Biological Invasions

, Volume 16, Issue 4, pp 859–873 | Cite as

Ash (Fraxinus spp.) mortality, regeneration, and seed bank dynamics in mixed hardwood forests following invasion by emerald ash borer (Agrilus planipennis)

  • Wendy S. Klooster
  • Daniel A. Herms
  • Kathleen S. Knight
  • Catherine P. Herms
  • Deborah G. McCullough
  • Annemarie Smith
  • Kamal J. K. Gandhi
  • John Cardina
Original Paper

Abstract

Emerald ash borer (EAB; Agrilus planipennis) has killed millions of ash trees and threatens ash throughout North America, and long-term persistence of ash will depend on the potential for regeneration. We quantified ash demography, including mortality and regeneration, of Fraxinus americana (white ash), Fraxinus pennsylvanica (green ash), and Fraxinus nigra (black ash) in mixed hardwood forests near the epicenter of the EAB invasion in southeastern Michigan and throughout Ohio. Plots were established across a gradient of ash densities. Ash was the most important species in hydric sites, and ranked second among all species in mesic and xeric sites. In sites nearest the epicenter in Michigan, ash mortality exceeded 99 % by 2009, and few or no newly germinated ash seedlings were observed, leaving only an “orphaned cohort” of established ash seedlings and saplings. As ash mortality increased, the number of viable ash seeds in soil samples decreased sharply, and no viable seeds were collected in 2007 or 2008. In Ohio sites farther from the epicenter, densities of new ash seedlings were much higher in plots with healthy ash trees compared to plots where trees had died. EAB was still present in low densities in Michigan and Ohio stands in 2012 where average mortality of ash was nearly 100 %. The future of ash at these sites will depend on the outcome of the dynamic interaction between the orphaned cohort of previously established ash seedlings and saplings and low density EAB populations.

