Abstract
The invasive, Halyomorpha halys (Hemiptera: Pentatomidae), is a severe economic insect pest native to East Asia. A strong effort has been made to identify natural egg parasitoids of H. halys in invaded regions, but parasitism rates reported from these studies have been inconsequentially low. To determine the species composition, phenology, and efficiency of egg parasitoids in the native region of H. halys, we deployed fresh and frozen sentinel H. halys egg masses from March through December in Kyoto, Japan. Our findings provide valuable insights on the abundance and parasitism rates of native H. halys parasitoids in Japan. A total of seven parasitoid species emerged from the sentinel egg masses, but Trissolcus japonicus had the highest parasitism rate of all parasitoids recovered (84% on fresh egg masses) and maintained the largest portion of the total parasitoid species composition (60% on fresh egg masses). The early season parasitoid community in Kyoto, Japan, is dominated by T. japonicus, with the first parasitism activity occurring in March. Throughout the course of the field study, T. japonicus also sustained a significantly higher parasitism rate on fresh H. halys eggs than frozen. The results from this research help expand the understanding of parasitoids in the native region of H. halys and hold importance for the future development of biological control programs against this invasive pest.
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All the sequences have been deposited in GenBank with accession numbers provided in the main text. All parasitoid samples can be made accessible upon request to the first and corresponding authors.
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References
Abram PK, Gariepy TD, Boivin G, Brodeur J (2014) An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biol Invasions 16:1387–1395. https://doi.org/10.1007/s10530-013-0576-y
Abram PK, Brodeur J, Burte V, Boivin G (2016) Parasitoid-induced host egg abortion: an underappreciated component of biological control services provided by egg parasitoids. Biol Control 98:52–60. https://doi.org/10.1016/j.biocontrol.2016.04.002
Abram PK, Hoelmer KA, Acebes-Doria A et al (2017) Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. J Pest Sci 90:1009–1020. https://doi.org/10.1007/s10340-017-0891-7
Abram PK, Brodeur J, Urbaneja A, Tena A (2019) Nonreproductive effects of insect parasitoids on their hosts. Annu Rev Entomol 64:259–276. https://doi.org/10.1146/annurev-ento-011118-111753
Arakawa R, Namura Y (2002) Effects of temperature on development of three Trissolcus spp. (Hymenoptera: Scelionidae), egg parasitoids of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Entomol Sci 5:215–218. https://doi.org/10.1303/aez.2004.177
Avila GA, Charles JG (2018) Modelling the potential geographic distribution of Trissolcus japonicus: a biological control agent of the brown marmorated stink bug, Halyomorpha halys. BioControl 63:505–518. https://doi.org/10.1007/s10526-018-9866-8
Avila GA, Chen J, Li W, Alavi M, Mi Q, Sandanayaka M, Zhang F, Zhang J (2021) Seasonal abundance and diversity of egg parasitoids of Halyomorpha halys in kiwifruit orchards in China. Insects 12:428. https://doi.org/10.3390/insects12050428
Bertoldi V, Rondoni G, Brodeur J, Conti E (2019) An egg parasitoid efficiently exploits cues from a coevolved host but not those from a novel host. Front Physiol 10:746. https://doi.org/10.3389/fphys.2019.00746
Charles JG, Avila GA, Hoelmer KA, Hunt S, Gardner-Gee R, MacDonald F, Davis V (2019) Experimental assessment of the biosafety of Trissolcus japonicus in New Zealand, prior to the anticipated arrival of the invasive pest Halyomorpha halys. Biocontrol 64:367–379. https://doi.org/10.1007/s10526-019-09949-x
