Abstract
The emerald ash borer (Agrilus planipennis, Coleoptera: Buprestidae) is a wood-boring invasive pest devastating North American ash (Fraxinus spp.). A. planipennis overwinters primarily as a freeze-avoiding prepupa within the outer xylem or inner bark of the host tree. The range of this species is expanding outward from its presumed introduction point in southwestern Michigan. We hypothesized that loss of cold tolerance in response to mid-winter warm spells could limit survival and northern distribution of A. planipennis. We determined whether winter-acclimatised A. planipennis prepupae reduced their cold tolerance in response to mid-winter warm periods, and whether this plasticity was reversible with subsequent cold exposure. Prepupae subjected to mid-winter warm spells of 10 and 15°C had increased supercooling points (SCPs) and thus reduced cold tolerance. This increase in SCP was accompanied by a rapid loss of haemolymph cryoprotectants and the loss of cold tolerance was not reversed when the prepupae were returned to −10°C. Exposure to temperatures fluctuating from 0 to 4°C did not reduce cold hardiness. Only extreme warming events for several days followed by extreme cold snaps may have lethal effects on overwintering A. planipennis populations. Thus, distribution in North America is likely to be limited by the presence of host trees rather than climatic factors, but we conclude that range extensions of invasive species could be halted if local climatic extremes induce unidirectional plastic responses.
Similar content being viewed by others
References
Andreadis SS, Milonas PG, Savopoulou-Soultani M (2005) Cold hardiness of diapausing and non-diapausing pupae of the European grapevine moth, Lobesia botrana. Entomol Exp Appl 117:113–118
Angilletta MJ (2009) Thermal adaptation–a theoretical and empirical synthesis. Oxford University Press, New York
Aulchenko YS, Ripke S, Isaacs A, Van Duijn CM (2007) GenABEL: an R library for genorne-wide association analysis. Bioinformatics 23:1294–1296. doi:10.1093/bioinformatics/btm108ER
Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Phil Trans R Soc Lond B 357:849–861. doi:10.1098/rstb.2002.1074ER
Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994. doi:10.1242/jeb.037911ER
Bale JS, Block W, Worland MR (2000) Thermal tolerance and acclimation response of larvae of the sub-Antarctic beetle Hydromedion sparsutum (Coleoptera: Perimylopidae). Polar Biol 23:77–84
Bentz BJ, Mullins DE (1999) Ecology of mountain pine beetle (Coleoptera : Scolytidae) cold hardening in the intermountain west. Environ Entomol 28:577–587
Bray AM, Bauer LS, Haack RA, Poland T, Smith JJ (2007) Invasion genetics of emerald ash borer (Agrilus planipennis FAIRMAIRE) in North America. Proceedings from the third workshop on genetics of bark beetles and associated microorganisms 21–22
Cappaert D, McCullough DG, Poland TM, Siegert NW (2005) Emerald ash borer in North America: a research and regulatory challenge. Am Entomologist 51:152–165
Caprio JM, Quamme HA, Redmond KT (2009) A statistical procedure to determine recent climate change of extreme daily meteorological data as applied at two locations in Northwestern North America. Clim Change 92:65–81. doi:10.1007/s10584-008-9474-1
Cattiaux J, Vautard R, Cassou C, Yiou P, Masson‐Delmotte V, Codron F (2010) Winter 2010 in Europe: A cold extreme in a warming climate. Geophys Res Lett 37, doi:10.1029/2010GL044613
Chown SL, Nicolson SW (2004) Insect physiological ecology- mechanisms and patterns. Oxford University Press, Oxford
Chown SL, Terblanche JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33(33):50–152
Cooperative Emerald Ash Borer Project (2010) http://www.emeraldashborer.info/files/MultiState_EABpos.pdf. Accessed 23 November 2010
Crosthwaite JC, Sobek S, Lyons DB, Bernards MA, Sinclair BJ (2011) The overwintering physiology of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). J Insect Physiol 75:166–173
Duman JG, Walters KR, Sformo T, Carrasco MA, Nickell PK, Lin X, Barnes BM (2010) Antifreeze and ice-nucleator proteins. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, New York, pp 59–90
Elkinton JS, Preisser E, Boettner G, Parry D (2008) Factors influencing larval survival of the invasive browntail moth (Lepidoptera: Lymantriidae) in relict North American populations. Environ Entomol 37:1429–1437
Environment Canada (2009) Canada’s top ten weather stories for 2008. http://www.ec.gc.ca/meteo-weather/default.asp?lang=En&n=4EB93F4E-1. Accessed 8 December 2010
