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Do sterile males and females synergistically suppress pests targeted by the sterile insect technique?

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Abstract

The sterile insect technique (SIT) is a pest control method that releases a large number of sterile pests into the field to inhibit mating between wild pests, ultimately resulting in the eradication of wild pest populations. It has often been discussed whether releasing one sex (mainly males) of sterile insects enhances the pest control efficiency of SIT compared to releasing both sexes (bisexual release). The control efficiency of sterile females may be negatively affected by their release, because sterile males lose the opportunity to mate with wild females. In this study, we investigated whether sterile females have a positive effect on the control efficiency of SIT and whether there is an additive or synergistic effect of releasing both sexes using two weevil species, Cylas formicarius and Euscepes postfasciatus, which are serious pests of the sweet potato Ipomoea batatas and targets of SIT in Okinawa. The results showed that in both species, the reproduction rate of wild pests was significantly suppressed in the case of the sterile female-only release. Interestingly, the most effective method varied between male-only and bisexual release depending on the density of sterile individuals and weevil species. Synergistic effects of both sexes on bisexual release were observed but varied with the density of sterile individuals and weevil species. High-density bisexual release was most effective for the SIT of at least two weevil species.

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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abraham S, Cladera J, Goane L, Teresa Vera MT (2012) Factors affecting Anastrepha fraterculus female receptivity modulation by accessory gland products. J Insect Physiol 58:1–6. https://doi.org/10.1016/j.jinsphys.2011.08.007

    Article  CAS  PubMed  Google Scholar 

  • Adnan SM, Farhana I, Rempoulakis P, Taylor PW (2020) Methoprene-induced matings of young Queensland fruit fly males are effective at inducing sexual inhibition in females. J Appl Entomol 144:500–508. https://doi.org/10.1111/jen.12753

    Article  CAS  Google Scholar 

  • Ailam G, Galun R (1967) Optimal sex ratio for the control of insects by the sterility method. Ann Entomol Soc Am 60:41–43. https://doi.org/10.1093/aesa/60.1.41

    Article  CAS  PubMed  Google Scholar 

  • Bloem K, Bloem S, Rizzo N, Chambers D (1993) Female medfly refractory period: Effect of male reproductive status. In: Aluja M, Liedo P (eds) Fruit flies. Springer-Verlag, New York, pp 189–190

    Chapter  Google Scholar 

  • Fran G, Bourtzis K, Cáceres C (2021) Practical and operational genetic sexing systems based on classical genetic approaches in fruit flies, an example for other species amenable to large-scale rearing for the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated pest management, 2nd edn. CRC Press, Boc Raton, FL, pp 575–604

    Chapter  Google Scholar 

  • Harmer AM, Radhakrishnan P, Taylor PW (2006) Remating inhibition in female Queensland fruit flies: effects and correlates of sperm storage. J Insect Physiol 52:179–186. https://doi.org/10.1016/j.jinsphys.2005.10.003

    Article  CAS  PubMed  Google Scholar 

  • Hight SD, Carpenter JE, Bloem S, Bloem KA (2005) Developing a sterile insect release program for Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae): effective overflooding ratios and release-recapture field studies. Environ Entomol 34:850–856. https://doi.org/10.1603/0046-225X-34.4.850

    Article  Google Scholar 

  • Himuro C, Honma A, Ikegawa Y, Kumano N (2022a) The female Euscepes postfasciatus refractory period is induced by the male but length is determined by the female. J Insect Physiol 142:104427. https://doi.org/10.1016/j.jinsphys.2022.104427

    Article  CAS  PubMed  Google Scholar 

  • Himuro C, Ikegawa Y, Honma A (2017) Males use accessory gland substances to inhibit remating by females in West Indian sweetpotato weevil (Coleoptera: Curculionidae). Ann Entomol Soc Am 110:374–380. https://doi.org/10.1093/aesa/sax036

    Article  CAS  Google Scholar 

  • Himuro C, Honma A, Ikegawa Y, Ohishi T, Miyatake T (2021) Male body size does not affect the refractory period of females in the West Indian sweet potato weevil Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae) and the seed bug Togo hemipterus (Scott) (Heteroptera: Lygaeidae). J Ethol 39:39–46. https://doi.org/10.1007/s10164-020-00669-9

    Article  Google Scholar 

  • Himuro C, Kohama T, Matsuyama T, Sadoyama Y, Kawamura F, Honma A, Ikegawa Y, Haraguchi D (2022b) First case of successful eradication of the sweet potato weevil, Cylas formicarius (Fabricius), using the sterile insect technique. PLoS ONE 17:e0267728. https://doi.org/10.1371/journal.pone.0267728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Himuro C, Misa K, Honma A, Ikegawa Y, Ohishi T, Kumano N (2022c) Effects of larval diet on the male reproductive traits in the West Indian sweet potato weevils Euscepes postfasciatus (Coleoptera: Curculionidae). InSects 13:389. https://doi.org/10.3390/insects13040389