Chen YM, Gibson GAP, Peng LF, Iqbal A, Zang LS (2019) Anastatus Motschulsky (Hymenoptera, Eupelmidae): egg parasitoids of Caligula japonica Moore (Lepidoptera, Saturniidae) in China. ZooKeys 881:109–134. https://doi.org/10.3897/zookeys.881.34646
Conti E, Colazza S (2012) Chemical ecology of egg parasitoids associated with true bugs. Psyche. https://doi.org/10.1155/2012/651015
Cornelius M, Dieckhoff C, Vinyard BT, Hoelmer KA (2016) Parasitism and predation on sentinel egg masses of the brown marmorated stink bug (Hemiptera: Pentatomidae) in three vegetable crops: importance of dissections for evaluating the impact of native parasitoids on an exotic pest. Environ Entomol 45:1536–1542. https://doi.org/10.1093/ee/nvw134
Costi E, Wong WHL, Cossentine J, Acheampong S, Maistrello L, Haye T, Talamas EJ, Abram PK (2020) Variation in levels of acceptance, developmental success, and abortion of Halyomorpha halys eggs by native North American parasitoids. Biol Control 151:104396. https://doi.org/10.1016/j.biocontrol.2020.104396
Dieckhoff C, Tatman KM, Hoelmer KA (2017) Natural biological control of Halyomorpha halys by native egg parasitoids: a multi-year survey in northern Delaware. J Pest Sci 90:1143–1158. https://doi.org/10.1007/s10340-017-0868-6
Evans HF, Speight MR (2004) Health and protection | Integrated pest management practices. In: Burley J (ed) Encyclopedia of forest sciences. Elsevier Ltd, Oxford, pp 318–333
Faúndez EI, Rider DA (2017) The brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) in Chile. Arq Entomolóxicos 17:305–307
Fogain R, Graff S (2011) First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Ontario and Quebec. J Entomol Soc Ont 142:45–48
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Gariepy TD, Haye T, Fraser H, Zhang J (2014) Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. J Pest Sci 87:17–28. https://doi.org/10.1007/s10340-013-0529-3
Haye T, Gariepy T, Hoelmer K, Rossi J-P, Streito J-C, Tassus X, Desneux N (2015a) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88:665–673. https://doi.org/10.1007/s10340-015-0670-2
Haye T, Fischer S, Zhang J, Gariepy T (2015b) Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe? J Pest Sci 88:693–705. https://doi.org/10.1007/s10340-015-0671-1
Haye T, Moraglio ST, Stahl J, Visentin S, Gregorio T, Tavella L (2020) Fundamental host range of Trissolcus japonicus in Europe. J Pest Sci 93:171–182. https://doi.org/10.1007/s10340-019-01127-3
Hedstrom C, Lowenstein D, Andrews H, Bai B, Wiman N (2017) Pentatomid host suitability and the discovery of introduced populations of Trissolcus japonicus in Oregon. J Pest Sci 90:1169–1179. https://doi.org/10.1007/s10340-017-0892-6
Herlihy MV, Talamas EJ, Weber DC, Falabella P (2016) Attack and success of native and exotic parasitoids on eggs of Halyomorpha halys in three Maryland habitats. PLoS ONE 11(3):e0150275. https://doi.org/10.1371/journal.pone.0150275
Hirashima Y, Yamagishi K (1981) Redescriptions of the types of some Japanese Scelionidae preserved in the United States National Museum (Hymenoptera, Proctotrupoidea). J Fac Agr Kyushu Univ 25:153–159.https://doi.org/10.5109/23726
Hoddle MS (2004) Restoring balance: using exotic species to control invasive exotic species. Conserv Biol 18:38–49. https://doi.org/10.1111/j.1523-1739.2004.00249.x
Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237
Hull LA, VanStarner R (1983) Impact of four synthetic pyrethroids on major natural enemies and pests of apple in Pennsylvania. J Econ Entomol 76:122–130. https://doi.org/10.1093/jee/76.1.122
James DG (1988) Fecundity, longevity, and overwintering of Trissolcus biproruli Girault (Hymenoptera: Scelionidae) a parasitoid of Biprorulus bibax Breddin (Hemiptera: Pentatomidae). J Aust Ent Soc 27:297–301. https://doi.org/10.1111/j.1440-6055.1988.tb01177.x