Keywords

Ash regeneration Demography Invasive forest pest Seedlings 

References

  1. 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 33:338–349Google Scholar
  2. Barnes BV (1976) Succession in deciduous swamp communities of southeastern Michigan formerly dominated by American elm. Can J Bot 54:19–24CrossRefGoogle Scholar
  3. Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San DiegoGoogle Scholar
  4. Bauer L, Gould J, Duan J, et al. (2010) Emerald ash borer biological control. In: McManus K, Gottschalk KW (eds) 21st US Department of Agriculture Interagency Research Forum on Invasive Species. USDA Forest Service, Annapolis, pp 70–73Google Scholar
  5. BenDor TK, Metcalf SS, Fontenot LE et al (2006) Modeling the spread of the emerald ash borer. Ecol Model 197:221–236CrossRefGoogle Scholar
  6. Boerner REJ, Brinkman JA (1996) Ten years of tree seedling establishment and mortality in an Ohio deciduous forest complex. Bull Torrey Bot Club 123:309–317CrossRefGoogle Scholar
  7. Bonner FT (2008) Fraxinus L. ash. In: Bonner FT, Karrfalt RP (eds) The woody plant seed manual. Agricultural handbook 727. US Department of Agriculture, Forest Service, Washington, pp 537–543Google Scholar
  8. Burns RM, Honkala BH (1990) Silvics of North America: 1. Conifers; 2. Hardwoods. Agriculture handbook 654. 2. US Department of Agriculture, Forest Service, WashingtonGoogle Scholar
  9. Cappaert D, McCullough DG (2009) Occurrence and seasonal abundance of Atanycolus cappaerti (Hymenoptera: Braconidae) a native parasitoid of emerald ash borer, Agrilus plonipennis (Coleoptera: Buprestidae). Great Lakes Entomol 42:16–29Google Scholar
  10. Cappaert DL, McCullough DG, Poland TM et al (2005) Emerald ash borer in North America: a research and regulatory challenge. Am Entomol 51:152–165Google Scholar
  11. Cardina J, Sparrow DH (1996) A comparison of methods to predict weed seedling populations from the soil seedbank. Weed Sci 44:46–51Google Scholar
  12. Clark FB (1962) White ash, hackberry, and yellow-poplar seed remain viable when stored in the forest litter. Proceed Indiana Acad Sci 72:112–114Google Scholar
  13. Crosthwaite JC, Sobek S, Lyons DB et al (2011) The overwintering physiology of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). J Insect Physiol 57:166–173PubMedCrossRefGoogle Scholar
  14. D’Amato AW (2010) Silvicultural options for black ash communities facing the threat of emerald ash borer. Black ash symposium. USDA Forest Service. Bemidji. http://www.fs.usda.gov/Internet/FSE_DOCUMENTS/stelprdb5191802.pdf
  15. Dietze MC, Clark JS (2008) Changing the gap dynamics paradigm: vegetative regeneration control on forest response to disturbance. Ecol Monogr 78:331–347CrossRefGoogle Scholar
  16. Duan JJ, Bauer LS, Abell KJ et al (2012) Population responses of hymenopteran parasitoids to the emerald ash borer (Coleoptera: Buprestidae) in recently invaded areas in north central United States. Bio Control 57:199–209Google Scholar
  17. Ellis RH, Hong TD, Roberts EH (1985) Handbook of seed technology for genebanks II. Compendium of specific germination information and test recommendations. International Board for Plant Genetic Resources, RomeGoogle Scholar
  18. Eschtruth AK, Cleavitt NL, Battles JJ et al (2006) Vegetation dynamics in declining eastern hemlock stands: 9 years of forest response to hemlock woolly adelgid infestation. Can J For Res 36:1435–1450CrossRefGoogle Scholar
  19. Faanes CA (1984) Wooded islands in a sea of prairie. Am Birds 38:3–6Google Scholar
  20. Flower CE, Knight KS, Rebbeck J et al (2013) The relationship between the emerald ash borer (Agrilus planipennis) and ash (Fraxinus spp.) tree decline: using visual canopy condition assessments and leaf isotope measurements to assess pest damage. For Ecol Manag 303:143–147CrossRefGoogle Scholar
  21. Franklin JF, Spies TA, Pelt RV et al (2002) Disturbances and structural development of natural forest ecosystems with silvicultural implications, using Douglas-fir forests as an example. For Ecol Manag 155:399–423CrossRefGoogle Scholar
  22. Gandhi KJK, Herms DA (2010a) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol Invasions 12:389–405CrossRefGoogle Scholar
  23. Gandhi KJK, Herms DA (2010b) North American arthropods at risk due to widespread Fraxinus mortality caused by the alien emerald ash borer. Biol Invasions 12:1839–1846CrossRefGoogle Scholar
  24. Griffith RS (1991) Fraxinus americana. In: Fire effects information system (online). USDA Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory, p 32Google Scholar
  25. Gucker CL (2005a) Fraxinus nigra. In: Fire effects information system (online). USDA Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory, p 32Google Scholar
  26. Gucker CL (2005b) Fraxinus pennsylvanica. In: Fire effects information system (online). USDA Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory, p 32Google Scholar
  27. Hyatt LA, Casper BB (2000) Seed bank formation during early secondary succession in a temperate deciduous forest. J Ecol 88:516–527CrossRefGoogle Scholar
  28. Kennedy HE (1990) Fraxinus pennsylvanica Marsh. green ash. In: Burns RM, Honkala BH (eds) Silvics of North American. Agricultural handbook, vol 654. US Department of Agriculture, Forest Service, Washington, pp 348–354Google Scholar
  29. Klooster WS (2012) Forest responses to emerald ash borer-induced ash mortality (Doctoral dissertation). The Ohio State University, Columbus, p 205Google Scholar
  30. Knight KS, Herms DA, Plumb R, et al. (2012) Dynamics of surviving ash (Fraxinus spp.) in areas long infested by emerald ash borer (Agrilus planipennis). In: Sniezko R, Yanchuk A, Kliejunas J, Palmieri K, Alexander J, Frankel S (eds) Proceedings of the 4th international workshop on the genetics of host-parasite interactions in forestry: disease and insect resistance in forest trees. Eugene. Genetics technical report PSW-GTR-240. US Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, pp 143–152Google Scholar
