False ring formation in eastern hemlock branches: Impacts of hemlock woolly adelgid and elongate hemlock scale

Environmental Entomology

Volumn 41, Issue 3, 2012, Pages 523-531

  Liahna, Gonda King ^a   Radville, Laura ^a   Preisser, Evan L ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

Adelges tsugae; false rings; Fiorinia externa; herbivory; Tsuga canadensis

Indexed keywords

DECIDUOUS TREE; EXPERIMENTAL STUDY; FEEDING; FOREST HEALTH; GROWTH; HERBIVORY; INSECT; INVASIVE SPECIES; PEST SPECIES; PHYSIOLOGY; PLANT-HERBIVORE INTERACTION; TREE RING; WATER STRESS; WOOD;

ANIMAL; ARTICLE; FOOD CHAIN; GROWTH, DEVELOPMENT AND AGING; HEMIPTERA; HERBIVORY; INTRODUCED SPECIES; PHYSIOLOGY; SPECIES DIFFERENCE; TREE; TSUGA; UNITED STATES;

ANIMALS; FOOD CHAIN; HEMIPTERA; HERBIVORY; INTRODUCED SPECIES; MASSACHUSETTS; SPECIES SPECIFICITY; TREES; TSUGA;

EID: 84862508857     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN11227     Document Type: Article

References (104)

