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Intraspecific variation in Fraxinus pennsylvanica responses to emerald ash borer (Agrilus planipennis)

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Abstract

The emerald ash borer (EAB; Agrilus planipennis Fairmaire) is a bark and wood boring beetle native to east Asia that was first discovered in North America in 2002. Since then, entire stands of highly susceptible green ash (Fraxinus pennsylvanica Marshall) have been killed within a few years of infestation. We have identified a small number of mature green ash trees which have been attacked by EAB, yet survived the peak EAB infestation that resulted in mortality of the rest of the ash cohort. Adult landing and feeding preference bioassays, leaf volatile quantification and EAB egg bioassay experiments were used to characterize potential differences in responses of these select “lingering” green ash trees relative to known EAB susceptible controls. Three selections were identified as being significantly less preferred for adult feeding, but no specific leaf volatile profile was associated with this reduced preference. Egg bioassays identified two ash selections that had significant differences in larval survival and development; one having a higher number of larvae killed by apparent host tree defenses and the other having lower larval weight. Correlation and validation of the bioassay results in replicated plantings to assess EAB resistance in the field is still necessary. However, the differences between lingering ash selections and susceptible controls measured by these bioassays indicate that more than one mechanism is responsible for the increased resistance to EAB that resulted in these selections surviving longer than their counterparts. Efforts to further increase ash resistance to EAB through use of these selections in a breeding program are underway.

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References

  • Abell KJ, Duan JJ, Bauer L, Lelito JP, Van Driesche RG (2012) The effect of bark thickness on host partitioning between Tetrastichus planipennisi (Hymen: Eulophidae) and Atanycolus spp. (Hymen: Braconidae), two parasitoids of emerald ash borer (Coleop: Buprestidae). Biol Control 63:320–325. doi:10.1016/j.biocontrol.2012.08.009

    Article  Google Scholar 

  • Anulewicz AC, McCullough DG, Cappaert DL (2007) Emerald ash borer (Agrilus planipennis) density and canopy dieback in three North American ash species. Arboric Urban For 33:338–349

    Google Scholar 

  • Anulewicz AC, McCullough DG, Cappaert DL, Poland TM (2008) Host range of the emerald ash borer (Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), in North America: results of multiple-choice field experiments. Environ Entomol 37:230–241. doi:10.1603/0046-225X(2008)37[230:HROTEA]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Cappaert D, McCullough DG, Poland TM, Siegert NW (2005) Emerald ash borer in North America: a research and regulatory challenge. Am Entomol 51:152–164

    Article  Google Scholar 

  • Carey DW, Mason ME, Bloese P, Koch JL (2013) Hot callusing for propagation of American beech by grafting. HortScience 48:620–624

    Google Scholar 

  • Chamorro ML, Volkovitsh MG, Poland TM, Haack RA, Lingafelter SW (2012) Preimaginal stages of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae): an invasive pest on ash trees (Fraxinus). PLoS ONE 7(3):e33185. doi:10.1371/journal.pone.0033185

    Article  PubMed Central  PubMed  Google Scholar 

  • Chen Y, Poland TM (2009a) Interactive influence of leaf age, light intensity, and girdling on green ash foliar chemistry and emerald ash borer development. J Chem Ecol 35:806–815. doi:10.1007/s10886-009-9661-1

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Poland TM (2009b) Biotic and abiotic factors affect green ash volatile production and emerald ash borer feeding performance. Environ Entomol 38:1756–1764. doi:10.1603/022.038.0629

    Article  CAS  PubMed  Google Scholar 

  • Crook DJ, Mastro VC (2010) Chemical ecology of the emerald ash borer Agrilus planipennis. J Chem Ecol 36:101–112. doi:10.1007/s10886-009-9738-x

    Article  CAS  PubMed  Google Scholar 

  • Crook DA, Khrimian A, Francese JA, Fraser I, Poland TM, Sawyer AJ, Mastro VC (2008) Development of a host-based semiochemical lure for trapping emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae). Environ Entomol 37:356–365. doi:10.1093/ee/37.2.356

    Article  CAS  PubMed  Google Scholar 

  • de Groot P, Grant GG, Poland TM, Scharbach R, Buchan L, Nott RW, MacDonald L, Pitt D (2008) Electrophysiological response and attraction of emerald ash borer to green leaf volatiles (GLVs) emitted by host foliage. J Chem Ecol 34:1170–1179. doi:10.1007/s10886-008-9514-3