  31. Kurmis V, Kim JH (1989) Black ash stand composition and structure in Carlton County, Minnesota. Department of Forest Resources Staff Paper Series, no. 69. University of Minnesota, Twin CitiesGoogle Scholar
  32. Leak WB (1963) Delayed germination of white ash seeds under forest conditions. J For 61:768–772Google Scholar
  33. Lesica P (2001) Recruitment of Fraxinus pennsylvanica (Oleaceae) in eastern Montana woodlands. Madroño 48:286–292Google Scholar
  34. Liu H, Bauer LS, Gao R et al (2003) Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and its natural enemies in China. Great Lakes Entomol 36:191–204Google Scholar
  35. Lovett GM, Canham CD, Arthur MA et al (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405CrossRefGoogle Scholar
  36. MacFarlane DW, Meyer SP (2005) Characteristics and distribution of potential ash tree hosts for emerald ash borer. For Ecol Manag 213:15–24CrossRefGoogle Scholar
  37. Marquis DA (1975) Seed storage and germination under northern hardwood forests. Can J For Res 5:478–484CrossRefGoogle Scholar
  38. Martin AC, Zim HS, Nelson AL (1951) American wildlife and plants: a guide to wildlife food habits. Dover Publications, Inc., New YorkGoogle Scholar
  39. McCullough DG, Schneeberger NF, Katovich SA (2008) Emerald ash borer pest alert. NA-PR-02-04. USDA Forest ServiceGoogle Scholar
  40. Orwig DA (2002) Ecosystem to regional impacts of introduced pests and pathogens: historical context, questions and issues. J Biogeogr 29:1471–1474CrossRefGoogle Scholar
  41. Palik BJ, Ostry ME, Venette RC et al (2012) Tree regeneration in black ash (Fraxinus nigra) stands exhibiting crown dieback in Minnesota. For Ecol Manag 269:26–30CrossRefGoogle Scholar
  42. Parker GR, Leopold DJ (1983) Replacement of Ulmus americana L. in a mature east-central Indiana woods. Bull Torrey Bot Club 110:482–488CrossRefGoogle Scholar
  43. Peters J (2005) Tetrazolium testing handbook. Handbook on seed testing, 6th edn. Association of Official Seed AnalystsGoogle Scholar
  44. Pickett STA, McDonnell MJ (1989) Seed bank dynamics in temperate deciduous forest. In: Leck MA, Parker VT, Simpson RL (eds) Ecology of soil seed banks. Academic Press, San Diego, p 462Google Scholar
  45. Poland TM, McCullough DG (2006) Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. J For 104:118–124Google Scholar
  46. Pugh SA, Liebhold AM, Morin RS (2011) Changes in ash tree demography associated with emerald ash borer invasion, indicated by regional forest inventory data from the Great Lakes States. Can J For Res 41:2165–2175CrossRefGoogle Scholar
  47. Rebek EJ, Herms DA, Smitley DR (2008) Interspecific variation in resistance to emerald ash borer (Coleoptera: Buprestidae) among North American and Asian ash (Fraxinus spp.). Environ Entomol 37:242–246PubMedCrossRefGoogle Scholar
  48. Reiners WA, Reiners NM (1970) Energy and nutrient dynamics of forest floors in three Minnesota forests. J Ecol 58:497–519CrossRefGoogle Scholar
  49. Richardson CJ, Cares CW (1976) An analysis of elm (Ulmus americana) mortality in a second-growth hardwood forest in southeastern Michigan. Can J Bot 54:1120–1125CrossRefGoogle Scholar
  50. Sawma JT, Mohler CL (2002) Evaluating seed viability by an unimbibed seed crush test in comparison with the tetrazolium test. Weed Technol 16:781–786CrossRefGoogle Scholar
  51. Schlesinger RC (1990) Fraxinus americana L. white ash. In: Burns RM, Honkala BH (eds) Silvics of North America. Agricultural handbook, vol 654. US Department of Agriculture, Forest Service, Washington, pp 333–338Google Scholar
  52. Siegert NW, McCullough DG, Liebhold AM, et al. (2008) Dendrochronological reconstruction of the establishment and spread of emerald ash borer. In: Mastro V, Lance D, Reardon R, Parra G (eds) Emerald ash borer research and development meeting. Pittsburgh, PA. FHTET 2008–2007. US Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, pp 4–5Google Scholar
  53. 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 (Master’s thesis). The Ohio State University, Columbus, p 122Google Scholar
  54. Tanis SR, McCullough DG (2012) Differential persistence of blue ash and white ash following emerald ash borer invasion. Can J For Res 42:1542–1550CrossRefGoogle Scholar
  55. US Forest Service (2007) Forest inventory and analysis national core field guide, vol 1. Field data collection procedures for phase 2 plots. Version 4.0. Available from http://www.fia.fs.fed.us/library/field-guides-methods-proc/docs/2013/Core%20FIA%20P2%20field%20guide_6-0_6_27_2013.pdf. Accessed 28 February 2012
  56. Whitehill JG, Herms DA, Bonello P (2009) Comparative constituitive and induced phloem chemistry of North American, European, and Asian ash species that vary in resistance to emerald ash borer. In: Lance D, Buck J, Binion D, Reardon R, Mastro V (eds) Emerald ash borer research and technology development meeting. Forest Health Technology Enterprise Team, Pittsburgh, pp 56–57Google Scholar
  57. Wright JW, Rauscher HM (1990) Fraxinus nigra Marsh. black ash. In: Burns RM, Honkala BH (eds) Silvics of North America. Agricultural handbook, vol 654. US Department of Agricuture, Forest Service, Washington, pp 344–347Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Wendy S. Klooster
    • 1
  • Daniel A. Herms
    • 2
  • Kathleen S. Knight
    • 3
  • Catherine P. Herms
    • 1
  • Deborah G. McCullough
    • 4
  • Annemarie Smith
    • 2
  • Kamal J. K. Gandhi
    • 2
    • 5
  • John Cardina
    • 1
  1. 1.Department of Horticulture and Crop Science, Ohio Agricultural Research and Development CenterThe Ohio State UniversityWoosterUSA
  2. 2.Department of Entomology, Ohio Agricultural Research and Development CenterThe Ohio State UniversityWoosterUSA
  3. 3.Forestry Sciences Laboratory, Northern Research StationUSDA Forest ServiceDelawareUSA
  4. 4.Departments of Entomology and ForestryMichigan State UniversityEast LansingUSA
  5. 5.Daniel B. Warnell School of Forestry and Natural ResourcesThe University of GeorgiaAthensUSA

Personalised recommendations