Persistence, horizontal movement, and efficacy of the Thai indigenous entomopathogenic nematode, Steinernema hermaphroditum EPNKU60 against larvae and pupae of stable fly, Stomoxys calcitrans L. (Diptera: Muscidae) under laboratory conditions
Main Article Content
Abstract
The stable fly (Stomoxys calcitrans) is an important insect pest in livestock production because it is both a nuisance and a disease carrier. The use of chemical insecticides on farms is reduced via biological control of stable fly populations. The use of the entomopathogenic nematodes (EPN) has been successful in controlling many insects worldwide, especially those that live on the ground. The purpose of this study was to investigate the ability of the EPN, Steinernema hermaphroditum EPNKU60 against the stable fly under laboratory conditions. The death rate of the last instar of the greater wax worm (Galleria mellonella) employed as bait was used to determine the EPN's persistence and horizontal movement ability in cow manure. The EPN survived in cow manure at 1, 3, 5, and 7 days, with all treatments killing 100% of wax moth larvae within 72 hours of testing. The EPN approached the prey horizontally at distances of 0, 5, 10, and 15 cm, with all treatments resulting in a mortality rate of wax moth larvae ranging from 98-100% within 72 hours of testing. Furthermore, the second instar of stable fly was more susceptible to the EPN than the third instar, however the EPN did not infect the pupal stage. At 144 hours following testing, the EPN at rates of 12, 25, 50, and 100 IJs/cm2 killed the second and third instars of stable fly larvae at 70-100% and 47-87%, respectively. In conclusion, S. hermaphroditum EPNKU60 may survive and hunt for prey in cow manure. It is also useful in controlling stable fly larvae.
Article Details

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
จุรีพร สุคติภูมิ, นริศ ท้าวจันทร์ และประกายจันทร์ นิ่มกิ่งรัตน์. 2565. ศักยภาพในการควบคุมแมลงวันแตง Zeugodacus cucurbitae Coquillett (Diptera: Tephritidae) โดยไส้เดือนฝอยและเชื้อราก่อโรคแก่แมลง. แก่นเกษตร. 50(5): 1459-1471.
ประกายจันทร์ นิ่มกิ่งรัตน์ และทิพย์สุคนธ์ อนุภาพ. 2560. ประสิทธิภาพไส้เดือนฝอยศัตรูแมลงสายพันธุ์ไทย Steinernema siamkayai ร่วมกับสารเคมีกำจัดแมลง. แก่นเกษตร. 45(ฉบับพิเศษ 1): 475-480.
รัตนาวดี อ่อนวงษ์, นิยาภรณ์ ขวัญเกตุ, อัศเลข รัตนวรรณี, ประกาย ราชณุวงษ์ และอธิราช หนูสีดำ. 2564. การจำแนกไส้เดือนฝอยศัตรูแมลง สกุล Heterorhabditis ในประเทศไทยด้วยวิธีทางชีวโมเลกุลและการก่อโรคต่อหนอนกินรังผึ้ง, Galleria mellonella L. (Lepidoptera: Pyralidae). แก่นเกษตร. 49(6): 1583-1596.
Azevedo, L. H., M. P. Ferreira, R. C. Castilho, P. D. Cancado, and G. J. Moraes. 2018. Potential of Macrocheles species (Acari: Mesostigmata: Macrochelidae) as control agents of harmful flies (Diptera) and biology of Macrocheles embersoni Azevedo, Castilho and Berto on Stomoxys calcitrans (L.) and Musca domestica L. (Diptera: Muscidae). Biological Control. 123: 1-8.
Bedding, R. A., A. S. Molyneux, and R. J. Akhurst. 1983. Heterorhabditis spp., Neoaplectana spp., and Steinernema kraussei: Interspecific and intraspecific differences in infectivity for insects. Experimental Parasitology. 55: 249-257.
Campos-Herrera, R., J.M. Go´mez-Ros, M. Escuer, L. Cuadra, L. Barrios, and C. Gutierrez. 2008. Diversity, occurrence, and life characteristics of natural entomopathogenic nematode populations from La Rioja (Northern Spain) under different agricultural management and their relationships with soil factors. Soil Biological Chemistry. 40(6): 1474-1484.
Clark, B. 2001. Virulence and persistence of entomopathogenic nematodes toward filth flies in cattle feedlot manure. M. S. Thesis. University of Nebraska Lincoln, NE.