    Article  PubMed  Google Scholar 

  • Duan JJ, Ulyshen MD, Bauer LS, Gould J, Van Driesche R (2010) Measuring impact of biotic factors on populations of immature emerald ash borers (Coleoptera: Buprestidae). Environ Entomol 39:1513–1522. doi:10.1603/EN10023

    Article  PubMed  Google Scholar 

  • Duan JJ, Yurchenko G, Fuester R (2012) Occurrence of emerald ash borer (Coleoptera: Buprestidae) and biotic factors affecting its immature stage in the Russian Far East. Environ Entomol 41:245–354. doi:10.1603/EN11318

    Article  PubMed  Google Scholar 

  • Duan JJ, Bauer LS, Abell KJ, Lelito JP, van Driesche R (2013a) Establishment and abundance of Testrastichus planipennisi (Hymenoptera: Eulophidae) in Michigan: potential for success in classical biocontrol of the invasive emerald ash borer (Coleoptera: Buprestidae). J Econ Entomol 106:1145–1154. doi:10.1603/EC13047

    Article  PubMed  Google Scholar 

  • Duan JJ, Larson K, Watt T, Gould J, Lelito JP (2013b) Effects of host plant and larval density on intraspecific competition in larvae of the emerald ash borer (Coleoptera: Buprestidae). Environ Entomol 42:1193–1200. doi:10.1603/EN13209

    Article  PubMed  Google Scholar 

  • Duan JJ, Watt T, Taylor P, Larson K, Lelito JP (2013c) Effects of ambient temperature on egg and larval development of the invasive emerald ash borer (Coleoptera:Buprestidae): implications for laboratory rearing. J Econ Entomol 106:2101–2108. doi:10.1603/EC13131

    Article  PubMed  Google Scholar 

  • Duan JJ, Abell KJ, Bauer LS, Gould J, VanDriesche R (2014) Natural enemies implicated in the regulation of an invasive pest: a life table analysis of the population dynamics of the emerald ash borer. Agric For Entomol 16:406–416. doi:10.1111/afe.12070

    Article  Google Scholar 

  • Gandhi KJK, Smith A, Hartzler DM, Herms DA (2014) Indirect effects of emerald ash borer-induced ash mortality and canopy gap formation on epigaeic beetles. Environ Entomol 43:546–555. doi:10.1603/EN13227

    Article  PubMed  Google Scholar 

  • Haack RA, Jendek E, Liu H, Marchant KR, Petrice TR, Poland TM, Ye H (2002) The emerald ash borer: A new exotic pest in North America. Newsl of the Michigan Entomol Soc 47:1–5

    Google Scholar 

  • Herms DA, McCullough DG (2014) Emerald ash borer invasion of North America: history, biology, ecology, impact and management. Annu Rev Entomol 59:13–30. doi:10.1146/annurev-ento-011613-162051

    Article  CAS  PubMed  Google Scholar 

  • Herms DA, Cipollin D, Knight KS, Koch JL, Poland TM, Rigsby C, Whitehill JGA, Bonello P (2015) The quest for resistance to emerald ash borer: towards a mechanistic understanding. In: Proceedings of the 26th USDA interagency forum on invasive species. Gen Tech Rep USDA Forest Service Northern Research Station (in press)

  • Honěk A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492. doi:10.2307/3544943

    Article  Google Scholar 

  • Jennings DE, Taylor PB, Duan JJ (2014) The mating and oviposition behavior of the invasive emerald ash borer (Agrilus planipennis), with reference to the influence of host tree condition. J Pest Sci 87:71–78. doi:10.1007/s10340-013-0539-1

    Article  Google Scholar 

  • Keena MA (2002) Anoplophora glabripennis (Coleoptera: Cerambycidae) fecundity and longevity under laboratory conditions: comparison of populations from New York and Illinois on Acer Saccharum. Environ Entomol 31:490–498. doi:10.1603/0046-225X-31.3.490

    Article  Google Scholar 

  • Klooster WS, Herms DA, Knight KS, Herms CP, McCullough DG, Smith AS, Gandhi KJK, Cardina J (2014) Ash (Fraxinus spp.) mortality, regeneration, and seed bank dynamics in mixed hardwood forests following invasion by emerald ash borer (Agrilus planipennis). Biol Invas 16:859–873. doi:10.1007/s10530-013-0543-7

    Article  Google Scholar 

  • Knight KS, Herms DA, Plumb R, Sawyer E, Spalink D, Pisarczyk E, Wiggin B, Kappler R, Ziegler E, Menard K (2012) Dynamics of surviving ash (Fraxinus spp.) populations in areas long infested by emerald ash borer (Agrilus planipennis). In: Sniezko RA, Yanchuk AD, Kliejunas JT, Palmieri KM, Alexander JM, Frankel SJ (eds) Proceedings of the 4th international workshop on genetics host–parasite interactions in forestry, USDA Forest Service Pacific Southwest Research Station, PSW-GTR-240, pp 143–152

