Efficiency of temperature and storage duration on some morphological measurements and reproductive capacity of the entomopathogenic nematode Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae)’s Turkish HBH hybrid strain

Year 2023, Volume: 47 Issue: 4 - Year: 2023 Volume: 47 Issue: 4, 469 - 476, 01.12.2023

Alperen Kaan Bütüner , Alper Susurluk

https://doi.org/10.16970/entoted.1331987

Cited By: 6

Abstract

Entomopathogenic nematodes (EPNs) are successfully used in the biological control of agricultural insect pests. This study aims to determine the body length of hermaphrodite individuals, egg diameter and reproductive capacity obtained from Infective Juveniles (IJs) stored at different temperatures and durations. Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae)’s Hybrid Strain HBH was used in the study. IJs stored at 15, 25 and 35°C for 7, 14 and 21 days were inoculated onto Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) last instar larvae at a dose of 100 IJs. On the 2nd day of infection, hermaphrodite individuals and eggs were obtained by dissecting the larvae. The reproductive capacity was determined 10-12 days after infection. The study was conducted in Bursa Uludağ University, Faculty of Agriculture, Plant Protection Department, Nematology Laboratory in 2023. In conclusion, the longest hermaphrodite individuals and egg diameter were obtained as 6207.22 µm and 55.65 µm, respectively from the IJs stored for 7 days at 15°C. The highest reproductive capacity was also observed as 167.500 IJs per G. mellonella larva in IJs stored under the same conditions with respect to temperature and time. This study is important for assessing the morphological effects of different temperature values and storage durations on EPNs.

Keywords

Body length, egg diameter, hermaphrodite, Heterorhabditis bacteriophora, reproductive capacity

Supporting Institution

TUBITAK (The Scientific and Technological Research Council of Türkiye)

Project Number

219O370

Thanks

This study was financially supported by the TÜBİTAK (The Scientific and Technological Research Council of Türkiye), with the project number: 219O370. We would like to thank Asst. Prof. Tufan Can Ulu for the statistical support, and Merve İlktan for the technical support.

Entomopatojen nematod Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae)’nın Türk HBH hibrit ırkının bazı morfolojik özellikleri ve üreme kapasitesi üzerinde sıcaklığın ve depolama süresinin etkisi

Abstract

Entomopatojen nematodlar (EPN), tarımsal zararlıların biyolojik mücadelesinde başarıyla kullanılmaktadır. Bu çalışmanın amacı farklı gün ve sıcaklıklarda depolanmış olan Infektif Juvenillerden (IJ) elde edilen hermafrodit bireylerin vücut uzunluğunun, yumurta çapının ve üreme gücünün belirlenmesidir. Bu çalışmada Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae)’nın Hibrit Irkı HBH kullanılmıştır. 15, 25 ve 35°C'de 7,14 ve 21 gün depolanmış olan IJ’ler 100 IJ dozunda Galleria mellonella L., 1758 (Lepidoptera: Pyralidae)’nın son dönem larvası üzerine inoküle edilmiştir. Enfeksiyonun gerçekleştiği 2. gün sonunda larvalar disekte edilmiş, hermafrodit bireyler ve yumurtalar elde edilmiştir. Üreme gücü ise enfeksiyon gerçekleştikten 10-12 gün sonra belirlenmiştir. Bu çalışma 2023 yılında Bursa Uludağ Üniversitesi, Ziraat Fakültesi, Bitki Koruma Bölümü, Nematoloji Laboratuvarı’nda yürütülmüştür. Sonuç olarak, en uzun hermafrodit bireyler ve yumurta çapı 15°C’de 7 gün muhafaza edilmiş olan IJ’lerden elde edilmiştir. Bu değerler sırasıyla 6207.22 µm ve 55.65 µm olarak belirlenmiştir. En yüksek üreme gücüde aynı sıcaklık ve günde tutulmuş olan IJ’lerde görülmüştür. Bu değer 167.500 IJs/G. mellonella larva olarak belirlenmiştir. Bu çalışma farklı sıcaklık değerlerinin ve depolama süresinin EPN’lerin üzerindeki morfolojik etkilerin belirlenmesini içeren önemli bir çalışmadır.

