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Cold tolerance and overwintering survival of Aphelinus certus (Hymenoptera: Aphelinidae), a parasitoid of the soybean aphid (Hemiptera: Aphididae) in North America

Published online by Cambridge University Press:  26 June 2023

Carl M. Stenoien*
Affiliation:
Department of Entomology, University of Minnesota, St. Paul, Minnesota 55108, USA
Lindsey Christianson
Affiliation:
Department of Entomology, University of Minnesota, St. Paul, Minnesota 55108, USA
Kelton Welch
Affiliation:
Department of Entomology, University of Minnesota, St. Paul, Minnesota 55108, USA
Jonathan Dregni
Affiliation:
Department of Entomology, University of Minnesota, St. Paul, Minnesota 55108, USA
Keith R. Hopper
Affiliation:
USDA, ARS, Beneficial Insect Introductions Research Unit, Newark, DE 19713D, USA
George E. Heimpel
Affiliation:
Department of Entomology, University of Minnesota, St. Paul, Minnesota 55108, USA
*
Corresponding author: Carl M. Stenoien; Email: sten0364@umn.edu

Abstract

Broad-spectrum insecticides are the main control measure of the invasive and economically damaging soybean aphid (Aphis glycines) in North America, although biological control by resident natural enemies can also greatly diminish population levels. One such natural enemy is the accidentally introduced Eurasian parasitoid Aphelinus certus (Hymenoptera: Aphelinidae), though its impact appears to be limited by low rates of parasitism early in the growing season. We tested the hypothesis that A. certus might experience high overwintering mortality. In the laboratory, we used thermocouple thermometry to measure the supercooling points of diapausing parasitoids and assessed parasitoid survival after exposure to ecologically relevant durations of low temperature. We found A. certus to be freeze-intolerant with a median supercooling point of −28°C. When exposed to temperatures of 0°C for up to 7 months, adults emerged only after exposures of at least 60 days and survival decreased with durations beyond 150 days. We also conducted in-field studies at sites from northern Minnesota to southern Iowa to determine if diapausing A. certus could overwinter above and below the snowpack. Survival was negatively correlated with increasing latitude and was greater for parasitoids placed on the ground than 1 meter off the ground, likely due to the warmer and stabler temperatures of the subnivean microclimate. Our results suggest that A. certus is capable of overwintering in the region inhabited by soybean aphid but may experience substantial mortality even under ideal conditions. Climate change is predicted to bring warmer, drier winters to the North American Midwest, with decreased depth and duration of snow cover, which may further reduce overwintering survival.

Type
Research Paper
Creative Commons
This is a work of the US Government and is not subject to copyright protection within the United States. Published by Cambridge University Press.
Copyright
Copyright © United States Department of Agriculture, 2023

