in

Olfactory responses of Trissolcus mitsukurii to plants attacked by target and non-target stink bugs suggest low risk for biological control

  • 1.

    Kenis, M., Hurley, B. P., Hajek, A. E. & Cock, M. J. W. Classical biological control of insect pests of trees: Facts and figures. Biol. Invasions 19, 3401–3417 (2017).

    Google Scholar 

  • 2.

    Hoddle, M. S. Restoring balance: Using exotic species to control invasive exotic species. Conserv. Biol. 18, 38–49 (2004).

    Google Scholar 

  • 3.

    van Lenteren, J. C. & Loomans, A. J. M. Environmental risk assessment: Methods for comprehensive evaluation and quick scan. In Environmental Impact of Invertebrates for Biological Control of Arthropods: Methods and Risk Assessment Vol. 10 (eds Bigler, F. et al.) 254–272 (CABI Publishing, 2006).

    Google Scholar 

  • 4.

    Loomans, A. J. M. Every generalist biological control agent requires a special risk assessment. Biocontrol 66, 23–35 (2021).

    Google Scholar 

  • 5.

    Mason, P. G., Everatt, M. J., Loomans, A. J. M. & Collatz, J. Harmonizing the regulation of invertebrate biological control agents in the EPPO region: Using the NAPPO region as a model. EPPO Bull. 47, 79–90 (2017).

    Google Scholar 

  • 6.

    Sabbatini-Peverieri, G. et al. Combining physiological host range, behavior and host characteristics for predictive risk analysis of Trissolcus japonicus. J. Pest Sci. 94, 1003–1016 (2021).

    Google Scholar 

  • 7.

    Abram, P. K., Labbe, R. M. & Mason, P. G. Ranking the host range of biological control agents with quantitative metrics of taxonomic specificity. Biol. Control 152, 104427 (2021).

    CAS 

    Google Scholar 

  • 8.

    Haye, T. et al. Fundamental host range of Trissolcus japonicus in Europe. J. Pest Sci. 93, 171–182 (2020).

    Google Scholar 

  • 9.

    Hilker, M. & Meiners, T. Chemoecology of Insect Eggs and Egg Deposition (Blackwell, 2008).

    Google Scholar 

  • 10.

    Meiners, T. & Peri, E. Chemical ecology of insect parasitoids: Essential elements for developing effective biological control programmes. In Chemical Ecology of Insect Parasitoids (eds Wajnberg, E. & Colazza, S.) 191–224 (Wiley-Blackwell, 2013).

    Google Scholar 

  • 11.

    Conti, E. & Colazza, S. Chemical ecology of egg parasitoids associated with true bugs. Psyche 2012, 651015 (2012).

    Google Scholar 

  • 12.

    Desurmont, G. A. et al. Alien interference: Disruption of infochemical networks by invasive insect herbivores. Plant Cell Environ. 37, 1854–1865 (2014).

    PubMed 

    Google Scholar 

  • 13.

    Martorana, L. et al. An invasive insect herbivore disrupts plant volatile-mediated tritrophic signalling. J. Pest Sci. 90, 1079–1085 (2017).

    Google Scholar 

  • 14.

    van Driesche, R. G. & Murray, T. J. Parameters used in laboratory host range tests. In Assessing Host Ranges of Parasitoids and Predators Used for Classical Biological Control: A Guide to Best Practice (eds van Driesche, R. & Reardon, R.) 55–67 (US Department Agriculture Forest Health Technology Enterprise Team, 2004).

    Google Scholar 

  • 15.

    Conti, E., Salerno, G., Bin, F. & Vinson, S. B. The role of host semiochemicals in parasitoid specificity: A case study with Trissolcus brochymenae and Trissolcus simoni on pentatomid bugs. Biol. Control 29, 435–444 (2004).

    CAS 

    Google Scholar 

  • 16.

    Ferracini, C. et al. Non-target host risk assessment for the parasitoid Torymus sinensis. Biocontrol 60, 583–594 (2015).

    Google Scholar 

  • 17.

    Avila, G. A., Withers, T. M. & Holwell, G. I. Laboratory odour-specificity testing of Cotesia urabae to assess potential risks to non-target species. Biocontrol 61, 365–377 (2016).

    Google Scholar 

  • 18.

