Evidence of damage from exotic invasive earthworm activity was highly correlated to sugar maple dieback in the Upper Great Lakes region

  • Tara L. Bal
  • Andrew J. Storer
  • Martin F. Jurgensen
Original Paper

Abstract

Sugar maple (Acer sacharrum Marsh.) in the western Upper Great Lakes region has recently been reported with increased crown dieback symptoms, prompting investigation of the dieback etiology across the region. Evaluation of sugar maple dieback from 2009 to 2012 across a 120 plot network in Upper Michigan, northern Wisconsin, and eastern Minnesota has indicated that forest floor disturbance impacts from exotic invasive earthworms was significantly related to maple dieback. Other plot level variables tested showed significant relationships among dieback and increased soil carbon, decreased soil manganese, and reduced herbaceous cover, each of which was also be correlated to earthworm activity. Relationships between possible causal factors and recent growth trends and seedling counts were also examined. Maple regeneration counts were not correlated with the amount of dieback. The recent mean radial increment was significantly correlated with various soil features and nutrients. This study presents significant evidence correlating sugar maple dieback in the western Upper Great Lakes region with earthworm activity, and highlights the need for considering the impacts of non-native earthworm on soil properties when assessing sugar maple health and productivity.

Keywords

Sugar maple Crown dieback Earthworms Forest health Soil disturbance 

References

  1. Adams CM, Hutchison TC (1992) Fine-root growth and chemical composition in declining Central Ontario sugar maple stands. Can J For Res 22:1489–1503. doi:10.1139/x92-199 CrossRefGoogle Scholar
  2. Allen DC, Barnett CJ, Millers I, Lachance D (1992) Temporal change (1988–1990) in sugar maple health, and factors associated with crown condition. Can J For Res 22:1776–1784. doi:10.1139/x92-232 CrossRefGoogle Scholar
  3. Allen DC, Molloy AW, Cooke RR, Pendrel BA (1999) A ten-year regional assessment of sugar maple mortality. In: Proceedings of sugar maple ecology and health: an international symposium. Warren, MI. June 2–4, 1998. USDA Forest Service Gen Tech Rep NE-261 pp 27–45Google Scholar
  4. Amacher MC, Henderson RE, Breithaupt MD, Seale CL, LaBauve JM (1990) Unbuffered and buffered salt methods for exchangeable cations and effective cation-exchange capacity. Soil Sci Soc Am J 54:1036–1042. doi:10.2136/sssaj1990.03615995005400040018x CrossRefGoogle Scholar
  5. Anderson GW, Schmiege DC (1959) The forest insect and disease situation lake states 1958. USDA Forest Service Station Paper No 70Google Scholar
  6. Bal TL (2013) Evaluation of sugar maple dieback in the Upper Great Lakes region and development of a forest health youth education program. Dissertation. Michigan Technological UniversityGoogle Scholar
  7. Bal TL, Storer AJ (2015) Evaluation of sugar maple dieback trends in the Upper Great Lakes region. In: Potter KM, Conkling BL (eds) Forest health monitoring: national status, trends, and analysis 2014 USDA Forest Service Gen Tech Rep SRS-209, pp 119–124Google Scholar
  8. Bal TL, Richter DL, Storer AJ, Jurgensen MF (2013) The relationship of the sapstreak fungus, Ceratocystis virescens to sugar maple dieback and decay in Northern Michigan. Am J Plant Sci 4:436–443. doi:10.4236/ajps.2013.42A056 CrossRefGoogle Scholar
  9. Bal TL, Storer AJ, Jurgensen MF, Doskey PV, Amacher MC (2015) Nutrient stress predisposes and contributes to sugar maple dieback across its northern range: a review. Forestry 88:64–83. doi:10.1093/forestry/cpu051 CrossRefGoogle Scholar
