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          Dormancy Management to Enable Mass-rearing and Increase Efficacy of Sterile Insects and Natural Enemies

          Closed for proposals

          Project Type

          Coordinated Research Project

          Project Code

          D41025

          CRP

          1972

          Approved Date

          29 October 2012

          Status

          Closed

          Start Date

          13 February 2014

          Expected End Date

          30 June 2019

          Completed Date

          27 March 2020

          Description

          Biological control applications based on the use of sterile insects and natural enemies are sustainable and environment-friendly control methods that are increasingly being used against pest insects.? Dormancy is an integral component of many insect life cycles, wherein insects enter a state of developmental or reproductive arrest to avoid adverse conditions and synchronize their populations with favourable conditions. Dormancy responses are an obstacle to the effective implementation of mass rearing in many cases. The ability to manage dormancy could facilitate the development of new pest control programs that are currently constrained by species dormancy characteristics. Dormancy management could also offer opportunities to carefully time the supply of mass-reared insects upon demand and to enhance product quality. Specifically, dormancy management could enable effective mass rearing of insects that require dormancy, the ability to stockpile and mobilize them upon demand, maintenance of the genetic integrity of strains, and mitigating the stresses of sterilization, product shipment, and release. However, there is a clear gap in knowledge of the roles and mechanisms of dormancy on life cycle synchronization or stress resistance in sterile insects and natural enemies. The objectives of this CRP are: 1) to generate new knowledge about the induction, maintenance, and termination of dormancy in insects, 2) to disseminate and apply that knowledge to improve the efficacy of current biological control programs using sterile insects or natural enemies, and 3) to develop new programs for select insect pest species where dormancy has been a barrier. Furthermore, understanding dormancy responses may lead to novel pest management tools, such as dormancy disruption in the field.

          Objectives

          The objective of the project is to understand and harness dormancy management, physiological conditioning, and cold-storage approaches to enable mass-rearing of insect species previously difficult to rear and enhancing current mass-rearing efforts for biological control, specifically using sterile insects and natural enemies as part of an environmentally friendly, area-wide integrated pest management approach.

          Specific objectives

          Assess whether dormancy responses, physiological conditioning, and storage conditions can be used to decrease shipping-related damage and enhance post-shipping performance.

          Assess whether dormancy responses, physiological conditioning, and storage conditions can be used to reduce radiation injury and enhance sterile insect performance.

          Develop and assess new methods to manage dormancy responses, physiological conditioning, and storage conditions to facilitate mass rearing.

          Develop and assess new methods to use dormancy responses, physiological conditioning, and storage conditions to enable or enhance the shelf life of biological control agents, including sterile insects and natural enemies.

          Develop and assess new methods to use dormancy responses, physiological conditioning, and storage conditions to maintain the genetic integrity of laboratory strains.

          Develop methods to incorporate dormancy into phenological models to improve the timing of field releases.

          Explore the potential for dormancy responses to generate novel approaches for inducing “ecological suicide”.?

          Explore the role of the microbiome on dormancy responses, physiological conditioning, and cold storage to enhance mass rearing and shelf life of biological control agents.

          Impact

          The key achievements of the CRP were: 1) We evaluated chemical, endocrine, and environmental means to terminate diapause and accelerate development in mass-reared insects. While it is possible to modify development at a research scale, there exist many challenges to scaling these approaches to mass-rearing. 2) We demonstrated that fluctuating temperatures have profound and positive effects on insect performance, and can significantly extend shelf life of insects. The barriers to utilizing fluctuating temperatures in mass production are engineering, rather than biological. 3) While a range of cryoprotectants are associated with low temperature survival and performance, Proline (and some other free amino acids) emerges as a particularly valuable molecule because it appears to be effective at relatively low concentrations and can be administered in the diet. Addition of proline to diet would be reasonably easy to implement in mass-rearing. 4) We explored the roles of plasticity of SIT-relevant traits to environmental stressors, and its interaction with responses to other stressors associated with irradiation, transport, and release. Harnessing plasticity to improve rearing, handling, and field performance of insects holds great potential to enhance the efficacy of existing programs and facilitate development of new programs.