1. Abell, K. 2010. Population dynamics and biological control of elongate hemlock scale, Fiorinia externa. Ph.D. dissertation,University of Massachusetts-Amherst, Amherst.
2. Abràmoff, M. D., P. J. Magalhães, and S. J. Ram. 2004. Image processing with ImageJ. Biophotonics Int. 11: 36-42.
3. Arthur, F., and F. Hain. 1985. Development of wound tissue in the bark of fraser +r and its relation to injury by the balsam woolly adelgid. J. Entomol. Sci. 20: 129-135.
4. Arthur, F., and F. Hain. 1986. Water potential of Fraser +r infested with balsam woolly adelgid (Homoptera: Adelgidae). Environ. Entomol. 15: 911-913.
5. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate-A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57: 289-300.
6. Bezemer, T. M., R. Wagenaar, N. M. Van Dam, and F. L. Wackers. 2003. Interactions between above-and belowground insect herbivores as mediated by the plant defense system. Oikos 101: 555-562. (Pubitemid 36599476)
7. Bi, J., and G. Felton. 1995. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J. Chem. Ecol. 21: 1511-1530. (Pubitemid 3018121)
8. Bolton, A. J., and J. A. Petty. 1978. Model describing axialßow of liquids through conifer wood. Wood Sci. Technol. 12: 37-48.
9. Bonello, P., T. R. Gordon, D. A. Herms, D. L. Wood, and N. Erbilgin. 2006. Nature and ecological implications of pathogen-induced systemic resistance in conifers: a novel hypothesis. Physiol. Mol. Plant P. 68: 95-104. (Pubitemid 46274153)
10. Butin, E., E. Preisser, and J. Elkinton. 2007. Factors affecting settlement rate of the hemlock woolly adelgid, Adelges tsugae, on eastern hemlock, Tsuga canadensis. Agric. For. Entomol. 9: 215-219. (Pubitemid 47074992)
11. Cherubini, P., B. L. Gartner, R. Tognetti, O. U. Braker, W. Schoch, and J. L. Innes. 2003. Identi+cation, measurement and interpretation of tree rings in woody species from mediterranean climates. Biol. Rev. 78: 119-148. (Pubitemid 36253948)
12. Copenheaver, C. A., E. A. Pokorski, J. E. Currie, and M. D. Abrams. 2006. Causation of false ring formation in Pinus banksiana: a comparison of age, canopy class, climate and growth rate. For. Ecol. Manag. 236: 348-355. (Pubitemid 44803100)
13. Cornelissen, T., D. Negreiros, and G. Fernandes. 2002. Plant resistance against gall-forming insects: the role of hypersensitivity. In M. Wagner, K. Clancy, F. Lieutier and T. Paine (eds.), Mechanisms and deployment of resistance in trees to insects. Kluwer Academic, Boston, MA. 137-152.
14. Fernandes, G. W. 1990. Hypersensitivity: a neglected plantresistance mechanism against insect herbivores. Environ. Entomol. 19: 1173-1182.
15. Gómez, S., C. Orians, and E. Preisser. 2012. Exotic herbivores on a shared native host: tissue quality after individual, simultaneous, and sequential attack. Oecologia DOI: 10.1007/s00442-00012-02267-00442.
16. Heath, M. C. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44: 321-334. (Pubitemid 32143033)
17. Heijari, J., A. M. Nerg, J. K. Holopainen, and P. Kainulainen. 2010. Woodborer performance and wood characteristics of drought-stressed Scots pine seedlings. Entomol. Exp. Appl. 137: 105-110.
18. Hoffer, M., and J. C. Tardif. 2009. False rings in jack pine and black spruce trees from eastern Manitoba as indicators of dry summers. Can. J. For. Res./Rev. Can. Rech. For. 39: 1722-1736.
19. Hollingsworth, R., and F. Hain. 1991. Balsam woolly adelgid (Homoptera: Adelgidae) and spruce-+r decline in the southern Appalachians: assessing pest relevance in a damaged ecosystem. Fla. Entomol. 74: 179-187.
20. Hollingsworth, R., and F. Hain. 1992. Balsam woolly adelgid(Homoptera: Adelgidae) effects on wood and bark structure of Fraser +r and silver +r. Environ. Entomol. 21: 1103-1109.
21. Kaplan, I., R. Halitschke, A. Kessler, S. Sardanelli, and R. F. Denno. 2008. Effects of plant vascular architecture on aboveground-belowground-induced responses to foliar and root herbivores on Nicotiana tabacum. J. Chem. Ecol. 34: 1349-1359.
22. Karban, R., and I. T. Baldwin. 1997. Induced response to herbivory. University of Chicago Press, Chicago, IL.
23. Levin, D. A. 1973. Role of trichomes in plant defense. Q. Rev. Biol. 48: 3-15.
24. Liu, X., C. E. Williams, J. A. Nemacheck, H. Wang, S. Subramanyam, C. Zheng, and M. S. Chen. 2010. Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiol. 152: 985-999.
25. McClure, M. 1978. Seasonal development of Fiorinia externa, Tsugaspidiotus tsugae (Homoptera: Diaspididae), and their parasite, Aspidiotiphagus citrinus (Hymenoptera: Aphelinidae): importance of parasite-host synchronism to the population dynamics of two scale pests of hemlock. Environ. Entomol. 7: 863-870.
26. McClure, M. 1980. Competition between exotic species: scale insects on hemlock. Ecology 61: 1391-1401.
27. McClure, M. 1988. The armored scales of hemlock, pp. 45-65. In A. Berryman (ed.), Dynamics of forest insect populations: patterns, causes, implications. Plenum, New York.
28. McClure, M. 1989. Evidence of a polymorphic life cycle in the hemlock woolly adelgid Adelges tsugae (Homoptera: Adelgidae). Ann. Entomol. Soc. Am. 82: 50-54.
29. McClure, M. 1991. Density-dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae) on Tsuga canadensis. Environ. Entomol. 20: 258-264.
30. McClure, M., and C. Cheah. 1999. Reshaping the ecology of invading populations of hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae), in Eastern North America. Biol. Invasions 1: 241-254.