Cook, D. F., D. V. Telfer, J. B. Lindsey, and R. A. Deyl. 2018. Substrates across horticultural and livestock industries that support the development of stable fly, Stomoxys calcitrans (Diptera: Muscidae). Austral Entomology. 57(3): 1-5.
Glazer, I., and E. E. Lewis. 2000. Bioassays for entomopathogenic nematodes. pp. 229-247. In: A. Navon and K. R. S. Ascher. Bioassays of Entomopathogenic Microbes and Nematodes. CABI Publishing, Wallingford, The United Kingdom.
Griffin, C. T., N. E. Boemare, and E. E. Lewis. 2005. Biology and behaviour. pp. 47-64. In: P. S. Grewal, R. U. Ehlers, and D. I. Shapiro-Ilan. Nematodes as Biocontrol Agents. CABI Publishing. Wallingford. The United Kingdom.
Heve, W. K., F. E. El-Borai, D. Carrillo, and L. W. Duncan. 2017. Biological control potential of entomopathogenic nematodes for management of Caribbean fruit fly, Anastrepha suspensa Loew (Tephritidae). Pest Management Science. 73(6): 1220-1228.
Jabbour, R., and M. E. Barbercheck. 2008. Soil and habitat complexity effects on movement of the entomopathogenic nematode Steinernema carpocapsae in maize. Biological Control. 47(2): 235-243.
Kaya, H. K., and R. Gaugler. 1993. Entomopathogenic nematodes. Annual Review of Entomology. 38: 181-206.
Kung, S. P., R. R. Gaugler, and H. K. Kaya. 1990. Influence of soil pH and oxygen on persistence of Steinernema spp. Journal of Nematology. 22(4): 440-445.
Leal, L. C. S. R., C. M. O. Monteiro, A. É. Mendonça, V. R. E. P. Bittencourt, and A. J. Bittencourt. 2017. Potential of entomopathogenic nematodes of the genus Heterorhabditis for the control of Stomoxys calcitrans (Diptera: Muscidae). Revista Brasileira de Parasitologia Veterinaria. 26(4): 451-456.
Lewis, E. E., and D. J. Clarke. 2012. Nematode parasites and Entomopathogens. pp. 395-424. In: F. Vega and H. K. Kaya. Insect Pathology. Elsevier, Amsterdam, The Netherlands.
Machtinger, E. T., C. J. Geden, P. E. Kaufman, and A. M. House. 2015. Use of pupal parasitoids as biological control agents of filth flies on equine facilities. Journal of Integrated Pest Management. 6(1): 1-10.
Mahmoud, F. M., N. S. Mandour, and Y. I. Pomazkov. 2007. Efficacy of the entomopathogenic nematode Steinernema feltiae Cross N 33 against larvae and pupae of four fly species in the laboratory. Nematologia Mediterranea. 35(2): 221-226.
Malaithong, N., G. Duvallet, R. Ngoen-Klan, M. J. Bangs, and T. Chareonviriyaphap. 2019. Stomoxyinae flies in Thailand: A Précis, with abridged taxonomic key to the adult species. Vector-Borne Zoonotic Diseases. 19(6): 385-394.
Mihok, S., E. K. Kang'ethe, and G. K. Kamau. 1995. Trials of traps and attractants for Stomoxys spp. (Diptera: Muscidae). Journal of Medical Entomology. 32(3): 283-289.
Molyneux, A. S., R. A. Bedding, and R. J. Akhurst. 1983. Susceptibility of larvae of the sheep blow fly Lucilia cuprina to various Heterorhabditis spp., Neoaplectana spp. and an undescribed Steinernematid (Nematoda). Journal of Invertebrate Pathology. 42(1): 1-7.
Moraes, A. P. R. 2007. Stomoxys calcitrans: estabelecimento de colônia e efeito de Metarhizium anisopliae sobre seus estágios imaturos. M. S. Thesis. Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro.
Noitubtim, P., B. L. Caoili, and A. Noosidum. 2022. Productivity of five entomopathogenic nematodes in Galleria mellonella L. and their persistence in soil under laboratory conditions. International Journal of Agricultural Technology. 18(2): 667-678.
Noosidum, A., A. K. Hodson, E. E. Lewis, and A. Chandrapatya. 2010. Characterization of new entomopathogenic nematodes from Thailand: foraging behavior and virulence to the greater wax moth, Galleria mellonella L. (Lepidoptera: Pyralidae). Journal of Nematology. 42(4): 281-291.