  10. Bernier B, Brazeau M (1988) Nutrient deficiency symptoms associated with sugar maple dieback and decline in the Quebec Appalachians. Can J For Res 18:762–767. doi:10.1139/x88-116 CrossRefGoogle Scholar
  11. Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suárez E, Pelletier DM, Fahey RT (2004) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12. doi:10.1007/s10021-003-0126-z CrossRefGoogle Scholar
  12. Cameron EK, Bayne EM (2015) Spatial patterns and spread of exotic earthworms at local scales. Can J Zool 93:721–726. doi:10.1139/cjz-2014-0197 CrossRefGoogle Scholar
  13. Cleavitt NL, Fahey TJ, Battles JJ (2011) Regeneration ecology of sugar maple (Acer saccharum): seddling survival in relation to nutrition, site factors, and damage by insects and pathogens. Can J For Res 41:235–244. doi:10.1139/X10-210 CrossRefGoogle Scholar
  14. Coderre D, Mauffette Y, Gagnon D, Tousignant S, Bessette G (1995) Earthworm populations in healthy and declining sugar maple forests. Pedobiologia 39:86–96Google Scholar
  15. Coffman MS, Alyanak E, Kotar J, Ferris JE (1984) Field guide habitat classification system for upper Peninsula of Michigan and Northeast Wisconsin. Cooperative Research on Forest Soils; School of Forestry and Wood Products, Michigan Technological University, HoughtonGoogle Scholar
  16. Corio K, Wolf A, Draney M, Fewless G (2009) Exotic earthworms of Great Lakes Forests: a search for indicator plant species in maple forests. For Ecol Manag 258:1059–1066. doi:10.1016/j.foreco.2009.05.013 CrossRefGoogle Scholar
  17. Côté B, Ouimet R (1996) Decline of the maple-dominated forest in southern Quebec: impact of natural stresses and forest management. Environ Rev 4:133–148. doi:10.1139/a96-009 CrossRefGoogle Scholar
  18. David MB (2008) Use of loss-on-ignition to assess soil organic carbon in forest soils. Commun Soil Sci Plan 19:1593–1599. doi:10.1080/00103628809368037 CrossRefGoogle Scholar
  19. Day PR (1965) Hydrometer methods of particle size analysis. Methods of Soil Anal Agron 9:562–566Google Scholar
  20. Dempsey MA, Fisk MC, Fahey TJ (2011) Earthworms increase the ratio of bacteria to fungi in northern hardwood forest soils, primarily by eliminating the organic horizon. Soil Biol Biochem 43:2135–2141. doi:10.1016/j.soilbio.2011.06.017 CrossRefGoogle Scholar
  21. Drohan PJ, Stout SL, Petersen GW (2002) Sugar maple (Acer saccharum Marsh.) decline during 1979–1989 in northern Pennsylvania. For Ecol Manag 170:1–17. doi:10.1016/S0378-1127(01)00688-0 CrossRefGoogle Scholar
  22. Drouin M, Bradley R, Lapointe L, Whalen J (2014) Non-native anecic earthworms (Lumbricus terrestris L.) reduce seed germination and seedling survival of temperate and boreal trees species. Appl Soil Ecol 75:145–149. doi:10.1016/j.apsoil.2013.11.006 CrossRefGoogle Scholar
  23. Fisichelli NA, Frehlich LE, Reich PB, Eisenhauer N (2012) Linking direct and indirect pathways mediating earthworms, deer, and understory composition in Great Lakes forests. Biol Invasions 15:1057–1066. doi:10.1007/s10530-012-0350-6 CrossRefGoogle Scholar
  24. Fisk MC, Fahey TJ, Groffman PM, Bohlen PJ (2004) Earthworm invasion, fine-root distributions, and soil respiration in north temperate forests. Ecosystems 7:55–62. doi:10.1007/s10021-003-0130-3 CrossRefGoogle Scholar
  25. Frelich LE, Hale CM, Scheu S, Holdsworth AR, Heneghan L, Bohlen PJ, Reich PB (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–1245. doi:10.1007/s10530-006-9019-3 CrossRefGoogle Scholar
  26. Gilbert KD, Fahey TJ, Marez JC, Sherman RE, Bohlen P, Dombroskie JJ, Groffman PM, Yavitt JB (2014) Exploring carbon flow through the root channel in a temperate forest soil food web. Soil Biol Biochem 76:45–52. doi:10.1016/j.soilbio.2014.05.005 CrossRefGoogle Scholar