  • Knight KS, Brown JP, Long RP (2013) Factors affecting the survival of ash (Fraxinus spp.) trees infested by emerald ash borer (Agrilus planipennis). Biol Inv 15:371–383. doi:10.1007/s10530-012-0292-z

    Article  Google Scholar 

  • Knight KS, Flash BP, Kappler RH, Throckmorton JA, Grafton B, Flower CE (2014) Monitoring ash (Fraxinus spp.) decline and emerald ash borer (Agrilus planipennis) symptoms in infested areas. Gen Tech Rep NRS-139. U.S. Department of Agriculture, Forest Service, Northern Research Station, Newtown Square, PA

  • Koch JL (2010) Beech bark disease: The oldest “new” threat to American beech in the United States. Outlooks on Pest Management April 2010: 64-68

  • Koch JL, Mason ME, Carey DW, Nelson CD (2010) Assessment of beech scale resistance in full and half-sibling American beech families. Can J For Res 40:265–272. doi:10.1139/X09-189

    Article  Google Scholar 

  • Lelito JP, Fraser I, Mastro VC, Tumlinson JH, Boroczky K, Baker TC (2007) Visually mediated ‘paratrooper copulations’ in the mating behavior of Agrilus planipennis (Coleoptera: Buprestidae), a highly destructive invasive pest of North American ash trees. J Insect Behav 20:537–552. doi:10.1007/s10905-007-9097-9

    Article  Google Scholar 

  • Liu H, Bauer LS, Gao R, Zhao T, Petrice TR, Haack RA (2003) Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and its natural enemies in China. Great Lakes Entomol 36:191–204

    Google Scholar 

  • Liu J, Bauer LS, Miller DL, Zhao T, Gao R, Song L, Luan Q, Jin R, Gao C (2007) Seasonal abundance of Agrilus planipennis (Coleoptera: Buprestidae) and its natural enemies Oobius agrili (Hymenoptera: Encyrtidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae) in China. Biocontrol 42:61–71. doi:10.1016/j.biocontrol.2007.03.011

    Google Scholar 

  • Marshall JM, Porter MJ, Storer AJ (2012) Predicting emerald ash borer, Agrilus planipennis (Coleptera: Buprestidae), landing behavior on unwounded ash. Great Lakes Entomol 45:29–39

    Google Scholar 

  • Marshall JM, Smith EL, Mech R, Storer AJ (2013) Estimates of Agrilus planipennis infestation rates and potential survival of ash. Am Midland Nat 169:179–193. doi:10.1674/0003-0031-169.1.179

    Article  Google Scholar 

  • McCullough DG, Poland TM, Anulewicz AC, Cappaert D (2009) Emerald ash borer (Agrilus planipennis Fairmaire) (Coleoptera: Buprestidae) attraction to stressed or baited ash trees. Environ Entomol 38:1668–1679. doi:10.1603/022.038.06201668

    Article  PubMed  Google Scholar 

  • Minitab Inc. (2013) Getting started with Minitab 17. Minitab Inc., State College

    Google Scholar 

  • Oten LFK, Merkle SA, Jetton RM, Smith BC, Talley ME, Hain FP (2014) Understanding and developing resistance in hemlocks to the hemlock wooly adelgid. Southeast Nat 13:147–167. doi:10.1656/058.013.s610

    Google Scholar 

  • Poland TM, Chen Y, Koch J, Pureswaran D (2015) Review of the emerald ash borer (Coleoptera: Buprestidae), life history, mating behaviors, host plant selection and host plant resistance. Can Entomol 147:252–262. doi:10.4039/tce.2015.4

    Article  Google Scholar 

  • Puraswaran DS, Poland TM (2009) Host selection and feeding preference of Agrilus planipennis (Coleoptera: Buprestidae) on ash (Fraxinus spp.). Environ Entomol 38:757–765. doi:10.1603/022.038.0328

    Article  Google Scholar 

  • Rebek EJ, Herms DA, Smitley DR (2008) Interspecific variation in resistance to emerald ash borer (Coleoptera: Buprestidae) along North American and Asian ash (Fraxinus spp.). Environ Entomol 37:242–246. doi:10.1603/0046-225X(2008)37[242:IVIRTE]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Rigsby CM, Showalter DN, Herms DA, Koch JL, Bonello P, Cipollini D (2015) Physiological responses of emerald ash borer larvae to feeding on different ash species reveal putative resistance mechanisms and insect counter-adaptations. J Insect Phys 78:47–54. doi:10.1016/j.jinsphys.2015.05.001