Jones AL, Jennings DE, Hooks CRR, Shrewsbury PM (2014) Sentinel eggs underestimate rates of parasitism of the exotic brown marmorated stink bug Halyomorpha halys. Biol Control 78:61–66. https://doi.org/10.1016/j.biocontrol.2014.07.011
Kamiyama MT, Schreiner Z, Guédot C (2019) Diversity and abundance of natural enemies of Drosophila suzukii in Wisconsin, USA fruit farms. BioControl 64:665–676. https://doi.org/10.1007/s10526-019-09966-w
Kamiyama MT, Matsuura K, Yoshimura T, Yang CCY (2021a) Predation of the brown marmorated stink bug, Halyomorpha halys by the Japanese acrobat ants, Crematogaster matsumurai and Crematogaster osakensis. Biol Control. https://doi.org/10.1016/j.biocontrol.2021.104570
Kamiyama MT, Matsuura K, Yoshimura T, Yang CCY (2021b) Improving invasive species management using predictive phenology models: an example from brown marmorated stink bug (Halyomorpha halys) in Japan. Pest Manag Sci. https://doi.org/10.1002/ps.6589
Kaser JM, Akotsen-Mensah C, Talamas EJ, Nielsen AL (2018) First Report of Trissolcus japonicus parasitizing Halyomorpha halys in North American agriculture. Fla Entomol 101:680–683. https://doi.org/10.1653/024.101.0406
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. https://doi.org/10.1016/S0169-5347(02)02499-0
Konopka JK, Haye T, Gariepy T, Mason P, Gillespie D, McNeil JN (2017) An exotic parasitoid provides an invasional lifeline for native parasitoids. Ecol Evol 7:277–284. https://doi.org/10.1002/ece3.2577
Kriticos DJ, Kean JM, Phillips CB, Senay SD, Acosta H, Haye T (2017) The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. J Pest Sci 90:1033–1043. https://doi.org/10.1007/s10340-017-0869-5
Kuhar TP, Kamminga KL, Whalen J, Dively GP, Brust G, Hooks CRR, Hamilton G, Herbert DA (2012) The pest potential of brown marmorated stink bug on vegetable crops. Plant Health Prog. https://doi.org/10.1094/PHP-2012-0523-01-BR
Kuhar TP, Kamminga K (2017) Review of the chemical control research on Halyomorpha halys in the USA. J Pest Sci 90:2021–2031. https://doi.org/10.1007/s10340-017-0859-7
Kuki D, Wada Y, Tsunashima A, Itoyama K (2019) Developmental properties and parasitism capacity of the egg parasitoid Trissolcus japonicus (Hymenoptera: Scelionidae), reared on eggs of Glaucias subpunctatus (Hemiptera: Pentatomidae). Appl Entomol Zool 54:307–312. https://doi.org/10.1007/s13355-019-00627-z
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lara JR, Pickett CH, Kamiyama MT, Figueroa S, Romo M, Cabanas C, Bazurto V, Strode V, Briseno K, Lewis M, Oliva J, Hernandez G, Hoddle MS (2019) Physiological host range of Trissolcus japonicus in relation to Halyomorpha halys and other pentatomids from California. Biocontrol 64:513–528. https://doi.org/10.1007/s10526-019-09950-4
Lee D-H, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641. https://doi.org/10.1603/EN13006
Lee D-H, Short BD, Nielsen AL, Leskey TC (2014) Impact of organic insecticides on the survivorship and mobility of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in the laboratory. Fla Entomol 97:414–421. https://doi.org/10.1653/024.097.0211
Leskey TC, Short BD, Butler BR, Wright SE (2012a) Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), Mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche 2012:1–14. https://doi.org/10.1155/2012/535062
Leskey TC, Lee D-H, Short BD, Wright SE (2012b) Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. J Econ Entomol 105:1726–1735. https://doi.org/10.1603/EC12096
Malek R, Kaser JM, Anfora G, Ciolli M, Khrimian A, Weber DC, Hoelmer KA (2021) Trissolcus japonicus foraging behavior: Implications for host preference and classical biological control. Biol Control. https://doi.org/10.1016/j.biocontrol.2021.104700
Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution. Front Ecol Environ 4:132–140. https://doi.org/10.1890/1540-9295(2006)004[0132:BCOISS]2.0.CO;2