  27. Godman RM, Yawney HW, Tubbs CH (1990) Acer saccharum Marsh. Sugar Maple. In Burns, RM Honkala BH (eds) Silvics of North America, vol 2. Hardwoods. USDA Forest Service Agricultural Handbook 654. USDA Forest Service, Washington, pp 78–91Google Scholar
  28. Groffman PM, Bohlen PJ, Fisk MC, Fahey TJ (2004) Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems 7:45–54. doi:10.1007/s10021-003-0129-9 CrossRefGoogle Scholar
  29. Hale CM (2007) Earthworms of the Great Lakes. Kollath-Stensaas, Duluth, p 36Google Scholar
  30. Hale CM, Frelich LE, Reich PB, Pastor J (2005) Effects of European earthworm invasion on soil characteristics in northern hardwood forests of Minnesota, U.S.A. Ecosystems 8:911–927. doi:10.1007/s10021-005-0066-x CrossRefGoogle Scholar
  31. Hale CM, Frehlich LE, Reich PB (2006) Changes in cold-temperate hardwood forest understory plant communities in response to European earthworm introductions. Ecology 87:1637–1649. doi:10.1890/0012-9658(2006)87[1637:CIHFUP]2.0.CO;2Google Scholar
  32. Hale CM, Frelich LE, Reich PB, Pastor J (2008) Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 155:509–518. doi:10.1007/s00442-007-0925-6 CrossRefPubMedGoogle Scholar
  33. Hendrix PF, Bohlen PJ (2002) Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 52:801–811. doi:10.1641/0006-3568(2002)052[0801:EEIINA]2.0.CO;2
  34. Holdsworth AR, Frehlich LE, Reich PB (2007a) Effects of earthworm invasion on plant species richness in Northern hardwood forests. Conserv Bio 21:997–1008. doi:10.1111/j.1523-1739.2007.00740.x CrossRefGoogle Scholar
  35. Holdsworth AR, Frehlich LE, Reich PB (2007b) Regional extent of an ecosystem engineer: earthworm invasion in Northern hardwood forests. Ecol Appl 17:1666–1677. doi:10.1890/05-2003.1 CrossRefPubMedGoogle Scholar
  36. Holdsworth AR, Frehlich LE, Reich PB (2012) Leaf litter disappearance in earthworm-invaded Northern hardwood forests: role of tree species and the chemistry and diversity of litter. Ecosystems 15:913–926. doi:10.1007/s10021-012-9554-y CrossRefGoogle Scholar
  37. Horsley SB, Long RP (eds) (1999) Sugar maple ecology and health: an international symposium. USDA Forest Service General Technical Report NE-261, Warren, June 2–4, 1998Google Scholar
  38. Horsley SB, Long RP, Bailey SW, Hallett RA, Hall TJ (2000) Factors associated with the decline disease of sugar maple on the Allegheny Plateau. Can J For Res 30:1365–1378. doi:10.1139/x00-057 CrossRefGoogle Scholar
  39. Houston DR (1992) A host–saprogen model for forest dieback-decline diseases. In: Manion PD, Lachance D (eds) Forest decline concepts. APS Press, New York, pp 3–25Google Scholar
  40. Houston DR (1999) History of sugar maple decline. In: Horsley SB, Long RP (eds) Sugar maple ecology and health, USDA Forest Service General Technical Report NE-261, pp 19–26Google Scholar
  41. Kessler KJ Jr (1965) Dieback of managed, old growth northern hardwoods in upper Michigan, 1954–1964: a case history. Plant Dis Rep 49:483–486Google Scholar
  42. Kolb TE, McCormick LH (1993) Etiology of a sugar maple decline in four Pennsylvania stands. Can J For Res 23:2395–2402. doi:10.1139/x93-296 CrossRefGoogle Scholar
  43. Larcombe MJ, Silva JS, Vaillancourt RE, Potts BM (2013) Assessing the invasive potential of Eucalyptus globulus in Australia: quantification of wildling establishment from plantations. Biol Invasions 15:2763–2781. doi:10.1007/s10530-013-0492-1 CrossRefGoogle Scholar
  44. Larson ER, Kipfmueller KF, Hale CM, Frelich LE, Reich PB (2010) Tree rings detect earthworm invasions and their effects in Northern hardwood forests. Biol Invasions 12:1053–1066. doi:10.1007/s10530-009-9523-3 CrossRefGoogle Scholar
  45. Lawrence B, Fisk MC, Fahey TJ, Suarez ER (2001) Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytol 157:145–153. doi:10.1046/j.1469-8137.2003.00649.x CrossRefGoogle Scholar