    Wyckhuys, K. A. G. & Heimpel, G. E. Response of the soybean aphid parasitoid Binodoxys communis to olfactory cues from target and non-target host-plant complexes. Entomol. Exp. Appl. 123, 149–158 (2007).

    Google Scholar 

  • 19.

    Gohole, L. S., Overholt, W. A., Khan, Z. R. & Vet, L. E. M. Role of volatiles emitted by host and non-host plants in the foraging behaviour of Dentichasmias busseolae, a pupal parasitoid of the spotted stemborer Chilo partellus. Entomol. Exp. Appl. 107, 1–9 (2003).

    CAS 

    Google Scholar 

  • 20.

    Leskey, T. C. & Nielsen, A. L. Impact of the invasive Brown Marmorated Stink Bug in North America and Europe: History, biology, ecology, and management. Annu. Rev. Entomol. 63, 599–618 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 21.

    Nixon, L. J. et al. Volatile release, mobility, and mortality of diapausing Halyomorpha halys during simulated shipping movements and temperature changes. J. Pest Sci. 92, 633–641 (2019).

    Google Scholar 

  • 22.

    Hoebeke, E. R. & Carter, M. E. Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): A polyphagous plant pest from Asia newly detected in North America. Proc. Entomol. Soc. Washingt. 105, 225–237 (2003).

    Google Scholar 

  • 23.

    Haye, T., Abdallah, S., Gariepy, T. & Wyniger, D. Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, Europe. J. Pest Sci. 87, 407–418 (2014).

    Google Scholar 

  • 24.

    Maistrello, L. et al. Tracking the spread of sneaking aliens by integrating crowdsourcing and spatial modeling: The Italian invasion of Halyomorpha halys. Bioscience 68, 979–989 (2018).

    Google Scholar 

  • 25.

    Bariselli, M., Bugiani, R. & Maistrello, L. Distribution and damage caused by Halyomorpha halys in Italy. EPPO Bull. 46, 332–334 (2016).

    Google Scholar 

  • 26.

    Rot, M. et al. Native and non-native egg parasitoids associated with brown marmorated stink bug (Halyomorpha halys [stål, 1855]; Hemiptera: Pentatomidae) in western Slovenia. Insects 12, 505 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 27.

    Conti, E. et al. Biological control of invasive stink bugs: Review of global state and future prospects. Entomol. Exp. Appl. 169, 28–51 (2021).

    Google Scholar 

  • 28.

    Zapponi, L. et al. Assessing the distribution of exotic egg parasitoids of Halyomorpha halys in Europe with a large-scale monitoring program. Insects 12, 316 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 29.

    Zhang, J. et al. Seasonal parasitism and host specificity of Trissolcus japonicus in northern China. J. Pest Sci. 90, 1127–1141 (2017).

    ADS 

    Google Scholar 

  • 30.

    Yang, Z. Q., Yao, Y. X., Qiu, L. F. & Li, Z. X. 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 (2009).

    Google Scholar 

  • 31.

    Abram, P. K., Talamas, E. J., Acheampong, S., Mason, P. G. & Gariepy, T. D. First detection of the samurai wasp, Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae), Canada. J. Hymenopt. Res. 68, 29–36 (2019).

    Google Scholar 

  • 32.

    Kaser, J. M., Akotsen-Mensah, C., Talamas, E. J. & Nielsen, A. L. First Report of Trissolcus japonicus parasitizing Halyomorpha halys in North American agriculture. Florida Entomol. 101, 680–683 (2018).

    Google Scholar 

  • 33.

    Moraglio, S. T. et al. A 3-year survey on parasitism of Halyomorpha halys by egg parasitoids in northern Italy. J. Pest Sci. 93, 183–194 (2020).

    Google Scholar 

  • 34.

    Sabbatini-Peverieri, G. et al. Two Asian egg parasitoids of Halyomorpha halys (Stål) (Hemiptera, Pentatomidae) emerge in northern Italy: Trissolcus mitsukurii (Ashmead) and Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae). J. Hymenopt. Res. 67, 37–53 (2018).

    Google Scholar 

  • 35.

    Scaccini, D. et al. An insight into the role of Trissolcus mitsukurii as biological control agent of Halyomorpha halys in Northeastern Italy. Insects 11, 306 (2020).

    PubMed Central 

    Google Scholar 

  • 36.