Meteoblue (2021) Weather archive Uji In: https://www.meteoblue.com/en/weather/ historyclimate/climatemodelled/uji_japan_1849372. Accessed 20 Jan 2021
Milnes JM, Beers EH (2019) Trissolcus japonicus (Hymenoptera:Scelionidae) causes low levels of parasitism in three North American pentatomids under field conditions. J Insect Sci 19:4. https://doi.org/10.1093/jisesa/iez074
Moraglio ST, Tortorici F, Pansa MG, Castelli G, Pontini M, Scovero S, Visentin S, Tavella L (2020) A 3-year survey on parasitism of Halyomorpha halys by egg parasitoids in northern Italy. J Pest Sci 93:183–194. https://doi.org/10.1007/s10340-019-01136-2
Morrison WR, Mathews CR, Leskey TC (2016) Frequency, efficiency, and physical characteristics of predation by generalist predators of brown marmorated stink bug (Hemiptera: Pentatomidae) eggs. Biol Control 97:120–130. https://doi.org/10.1016/j.biocontrol.2016.03.008
Nielsen AL, Hamilton GC, Matadha D (2008) Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environ Entomol 37:348–355. https://doi.org/10.1093/ee/37.2.348
Nielsen AL, Hamilton GC (2009) Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J Econ Entomol 102:1133–1140. https://doi.org/10.1603/029.102.0335
Nielsen AL, Holmstrom K, Hamilton GC, Cambridge J, Ingerson-Mahar J (2013) Use of black light traps to monitor the abundance, spread, and flight behavior of Halyomorpha halys (Hemiptera: Pentatomidae). J Econ Entomol 106:1495–1502. https://doi.org/10.1603/EC12472
Ogburn EC, Bessin R, Dieckhoff C, Dobson R, Grieshop M, Hoelmer KA, Mathews C, Moore J, Nielsen AL, Poley K, Pote JM, Rogers M, Welty C, Walgenbach JF (2016) Natural enemy impact on eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in organic agroecosystems: a regional assessment. Biol Control 101:39–51. https://doi.org/10.1016/j.biocontrol.2016.06.002
Pimentel D, Lach L, Zunigia R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65. https://doi.org/10.1641/0006-3568(2000)050[0053:EAECON]2.3.CO;2
Pote JM, Nielsen AL (2017) Life stage specific predation of Halyomorpha halys (Stål) by generalist predators. Biol Control 114:1–7. https://doi.org/10.1016/j.biocontrol.2017.07.007
R Core Team (2018) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing
Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks CR, Jones A, Krawczyk G, Kuhar T, Martinson H, Mitchell W, Nielson AL, Pfeiffer DG, Raupp MJ, Rodrigues-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman NG, Leskey TC, Tooker JF (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5:A1–A13. https://doi.org/10.1603/IPM14002
Roversi PF, Binazzi F, Marianelli L, Costi E, Maistrello L, Sabbatini-Peverieri G (2016) Searching for native egg-parasitoids of the invasive alien species, Halyomorpha halys Stål (Heteroptera Pentatomidae) in Southern Europe. Redia 99:63–70. https://doi.org/10.19263/REDIA-99.16.01http://dx.doi.org/
Saunders TE, Avila GA, Holwell GI (2021) Pre-emptive host-specificity testing of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) reveals high parasitism levels against the endemic New Zealand alpine shield bug in laboratory no-choice tests. Austral Entomol 60:455–460. https://doi.org/10.1111/aen.12532
Stevens L, McCauley DE (1989) Mating prior to overwintering in the imported willow leaf beetle, Plagiodera versicolora (Coleoptera: Chrysomelidae). Ecol Entomol 14:219–223. https://doi.org/10.1111/j.1365-2311.1989.tb00772.x
Strand MR, Quarles JM, Meola SM, Vinson SB (1985) Cultivation of teratocytes of the egg parasitoid Telenomus heliothidis (Hymenoptera: Scelionidae). In Vitro Cell Dev Biol 21:361–367. https://doi.org/10.1007/BF02623466
Talamas EJ, Herlihy MV, Dieckhoff C, Hoelmer KA, Buffington ML, Bon M-C, Weber DC (2015) Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America. J Hymenopt Res 43:119–128. https://doi.org/10.3897/JHR.43.4661