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References

Asplen, MK, Wyckhuys, K and Heimpel, GE (2011) Parasitism of autumnal morphs of the soybean aphid (Hemiptera: Aphididae) by Binodoxys communis (Hymenoptera: Braconidae) on buckthorn. Annals of the Entomological Society of America 104, 935944.CrossRefGoogle Scholar
Asplen, MK, Chacón, JM and Heimpel, GE (2016) Sex-specific dispersal by a parasitoid wasp in the field. Entomologia Experimentalis et Applicata 159, 252259.CrossRefGoogle Scholar
Bates, D, Mächler, M, Bolker, BM and Walker, SC (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.CrossRefGoogle Scholar
Calvo-Agudo, M, Dregni, JS, González-Cabrera, J, Dicke, M, Heimpel, GE and Tena, A (2021) Neonicotinoids from coated seeds toxic for honeydew-feeding biological control agents. Environmental Pollution 289, 117813.CrossRefGoogle ScholarPubMed
Chacón, JM and Heimpel, GE (2010) Density-dependent intraguild predation of an aphid parasitoid. Oecologia 164, 213220.CrossRefGoogle ScholarPubMed
Claassen, R, Bowman, M, Wallander, J, David, M and Steven, S (2018) Tillage intensity and conservation cropping in the United States, Sept. 2018.Google Scholar
Demaria, EMC, Roundy, JK, Wi, S and Palmer, RN (2016) The effects of climate change on seasonal snowpack and the hydrology of the Northeastern and Upper Midwest United States. Journal of Climate 29, 65276541.CrossRefGoogle Scholar
Dieckhoff, C, Theobald, JC, Wäckers, FL and Heimpel, GE (2014) Egg load dynamics and the risk of egg and time limitation experienced by an aphid parasitoid in the field. Ecology and Evolution 4, 17391750.CrossRefGoogle ScholarPubMed
Douglas, MR and Tooker, JF (2015) Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in U.S. Field crops. Environmental Science and Technology 49, 50885097.CrossRefGoogle ScholarPubMed
Frewin, AJ, Xue, Y, Welsman, JA, Broadbent, B, Schaafsma, AW and Hallett, RH (2010) Development and parasitism by Aphelinus certus (Hymenoptera: Aphelinidae), a parasitoid of Aphis glycines (Hemiptera: Aphididae). Environmental Entomology 39, 15701578.CrossRefGoogle ScholarPubMed
Gariepy, V, Boivin, G and Brodeur, J (2015) Why two species of parasitoids showed promise in the laboratory but failed to control the soybean aphid under field conditions. Biological Control 80, 17.CrossRefGoogle Scholar
Ghising, K, Harmon, JP, Beauzay, PB, Prischmann-Voldseth, DA, Helms, TC, Ode, PJ and Knodel, JJ (2012) Impact of rag1 aphid resistant soybeans on Binodoxys communis (Hymenoptera: Braconidae), a parasitoid of soybean aphid (Hemiptera: Aphididae). Environmental Entomology 41, 282288.CrossRefGoogle ScholarPubMed
Hallett, RH, Bahlai, CA, Xue, Y and Schaafsma, AW (2014) Incorporating natural enemy units into a dynamic action threshold for the soybean aphid, Aphis glycines (Homoptera: Aphididae). Pest Management Science 70, 879888.CrossRefGoogle ScholarPubMed
Hanson, AA and Venette, RC (2013) Thermocouple design for measuring temperatures of small insects. CryoLetters 34, 261266.Google ScholarPubMed
Hanson, AA, Menger-Anderson, J, Silverstein, C, Potter, BD, Macrae, IV, Hodgson, EW and Koch, RL (2017) Evidence for soybean aphid (Hemiptera: Aphididae) resistance to pyrethroid insecticides in the Upper Midwestern United States. Journal of Economic Entomology 110, 22352246.CrossRefGoogle ScholarPubMed
Heimpel, GE and Asplen, MK (2011) A ‘Goldilocks’ hypothesis for dispersal of biological control agents. BioControl 56, 441450.CrossRefGoogle Scholar
Heimpel, GE, Ragsdale, DW, Venette, RC, Hopper, KR, O'Neil, RJ, Rutledge, CE and Wu, Z (2004) Prospects for importation biological control of the soybean aphid: anticipating potential costs and benefits. Annals of the Entomological Society of America 97, 249258.CrossRefGoogle Scholar
Heimpel, GE, Frelich, LE, Landis, DA, Hopper, KR, Hoelmer, KA, Sezen, Z, Asplen, MK and Wu, K (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biological Invasions 12, 29132931.CrossRefGoogle Scholar
Heimpel, GE, Yang, Y, Hill, JD and Ragsdale, DW (2013) Environmental consequences of invasive species: greenhouse gas emissions of insecticide use and the role of biological control in reducing emissions. PLoS ONE 8, 17.CrossRefGoogle ScholarPubMed