    Hokyo, N. & Kiritani, K. Two species of egg parasites as contemporaneous mortality factors in the egg population of the southern green stink bug, Nezara viridula. Jpn. J. Appl. Entomol. Zool. 7, 214–227 (1963).

    Google Scholar 

  • 37.

    Arakawa, R., Miura, M. & Fujita, M. Effects of host species on the body size, fecundity, and longevity of Trissolcus mitsukurii (Hymenoptera: Scelionidae), a solitary egg parasitoid of stink bugs. Appl. Entomol. Zool. 39, 177–181 (2004).

    Google Scholar 

  • 38.

    Arakawa, R. & Namura, Y. 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 (2002).

    Google Scholar 

  • 39.

    Chen, H., Talamas, E. J. & Pang, H. Notes on the hosts of Trissolcus ashmead (Hymenoptera: Scelionidae) from China. Biodivers. Data J. 8, e53786 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 40.

    Ryu, J. & Hirashima, Y. Taxonomic studies on the genus Trissolcus Ashmead of Japan and Korea (Hymenoptera, Scelionidae). J. Fac. Agric. Kyushu Univ. 29, 35–58 (1984).

    Google Scholar 

  • 41.

    Bout, A. et al. First detection of the adventive egg parasitoid of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) in France. Insects 12, 761 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 42.

    Caron, V. et al. Preempting the arrival of the brown marmorated stink bug, Halyomorpha halys: Biological control options for Australia. Insects 12, 581 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 43.

    Giovannini, L. et al. Physiological host range of Trissolcus mitsukurii, a candidate biological control agent of Halyomorpha halys in Europe. J. Pest Sci. https://doi.org/10.1007/s10340-021-01415-x (2021).

    Article 

    Google Scholar 

  • 44.

    Bertoldi, V., Rondoni, G., Brodeur, J. & Conti, E. An egg parasitoid efficiently exploits cues from a coevolved host but not those from a novel host. Front. Physiol. 10, 746 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 45.

    Colazza, S. et al. Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J. Exp. Biol. 207, 47–53 (2004).

    PubMed 

    Google Scholar 

  • 46.

    Tognon, R. et al. Volatiles mediating parasitism of Euschistus conspersus and Halyomorpha halys eggs by Telenomus podisi and Trissolcus erugatus. J. Chem. Ecol. 42, 1016–1027 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • 47.

    Borges, M. & Blassioli-Moraes, M. C. The semiochemistry of Pentatomidae. In Stink Bugs: Biorational Control Based on Communication Processes 95–124 (CRC Press, 2017).

  • 48.

    Conti, E., Salerno, G., Leombruni, B., Frati, F. & Bin, F. Short-range allelochemicals from a plant-herbivore association: A singular case of oviposition-induced synomone for an egg parasitoid. J. Exp. Biol. 213, 3911–3919 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • 49.

    De Clercq, P. Predaceous Stinkbugs (Pentatomidae: Asopinae). In Heteroptera of Economic Importance (eds Schaefer, C. W. & Panizzi, A. R.) 737–789 (CRC Press, 2000).

    Google Scholar 

  • 50.

    Hamilton, G. C. et al. Halyomorpha halys (Stål). In Invasive Stink Bugs and Related Species (Pentatomoidea) (ed. McPherson, J. E.) 243–292 (CRC Press, 2018).

    Google Scholar 

  • 51.

    Panizzi, A., McPherson, J., James, D., Javahery, M. & McPherson, R. Stink bugs (Pentatomidae). In Heteroptera of Economic Importance (eds Schaefer, C. & Panizzi, A.) 421–474 (CRC Press, 2000).

    Google Scholar 

  • 52.

    Rider, D. A. Family Pentatomidae. In Catalogue of the Heteroptera of the Palaearctic Region Vol. 5 (eds Aukema, B. & Rieger, C.) 233–402 (The Netherlands Entomological Society, 2006).

    Google Scholar 

  • 53.

    Milnes, J. M. & Beers, E. H. Trissolcus japonicus (Hymenoptera: Scelionidae) causes low levels of parasitism in three North American pentatomids under field conditions. J. Insect Sci. 19, 15 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 54.

    Peiffer, M. & Felton, G. W. Insights into the saliva of the brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae). PLoS ONE 9, e88483 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 55.

