, J. Köhl, P. Marrone, L. Morin & A. Stewart, 2012. Have biopesticides come of age? Trends in Biotechnology, 30 (5): 250-258.
  • Grewal, P. S., 2000. Enhanced ambient storage stability of an entomopathogenic nematode through anhydrobiosis. Pest Management Science, 56 (5): 401-406.
  • Hirao, A., R. Ehlers & O. Strauch, 2010. Life cycle and population development of the entomopathogenic nematodes Steinernema carpocapsae and S. feltiae (Nematoda, Rhabditida) in monoxenic liquid culture. Nematology, 12 (2): 201-210.
  • James, M., A. P. Malan & P. Addison, 2018. Surveying and screening South African entomopathogenic nematodes for the control of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Crop Protection, 105: 41-48.
  • Johnigk, S., S. Hollmer, O. Strauch, U. Wyss & R. Ehlers, 2002. Heritability of the liquid culture mass production potential of the entomopathogenic nematode Heterorhabditis bacteriophora. Biocontrol Science and Technology, 12 (2): 267-276.
  • Kagimu, N. & A. P. Malan, 2019. Formulation of South African entomopathogenic nematodes using alginate beads and diatomaceous earth. BioControl, 64 (4): 413-422.
  • Kaya, H. K. & R. Gaugler 1993. Entomopathogenic nematodes. Annual Review of Entomology, 38 (125): 181-206.
  • Kongu, Y. & I. A. Susurluk, 2014. Comparison of virulence of hybridized entomopathogenic nematode Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) strains and their parents. Turkish Journal of Entomology, 38 (2): 125-134.
  • Lacey, L. A. & R. Georgis, 2012. Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology, 44 (2): 218-225.
  • Malan, A. P. & S. D. Moore, 2016. Evaluation of local entomopathogenic nematodes for the control of false codling moth, Thaumatotibia leucotreta (Meyrick, 1913), in a citrus orchard in South Africa. African Entomology, 24 (2): 489-501.
  • Mokrini, F., S. E. Laasli, Y. Benseddik, A.B. Joutei, A. Blenzar, H. Lakhal, M. Sbaghi, M. Imren, G. Özer, T. Paulitz, R. Lahlali, & A. A. Dababat 2020. Potential of Moroccan entomopathogenic nematodes for the control of the Mediterranean fruit fly Ceratitis capitata Wiedemann (Diptera: Tephritidae). Scientific Reports, 10 (1): 19204.
  • Mukuka, J., O. Strauch, C. Hoppe & R. Ehlers, 2010. Improvement of heat and desiccation tolerance in Heterorhabditis bacteriophora through cross-breeding of tolerant strains and successive genetic selection. BioControl, 55 (4): 511-521.
  • Nimkingrat, P., S. Khanam, O. Strauch & R. Ehlers, 2013a. Hybridisation and selective breeding for improvement of low temperature activity of the entomopathogenic nematode Steinernema feltiae. BioControl, 58 (3): 417-426.
  • Nimkingrat, P., O. Strauch & R. Ehlers, 2013b. Hybridisation and genetic selection for improving desiccation tolerance of the entomopathogenic nematode Steinernema feltiae. Biocontrol Science and Technology, 23 (3): 348-361.
  • Perry, R. N., R. Ehlers & I. Glazer, 2012. A realistic appraisal of methods to enhance desiccation tolerance of entomopathogenic nematodes. Journal of Nematology, 44 (2): 185-190.
  • Ramakuwela, T., J. Hatting, M. D. Laing, S. Hazir & N. Thiebaut, 2016. In vitro solid-state production of Steinernema innovationi with cost analysis. Biocontrol Science and Technology, 26 (6): 792-808.
  • Sabino, P. H. S., A. S. Negrisoli, V. Andaló, C. C. Filgueiras, A. Moino & F. S. Sales, 2019. Combined application of entomopathogenic nematodes and insecticides in the control of leaf-miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on Tomato. Neotropical Entomology, 48 (2): 314-322.
  • Sajnaga, E. & W. Kazimierczak, 2020. Evolution and taxonomy of nematode-associated entomopathogenic bacteria of the genera Xenorhabdus and Photorhabdus: an overview. Symbiosis, 80 (1): 1-13.
  • Salame, L., I. Glazer, M. T. Chubinishvilli & T. Chkhubianishvili, 2010. Genetic improvement of the desiccation tolerance and host-seeking ability of the entomopathogenic nematode Steinernema feltiae. Phytoparasitica, 38 (4): 359-368.
  • Santhi, V. S., D. Ment, L. Salame, V. Soroker & I. Glazer, 2016. Genetic improvement of host-seeking ability in the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis bacteriophora toward the Red Palm Weevil Rhynchophorus ferrugineus. Biological Control, 100 (1): 29-36.
  • Shapiro-Ilan, D., I. Glazer & D. Segal, 1997. Genetic improvement of heat tolerance in Heterorhabditis bacteriophora through hybridization. Biological Control, 8 (2): 153-159.
  • Shapiro-Ilan, D. I., R. Han & C. Dolinksi, 2012. Entomopathogenic nematode production and application technology. Journal of Nematology, 44 (2): 206-217.
  • Susurluk, A., I. Dix, E. Stackebrandt, O. Strauch, U. Wyss & R. U. Ehlers, 2001. Identification and ecological characterisation of three entomopathogenic nematode-bacterium complexes from Turkey. Nematology, 3 (8): 833-841.
  • Susurluk, I. A., T. C. Ulu & Y. Kongu, 2013. Tolerances of hybridized entomopathogenic nematode Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) strains to heat and desiccation. Turkish Journal of Entomology, 37 (2): 221-228.
  • Ulu, T. C. & A. Susurluk, 2018. Effects of several ingredients on in vitro mass production of Heterorhabditis bacteriophora HBH strain. Mediterranean Agricultural Sciences, 31 (3): 209-212.
  • Upadhyay, D. 2015. Lab-scale in vitro mass production of the entomopathogenic nematode Heterorhabditis bacteriophora using liquid culture fermentation technology. American Journal of Bioscience and Bioengineering, 3 (6): 203-207.
  • van Niekerk, S. & A. P. Malan, 2014. Compatibility of biological control agents and agrochemicals to entomopathogenic nematodes, Steinernema yirgalemense and Heterorhabditis zealandica. African Entomology, 22 (1): 49-56.
  • van Zyl, C. & A. Malan, 2014. Optimization of inoculation techniques for in vivo mass culture of entomopathogenic nematodes through nematode and insect host manipulation. African Entomology, 22 (2): 405-416.
  • Wright, D. J., A. Peters, S. Schroer & J. Fife, 2005. "Application Technology, 91-106". In: Nematodes as Biocontrol Agents (Eds. P. S. Grewal, R. U. Ehlers & D. I. Shapiro-Ilan), CABI, Wallingford, UK, 528 pp.
There are 42 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Tufan C Ulu 0000-0003-3640-1474