Talamas EJ, Buffington ML, Hoelmer K (2017) Revision of Palearctic Trissolcus Ashmead (Hymenoptera, Scelionidae). J Hymenopt Res 56:3–185. https://doi.org/10.3897/jhr.56.10158
Tillman G, Toews M, Blaauw B, Sial A, Cottrell T, Talamas E, Buntin D, Joseph S, Balusu R, Fadamiro H, Lahiri S, Patel D (2020) Parasitism and predation of sentinel eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in the southeastern US. Biol Control. https://doi.org/10.1016/j.biocontrol.2020.104247
Tognon R, Aldrich JR, Buffington ML, Talamas EJ, Sant’Ana J, Zalom FG (2017) Halyomorpha halys (Heteroptera: Pentatomidae) egg surface chemicals inhibit North American Telenomus and Trissolcus (Hymenoptera: Scelionidae) parasitism. Biol Control 114:39–44. https://doi.org/10.1016/j.biocontrol.2017.07.014
Tsutsumi T (2003) Fruit tree stink bug- interesting ecology and clever prevention. Rural Culture Association, Tokyo (In Japanese, ISBN-10 is 4540021257)
Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stal (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Bull Soc Entomologique Suisse 81:1–8
Wong WHL, Walz MA, Oscienny AB, Sherwood JL, Abram PK (2020) An effective cold storage method for stockpiling Halyomorpha halys (Hemiptera: Pentatomidae) eggs for field surveys and laboratory rearing of Trissolcus japonicus (Hymenoptera: Scelionidae). J Econ Entomol 114:571–581. https://doi.org/10.1093/jee/toaa307
Yang Z-Q, Yao Y-X, Qiu L-F, Li Z-X (2009) A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology. Ann Entomol Soc Am 102:39–47. https://doi.org/10.1603/008.102.0104
Yonow T, Kriticos DJ, Ota N, Avila GA, Hoelmer KA, Chen H, Caron V (2021) Modelling the potential geographic distribution of two Trissolcus species for the brown marmorated stink bug Halyomorpha halys. Insects 12:491. https://doi.org/10.3390/insects12060491
Zhang YZ, Wie L, Huang DW (2005) A taxonomic study of Chinese species of Ooencyrtus insecta: Hymenoptera: Encyrtidae). Zool Stud 44:347–360
Zhang J, Zhang F, Gariepy T, Mason P, Gillespie D, Talamas E, Haye T (2017) Seasonal parasitism and host specificity of Trissolcus japonicus in northern China. J Pest Sci 90:1127–1141. https://doi.org/10.1007/s10340-017-0863-y
Zhu G, Bu W, Gao Y, Liu G (2012a) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PloS ONE 7(2):e31246. https://doi.org/10.1371/journal.pone.0031246
Zhu D-H, Cui S-S, Fan YS, Liu Z (2012b) Adaptive strategies of overwintering adults: reproductive diapause and mating behavior in a grasshopper, Stenocatantops splendens (Orthoptera: Catantopidae). Insect Sci 20:235–244. https://doi.org/10.1111/j.1744-7917.2011.01493.x
Zhu F, Cusumano A, Bloem J, Weldegergis BT, Villela A, Fatouros NE, van Loon JJA, Dicke M, Harvey JA, Vogel H, Poelmea EH (2018) Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1717904115
Acknowledgements
We express the deepest gratitude and sympathy to the family, friends, colleges, and collaborators of Dr. Tsuyoshi Yoshimura from Kyoto University, a co-author who tragically passed away during this research. We would like to thank the Earth Corporation Ako Plant and the Hohto Shoji Co. for providing funding (to CCSY) as well as insects for this research. We also thank Prof. Chow-Yang Lee from University of California, Riverside, for supplying essential tools for our field work. Funding was also provided by the Japanese Government Monbukagakusho (MEXT) (to MTK) Scholarship and the Virginia Tech Faculty Start-up Research Fund (to CCSY).
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Kamiyama, M.T., Matsuura, K., Hata, T. et al. Seasonal parasitism of native egg parasitoids of brown marmorated stink bug (Halyomorpha halys) in Japan. J Pest Sci 95, 1067–1079 (2022). https://doi.org/10.1007/s10340-021-01455-3
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DOI: https://doi.org/10.1007/s10340-021-01455-3