Hopper, KR and Diers, BW (2014) Parasitism of soybean aphid by Aphelinus species on soybean susceptible versus resistant to the aphid. Biological Control 76, 101106.CrossRefGoogle Scholar
Hopper, KR, Lanier, K, Rhoades, JH, Hoelmer, KA, Meikle, WG, Heimpel, GE, O'Neil, RJ, Voegtlin, DG and Woolley, JB (2017) Host specificity of Aphelinus species collected from soybean aphid in Asia. Biological Control 115, 5573.CrossRefGoogle Scholar
Hopper, KR, Oppenheim, SJ, Kuhn, KL, Lanier, K, Hoelmer, KA, Heimpel, GE, Meikle, WG, O'Neil, RJ, Voegtlin, DG, Wu, K, Woolley, JB and Heraty, JM (2019) Counties not countries: variation in host specificity among populations of an aphid parasitoid. Evolutionary Applications 12, 815829.CrossRefGoogle Scholar
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346363.CrossRefGoogle ScholarPubMed
Kaser, JM (2016) Risk and Efficacy in Biological Control: An Evaluation of the Aphid Parasitoid Aphelinus certus in North America. Minneapolis: University of Minnesota.Google Scholar
Kaser, JM and Heimpel, GE (2018) Impact of the parasitoid Aphelinus certus on soybean aphid populations. Biological Control 127, 1724.CrossRefGoogle Scholar
Koch, RL, Potter, BD, Glogoza, PA, Hodgson, EW, Krupke, CH, Tooker, JF, DiFonzo, CD, Michel, AP, Tilmon, KJ, Prochaska, TJ, Knodel, JJ, Wright, RJ, Hunt, TE, Jensen, B, Varenhorst, AJ, McCornack, BP, Estes, KA and Spencer, JL (2016) Biology and economics of recommendations for insecticide-based management of soybean aphid. Plant Health Progress 17, 265269.CrossRefGoogle Scholar
Leblanc, A and Brodeur, J (2018) Estimating parasitoid impact on aphid populations in the field. Biological Control 119, 3342.CrossRefGoogle Scholar
Lee, RJ (2010) A primer on insect cold-tolerance. In Denlinger, D and Lee, RJ (eds), Low Temperature. Biology of Insects. Cambridge: Cambridge University Press, pp. 334.CrossRefGoogle Scholar
Liess, S, Twine, TE, Snyder, PK, Hutchison, WD, Konar-Steenberg, G, Keeler, BL and Brauman, KA (2022) High-resolution climate projections over Minnesota for the 21st century. Earth and Space Science 9, 116.CrossRefGoogle Scholar
Liu, J, Wu, K, Hopper, KR and Zhao, K (2004) Population dynamics of Aphis glycines (Homoptera: Aphididae) and its natural enemies in soybean in northern China. Annals of the Entomological Society of America 97, 235239.CrossRefGoogle Scholar
Miksanek, JR and Heimpel, GE (2019) A matrix model describing host-parasitoid population dynamics: the case of Aphelinus certus and soybean aphid. PLoS ONE 14, e0218217.CrossRefGoogle ScholarPubMed
Miksanek, JR and Heimpel, GE (2020 a) A field-based assessment of the parasitoid Aphelinus certus as a biological control agent of soybean aphid in North America. Biological Control 146, 104284.CrossRefGoogle Scholar
Miksanek, JR and Heimpel, GE (2020 b) Density-dependent lifespan and estimation of life expectancy for a parasitoid with implications for population dynamics. Oecologia 194, 311320.CrossRefGoogle ScholarPubMed
Monticelli, LS, Desneux, N and Heimpel, GE (2021) Parasitoid-mediated indirect interactions between unsuitable and suitable hosts generate apparent predation in microcosm and modeling studies. Ecology and Evolution 11, 24492460.CrossRefGoogle ScholarPubMed
Overgaard, J and Macmillan, HA (2017) The integrative physiology of insect chill tolerance. Annual Review of Physiology 79, 187208.CrossRefGoogle ScholarPubMed
Pauli, JN, Zuckerberg, B, Whiteman, JP and Porter, W (2013) The subnivium: a deteriorating seasonal refugium. Frontiers in Ecology and the Environment 11, 260267.CrossRefGoogle Scholar
Petty, SK, Zuckerberg, B and Pauli, JN (2015) Winter conditions and land cover structure the subnivium, a seasonal refuge beneath the snow. PLoS ONE 10, e0127613.CrossRefGoogle ScholarPubMed
Ragsdale, DW, Voegtlin, DJ and O'Neil, RJ (2004) Soybean aphid biology in North America. Annals of the Entomological Society of America 97, 204208.CrossRefGoogle Scholar
Ragsdale, DW, Landis, DA, Brodeur, J, Heimpel, GE and Desneux, N (2011) Ecology and management of the soybean aphid in North America. Annual Review of Entomology 56, 375399.CrossRefGoogle ScholarPubMed