    Rondoni, G. et al. Vicia faba plants respond to oviposition by invasive Halyomorpha halys activating direct defences against offspring. J. Pest Sci. 91, 671–679 (2018).

    Google Scholar 

  • 56.

    Giacometti, R. et al. Early perception of stink bug damage in developing seeds of field-grown soybean induces chemical defences and reduces bug attack. Pest Manag. Sci. 72, 1585–1594 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • 57.

    Timbó, R. V. et al. Biochemical aspects of the soybean response to herbivory injury by the brown stink bug Euschistus heros (Hemiptera: Pentatomidae). PLoS ONE 9, e109735 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 58.

    Vet, L. E. M. & Dicke, M. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37, 141–172 (1992).

    Google Scholar 

  • 59.

    Zapponi, L. et al. Assemblage of the egg parasitoids of the invasive stink bug Halyomorpha halys: Insights on plant host associations. Insects 11, 588 (2020).

    PubMed Central 

    Google Scholar 

  • 60.

    Scala, M. et al. Risposte di Trissolcus mitsukurii alle tracce chimiche volatili rilasciate da Halyomorpha halys. in XXVI Italian Congress of Entomology, 7–11 June 2021, 318 (2021).

  • 61.

    Kiritani, K. & Hôkyo, N. Studies on the life table of the southern green stink bug, Nezara viridula. Jpn. J. Appl. Entomol. Zool. 6, 124–140 (1962).

    Google Scholar 

  • 62.

    Hokyo, N., Kiritani, K., Nakasuji, F. & Shiga, M. Comparative biology of the two Scelionid egg parasites of Nezara viridula L. (Hemiptera : Pentatomidae). Appl. Entomol. Zool. 1, 94–102 (1966).

    Google Scholar 

  • 63.

    Esquivel, J. F. et al. Nezara viridula (L.). In Invasive Stink Bugs and Related Species (Pentatomoidea) (ed. McPherson, J. E.) 351–424 (CRC Press, 2018).

    Google Scholar 

  • 64.

    Kobayashi, T. Insect pests of soybeans in Japan. Misc. Publ. Tohoku Natl. Agric. Exp. Stn. 2, 1–39 (1981).

    ADS 

    Google Scholar 

  • 65.

    Nakamura, K. & Numata, H. Effects of photoperiod and temperature on the induction of adult diapause in Dolycoris baccarum (L.) (Heteroptera: Pentatomidae) from Osaka and Hokkaido, Japan. Appl. Entomol. Zool. 41, 105–109 (2006).

    Google Scholar 

  • 66.

    Mahmoud, A. M. A. & Lim, U. T. Host discrimination and interspecific competition of Trissolcus nigripedius and Telenomus gifuensis (Hymenoptera: Scelionidae), sympatric parasitoids of Dolycoris baccarum (Heteroptera: Pentatomidae). Biol. Control 45, 337–343 (2008).

    Google Scholar 

  • 67.

    Lim, U.-T., Park, K.-S., Mahmoud, A. M. A. & Jung, C.-E. Areal distribution and parasitism on other soybean bugs of Trissolcus nigripedius (Hymenoptera: Scelionidae), an egg parasitoid of Dolycoris baccarum (Heteroptera: Pentatomidae). Korean J. Appl. Entomol. 46, 79–85 (2007).

    Google Scholar 

  • 68.

    Wäckers, F. L. Assessing the suitability of flowering herbs as parasitoid food sources: Flower attractiveness and nectar accessibility. Biol. Control 29, 307–314 (2004).

    Google Scholar 

  • 69.

    Gillespie, D. R. & Mcgregor, R. R. The functions of plant feeding in the omnivorous predator Dicyphus hesperus: Water places limits on predation. Ecol. Entomol. 25, 380–386 (2000).

    Google Scholar 

  • 70.

    Bouagga, S. et al. Zoophytophagous mirids provide pest control by inducing direct defences, antixenosis and attraction to parasitoids in sweet pepper plants. Pest Manag. Sci. 74, 1286–1296 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 71.

    Martorana, L. et al. Egg parasitoid exploitation of plant volatiles induced by single or concurrent attack of a zoophytophagous predator and an invasive phytophagous pest. Sci. Rep. 9, 18956 (2019).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 72.

