Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-24T14:10:19.474Z Has data issue: false hasContentIssue false
  • English
  • Français

Diel patterns of emergence and reproductive behaviour in the invasive swede midge (Diptera: Cecidomyiidae)

Published online by Cambridge University Press:  18 June 2019

Elisabeth A. Hodgdon ,
Rebecca H. Hallett ,
Chase A. Stratton  and
Yolanda H. Chen
Elisabeth A. Hodgdon*
Affiliation:
Department of Plant and Soil Science, University of Vermont, 63 Carrigan Drive, Burlington, Vermont, 05405, United States of America
Rebecca H. Hallett
Affiliation:
School of Environmental Sciences, University of Guelph, 50 Stone Road East, Guelph, Ontario, N1G 2W1, Canada
Chase A. Stratton
Affiliation:
Department of Plant and Soil Science, University of Vermont, 63 Carrigan Drive, Burlington, Vermont, 05405, United States of America
Yolanda H. Chen*
Affiliation:
Department of Plant and Soil Science, University of Vermont, 63 Carrigan Drive, Burlington, Vermont, 05405, United States of America
*
1Corresponding authors (e-mail: elisabeth.hodgdon@gmail.com; e-mail: yolanda.chen@uvm.edu).
1Corresponding authors (e-mail: elisabeth.hodgdon@gmail.com; e-mail: yolanda.chen@uvm.edu).
Get access Rights & Permissions [Opens in a new window]

Abstract

Swede midge (Contarinia nasturtii (Kieffer); Diptera: Cecidomyiidae) is a serious invasive pest of Brassica Linnaeus (Brassicaceae) oilseed and vegetable crops in Canada and the United States of America. Pheromone mating disruption is a promising new tactic for managing this difficult pest, but research is needed to determine how pheromone delivery can be optimised. With an understanding of swede midge diel mating patterns, pest managers could limit pheromone release to periods when midges are sexually active. We conducted a series of 24-hour trials to test whether swede midge exhibit diel periodicity of emergence, female calling, and male capture in pheromone traps. We found that females began releasing pheromones almost immediately following emergence within the first five hours after dawn. In the field, we found that males were most active from dawn until late morning, indicating that midges mate primarily during the first five hours of photophase. Low levels of reproductive activity during midday and nighttime hours present opportunities to turn off dispensers and reduce the cost of pheromone inputs in a swede midge mating disruption system.

Résumé

La cécidomyie du chou-fleur (Contarinia nasturtii (Kieffer); Diptera: Cecidomyiidae) est un ravageur envahissant des oléagineux et des légumes du genre Brassica Linnaeus (Brassicaceae) au Canada et aux États-Unis d’Amérique. La confusion sexuelle par phéromones est une nouvelle tactique prometteuse pour lutter contre ce ravageur difficile à gérer, mais plus de recherche est encore nécessaire pour optimiser la méthode de diffusion des phéromones. Avec une meilleure connaissance des schémas d’accouplement diurnes de la cécidomyie du chou-fleur, les personnes responsables de la lutte contre ce ravageur pourraient restreindre la distribution de phéromones aux périodes où la cécidomyie du chou-fleur est sexuellement active. Nous avons donc fait une série d’expériences de 24 heures pour déterminer si la cécidomyie du chou-fleur démontre des schémas diurnes d’émergence, de l’appel des femelles, et de la capture des mâles dans les pièges de phéromones. Nous avons constaté que les femelles commencent à émettre des phéromones presque immédiatement après leur émergence, durant les premières heures suivant l’aube. Dans les champs, nous avons constaté que les mâles sont le plus actif de l’aube jusqu’à la fin du matin, en indiquant ainsi que la cécidomyie du chou-fleur s’accouple pendent les cinq premières heures de la photophase. Les faibles niveaux d’activité sexuelle durant le milieu de la journée et pendant la nuit offrent des occasions d’éteindre les diffuseurs programmables et pour réduire les coûts des intrants de phéromones dans un système de la confusion sexuelle de la cécidomyie du chou-fleur.