    Article  CAS  Google Scholar 

  • Rodriguez-Saona C, Poland TM, Miller JR, Stelinski LL, Grant GG, de Groot P, Buchan MacDonald L (2006) Behavioral and electrophysiological responses of the emerald ash borer, Agrilus planipennis, to induced volatiles of Manchurian ash, Fraxinus mandshurica. Chemoecology 16:75–86. doi:10.1007/s00049-005-0329-1

    Article  CAS  Google Scholar 

  • Schiers J, De Bruyn L (2002) Integrating optimal foraging and optimal oviposition preference in plant–insect research. Oikos 96:187–191. doi:10.1034/j.1600-0706.2002.960121.x

    Article  Google Scholar 

  • Siegert NW, McCullough DG, Leibhold AM, Telewski FW (2014) Dendrochronological reconstruction of the epicentre and early spread of emerald ash borer in North America. Divers Distrib 20:847–858. doi:10.1111/ddi.12212

    Article  Google Scholar 

  • Smith A (2006) Effects of community structure on forest susceptibility and response to the emerald ash borer invasion of the Huron River Watershed in southeastern Michigan. Thesis, The Ohio State University. Permalink: http://rave.ohiolink.edu/etdc/view?acc_num=osu1394801603

  • Tanis SR, McCullough DG (2012) Differential persistence of blue ash and white ash following emerald ash borer invasion. Can J For Res 42:1542–1550. doi:10.1139/x2012-103

    Article  Google Scholar 

  • Tubesing CE (1987) Chip budding of magnolias. Comb Proc Intl Plant Prop Soc 37:377–379

    Google Scholar 

  • Wang Q, Shi G, Song D, Rogers DJ, Davis LK, Chen X (2002) Development, survival, body weight, longevity, and reproductive potential of Oemena hirta (Coleoptera: Cerambycidae) under different rearing conditions. J Econ Entomol 95:563–569. doi:10.1603/0022-0493-95.3.563

    Article  PubMed  Google Scholar 

  • Wei X, Reardon D, Wu Y, Sun J (2004) Emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), in China: a review and distribution survey. Acta Entomol Sin 47:679–685

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank Debbie Miller and Tina Ciaramataro for assistance in rearing EAB eggs and the performance of adult landing and feeding bioassays, Rachel Kappler for assisting with scion collections and field data collection, Ryan Matko and Mark Miller for assistance in plant rearing and egg bioassays and the many summer seasonal employees of the USDA Forest Service Northern Research Station, the Ohio State University, and Metroparks of the Toledo area who assisted with field data collection. We are grateful to Dr. Daniel A. Herms for sharing data from his monitoring plots in southeastern Michigan and to Diane Hartzler for help with compilation of that data. We also thank Dr. Margaret Staton and Dr. Jeanne Romero-Severson as well as two anonymous reviewers for their helpful comments on an earlier draft of the manuscript. This work was funded by the USDA Forest Service Northern Research Station, the USDA APHIS Accelerated Emerald Ash Borer Research Program and by the Toledo Metroparks through a Grant from the American Recovery and Reinvestment Act (ARRA).

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Authors and Affiliations

  1. US Forest Service, Northern Research Station, 359 Main Rd., Delaware, OH, 43015, USA

    J. L. Koch, D. W. Carey & K. S. Knight

  2. Ohio Agricultural Research and Development Center, Department of Entomology, The Ohio State University, 1680 Madison Ave., Wooster, OH, 44691, USA

    M. E. Mason

  3. US Forest Service, Northern Research Station, 3101 Technology Blvd., Suite F, Lansing, MI, 48910, USA

    T. M. Poland

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  1. J. L. Koch
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Correspondence to J. L. Koch.

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Figure S1

Examples of host defense killed larvae in two EAB-resistant Asian Fraxinus species, F. mandshurica (Manchurian ash) and F. chinensis (Chinese ash) compared to host defense killed larvae in the EAB-susceptible North American species F. pennsylvanica (green ash). (JPEG 167 kb)

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Koch, J.L., Carey, D.W., Mason, M.E. et al. Intraspecific variation in Fraxinus pennsylvanica responses to emerald ash borer (Agrilus planipennis). New Forests 46, 995–1011 (2015). https://doi.org/10.1007/s11056-015-9494-4

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