    Article  PubMed  PubMed Central  Google Scholar 

  • Hiroyoshi S, Kohama T, Reddy GVP (2016) Age-related sperm production, transfer, and storage in the sweet potato weevil, Cylas formicarius (Fabricius) (Coleoptera: Curculionidae). J Insect Behav 29:689–707. https://doi.org/10.1007/s10905-016-9590-0

    Article  Google Scholar 

  • Hiroyoshi S, Reddy GVP, Kohama T (2017) Sperm supply from the testes to the seminal vesicle over consecutive matings in the sweetpotato weevil, Cylas formicarius (Fabricius) (Coleoptera: Curculionidae). Am J Life Sci. https://doi.org/10.11648/j.ajls.20170504.12

    Article  Google Scholar 

  • Hiroyoshi S, Mitsunaga T, Kohama T, Reddy GVP (2023) Effects of ejaculate size on remating, attractiveness, and oviposition in females of the sweetpotato weevil, Cylas formicarius. Entomol Exp Appl 171:268–276. https://doi.org/10.1111/eea.13275

    Article  Google Scholar 

  • Ikegawa Y, Ito K, Himuro C, Honma A (2021) Sterile males and females can synergistically suppress wild pests targeted by sterile insect technique. J Theor Biol 530:110878. https://doi.org/10.1016/j.jtbi.2021.110878

    Article  PubMed  Google Scholar 

  • Ikegawa Y, Kawamura F, Sadoyama Y, Kinjo K, Haraguchi D, Honma A, Himuro C, Matsuyama T (2022) Eradication of sweetpotato weevil, Cylas formicarius, from Tsuken Island, Okinawa, Japan, under transient invasion of males. J Appl Entomol 146:850–859. https://doi.org/10.1111/jen.13004

    Article  Google Scholar 

  • Klassen W, Curtis CF, Hendrichs J (2021) History of the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: Principles and practice in area-wide integrated pest management, 2nd edn. CRC Press, Boc Raton, FL, pp 1–44

    Google Scholar 

  • Knipling EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462. https://doi.org/10.1093/jee/48.4.459

    Article  Google Scholar 

  • Knipling EF (1959) Sterile-male method of population control. Science 130:902–904. https://doi.org/10.1126/science.130.3380.902

    Article  CAS  PubMed  Google Scholar 

  • Knipling EF (1979) The basic principles of insect population suppression and management, vol 512. United States Department of Agriculture, US

    Google Scholar 

  • Kohama T, Shimoji Y (1998) Reproductive maturity of the female West Indian sweet potato weevil, Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae). Appl Entomol Zool 33:1–4. https://doi.org/10.1303/aez.33.1

    Article  Google Scholar 

  • Kohama T, Sugiyama M (2000) External characteristics for sexing the West Indian sweet potato weevil, Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae). Entomol Sci 3:43–46

    Google Scholar 

  • Kohama T, Yamagishi M, Kuba H, Kinjo K (2003) A progress report on the eradication program of the sweet potato weevil, Cylas formicarius (Fabricius) (Coleoptera: Brentidae), with both male annihilation using sex pheromone and sterile insect releases in Kume Island, Okinawa, Japan. In: Recent trends on sterile insect technique and area wide integrated pest management: economic feasibility, control projects, farmer organization and Bactrocera dorsalis complex control study. Research Institute for Subtropics, Naha, Japan, pp 65–69

  • Kuba H, Kohama T, Haraguchi D (2003) Eradication projects of exotic sweet potato weevils using SIT in Okinawa. In: Oka M, Matsui M, Shiomi T, Ogawa Y, Tsuchiya K (eds) Proceedings of the NIAES-FFTC joint international seminar on biological invasions: Environmental impacts and the development of a database for the Asian-Pacific region. National Institute for Agro-Environmental Sciences & Food and Fertilizer Technology Center for the Asian and Pacific Region, Tsukuba, Japan, p 273–287

  • Kumano N (2014) Recent advances in the study on sterile technique for the West Indian sweet potato weevil, Euscepes postfasciatus. Jpn J Appl Entomol Zool. https://doi.org/10.1303/jjaez.2014.217. (in Japanese with English abstract)