Evans AM, Gregoire TG (2007) A geographically variable model of hemlock woolly adelgid spread. Biol Invasions 9:369–382. doi:10.1007/s10530-006-9039-z
Fields PG, Fleurat-Lessard F, Lavenseau L, Febvay G, Peypelut L, Bonnot G (1998) The effect of cold acclimation and deacclimation on cold tolerance, trehalose and free amino acid levels in Sitophilus granarius and Cryptolestes ferrugineus (Coleoptera). J Insect Physiol 44:955–965
Fortin G (2010) Variability and frequency of the freeze thaw cycles in Quebec region, 1977–2006. Can Geogr 54:196–208. doi:10.1111/j.1541-0064.2009.00291.x
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407. doi:10.1111/j.1365-2435.2007.01283.xER
Gibert P, Huey RB, Gilchrist GW (2001) Locomotor performance of Drosophila melanogaster: interactions among developmental and adult temperatures, age, and geography. Evolution 55:205–209
Han EN, Bauce E (1998) Timing of diapause initiation, metabolic changes and overwintering survival of the spruce budworm, Choristoneura fumiferana. Ecol Entomol 23:160–167
Hawes TC, Bale JS, Worland MR, Convey P (2007) Plasticity and superplasticity in the acclimation potential of the Antarctic mite Halozetes belgicae (Michael). J Exp Biol 210:593–601. doi:10.1242/jeb.02691ER
Hayes CJ, Hofstetter RW, DeGomez TE, Wagner MR (2009) Effects of sunlight exposure and log size on pine engraver (Coleoptera: Curculionidae) reproduction in ponderosa pine slash in Northern Arizona, USA. Agricult For Entomol 11:341–350. doi:10.1111/j.1461-9563.2009.00433.xER
IPCC (2007) Climate Change 2007, Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva, Switzerland: IPCC
Irwin JT, Lee RE (2000) Mild winter temperatures reduce survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). J Insect Physiol 46:655–661
Irwin JT, Lee RE (2003) Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100:71–78
Kim Y, Song WR (2000) Effect of thermoperiod and photoperiod on cold tolerance of Spodoptera exigua (Lepidoptera : Noctuidae). Environ Entomol 29:868–873
Lee RE (1991) Principles of insect low temperature tolerance. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman & Hall, New York, NY, pp 17–46
Lombardero MJ, Ayres MP, Ayres BD, Reeve JD (2000) Cold tolerance of four species of bark beetle (Coleoptera : Scolytidae) in North America. Environ Entomol 29:421–432
Lyons DB, Jones GC (2005) The biology and phenology of the emerald ash borer. In: Gottschalk KW (ed) Proceedings, 16th U.S. Department of Agriculture interagency research forum on gypsy moth and other invasive species, January 18–21, 2005, Annapolis, MD. Gen. Tech. Rep. NE-337 (abstract), pp 62–63
Marais E, Terblanche JS, Chown SL (2009) Life stage-related differences in hardening and acclimation of thermal tolerance traits in the kelp fly, Paractora dreuxi (Diptera, Helcomyzidae). J Insect Physiol 55:336–343. doi:10.1016/j.jinsphys.2008.11.016
McCullough DG, Schneeberger NF, Katovich SA (2004) Pest alert Emerald Ash Borer NA-PR-02-04. Newtown Square, PA: U.S. Dept. of Agriculture, Forest Service, Northeastern Area, State & Private Forestry
Milan JD, Harmon BL, Prather TS, Schwarzlander M (2006) Winter mortality of Aceria chondrillae, a biological control agent released to control rush skeletonweed (Chondrilla juncea) in the western United States. J Appl Entomol 130:473–479. doi:10.1111/j.1439-0418.2006.01090.xER
Natural Regions Committee (2006) Natural Regions and Subregions of Alberta. Government of Alberta, Pub. No. T/852
Natural Resources Canada (2010) The atlas of Canada- Weather. http://atlas.nrcan.gc.ca.proxy1.lib.uwo.ca:2048/site/english/learningresources/facts/superweather.html. Accessed 8 December 2010
Paradis A, Elkinton J, Hayhoe K, Buonaccorsi J (2008) Role of winter temperature and climate change on the survival and future range expansion of the hemlock woolly adelgid (Adelges tsugae) in eastern North America. Mitig Adapt Strat Glob Change 13:541–554
Parker BL, Skinner M, Gouli S, Ashikaga T, Teillon HB (1998) Survival of hemlock woolly adelgid (Homoptera: Adelgidae) at low temperatures. For Sci 44:414–420
Parker BL, Skinner M, Gouli S, Ashikaga T, Teillon HB (1999) Low lethal temperature for hemlock woolly adelgid (Homoptera: Adelgidae). Environ Entomol 28:1085–1091
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. doi:10.1146/annurev.ecolsys.37.091305.110100
Pelini SL, Dzurisin JDK, Prior KM, Williams CM, Marsico TD, Sinclair BJ, Hellmann JJ (2009) Translocation experiments with butterflies reveal limits to enhancement of poleward populations under climate change. Proc Natl Acad Sci USA 106:11160–11165. doi:10.1073/pnas.0900284106