          Relevance

          The specific objectives of the CRP were achieved: (a) we developed and assessed new methods to manage dormancy responses, physiological conditioning, and storage conditions to facilitate mass rearing; (b) we examined the genetic architecture of dormancy responses, physiological conditioning, and storage conditions; (c) we developed methods to incorporate dormancy into phenological models; (d) we explored the potential of dormancy responses, physiological conditioning, and storage conditions to enable or enhance the shelf life of biological control agents, including sterile insects, natural enemies, and other beneficial insects; (e) we assessed the interactions between dormancy responses, physiological conditioning, and storage conditions in reducing radiation injury and enhancing sterile insect performance; (f) we showed that dormancy responses and physiological conditioning decrease shipping-related damage and enhance post-shipping performance; (g) we characterized the role of the microbiome on dormancy responses, physiological conditioning, and low temperature biology in insects; (h) we laid groundwork for understanding the potential for dormancy responses to generate novel approaches for inducing “ecological suicide”; (i) we summarized the state of knowledge of low temperature biology in a format useful for risk assessors. An important next step will be to transfer these advances to colony and strain maintenance, mass rearing, and field application.

          CRP Publications

          Year

          2015

          Description

          Bentley M.T., F.M. Oi, S.A. Gezan and D.A. Hahn. 2015. Tunneling performance increases at lower temperatures for Solenopsis invicta (Buren) but not for Nylandaria fulva (Mayr). Insects. 6: 686-695.

          Country/Organization

          USA

          Year

          2015

          Description

          Coleman P.C., J.S. Bale and S.A.L. Hayward. 2015. Protein feeding affects the rapid cold hardening and thermal activity thresholds of adult Calliphora vicina (Diptera: Calliphoridae). PLoS ONE: e0131301.

          Country/Organization

          UK

          Year

          2015

          Description

          Sinclair B.J., L.E. Coello Alvarado, and L.V. Ferguson. 2015. An invitation to measure insect cold tolerance: Methods, approaches, and workflow. Journal of Thermal Biology 53: 180-197

          Country/Organization

          Canada

          Year

          2015

          Description

          MacMillan H.A., L.V. Ferguson, A. Nicolai, A. Donini, J.F. Staples and B.J. Sinclair. 2015. Parallel ionoregulatory adjustments underlie phenotypic plasticity and evolution of Drosophila cold tolerance. Journal of Experimental Biology 218: 423-432.

          Country/Organization

          Canada

          Year

          2015

          Description

          Gerken A.R., O.C. Eller, D.A. Hahn, and T.J. Morgan. 2015. Constraints, independence, and evolution of thermal plasticity; probing the genetic architecture of long and short-term thermal acclimation. Proceedings of the National Academy of Sciences. 112: 4399-4404.

          Country/Organization

          USA

          Year

          2015

          Description

          Meuti M.E., C.A. Short and D.L. Denlinger. 2015. Mom matters: diapause characteristics of Culex pipiens-Cx. quinquefasciatus (Diptera: Culicidae) hybrid mosquitoes. Journal of Medical Entomology 52: 131-137.

          Country/Organization

          USA

          Year

          2015

          Description

          Sim C., D.S. Kang, S. Kim, X. Bai and D.L. Denlinger. 2015. Identification of FOXO targets that generate the diverse features of the diapause phenotype in the mosquito Culex pipiens. Proceedings of the National Academy of Sciences, USA 112: 3811-3816.

          Country/Organization

          USA

          Year

          2014

          Description

          Luypaert G., J. Witters, J. Van Huylenbroeck, M. Maes, J. De Riek and P. De Clercq. 2014. Temperature-dependent development of the broad mite Polyphagotarsonemus latus (Acari: Tarsonemidae) on Rhododendron simsii. Experimental and Applied Acarology 63: 389-400.

          Country/Organization

          Belgium

          Year

          2016

          Description

          Kang D.S., M.A. Cotten, D.L. Denlinger and C. Sim. 2016. Comparative Transcriptomics Reveals Key Gene Expression Differences between Diapausing and Non-Diapausing Adults of Culex pipiens. PLoS ONE 11: e0154892.

          Country/Organization

          USA

          Year

          2014

          Description

          Denlinger D.L. and P.A. Armbruster. 2014. Mosquito diapause. Annual Review of Entomology 59: 73-93.

          Country/Organization

          USA

          Year

          2015

          Description

          Coello Alvarado L.E., H.A. MacMillan and B.J. Sinclair. 2015. Chill-tolerant Gryllus crickets maintain ion balance at low temperatures. Journal of Insect Physiology 77: 15-25.

          Country/Organization

          Canada

          Year

          2016

          Description

          Owen E.L., J.S. Bale and S.A.L. Hayward. 2016. Establishment risk of the commercially imported bumblebee Bombus terrestris dalamtinus – can they survive UK winters? Apidologie 47: 66-75.

          Country/Organization

          UK

          Year

          2015

          Description

          Zhang Q., R.J. Nachman and D.L. Denlinger. 2015. Diapause hormone in the Helicoverpa/Heliothis complex: a review of gene expression, peptide structure and activity, analog and antagonist development, and the receptor. Peptides 72: 196-201.