    Article  Google Scholar 

  • Kumano N, Kawamura F, Haraguchi D, Kohama T (2009) Irradiation does not affect field dispersal ability in the West Indian sweetpotato weevil, Euscepes postfasciatus. Entomol Exp Appl 130:63–72. https://doi.org/10.1111/j.1570-7458.2008.00795.x

    Article  Google Scholar 

  • Kuriwada T (2013) Recent advances in the study for eradication projects of the sweet potato weevil. Jpn J Appl Entomol Zool. https://doi.org/10.1303/jjaez.2013.1. (in Japanese with English abstract)

    Article  Google Scholar 

  • Kuriwada T, Kumano N, Shiromoto K, Haraguchi D (2013) Effects of intra-and inter-specific competition on fitness of sweetpotato weevil and West Indian sweetpotato weevil. J Appl Entomol 137:310–316. https://doi.org/10.1111/j.1439-0418.2012.01745.x

    Article  Google Scholar 

  • Lance DR, McInnis DO (2021) Biological basis of the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated pest management, 2nd edn. CRC Press, Boca Raton, FL, pp 113–142

    Chapter  Google Scholar 

  • Lees RS, Carvalho DO, Bouyer J (2021) Potential impact of integrating the sterile insect technique in to the fight against disease-transmitting mosquitoes. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated pest management, 2nd edn. CRC Press, Boca Raton, FL, pp 1081–1118

    Chapter  Google Scholar 

  • McInnis DO, Lance DR, Jackson CG (1996) Behavioral resistance to the sterile insect technique by Mediterranean fruit fly (Diptera: Tephritidae) in Hawaii. Ann Entomol Soc Am 89:739–744. https://doi.org/10.1093/aesa/89.5.739

    Article  Google Scholar 

  • McInnis DO, Wong TTY, Tam SYT (1986) Mediterranean fruit fly (Diptera: Tephritidae): suppression efficiencies of unisexual and bisexual sterilized release populations in field cages. Ann Entomol Soc Am 79:931–937. https://doi.org/10.1093/aesa/79.6.931

    Article  Google Scholar 

  • Miyaji K, Nishihara S, Hara Y, Tokunaga T, Hatano T, Kamikado T, Ito S, Iwamoto J, Aramaki Y, Kinjo K, Sokei Y (2000) Eradication of weevils by sterile-insect-release method (6) methods of mass rearing, sterilization, marking, and release of Cylas formicarius. Plant Prot 54:30–33 (in Japanese)

    Google Scholar 

  • Miyatake T, Chapman T, Partridge L (1999) Mating-induced inhibition of remating in female Mediterranean fruit flies Ceratitis capitata. J Insect Physiol 45:1021–1028. https://doi.org/10.1016/S0022-1910(99)00083-9

    Article  CAS  PubMed  Google Scholar 

  • Moriya S (1995) A preliminary study on the flight ability of the Sweetpotato weevil, Cylas formicarius (Fabricius) (Coleoptera: Apionidae) using a flight mill. Appl Entomol Zool 30:244–246. https://doi.org/10.1303/aez.30.244

    Article  Google Scholar 

  • Moriya S, Miyatake T (2001) Eradication programs of two Sweetpotato pests, Cylas formicarius and Euscepes postfasciatus, in Japan with special reference to their dispersal ability. JARQ 35:227–234. https://doi.org/10.6090/jarq.35.227

    Article  Google Scholar 

  • Ohishi T, Matsuyama T, Himuro C, Ohno S, Sadoyama Y, Kinjo M, Honma A (2018) The eradication projects and the phytosanitary measures for quarantine pests in Okinawa. In: Proceedings of the 2018 international symposium on proactive technologies for enhancement of integrated pest management on key crop, p 31–48

  • Okinawa Prefectural Plant Protection Center (2012) Project report on control of special diseases and insect pests in Okinawa Prefecture 2012, vol 38. Okinawa Prefectural Plant Protection Center, Naha, p 165 (in Japanese)

  • Okinawa Prefectural Plant Protection Center (2020) Project report on control of special diseases and insect pests in Okinawa Prefecture 2012, vol 46. Okinawa Prefectural Plant Protection Center, Naha, p 170–202 (in Japanese)

  • Parker AG, Mamai W, Maiga H (2021) Mass-rearing for the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated pest management, 2nd edn. CRC Press, Boc Raton, FL, pp 283–316

    Chapter  Google Scholar 

  • R Core Team (2016). R: A Language and Environment for Statistical Computing. https://www.R-project.org/. R Foundation for Statistical Computing, Vienna

  • Radhakrishnan P, Taylor PW (2007) Seminal fluids mediate sexual inhibition and short copula duration in mated female Queensland fruit flies. J Insect Physiol 53:741–745. https://doi.org/10.1016/j.jinsphys.2006.10.009