    Lara, J. R. et al. Physiological host range of Trissolcus japonicus in relation to Halyomorpha halys and other pentatomids from California. Biocontrol 64, 513–528 (2019).

    Google Scholar 

  • 73.

    Zhao, Q., Jiufeng, W., Wenjun, B., Guoqing, L. & Zhang, H. Synonymize Arma chinensis as Arma custos based on morphological, molecular and geographical data. Zootaxa 4455, 161–176 (2018).

    PubMed 

    Google Scholar 

  • 74.

    Zou, D. et al. Taxonomic and bionomic notes on Arma chinensis (Fallou) (Hemiptera: Pentatomidae: Asopinae). Zootaxa, 3382, 41–52 (2012).

    Google Scholar 

  • 75.

    Zou, D. Y. et al. A meridic diet for continuous rearing of Arma chinensis (Hemiptera: Pentatomidae: Asopinae). Biol. Control 67, 491–497 (2013).

    Google Scholar 

  • 76.

    Wu, S. et al. Egg cannibalism varies with sex, reproductive status, and egg and nymph ages in Arma custos (Hemiptera: Asopinae). Front. Ecol. Evol. 9, 3389 (2021).

    Google Scholar 

  • 77.

    Endo, J. & Numata, H. Synchronized hatching as a possible strategy to avoid sibling cannibalism in stink bugs. Behav. Ecol. Sociobiol. 74, 16 (2020).

    Google Scholar 

  • 78.

    Afsheen, S., Xia, W., Ran, L., Zhu, C. S. & Lou, Y. G. Differential attraction of parasitoids in relation to specificity of kairomones from herbivores and their by-products. Insect Sci. 15, 381–397 (2008).

    Google Scholar 

  • 79.

    Rondoni, G. et al. Native egg parasitoids recorded from the invasive Halyomorpha halys successfully exploit volatiles emitted by the plant–herbivore complex. J. Pest Sci. 90, 1087–1095 (2017).

    Google Scholar 

  • 80.

    Bertoldi, V., Rondoni, G., Peri, E., Conti, E. & Brodeur, J. Learning can be detrimental for a parasitic wasp. PLoS ONE 16, e0238336 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 81.

    Conti, E., Salerno, G., Bin, F., Williams, H. J. & Vinson, S. B. Chemical cues from Murgantia histrionica eliciting host location and recognition in the egg parasitoid Trissolcus brochymenae. J. Chem. Ecol. 29, 115–130 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • 82.

    Fatouros, N. E., Dicke, M., Mumm, R., Meiners, T. & Hilker, M. Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19, 677–689 (2008).

    Google Scholar 

  • 83.

    Vinson, S. B. The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol. Control 11, 79–96 (1998).

    Google Scholar 

  • 84.

    Michereff, M. F. F. et al. The influence of volatile semiochemicals from stink bug eggs and oviposition-damaged plants on the foraging behaviour of the egg parasitoid Telenomus podisi. Bull. Entomol. Res. 106, 663–671 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • 85.

    Bonnemaison, L. Insect pests of crucifers and their control. Annu. Rev. Entomol. 10, 233–256 (1965).

    Google Scholar 

  • 86.

    Rondoni, G., Chierici, E., Agnelli, A. & Conti, E. Microplastics alter behavioural responses of an insect herbivore to a plant-soil system. Sci. Total Environ. 787, 147716 (2021).

    ADS 
    CAS 

    Google Scholar 

  • 87.

    Blumstein, D. T., Evans, C. S. & Daniels, J. C. JWatcher (Version 3, 1.0). (2006). http://www.jwatcher.ucla.edu. Accessed April 2021.

  • 88.

    Peri, E., Cusumano, A., Agrò, A. & Colazza, S. Behavioral response of the egg parasitoid Ooencyrtus telenomicida to host-related chemical cues in a tritrophic perspective. Biocontrol 56, 163–171 (2011).

    Google Scholar 

  • 89.

    Rondoni, G., Ielo, F., Ricci, C. & Conti, E. Behavioural and physiological responses to prey-related cues reflect higher competitiveness of invasive vs. native ladybirds. Sci. Rep. 7, 3716 (2017).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 90.

    R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020). https://www.R-project.org (2020).


  • Source: Ecology - nature.com

    Reducing methane emissions at landfills

    Students dive into research with the MIT Climate and Sustainability Consortium