Keywords

Vücut uzunluğu, yumurta çapı, hermafrodit, Heterorhabditis bacteriophora, üreme gücü

Project Number

219O370

References

• Bilgrami, A. & R. Gaugler, 2007. Effects of various stress factors on heat tolerance by Heterorhabditis bacteriophora and Steinernema carpocapsae. Nematology, 9 (2): 161-167.
• 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.
• Boff, M. I., G. L. Wiegers & P. H. Smits, 2000. Effect of storage time and temperature on infectivity, reproduction and development of Heterorhabditis megidis in Galleria mellonella. Nematology, 2 (6): 635-644.
• Bütüner, A. K., M. İlktan & A. Susurluk, 2023. Effects of storage temperature on viability and virulence of entomopathogenic nematodes Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae), Steinernema carpocapsae Weiser, 1955 and Steinernema feltiae Filipjev, 1934 (Rhabditida: Steinernematidae). Turkish Journal of Entomology, 47 (3): 247-257.
• Campos-Herrera, R., M. Barbercheck, C. W. Hoy & S. P. Stock, 2012. Entomopathogenic nematodes as a model system for advancing the frontiers of ecology. Journal of Nematology, 44 (2): 162-176.
• Dede, E., A. K. Bütüner & A. Susurluk, 2022. Biocontrol potential of Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH hybrid strain against the beet webworm, Loxostege sticticalis L., 1761 (Lepidoptera: Pyralidae). Turkish Journal of Entomology, 46 (4): 399-405.
• Dzięgielewska, M., K. Kaczmarek & K. Kruk, 2023. The influence of temperature on the biological activity of selected nematode species (Steinernematidae and Heterorhabditidae) under the conditions of their coexistence. Plant Protection Science, 59 (2): 193-201.
• Ehlers, R. U., 1996. Current and future use of nematodes in biocontrol: practice and commercial aspects with regard to regulatory policy issues. Biocontrol Science and Technology, 6 (3): 303-316.
• Ehlers, R. U., 2001. Mass production of entomopathogenic nematodes for plant protection. Applied Microbiology and Biotechnology, 56 (5-6): 623-633.
• Ehlers, R. U. & D. I. Shapiro-Ilan, 2005. “Mass Production, 65-78”. In: Nematodes as Biocontrol Agents (Eds. P. S. Grewal, R. U. Ehlers & D. I. Shapiro-Ilan). CABI Publishing, Wallingford, UK, 523 pp.
• El-Lakwah, S. F. & H. Yousef, 2013. Relation between Energy Reserves Content and Infectivity of the Heterorhabditid and Steinernematid Entomopathogenic Nematodes under Low Soil Moisture. Egyptian Journal of Biological Pest Control, 23 (1): 103-107.
• Fitters, P. F., R. Dunne & C. T. Griffin, 2001. Improved control of Otiorhynchus sulcatus at 9ºC by cold-stored Heterorhabditis megidis UK211. Biocontrol Science and Technology, 11 (4): 483-492.
• Forst, S. & K. Nealson, 1996. Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiological reviews, 60 (1): 21-43.
• Gaugler, R., 1988. Ecological considerations in the biological control of soil-inhabiting insects with entomopathogenic nematodes. Agriculture, Ecosystems & Environment, 24 (1-3): 351-360.
• Gaugler, R., E. Lewis & R. J. Stuart, 1997. Ecology in the service of biological control: the case of entomopathogenic nematodes. Oecologia, 109 (4): 483-489.
• Grant, J. A. & M. G. Villani, 2003. Soil moisture effects on entomopathogenic nematodes. Environmental Entomology, 32 (1): 80-87.
• Griffin, C. T., 1996. Effects of prior storage conditions on the infectivity of Heterorhabditis sp. (Nematoda: Heterorhabditidae). Fundamental and Applied Nematology, 19 (1): 95-102.
• Johnigk, S. A. & R. U. Ehlers, 1999. Juvenile development and life cycle of Heterorhabditis bacteriophora and H. indica (Nematoda: Heterorhabditidae). Nematology, 1 (3): 251-260.
• Kahel‐Raifer, H. & I. Glazer, 2000. Environmental factors affecting sexual differentiation in the entomopathogenic nematode Heterorhabditis bacteriophora. Journal of Experimental Zoology, 287 (2): 158-166.
• Kaya, H. K. & R. Gaugler, 1993. Entomopathogenic nematodes. Annual Review of Entomology, 38 (1): 181-206.
• Kaya, H. K. & P. Stock, 1997. “Techniques in Insect Nematology, 281-324”. In: Manual of Techniques in Insect Pathology (Ed. A. Lawrence), Academic Press, 409 pp.
• Kung, S. P., R. Gaugler & H. K. Kaya, 1991. Effects of soil temperature, moisture, and relative humidity on entomopathogenic nematode persistence. Journal of Invertebrate Pathology, 57 (2): 242-249.
• Lephoto, T. E. & V. M. Gray, 2020. Desiccation stress tolerance of Steinernema australe and Heterorhabditis bacteriophora. Archives of Phytopathology and Plant Protection, 54 (11-12): 611-624.