    Article  CAS  PubMed  Google Scholar 

  • Rendón P, McInnis D, Lance D, Stewart J (2004) Medfly (Diptera: Tephritidae) genetic sexing: large-scale field comparison of males-only and bisexual sterile fly releases in Guatemala. J Econ Entomol 97:1547–1553. https://doi.org/10.1603/0022-0493-97.5.1547

    Article  PubMed  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. https://doi.org/10.2307/2409177

    Article  PubMed  Google Scholar 

  • Sato Y, Kohama T (2007) Post-copulatory mounting behavior of the West Indian sweetpotato weevil, Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae). Ethology 113:183–189. https://doi.org/10.1111/j.1439-0310.2006.01309.x

    Article  Google Scholar 

  • Seawright JA (1988) Genetic methods for control of mosquitoes and biting flies. https://www.iaea.org/sites/default/files/ipc-modern-insect-control.pdf. In: Proceedings of the symposium: Modern insect control: Nuclear techniques and biotechnology. STI/PUB/763. International Atomic Energy Agency and Food and Agriculture Organization of the United Nations, Vienna, Austria. International Arts and Entertainment Alliance, Vienna, Austria, p 179–191

  • Sherman M, Tamashiro M (1954) The sweet-potato weevils in Hawaii: their biology and control. Hawaii Agric Exp Sta Res Bull 23:1–36

    Google Scholar 

  • Sugimoto T, Sakuratani Y, Fukui H, Kiritani K, Okada T (1996) Estimating the reproductive properties of the sweet potato weevil, Cylas formicarius (Fabricius) (Coleoptera, Brentidae). Appl Entomol Zool 31:357–367. https://doi.org/10.1303/aez.31.357

    Article  Google Scholar 

  • Sutherland JA (1986) A review of the biology and control of the sweetpotato weevil Cylas formicarius (Fab). Trop Pest Manag 32:304–315. https://doi.org/10.1080/09670878609371084

    Article  CAS  Google Scholar 

  • Tsurui-Sato K, Ohishi T, Kumano N, Teruya K, Toyosato T, Tatsuta H, Tsuji K (2019) Spatial sexual segregation in the West Indian sweet potato weevil, Euscepes postfasciatus (Coleoptera: Curculionidae): a consideration in terms of behavioral mechanism suppressing population growth. Jpn J Environ Entomol Zool 30:151–159 (in Japanese with English abstract)

    Google Scholar 

  • Vreysen MJB, Barclay HJ, Hendrichs J (2006) Modeling of preferential mating in areawide control programs that integrate the release of strains of sterile males only or both sexes. Ann Entomol Soc Am 99:607–616. https://doi.org/10.1603/0013-8746(2006)99[607:MOPMIA]2.0.CO;2

    Article  Google Scholar 

  • Whitten MJ, Taylor WC (1970) A role for sterile females in insect control. J Econ Entomol 63:269–272. https://doi.org/10.1093/jee/63.1.269

    Article  CAS  PubMed  Google Scholar 

  • Wood SN (2017) Generalized additive models an introduction with R, 2nd edn. CRC Press, Boca Raton, FL

    Book  Google Scholar 

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Acknowledgements

The authors thank Mr. Satoshi Kinjo, Mr. Kazuya Uehara, Ms. Midori, Ms. Toyoko Izumi, Mr. Tomoaki Yohena, and DJ Flyday for their assistance in conducting the experiments. The authors also thank the members of the Okinawa Prefectural Plant Protection Center and Ryukyu Sankei Co. Ltd. for their assistance with this study. This study was supported by the Grants-in-Aid for Scientific Research (C) (No.18K05667 to C.H.) and Challenging Research (Exploratory) (No.21K19116 to C.H.) from the Japan Society for the Promotion of Science. The experiments conducted in this study complied with the current laws in Japan.

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The work of Chihiro Himuro was funded by Japan Society for the Promotion of Science, under Grant Nos. 18K05667 and 21K19116.

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Dr. Chihiro Himuro conceived and designed the study. The material preparation, data collection, and analysis were performed by Dr. Chihiro Himuro. Dr. Chihiro Himuro wrote the first draft of the manuscript. Dr. Yusuke Ikegawa commented on the previous versions of the manuscript. All the authors have read and approved the final version of the manuscript.

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Correspondence to Chihiro Himuro.

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Himuro, C., Ikegawa, Y. Do sterile males and females synergistically suppress pests targeted by the sterile insect technique?. Appl Entomol Zool 59, 185–193 (2024). https://doi.org/10.1007/s13355-024-00868-7

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