  46. Li X, Fisk MC, Fahey TJ, Bohlen PJ (2002) Influence of earthworm invasion on soil microbial biomass and activity in a Northern hardwood forest. Soil Bio Biochem 34:1929–1937. doi:10.1016/S0038-0717(02)00210-9 CrossRefGoogle Scholar
  47. Lorimer CG, Dahir SE, Singer MT (1999) Frequency of partial and missing rings in Acer saccharum in relation to canopy position and growth rate. Plant Ecol 143:189–202. doi:10.1023/A:1009847819158 CrossRefGoogle Scholar
  48. Loss SR, Hueffmeier RM, Hale CM, Host GE, Sjerven G, Frelich LE (2013) Earthworm invasions in Northern hardwood forests: a rapid assessment method. Nat Areas J 33:21–30. doi:10.3375/043.033.0103 CrossRefGoogle Scholar
  49. Mader DL, Thompson BW (1969) Foliar and soil nutrients in relation to sugar maple decline. Soil Sci Amer Proc 33:794–800. doi:10.2136/sssaj1969.03615995003300050046x CrossRefGoogle Scholar
  50. Manion PD, Lachance D (eds) (1992) Forest Decline concepts. American Phytopathological Society, St. PaulGoogle Scholar
  51. McLaughlin DL, Linxon SN, Dimma DE, McIlveen WD (1987) Sugar maple decline in Ontario. In: Hutchison TC, Meema KM (eds) Effects of atmospheric pollutants on forests, wetlands, and agricultural ecosystems. Springer, New York, pp 101–116CrossRefGoogle Scholar
  52. McTavish MJ, Basiliko N, Sackett TE (2013) Environmental factors influencing immigration behavior of the invasive earthworm Lumbricus terrestris. Can J Zool 91:859–865. doi:10.1139/cjz-2013-0153 CrossRefGoogle Scholar
  53. Michigan Department of Natural Resources and Environment, Forest Management Division, (2009) Michigan Forest Health Highlights. http://fhm.fs.fed.us/fhh/fhh_09/mi_fhh_09.pdf. Accessed 5 June 2015
  54. Michigan Department of Natural Resources and Environment, Forest Management Division, (2010) Michigan Forest Health Highlights. http://fhm.fs.fed.us/fhh/fhh_10/mi_fhh_10.pdf. Accessed 5 June 2015
  55. Michigan Department of Natural Resources, 2012. Forest Management Division, (2012) Forest Health Highlights https://www.michigan.gov/documents/dnr/ForestHH_409440_7.pdf. Accessed 5 June 2015
  56. Millers I, Lachance D. Burkman WG. Allen DC (1991). North American sugar maple decline project: organization and methods. General Technical Report NE-154. USDA, Forest Service, Northeastern Forest Experiment Station, RadnorGoogle Scholar
  57. Millers I, Shriner DS, Rizzo D (1989) History of hardwood decline in the Eastern United States. General Technical Report NE-126. USDA Forest Service, Northeastern Forest Experiment Station, BroomallGoogle Scholar
  58. Moore JD, Ouimet R, Bohlen PJ (2013) Effects of liming on survival and reproduction of two potentially invasive earthworm species in a Northern hardwood forest Podzol. Soil Biol Biochem 64:174–180. doi:10.1016/j.soilbio.2013.04.013 CrossRefGoogle Scholar
  59. Moore JD, Ouimet R, Long RP, Bukaveckas PA (2015) Ecological benefits and risks arising from liming sugar maple dominated forests in northeastern North America. Environ Rev 23:66–77. doi:10.1139/er-2014-0048 CrossRefGoogle Scholar
  60. O’Neill KP, Amacher MC, Perry CH (2005) Soils as an indicator of forest health: a guide to the collection, analysis, and interpretation of soil indicator data in the forest inventory and analysis program. General Technical Report NC-258. USDA, Forest Service, North Central Research Station, St. PaulGoogle Scholar
  61. Patterson SL, Zak DR, Burton AJ, Talhelm AF, Pregitzer KS (2012) Simulated N deposition negatively impacts sugar maple regeneration in a northern hardwood ecosystem. J App Ecol 49:155–163. doi:10.1111/j.1365-2664.2011.02090.x CrossRefGoogle Scholar
  62. Reich PB, Oleksyn J, Modryznski J, Mrozinski P, Hobbie SE, Eissesnstat DM, Chorover J, Chadwick OA, Hale CM, Tjoelker MG (2005) Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol Lett 8:811–818. doi:10.1111/j.1461-0248.2005.00779.x CrossRefGoogle Scholar