          Country/Organization

          USA

          Year

          2015

          Description

          Terhzaz S., N.M. Teets, P. Cabrero, L. Henderson, M.G. Ritchie, R.J. Nachman, J.A.T. Dow, D.L. Denlinger and S.-A. Davies. 2015. The insect capa neuropeptides impact desiccation and cold tolerance Proceedings of the National Academy of Sciences, USA 112: 2882-2887. Selected as Editors’ Choice in Science Signaling 8,ec54.

          Country/Organization

          USA

          Year

          2016

          Description

          Toxopeus J., R. Jakobs, L.V. Ferguson, T.D. Gariepy and B.J. Sinclair. 2016. Reproductive arrest and stress resistance in winter-acclimated Drosophila suzukii. Journal of Insect Physiology 89: 37-51.

          Country/Organization

          Canada

          Year

          2017

          Description

          Bonte J., D. Musolin, D. Conlong and P. De Clercq. 2016. Diapause and winter survival of two Orius species from southern Africa. BioControl 61: 519.

          Country/Organization

          Belgium

          Year

          2014

          Description

          Guz N., U. Toprak, A. Dageri, M. Oktay Gurkan and D.L. Denlinger. 2014. Identification of a putative antifreeze protein gene that is highly expressed during preparation for winter in the sunn pest, Eurygaster maura. Journal of Insect Physiology 68: 30-35.

          Country/Organization

          USA

          Year

          2014

          Description

          Li Y., L. Zhang, Q. Zhang, H. Chen and D.L. Denlinger. 2014. Host diapause status and host diets augmented with cryoprotectants enhance cold hardiness in the parasitoid Nasonia vitripennis. Journal of Insect Physiology 70: 8-14.

          Country/Organization

          USA

          Year

          2015

          Description

          Clemmensen S.F. and D.A. Hahn. 2015. Dormancy cues alter insect temperature-size relationships. Oecologia. 177: 113-121.

          Country/Organization

          USA

          Year

          2016

          Description

          Pateman R.M., C.D. Thomas, S.A.L. Hayward and J.K. Hill. 2016. Macro- and micro-climate interactions drive variation in species’ habitat associations. Glob. Change Biol. 22: 556-566.

          Country/Organization

          UK

          Year

          2015

          Description

          Poupardin R., K. Sch?ttner, J. Korbelová, J. Provazník, D. Dole?el, D. Pavlinic, V. Bene? and V. Ko?tál. 2015. Early transcriptional events linked to induction of diapause revealed by RNAseq in larvae of drosophilid fly, Chymomyza costata. BMC Genomics 16: 720.

          Country/Organization

          Czech Republic

          Year

          2015

          Description

          Cascone P., S. Carpenito, S. Slotsbo, L. Iodice, J.G. S?rensen, M. Holmstrup and E. Guerrieri. 2015. Improving the efficiency of Trichogramma achaeae to control Tuta absoluta. Biological Control 60: 761-771.

          Country/Organization

          Denmark

          Year

          2014

          Description

          Knutson, A., A. Mukherjee, D.A. Hahn and K.M. Heinz. 2014. Biological control of giant salvinia (Salvinia molesta) in a temperate region: cold tolerance and low temperature oviposition of Cyrtobagous salviniae. BioControl. 59: 781-790.

          Country/Organization

          USA

          Year

          2015

          Description

          Stevenson T.J., M.E. Visser, W. Arnold, P. Barrett, S. Biello, A. Dawson, D.L. Denlinger, D. Dominoni, F.J. Ebling, S.Elton, N. Evans, H.M. Ferguson, R.G. Foster, M Hau, D.T. Haydon, D.G.Halerigg, P. Heideman, J.G.C. Hopcraft, N.N. Jonsson, N. Kronfeld-Schor, V. Kumar, G.A. Lincoln, R. MacLeod, S.A.M. Martin, M. Martinez-Bakker, R.J. Nelson, T. Reed, J.E. Robinson, D.Rock, W.J. Schwartz, I. Steffan-Dewenter, E. Tauber, S.J. Thackeray, C. Umstattter, T. Yoshimura and B. Helm. 2015. Disrupted seasonal biology impacts health, food security, and ecosystems. Proceedings of the Royal Society B 282: 20151453.

          Country/Organization

          USA

          Year

          2014

          Description

          Williams C.M., M. Watanabe, M. Guarracino, M.B. Ferraro, A.S. Edison, T.J. Morgan, A. Boroujerdi and D.A. Hahn. 2014. Cold adaptation shapes the robustness of metabolic networks in Drosophila melanogaster. Evolution. 68: 3505-3523.