Rako L, Hoffmann AA (2006) Complexity of the cold acclimation response in Drosophila melanogaster. J Insect Physiol 52:94–104. doi:10.1016/j.jinsphys.2005.09.007
Robinet C, Roques A (2010) Direct impacts of recent climate warming on insect populations. Integr Zool 5:132–142. doi:10.1111/j.1749-4877.2010.00196.xER
Scotter AJ, Marshall CB, Graham LA, Gilbert JA, Garnham CP, Davies PL (2006) The basis for hyperactivity of antifreeze proteins. Cryobiology 53:229–239. doi:10.1016/j.cryobiol.2006.06.006ER
Simberloff D, Gibbons L (2004) Now you see them, now you don’t–population crashes of established introduced species. Biol Invasions 6:161–172
Sinclair BJ, Vernon P, Klok CJ, Chown SL (2003) Insects at low temperatures: an ecological perspective. Trends Ecol Evol 18:257–262. doi:10.1016/S0169-5347(03)00014-4ER
Skinner M, Parker BL, Gouli S, Ashikaga T (2003) Regional responses of hemlock woolly adelgid (Homoptera : Adelgidae) to low temperatures. Environ Entomol 32:523–528
Slabber S, Worland MR, Leinaas HP, Chown SL (2007) Acclimation effects on thermal tolerances of springtails from sub-Antarctic Marion Island: Indigenous and invasive species. J Insect Physiol 53:113–125. doi:10.1016/j.jinsphys.2006.10.010ER
Storey JM, Storey KB (2004) Cold hardiness and freeze tolerance. In: Storey KB (ed) Functional metabolism: regulation and adaptation. Wiley-Liss, Hoboken, New Jersey, pp 473–503
R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.r-project.org
Terblanche JS, Sinclair BJ, Klok CJ, McFarlane ML, Chown SL (2005) The effects of acclimation on thermal tolerance, desiccation resistance and metabolic rate in Chirodica chalcoptera (Coleoptera: Chrysomelidae). J Insect Physiol 51:1013–1023. doi:10.1016/j.jinsphys.2005.04.016ER
Tran JK, Ylioja T, Billings RF, Regniere J, Ayres MP (2007) Impact of minimum winter temperatures on the population dynamics of Dendroctonus frontalis. Ecol Appl 17:882–899
Trotter RT, Shields KS (2009) Variation in winter survival of the invasive hemlock woolly adelgid (Hemiptera: Adelgidae) across the eastern United States. Environ Entomol 38:577–587
Ungerer MJ, Ayres MP, Lombardero MJ (1999) Climate and the northern distribution limits of Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae). J Biogeogr 26:1133–1145
USDA–APHIS (2009) Emerald Ash Borer Program Manual, Agrilus planipennis (Fairmaire) USDA–APHIS–PPQ–Emergency and Domestic Programs–Emergency Planning, Riverdale, Maryland
Wang XY, Yang ZQ, Gould JR, Zhang YN, Liu GJ, Liu ES (2010) The biology and ecology of the emerald ash borer, Agrilus planipennis, in China. J Insect Sci 10(128):1–23.http://www.insectscience.org/10.128/
Wei X, Wu Y, Reardon R, Sun TH, Lu M, Sun JH (2007) Biology and damage traits of emerald ash borer (Agrilus planipennis Fairmaire) in China. Insect Science 14:367–373. doi:10.1111/j.1744-7917.2007.00163.xER
Whitman DW, Agrawal AA (2009) What is phenotypic plasticity and why is it important? In: Whitman DW, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanisms and consequences. Science Publishers, Enfield, New Hampshire, pp 1–62
Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524
Zeng JP, Ge F, Su JW, Wang Y (2008) The effect of temperature on the diapause and cold hardiness of Dendrolimus tabulaeformis (Lepidoptera: Lasiocampidae). Eur J Entomol 105:599–606
Acknowledgments
This project was supported by an NSERC (Natural Sciences and Engineering Research Council of Canada) Strategic Grant to B.J.S. & D.B.L. and by the Canadian Foundation for Innovation. We are grateful to the Canadian Food Inspection Agency, the Canadian Forest Service, and the Sarnia Golf and Curling Club for advice and access to field sites. Part of this work was conducted in the Biotron Centre for Experimental Climate Change Research at the University of Western Ontario. Thanks also to David (Xinyang) Bing, Joshua Farhi and Greg Watkinson, who assisted with lab and field work. We are grateful to two anonymous referees for their valuable contributions to improve the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sobek-Swant, S., Crosthwaite, J.C., Lyons, D.B. et al. Could phenotypic plasticity limit an invasive species? Incomplete reversibility of mid-winter deacclimation in emerald ash borer. Biol Invasions 14, 115–125 (2012). https://doi.org/10.1007/s10530-011-9988-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-011-9988-8