• Lewis, E. E., J. Campbell, C. Griffin, H. Kaya & A. Peters, 2006. Behavioral ecology of entomopathogenic nematodes. Biological control, 38 (1): 66-79.
• Lillis, P. E., C. T. Griffin & J. C. Carolan, 2022. The effect of temperature conditioning (9ºC and 20ºC) on the proteome of entomopathogenic nematode infective juveniles. PloS one, 17 (4): e0266164.
• Lillis, P. E., I. P. Kennedy, J. C. Carolan & C. T. Griffin, 2023. Low-temperature exposure has immediate and lasting effects on the stress tolerance, chemotaxis and proteome of entomopathogenic nematodes. Parasitology, 150 (1): 15-28.
• Mejia-Torres, M. C. & A. Saenz, 2013. Ecological characterisation of the Colombian entomopathogenic nematode Heterorhabditis sp. SL0708. Brazilian Journal of Biology, 73 (2): 239-243.
• Nouh, G. M., 2022. Effect of temperature and soil moisture on the efficacy of indigenous and imported strains of the entomopathogenic nematode, Heterorhabditis sp. against the black cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae). Egyptian Journal of Biological Pest Control, 32 (1): 1-7.
• Půža, V. & Z. Mráček, 2007. Natural population dynamics of entomopathogenic nematode Steinernema affine (Steinernematidae) under dry conditions: Possible nematode persistence within host cadavers? Journal of Invertebrate Pathology, 96 (1): 89-92.
• Ringer, S., 1882. Concerning the influence exerted by each of the constituents of the blood on the contraction of the ventricle. The Journal of Physiology, 3 (5-6): 380-393.
• Shapiro-Ilan, D. I., D. H. Gouge, S. J. Piggott & J. P. Fife, 2006. Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biological Control, 38 (1): 124-133.
• Shapiro-Ilan, D. I., T. C. Leskey & S. E. Wright, 2011. Virulence of entomopathogenic nematodes to plum curculio, Conotrachelus nenuphar: Effects of strain, temperature, and soil type. Journal of Nematology, 43 (3-4): 187-195.
• Shaurub, E. H., N. A. Soliman, A. G. Hashem & A. M. Abdel-Rahman, 2015. Infectivity of four entomopathogenic nematodes in relation to environmental factors and their effects on the biochemistry of the Medfly Ceratitis capitata (Wied.) (Diptera: Tephritidae). Neotropical Entomology, 44 (6): 610-618.
• Stuart, R. J., M. E. Barbercheck, P. S. Grewal, R. A. Taylor & C. W. Hoy, 2006. Population biology of entomopathogenic nematodes: concepts, issues, and models. Biological Control, 38 (1): 80-102.
• Susurluk, I. A., 2008. Influence of temperature on the vertical movement of the entomopathogenic nematodes Steinernema feltiae (TUR-S3) and Heterorhabditis bacteriophora (TUR-H2), and infectivity of the moving nematodes. Nematology, 10 (1): 137-141.
• Susurluk, A. & R. U. Ehlers, 2008. Field persistence of the entomopathogenic nematode Heterorhabditis bacteriophora in different crops. BioControl, 53 (4): 627-641.
• Şahin, Y. S., A. Boucharı, T. C. Ulu, B. Sadıç & A. Susurluk, 2018. New application method for entomopathogenic nematode Heterorhabditis bacteriophora (Poinar, 1976) (Rhabditida: Heterorhabditidae) HBH strain against Locusta migratoria (Linnaeus, 1758) (Orthoptera: Acrididae). Turkish Journal of Entomology, 42 (4): 305-312.
• Ulu, T. C. & I. A. Susurluk, 2014. Heat and desiccation tolerances of Heterorhabditis bacteriophora strains and relationships between their tolerances and some bioecological characteristics. Invertebrate Survival Journal, 11 (1): 4-10.
• Ulu, T. C., B. Sadic & I. A. Susurluk, 2016. Effects of different pesticides on virulence and mortality of some entomopathogenic nematodes. Invertebrate Survival Journal, 13 (1): 111-115.
• Ulu, T. C. & I. A. Susurluk, 2021. Optimization of in vitro solid culture of Heterorhabditis bacteriophora Poinar, 1976 (Rhabditida: Heterorhabditidae) HBH hybrid strain. Turkish Journal of Entomology, 45 (4): 441-449.
• Ulu, T. C., G. Özbudak, E. Ö. Düzenli, Ş. H. Çakır & A. Susurluk, 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.
• Vashisth, S., Y. S. Chandel & P. K. Sharma, 2013. Entomopathogenic nematodes-A review. Agricultural Reviews, 34 (3): 163-175.
• Wang, X. & P. S. Grewal, 2002. Rapid genetic deterioration of environmental tolerance and reproductive potential of an entomopathogenic nematode during laboratory maintenance. Biological Control, 23 (1): 71-78.
• Zhang, F., W. E. Makirita, L. Wu, Y. Gou, Y. Liu, L. Peng, M. Chacha, E. R. Mbega, X. Li, N. He & T. Liu, 2019. Effects of growth conditions on the forms of Xenorhabdus nematophila: a symbiotic bacterium of the entomopathogenic Steinernema carpocapsae. Journal of Biobased Materials and Bioenergy, 13 (3): 346-352.