Ramløv, H (2000) Aspects of natural cold tolerance in ectothermic animals. Human Reproduction 15, 2646.CrossRefGoogle ScholarPubMed
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Renault, D, Salin, C, Vannier, G and Vernon, P (2002) Survival at low temperatures in insects: what is the ecological significance of the supercooling point? CryoLetters 23, 217228.Google ScholarPubMed
Salt, RW (1961) Principles of insect cold-hardiness. Annual Review of Entomology 6, 5574.CrossRefGoogle Scholar
Somme, L (1999) The physiology of cold hardiness in terrestrial arthropods. European Journal of Entomology 96, 110.Google Scholar
Stanley, DA, Garratt, MPD, Wickens, JB, Wickens, VJ, Potts, SG and Raine, NE (2015) Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528, 548550.CrossRefGoogle ScholarPubMed
Stockton, D, Wallingford, A, Rendon, D, Fanning, P, Green, CK, Diepenbrock, L, Ballman, E, Walton, VM, Isaacs, R, Leach, H, Sial, AA, Drummond, F, Burrack, H and Loeb, GM (2019) Interactions between biotic and abiotic factors affect survival in overwintering Drosophila suzukii (Diptera: Drosophilidae). Environmental Entomology 48, 454464.CrossRefGoogle Scholar
Su, M, Tan, X, Yang, Q, Wan, F and Zhou, H (2018) Temperature adaptability of two clades of Aphelinus mali (Hymenoptera: Aphelinidae) in China. Egyptian Journal of Biological Pest Control 28, 17.CrossRefGoogle Scholar
Suggitt, AJ, Gillingham, PK, Hill, JK, Huntley, B, Kunin, WE, Roy, DB and Thomas, CD (2011) Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 18.CrossRefGoogle Scholar
Tatsumi, E and Takada, H (2005) Effects of photoperiod and temperature on adult oligopause of Aphelinus asychis and larval diapause of A. albipodus (Hymenoptera: Aphelinidae). Applied Entomology and Zoology 40, 447456.CrossRefGoogle Scholar
Tatsumi, E and Takada, H (2006) Overwintering of the aphid parasitoids Aphelinus asychis and A. albipodus (Hymenoptera: Aphelinidae) under natural conditions in Kyoto, Japan. Applied Entomology and Zoology 41, 139144.CrossRefGoogle Scholar
Teets, NM and Denlinger, DL (2013) Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiological Entomology 38, 105116.CrossRefGoogle Scholar
Thompson, KL, Zuckerberg, B, Porter, WP and Pauli, JN (2018) The phenology of the subnivium. Environmental Research Letters 13, 064037.CrossRefGoogle Scholar
Trimble, RM, Blommers, LHM and Helsen, HHM (1990) Diapause termination and thermal requirements for postdiapause development in Aphelinus mali at constant and fluctuating temperatures. Entomologia Experimentalis et Applicata 56, 6169.CrossRefGoogle Scholar
Turnock, WJ and Fields, PG (2005) Winter climates and cold hardiness in terrestrial insects. European Journal of Entomology 102, 561576.CrossRefGoogle Scholar
Venette, RC and Ragsdale, DW (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Annals of the Entomological Society of America 97, 219226.CrossRefGoogle Scholar
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S, Fourth edition. New York: Springer. ISBN 0-387-95457-0, https://www.stats.ox.ac.uk/pub/MASS4CrossRefGoogle Scholar
Voegtlin, DJ, Halbert, SE and Qiao, GX (2004) A guide to separating Aphis glycines Matsumura and morphologically similar species that share its hosts. Annals of the Entomological Society of America 97, 227232.CrossRefGoogle Scholar
Voegtlin, DJ, O'Neil, RJ, Graves, WR, Lagos, D, Ho, A and Yoo, JS (2005) Potential winter hosts of soybean aphid. Annals of the Entomological Society of America 98, 690693.CrossRefGoogle Scholar
Wu, Z, Schenk-Hamlin, D, Zhan, W, Ragsdale, DW and Heimpel, GE (2004) The soybean aphid in China: a historical review. Annals of the Entomological Society of America 97, 209218.CrossRefGoogle Scholar
Yu, DS (1992) Effects of photoperiod and temperature on diapause of two Aphelinus spp. (Hymenoptera: Aphelinidae) parasitizing the Russian wheat aphid. The Canadian Entomologist 124, 853860.CrossRefGoogle Scholar
Zhu, L, Radeloff, VC and Ives, AR (2017) Characterizing global patterns of frozen ground with and without snow cover using microwave and MODIS satellite data products. Remote Sensing of Environment 191, 168178.CrossRefGoogle Scholar