  63. Resner K, Yoo K, Sebestyen SD, Aufdenkampe A, Hale C, Blum A (2015) Invasive earthworms deplete key soil inorganic nutrients (Ca, Mg, K, and P) in a Northern hardwood forest. Ecosystems 18:89–102. doi:10.1007/s10021-014-9814-0 CrossRefGoogle Scholar
  64. Roth AM, Whitefeld TJS, Lodge AG, Eisenhauer N, Frelich LE, Reich PB (2015) Invasive earthworms interact with abiotic conditions to influence the invasion of common buckthorn (Rhamnus cathartica). Oecologia 178:219–230. doi:10.1007/s00442-014-3175-4 CrossRefPubMedGoogle Scholar
  65. Sackett TE, Smith SM, Basiliiko N (2012) Exotic earthworm distribution in a mixed-use northern temperate forest region: influence of disturbance type, development age, and soils. Can J For Res 42:375–381CrossRefGoogle Scholar
  66. Sackett TE, Smith SM, Basiliko N (2013) Indirect and direct effects of exotic earthworms on soil nutrient and carbon pools in North American temperate forests. Soil Biol Biochem 57:459–467. doi:10.1139/x11-195 CrossRefGoogle Scholar
  67. Schmiege DC, Anderson GW (1960) The forest insect and disease situation, Lake States, 1959. USDA Forest Service Station Paper No 79Google Scholar
  68. Shartell LM, Corace RG, Storer AJ (2012) Exotic earthworm communities within upland deciduous forests of national wildlife refuges in the upper Midwest. J Fish Wildl Manag 3:332–340. doi:10.3996/042012-JFWM-033 CrossRefGoogle Scholar
  69. Shartell LM, Lilleskov EA, Storer AJ (2013) Predicting exotic earthworm distribution in the northern Great Lakes Region. Biol Invasions 15:1665–1675. doi:10.1007/s10530-012-0399-2 CrossRefGoogle Scholar
  70. Silva LR, Anand M, Leithead MD (2010) Recent widespread tree growth decline despite increasing atmospheric CO2. PLoS ONE 5:e11543. doi:10.1371/journal.pone.0011543 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Soil Survey Division Staff (1993) Soil survey manual. Soil conservation service. USDA Handbook 18Google Scholar
  72. Soil Survey Staff, Natural Resources Conservation Service, United States Department of Agriculture. Soil Survey Geographic (SSURGO) database for counties in WI and MI. Available online at http://soildatamart.nrcs.usda.gov. Accessed 12 Jan 2012
  73. St. Clair S, Sharpe WE, Lynch JP (2008) Key interactions between nutrient limitation and climatic factors in temperate forests: a synthesis of the sugar maple literature. Can J For Res 38:401–414. doi:10.1139/X07-161 CrossRefGoogle Scholar
  74. Stearns FW (1997) History of the Lake States Forests: natural and human impacts. In: Vasievich JM, Webster HH (eds) Lake States regional forest resources assessment: technical papers. USDA Forest Service, North Central Forest Experiment Station, Gen-Tech-Rep NC-189. pp 8–29Google Scholar
  75. U.S. Department of Agriculture, Forest Service (1999) Forest Health Monitoring 1999 Field Methods Guide. USDA Forest Service, National Forest Health Monitoring Program, Research Triangle Park, North CarolinaGoogle Scholar
  76. Watmough SA, Brydges T, Hutchison T (1999) The tree-ring chemistry of declining sugar maple in central Ontario, Canada. Ambio 28:613–618. doi:10.2307/4314967 Google Scholar
  77. Wironen M, Moore TR (2006) Exotic earthworm invasion increases soil carbon and nitrogen in an old-growth forest in southern Quebec. Can J For Res 36:845–854. doi:10.1139/x06-016 CrossRefGoogle Scholar
  78. Zurr AF, Ieno EN, Walker NJ, Saveliey AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Tara L. Bal
    • 1
  • Andrew J. Storer
    • 1
  • Martin F. Jurgensen
    • 1
  1. 1.Ecosystem Science Center, School of Forest Resources and Environmental ScienceMichigan Technological UniversityHoughtonUSA

Personalised recommendations