Type
Behaviour and Ecology
Information
The Canadian Entomologist , Volume 151 , Issue 4 , August 2019 , pp. 510 - 520
Copyright
© Entomological Society of Canada 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Suzanne Blatt

References

Agriculture and Agri-Food Canada. 2017. Canada’s organic products industry overview [online]. Available from www.agr.gc.ca/eng/industry-markets-and-trade/market-information-by-sector/organic-products/canada-s-organic-products-industry-overview/?id=1276292934938 [accessed 30 April 2018].Google Scholar
Allen, J., Fraser, H., and Hallett, R.H. 2009. The swede midge: a pest of crucifer crops [online]. Available from www.omafra.gov.on.ca/english/crops/facts/08-007.htm [accessed 9 May 2017].Google Scholar
Bergh, J.C., Harris, M.O., and Rose, S. 1990. Temporal patterns of emergence and reproductive behavior of the Hessian fly (Diptera: Cecidomyiidae). Annals of the Entomological Society of America, 83: 998–1004.CrossRefGoogle Scholar
Blackwell, A. 1997. Diel flight periodicity of the biting midge Culicoides impunctatus and the effects of meteorological conditions. Medical and Veterinary Entomology, 11: 361–367. https://doi.org/10.1111/j.1365-2915.1997.tb00423.x CrossRefGoogle ScholarPubMed
Boddum, T., Skals, N., Wirén, M., Baur, R., Rauscher, S., and Hillbur, Y. 2009. Optimisation of the pheromone blend of the swede midge, Contarinia nasturtii, for monitoring. Pest Management Science, 65: 851–856. https://doi.org/10.1002/ps.1762 CrossRefGoogle ScholarPubMed
Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H., and White, J.S.S. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution, 24: 127–135. https://doi.org/10.1016/j.tree.2008.10.008 CrossRefGoogle ScholarPubMed
Casado, D., Cave, F., and Welter, S. 2014. Puffer®-CM dispensers for mating disruption of codling moth: area of influence and impacts on trap finding success by males. International Organisation for Biological and Integrated Control – West Palaearctic Regional Section Bulletin, 99: 25–31.Google Scholar
Chen, M., Shelton, A.M., Hallett, R.H., Hoepting, C.A., Kikkert, J.R., and Wang, P. 2011. Swede midge (Diptera: Cecidomyiidae), ten years of invasion of crucifer crops in North America. Journal of Economic Entomology, 104: 709–716. https://doi.org/10.1603/EC10397 CrossRefGoogle Scholar
Delisle, J. and McNeil, J.N. 1986. The effect of photoperiod on the calling behaviour of virgin females of the true armyworm, Pseudaletia unipuncta (Haw.) (Lepidoptera: Noctuidae). Journal of Insect Physiology, 32: 199–206. https://doi.org/10.1016/0022-1910(86)90059-4 CrossRefGoogle Scholar
Fingerman, M. and Brown, F.A. 1952. A “Purkinje shift” in insect vision. Science, 116: 171–172.CrossRefGoogle Scholar
Gadenne, C., Barrozo, R.B., and Anton, S. 2016. Plasticity of insect olfaction: to smell or not to smell? Annual Review of Entomology, 61: 317–333. https://doi.org/10.1146/annurev-ento-010715-023523 CrossRefGoogle ScholarPubMed
Gagné, R.J. 1989. The plant-feeding gall midges of North America. Cornell University Press, Ithaca, New York, United States of America.Google Scholar
Groot, A.T. 2014. Circadian rhythms of sexual activities in moths: a review. Frontiers in Ecology and Evolution, 2: 1–21. https://doi.org/10.3389/fevo.2014.00043 CrossRefGoogle Scholar
Hall, D.R., Amarawardana, L., Cross, J. V., Francke, W., Boddum, T., and Hillbur, Y. 2012. The chemical ecology of cecidomyiid midges (Diptera: Cecidomyiidae). Journal of Chemical Ecology, 38: 2–22. https://doi.org/10.1007/s10886-011-0053-y CrossRefGoogle Scholar
