Advertisement

Biological Invasions

, Volume 14, Issue 1, pp 115–125 | Cite as

Could phenotypic plasticity limit an invasive species? Incomplete reversibility of mid-winter deacclimation in emerald ash borer

  • Stephanie Sobek-SwantEmail author
  • Jill C. Crosthwaite
  • D. Barry Lyons
  • Brent J. Sinclair
Original Paper

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.

Keywords

Acclimation Cold hardiness Exotic pests Saproxylic beetles Supercooling Thermal hysteresis 

Notes

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.

References

  1. 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 117:113–118CrossRefGoogle Scholar
  2. Angilletta MJ (2009) Thermal adaptation–a theoretical and empirical synthesis. Oxford University Press, New YorkGoogle Scholar
  3. 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 PubMedCrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994. doi: 10.1242/jeb.037911ER PubMedCrossRefGoogle Scholar
  6. 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 23:77–84CrossRefGoogle Scholar
  7. Bentz BJ, Mullins DE (1999) Ecology of mountain pine beetle (Coleoptera : Scolytidae) cold hardening in the intermountain west. Environ Entomol 28:577–587Google Scholar
  8. 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 21–22Google Scholar
  9. Cappaert D, McCullough DG, Poland TM, Siegert NW (2005) Emerald ash borer in North America: a research and regulatory challenge. Am Entomologist 51:152–165Google Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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
  12. Chown SL, Nicolson SW (2004) Insect physiological ecology- mechanisms and patterns. Oxford University Press, OxfordCrossRefGoogle Scholar
  13. Chown SL, Terblanche JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33(33):50–152Google Scholar
  14. Cooperative Emerald Ash Borer Project (2010) http://www.emeraldashborer.info/files/MultiState_EABpos.pdf. Accessed 23 November 2010
  15. 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 75:166–173CrossRefGoogle Scholar
  16. 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 59–90CrossRefGoogle Scholar
  17. 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 37:1429–1437PubMedCrossRefGoogle Scholar
  18. 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
  19. 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 CrossRefGoogle Scholar
  20. 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 44:955–965PubMedCrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. Gibert P, Huey RB, Gilchrist GW (2001) Locomotor performance of Drosophila melanogaster: interactions among developmental and adult temperatures, age, and geography. Evolution 55:205–209PubMedGoogle Scholar
  24. Han EN, Bauce E (1998) Timing of diapause initiation, metabolic changes and overwintering survival of the spruce budworm, Choristoneura fumiferana. Ecol Entomol 23:160–167CrossRefGoogle Scholar
  25. 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 PubMedCrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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: IPCCGoogle Scholar
  28. 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 46:655–661PubMedCrossRefGoogle Scholar
  29. 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 100:71–78CrossRefGoogle Scholar
  30. Kim Y, Song WR (2000) Effect of thermoperiod and photoperiod on cold tolerance of Spodoptera exigua (Lepidoptera : Noctuidae). Environ Entomol 29:868–873CrossRefGoogle Scholar
  31. 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 17–46Google Scholar
  32. Lombardero MJ, Ayres MP, Ayres BD, Reeve JD (2000) Cold tolerance of four species of bark beetle (Coleoptera : Scolytidae) in North America. Environ Entomol 29:421–432CrossRefGoogle Scholar
  33. 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 62–63Google Scholar
  34. 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 PubMedCrossRefGoogle Scholar
  35. 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 ForestryGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. Natural Regions Committee (2006) Natural Regions and Subregions of Alberta. Government of Alberta, Pub. No. T/852Google Scholar
  38. 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
  39. 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 13:541–554CrossRefGoogle Scholar
  40. Parker BL, Skinner M, Gouli S, Ashikaga T, Teillon HB (1998) Survival of hemlock woolly adelgid (Homoptera: Adelgidae) at low temperatures. For Sci 44:414–420Google Scholar
  41. Parker BL, Skinner M, Gouli S, Ashikaga T, Teillon HB (1999) Low lethal temperature for hemlock woolly adelgid (Homoptera: Adelgidae). Environ Entomol 28:1085–1091Google Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 PubMedCrossRefGoogle Scholar
  44. 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 PubMedCrossRefGoogle Scholar
  45. 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 PubMedCrossRefGoogle Scholar
  46. 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 PubMedCrossRefGoogle Scholar
  47. Simberloff D, Gibbons L (2004) Now you see them, now you don’t–population crashes of established introduced species. Biol Invasions 6:161–172CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. Skinner M, Parker BL, Gouli S, Ashikaga T (2003) Regional responses of hemlock woolly adelgid (Homoptera : Adelgidae) to low temperatures. Environ Entomol 32:523–528CrossRefGoogle Scholar
  50. 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 PubMedCrossRefGoogle Scholar
  51. 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 473–503CrossRefGoogle Scholar
  52. 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
  53. 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 PubMedCrossRefGoogle Scholar
  54. 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 17:882–899PubMedCrossRefGoogle Scholar
  55. Trotter RT, Shields KS (2009) Variation in winter survival of the invasive hemlock woolly adelgid (Hemiptera: Adelgidae) across the eastern United States. Environ Entomol 38:577–587PubMedCrossRefGoogle Scholar
  56. Ungerer MJ, Ayres MP, Lombardero MJ (1999) Climate and the northern distribution limits of Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae). J Biogeogr 26:1133–1145CrossRefGoogle Scholar
  57. USDA–APHIS (2009) Emerald Ash Borer Program Manual, Agrilus planipennis (Fairmaire) USDA–APHIS–PPQ–Emergency and Domestic Programs–Emergency Planning, Riverdale, MarylandGoogle Scholar
  58. 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/
  59. 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 CrossRefGoogle Scholar
  60. 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 1–62CrossRefGoogle Scholar
  61. Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524CrossRefGoogle Scholar
  62. 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 105:599–606Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Stephanie Sobek-Swant
    • 1
    • 2
    Email author
  • Jill C. Crosthwaite
    • 1
  • D. Barry Lyons
    • 3
  • Brent J. Sinclair
    • 1
  1. 1.Department of BiologyThe University of Western OntarioLondonCanada
  2. 2.Department of BiologyUniversity of WaterlooWaterlooCanada
  3. 3.Great Lakes Forestry CentreMarieCanada

Personalised recommendations