          Country/Organization

          USA

          Year

          2015

          Description

          Boardman L., J.G. S?rensen and John S. Terblanche. 2015. Physiological and molecular mechanisms associated with cross tolerance between hypoxia and low temperature in Thaumatotibia leucotreta. Journal of Insect Physiology 82: 75–84.

          Country/Organization

          South Africa & Denmark

          Year

          2015

          Description

          Li Y., L. Zhang, H. Chen, V. Kostal, P. Simek, M. Moos and D.L. Denlinger. 2015. Shifts in metabolomic profiles of the parasitoid Nasonia vitripennis associated with elevated cold tolerance induced by the parasitoid’s diapause, host diapause and host diet augmented with proline. Insect Biochemistry and Molecular Biology 63: 34-46.

          Country/Organization

          USA

          Year

          2016

          Description

          Hand S.C., D.L. Denlinger, J.E. Podrabsky and R. Roy. 2016. Mechanisms of animal diapause: recent developments from crustaceans, insects, nematodes and fish. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 310: R1193-R1211.

          Country/Organization

          USA

          Year

          2015

          Description

          Zhang Q., R.J. Nachman, K. Kaczmarek, K. Kierus, J. Zabrocki and D.L. Denlinger. 2015. Development of neuropeptide analogs capable of traversing the integument: a case study using diapause hormone analogs in Helicoverpa zea. Insect Biochemistry and Molecular Biology 67: 87-93.

          Country/Organization

          USA

          Year

          2015

          Description

          Benoit J.B., Q. Zhang, E.C. Jennings, A.J. Rosendale and D.L. Denlinger. 2015. Suppression of net transpiration by multiple mechanisms conserves water resources during pupal diapause in the corn earworm, Helicoverpa zea. Physiological Entomology 40:336-342.

          Country/Organization

          USA

          Year

          2015

          Description

          Meuti M.E., M. Stone, T. Ikeno and D.L. Denlinger. 2015. Functional circadian clock genes are essential for the overwintering diapause of the Northern house mosquito, Culex pipiens. Journal of Experimental Biology 218: 412-422.

          Country/Organization

          USA

          Year

          2014

          Description

          Kang D.S., D.L. Denlinger and C. Sim. 2014. Suppression of allatotropin simulates reproductive diapause in the mosquito Culex pipiens. Journal of Insect Physiology 64: 48-53.

          Country/Organization

          USA

          Year

          2016

          Description

          Urbanová V., O. Bazalová, H. Vanèccková and D. Dolezel. 2016. Photoperiod regulates growth of male accessory glands through juvenile hormone signaling in the linden bug, Pyrrhocoris apterus. Insect Biochemistry and Molecular Biology 70: 184-190.

          Country/Organization

          Czech Republic

          Year

          2015

          Description

          Van Damme V., N. Berkvens, R. Moerkens, E. Berckmoes, L. Wittemans, R. De Vis, H. Casteels, L. Tirry and P. De Clercq. 2015. Overwintering potential of the invasive leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) as a pest in greenhouse tomato production in Western Europe. Journal of Pest Science 88: 533-541.

          Country/Organization

          Belgium

          Year

          2015

          Description

          Colinet H., B.J. Sinclair, P. Vernon and D. Renault. 2015. Insects in Fluctuating Thermal Environments. Annual Review of Entomology 60: 123–40.

          Country/Organization

          France

          Year

          2014

          Description

          Terblanche J.S. 2014. Physiological performance of field-released insects Current Opinion in Insect Science 4: 60–66.

          Country/Organization

          South Africa

          Year

          2014

          Description

          Zhang Q., P.M. Piermarini, R.J. Nachman and D.L. Denlinger. 2014. Molecular identification and expression analysis of a diapause hormone receptor in the corn earworm, Helicoverpa zea. Peptides 53: 250-257.

          Country/Organization

          USA

          Year

          2016

          Description

          Ferguson L.V., D.E. Heinrichs and B.J. Sinclair. 2016. Paradoxical acclimation responses in the thermal performance of insect immunity. Oecologia 181: 77-85.

          Country/Organization

          Canada

          Year

          2016

          Description

          Des Marteaux L.E. and B.J. Sinclair. 2016. Ion and water balance in Gryllus crickets during the first twelve hours of cold exposure. Journal of Insect Physiology 89: 19-27.

          Country/Organization

          Canada

          Year

          2015

          Description

          Liu Y., Q. Zhang and D.L. Denlinger. 2015. Imidazole derivative KK-42 boosts pupal diapause incidence and delays diapause termination in several insect species. Journal of Insect Physiology 74: 38-44.

          Country/Organization

          USA

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