Hallett, R.H. 2007. Host plant susceptibility to the swede midge (Diptera: Cecidomyiidae). Journal of Chemical Ecology, 100: 1335–1343.Google Scholar
Hallett, R.H., Chen, M., Sears, M.K., and Shelton, A.M. 2009. Insecticide management strategies for control of swede midge (Diptera: Cecidomyiidae) on cole crops. Journal of Economic Entomology, 102: 2241–2254. https://doi.org/10.1603/029.102.0629 CrossRefGoogle ScholarPubMed
Hallett, R.H. and Heal, J.D. 2001. First Nearctic record of the swede midge (Diptera: Cecidomyiidae). The Canadian Entomologist, 133: 713–715.CrossRefGoogle Scholar
Harris, M.O., Galanihe, L.D., and Sandanayake, M. 1999. Adult emergence and reproductive behavior of the leafcurling midge Dasineura mali (Diptera: Cecidomyiidae). Annals of the Entomological Society of America, 92: 748–757.CrossRefGoogle Scholar
Heath, J.J., Zhang, A., Roelofs, W.L., and Smith, R.F. 2005. Flight activity and further evidence for a female-produced sex pheromone of the apple leaf midge, Dasineura mali, in Nova Scotia. Northeastern Naturalist, 16: 93–102.CrossRefGoogle Scholar
Higbee, B.S. and Burks, C.S. 2008. Effects of mating disruption treatments on navel orangeworm (Lepidoptera: Pyralidae) sexual communication and damage in almonds and pistachios. Journal of Chemical Ecology, 101: 1633–1642.Google ScholarPubMed
Hillbur, Y., Celander, M., Baur, R., Rauscher, S., Haftmann, J., Franke, S., and Francke, W. 2005. Identification of the sex pheromone of the swede midge, Contarinia nasturtii . Journal of Chemical Ecology, 31: 1807–1828. https://doi.org/10.1007/s10886-005-5928-3 CrossRefGoogle ScholarPubMed
Hoffman, A.A. and Ross, P.A. 2018. Rates and patterns of laboratory adaptation in (mostly) insects. Journal of Economic Entomology, 111: 501–509. https://doi.org/10.1093/jee/toy024 CrossRefGoogle Scholar
Knight, A.L., Weiss, M., and Weissling, T. 1994. Diurnal adult activity of four orchard pests (Lepidoptera: Tortricidae) measured by timing trap and actograph. Journal of Agricultural Entomology, 11: 126–136.Google Scholar
Miller, J.R. and Gut, L.J. 2015. Mating disruption for the 21st century: matching technology with mechanism. Environmental Entomology, 44: 427–453. https://doi.org/10.1093/ee/nvv052 CrossRefGoogle ScholarPubMed
Modini, M.P., Page, F.D., and Franzmann, B.A. 1987. Diurnal oviposition activity in grain sorghum by Contarinia sorghicola (Coquillett) (Diptera: Cecidomyiidae). Australian Journal of Entomology, 26: 293–294.CrossRefGoogle Scholar
Mori, B.A. and Evenden, M.L. 2015. Challenges of mating disruption using aerosol-emitting pheromone puffers in red clover seed production fields to control Coleophora deauratella (Lepidoptera: Coleophoridae). Environmental Entomology, 44: 34–43. https://doi.org/10.1093/ee/nvu001 CrossRefGoogle Scholar
Paini, D.R., Sheppard, A.W., Cook, D.C., De Barro, P.J., Worner, S.P., and Thomas, M.B. 2016. Global threat to agriculture from invasive species. Proceedings of the National Academy of Science, 113: 7575–7579. https://doi.org/10.1073/pnas.1602205113 CrossRefGoogle ScholarPubMed
Pellegrino, A.C., Peñaflor, M.F.G.V., Nardi, C., Bezner-Kerr, W., Guglielmo, C.G., Bento, J.M.S., and McNeil, J.N. 2013. Weather forecasting by insects: modified sexual behaviour in response to atmospheric pressure changes. Public Library of Science One, 8: 1–5. https://doi.org/10.1371/journal.pone.0075004 Google ScholarPubMed
Pivnick, K.A. and Labbé, E. 1992. Emergence and calling rhythms, and mating behavior of the orange wheat blossom midge, Sitodiplosis mosellana (Gehin) (Diptera: Cecidomyiidae). The Canadian Entomologist, 124: 501–507.CrossRefGoogle Scholar