Noosidum, A., P. Satwong, A. Chandrapatya, and E. E. Lewis. 2016. Efficacy of Steinernema spp. plus anti-desiccants to control two serious foliage pests of vegetable crops, Spodoptera litura F. and Plutella xylostella L. Biological Control. 97: 48-56.
Noosidum, A., S. Mangtab, and E. E. Lewis. 2021. Biological control potential of entomopathogenic nematodes against the striped flea beetle, Phyllotreta sinuata Stephens (Coleoptera: Chrysomelidae). Crop Protection. 144: 105448.
Parr, H. C. M. 1962. Studies on Stomoxys calcitrans (L.) in Uganda (Diptera). Journal of the Entomological Society of Southern Africa. 25(1): 73-81.
Pitzer, J. B., P. E. Kaufman, J. A. Hogsette, C. J. Geden, and S. H. Tenbroeck. 2011. Seasonal abundance of stable flies and filth fly pupal parasitoids (Hymenoptera: Pteromalidae) at Florida equine facilities. Veterinary Entomology. 104(3): 1108-1115.
Poinar, G. O., and A. Hom. 1986. Survival and horizontal movement of infective stage Neoaplectana carpocapsae in the field. Journal of Nematology. 18(1): 34-6.
Rochon, K., J. A. Hogsette, P. E. Kaufman, P. U. Olafson, S. L. Swiger, and D. B. Taylor. 2021. Stable Fly (Diptera: Muscidae)-biology, management, and research needs. Journal of Integrated Pest Management. 12(1): 38: 1-23.
Rohde, C., N. R. Mertz, and Jr. A. Moino. 2020. Entomopathogenic nematodes on control of Mediterranean fruit fly (Diptera: Tephritidae). Revista Caatinga. 33(4): 974-984.
Salem, A., M. Franc, P. Jacquiet, E. Bouhsira, and E. Liénard. 2012. Feeding and breeding aspects of Stomoxys calcitrans (Diptera: Muscidae) under laboratory conditions. Parasite. 19(4): 309-317.
Shapiro-Ilan, D. I., H. G. Dawn, J. P. Simon, and P. F. Jane. 2006. Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biological Control. 38(1): 124-133.
Shapiro-Ilan, D. I., S. Hazir, and I. Glazer. 2017. Basic and Applied Research: Entomopathogenic Nematodes. pp. 91-105. In: L. A. Lacey. Microbial Control of Insect and Mite Pests from Theory to Practice. Academic Press, Amsterdam, The Netherlands.
Sharifi, S., J. Karimi, M. Hosseini, and M. Rezapanah. 2014. Efficacy of two entomopathogenic nematode species as potential biocontrol agents against the rosaceae longhorned beetle, Osphranteria coerulescens, under laboratory conditions. Nematology. 16(6): 729-737.
Snodgrass, R. E. 1954. Insect Metamorphosis. The Smithsonian Institution, WA.
Taylor, D. B., R. D. Moon, and D. R. Mark. 2012. Economic impact of stable flies (Diptera: Muscidae) on dairy and beef cattle production. Journal of Medical Entomology. 49: 198-209.
Toledo, J. J., E. Ibarra, P. Liedo, A. Gómez, M. A. Rasgado, and T. Williams. 2005. Infection of Anastrepha ludens (Diptera: Tephritidae) larvae by Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) under laboratory and field conditions. Biocontrol Science and Technology. 15(6): 627-634.
Toledo, J. J., L. Gurgúa, P. Liedo, J. E. Ibarra, and A. Oropeza. 2001. Parasitismo de larvas y pupas de la mosca mexicana de la fruta, Anastrepha ludens (Loew) (Diptera: Tephritidae) por el nemátodo Steinernema feltiae (Filipjev) (Rhabditida: Steinernematidae). Vedalia. 8: 27-36.
Torr, P., S. Heritage, and M. J. Wilson. 2004. Vibrations as a novel signal for host location by parasitic nematodes. International Journal for Parasitology. 34(9): 997-999.
White, G. F. 1927. A method for obtaining infective nematode larvae from cultures. Science. 66(1709): 302-303.
Zumpt, F. K. E. 1973. The Stomoxyine Biting Flies of the World. Diptera: Muscidae. Taxonomy, biology, economic importance and control measures. Gustav Fischer Verlag. Stuttgart, Germany.