Gizem Özbudak This is me 0000-0002-4423-2490

Elif Özge Düzenli This is me 0000-0002-4328-4977

Şeyma Hümeyra Çakır This is me 0000-0003-3161-2117

Alper Susurluk 0000-0002-0699-1752

Project Number TOVAG 219O370
Publication Date June 1, 2021
Submission Date January 13, 2021
Acceptance Date April 3, 2021
Published in Issue Year 2021

Cite

APA Ulu, T. C., Özbudak, G., Düzenli, E. Ö., Çakır, Ş. H., et al. (2021). Comparison of hermaphrodites of hybrid Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH strain and its parents on reproduction capacity. Turkish Journal of Entomology, 45(2), 185-191. https://doi.org/10.16970/entoted.858061
AMA Ulu TC, Özbudak G, Düzenli EÖ, Çakır ŞH, Susurluk A. Comparison of hermaphrodites of hybrid Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH strain and its parents on reproduction capacity. TED. June 2021;45(2):185-191. doi:10.16970/entoted.858061
Chicago Ulu, Tufan C, Gizem Özbudak, Elif Özge Düzenli, Şeyma Hümeyra Çakır, and Alper Susurluk. “Comparison of Hermaphrodites of Hybrid Heterorhabditis Bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH Strain and Its Parents on Reproduction Capacity”. Turkish Journal of Entomology 45, no. 2 (June 2021): 185-91. https://doi.org/10.16970/entoted.858061.
EndNote Ulu TC, Özbudak G, Düzenli EÖ, Çakır ŞH, Susurluk A (June 1, 2021) Comparison of hermaphrodites of hybrid Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH strain and its parents on reproduction capacity. Turkish Journal of Entomology 45 2 185–191.
IEEE T. C. Ulu, G. Özbudak, E. Ö. Düzenli, Ş. H. Çakır, and A. Susurluk, “Comparison of hermaphrodites of hybrid Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH strain and its parents on reproduction capacity”, TED, vol. 45, no. 2, pp. 185–191, 2021, doi: 10.16970/entoted.858061.
ISNAD Ulu, Tufan C et al. “Comparison of Hermaphrodites of Hybrid Heterorhabditis Bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH Strain and Its Parents on Reproduction Capacity”. Turkish Journal of Entomology 45/2 (June 2021), 185-191. https://doi.org/10.16970/entoted.858061.
JAMA Ulu TC, Özbudak G, Düzenli EÖ, Çakır ŞH, Susurluk A. Comparison of hermaphrodites of hybrid Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH strain and its parents on reproduction capacity. TED. 2021;45:185–191.
MLA Ulu, Tufan C et al. “Comparison of Hermaphrodites of Hybrid Heterorhabditis Bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH Strain and Its Parents on Reproduction Capacity”. Turkish Journal of Entomology, vol. 45, no. 2, 2021, pp. 185-91, doi:10.16970/entoted.858061.
Vancouver Ulu TC, Özbudak G, Düzenli EÖ, Çakır ŞH, Susurluk A. Comparison of hermaphrodites of hybrid Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH strain and its parents on reproduction capacity. TED. 2021;45(2):185-91.