Rama, F., Reggiori, F., and Pratizzoli, W. 2002. Timed mating disruption: a new pheromone – dispensing device for the protection of orchards from Cydia pomonella, C. molesta and leafrollers. In Pheromones and other semiochemicals in integrated production. International Organisation for Biological and Integrated Control– West Palaearctic Regional Section Working Group, Erice, Italy.Google Scholar
Readshaw, J.L. 1961. The biology and ecology of the swede midge, Contarinia nasturtii (Kieffer), (Diptera; Cecidomyiidae). Ph.D. thesis. University of Durham, Durham, United Kingdom. Available from https://theses.ncl.ac.uk/dspace/bitstream/10443/1074/1/Readshaw%2061.pdf [accessed 13 March 2019].Google Scholar
Rodriguez, C.M., Madden, L.V., and Nault, L.R. 1992. Diel flight periodicity of Graminella nigrifrons (Homoptera: Cicadellidae). Annals of the Entomological Society of America, 85: 792–798.CrossRefGoogle Scholar
Rund, S.S.C., Lee, S.J., Bush, B.R., and Duffield, G.E. 2012. Strain- and sex-specific differences in daily flight activity and the circadian clock of Anopholes gambiae mosquitoes. Journal of Insect Physiology, 58: 1609–1619. https://doi.org/10.1016/j.jinsphys.2012.09.016 CrossRefGoogle ScholarPubMed
Samietz, J., Baur, R., and Hillbur, Y. 2012. Potential of synthetic sex pheromone blend for mating disruption of the swede midge, Contarinia nasturtii . Journal of Chemical Ecology, 38: 1171–1177. https://doi.org/10.1007/s10886-012-0180-0 CrossRefGoogle ScholarPubMed
Saunders, D.S. 1997. Insect circadian rhythms and photoperiodism. Invertebrate Neuroscience, 3: 155–164. https://doi.org/10.1007/BF02480370 CrossRefGoogle ScholarPubMed
Smith, M.A.H., Wise, I.L., and Lamb, R.J. 2007. Sex ratios of Sitodiplosis mosellana (Diptera: Cecidomyiidae): implications for pest management in wheat (Poaceae). Bulletin of Entomological Research, 94: 569–575. https://doi.org/10.1079/BER2004333 Google Scholar
Stelinski, L.L., Gut, L.J., Haas, M., McGhee, P., and Epstein, D. 2007. Evaluation of aerosol devices for simultaneous disruption of sex pheromone communication in Cydia pomonella and Grapholita molesta (Lepidoptera: Tortricidae). Journal of Pest Science, 80: 225–233. https://doi.org/10.1007/s10340-007-0176-7 CrossRefGoogle Scholar
Stratton, C.A., Hodgdon, E.A., Zuckerman, S., Shelton, A.M., and Chen, Y.H. 2018. Damage from a single swede midge (Diptera: Cecidomyiidae) larva can cause cauliflower plants to be unmarketable. Journal of Insect Science, 18: 1–6.CrossRefGoogle ScholarPubMed
United States Department of Agriculture Economic Research Service. 2017. Organic market overview [online]. Available from www.ers.usda.gov/topics/natural-resources-environment/organic-agriculture/organic-market-overview.aspx [accessed 30 April 2018].Google Scholar
Welter, S.C., Pickel, C., Millar, J., Cave, F., Van Steenwyk, R.A., and Dunley, J. 2008. Pheromone mating disruption offers selective management options for key pests. California Agriculture, 59: 16–22. https://doi.org/10.3733/ca.v059n01p16 CrossRefGoogle Scholar
Williams, I.H., Martin, A.P., and Kelm, M. 1987. The phenology of the emergence of brassica pod midge (Dasineura brassicae Winn.) and its infestation of winter oil-seed rape (Brassica napus L.). The Journal of Agricultural Science, 108: 579–589.CrossRefGoogle Scholar
Witzgall, P., Kirsch, P., and Cork, A. 2010. Sex pheromones and their impact on pest management. Journal of Chemical Ecology, 36: 80–100. https://doi.org/10.1007/s10886-009-9737-y CrossRefGoogle ScholarPubMed