31. Miller-Pierce, M., D. Orwig, and E. Preisser. 2010. Effects of hemlock woolly adelgid and elongate hemlock scale on eastern hemlock growth and foliar chemistry. Environ. Entomol. 39: 513-519.
32. Mitchell, R. 1967. Translocation of dye in grand and subalpine +rs infested by the balsam woolly aphid. Paci+c Northwest Forest Range Experimental Station, Portland, OR.
33. NOAA. National Oceanic and Atmostpheric Administration. 2011. Weather observation station data records.(http://www4.ncdc.noaa.gov/cgi-win/wwcgi.dll? wwDI StnSrch StnID 20017291).
34. Ollerstam, O., and S. Larsson. 2003. Salicylic acid mediates resistance in the willow Salix viminalis against the gall midge Dasineura marginemtorquens. J. Chem. Ecol. 29: 163-174. (Pubitemid 36204930)
35. Orwig, D., D. Foster, and D. Mausel. 2002. Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. J. Biogeogr. 29: 1475-1488.
36. Preisser, E. L., and J. S. Elkinton. 2008. Exploitative competition between invasive herbivores bene+ts a native host plant. Ecology 89: 2671-2677.
37. Preisser, E. L., A. G. Lodge, D. A. Orwig, and J. S. Elkinton. 2008. Range expansion and population dynamics of co-occurring invasive herbivores. Biol. Invasions 10: 201-213.
38. Preisser, E. L., M. R. Miller-Pierce, J. Vansant, and D. A. Orwig. 2011. Eastern hemlock (Tsuga canadensis) regeneration in the presence of hemlock woolly adelgid (Adelges tsugae) and elongate hemlock scale (Fiorinia externa). Can. J. For. Res./Rev. Can. Rech. For. 41: 2433-2439.
39. Priya, P. B., and K. M. Bhat. 1997. Woodanatomical changes in juvenile teak due to insect defoliation. International Association of Wood Anatomists 18: 311-317. (Pubitemid 27441847)
40. Puritch, G. S. 1971. Water permeability of the wood of grand +r (Abies grandis (Doug.) Lindl.) in relation to infestation by the balsam woolly aphid, Adelges piceae (Ratz.). J. Exp. Bot. 23: 936-945.
41. Radville, L., A. Chaves, and E. L. Preisser. 2011. Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlock (Tsuga canadensis). J. Chem. Ecol. 37: 592-597.
42. Sakai, A. K., F. W. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, S. Baughman, R. J. Cabin, J. E. Cohen, N. C. Ellstrand, et al. 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32: 305-332. (Pubitemid 34043164)
43. SAS Institute. 2010. JMP userÕs guide computer program, version 9.0. SAS Institute, Cary, NC.
44. Sopow, S. L., J. D. Shorthouse, W. Strong, and D. T. Quiring. 2003. Evidence for long-distance, chemical gall inductionby an insect. Ecol. Lett. 6: 102-105. (Pubitemid 36463397)
45. Souto, D., T. Luther, and B. Chianese. 1996. Past and current status of hemlock woolly adelgid in eastern and Carolina hemlock stands, pp. 9-15. In S. Salom, T. Tignor, and R. Reardon (eds.), First hemlock woolly adelgid review, 1996, Morgantown, WV. United States Forest Service.
46. Spicer, R., and B. L. Gartner. 1998. Hydraulic properties of Douglas-+r (Pseudotsuga menziesii) branches and branch halves with reference to compression wood. Tree Physiol. 18: 777-784. (Pubitemid 28532086)
47. Traw, M. B., and T. E. Dawson. 2002. Differential induction f trichomes by three herbivores of black mustard. Oecologia 131: 526-532. (Pubitemid 36080232)
48. USFS]. United States Forest Service. 2008. Hemlock woolly adelgid distribution map. Forest Health Protection Service, Newtown Square, PA.
49. Walker-Lane, L. 2009. The effect of hemlock woolly adelgid infestation on water relations of Carolina and eastern hemlock. M.S. thesis., NC State University Raleigh NC.
50. Wimmer, R., G. Strumia, and F. Holawe. 2000. Use of false rings in Austrian pine to reconstruct early growing season precipitation. Can. J. For. Res./Rev. Can. Rech. For. 30: 1691-1697. (Pubitemid 32045054)
51. Wong, B. L., and A. A. Berryman. 1977. Host resistance to the +r engraver beetle. 3. Lesion development and containment of infection by resistant Abes grandis inoculated with Trichosporium symbiotcum. Can. J. Bot. 55: 2358-2365.
52. Young, R., K. Shields, and G. Berlyn. 1995. Hemlock woolly adelgid (Homoptera: Adelgidae): stylet bundle insertion and feeding sites. Ann. Entomol. Soc. Am. 88: 827-835.
53. Abell, K. 2010. Population dynamics and biological control of elongate hemlock scale, Fiorinia externa. Ph.D. dissertation,University of Massachusetts-Amherst, Amherst.
54. Abràmoff, M. D., P. J. Magalhães, and S. J. Ram. 2004. Image processing with ImageJ. Biophotonics Int. 11: 36-42.
55. Arthur, F., and F. Hain. 1985. Development of wound tissue in the bark of fraser +r and its relation to injury by the balsam woolly adelgid. J. Entomol. Sci. 20: 129-135.
56. Arthur, F., and F. Hain. 1986. Water potential of Fraser +r infested with balsam woolly adelgid (Homoptera: Adelgidae). Environ. Entomol. 15: 911-913.
57. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate-A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57: 289-300.
58. Bezemer, T. M., R. Wagenaar, N. M. Van Dam, and F. L. Wackers. 2003. Interactions between above-and belowground insect herbivores as mediated by the plant defense system. Oikos 101: 555-562. (Pubitemid 36599476)
59. Bi, J., and G. Felton. 1995. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J. Chem. Ecol. 21: 1511-1530. (Pubitemid 3018121)
60. Bolton, A. J., and J. A. Petty. 1978. Model describing axialßow of liquids through conifer wood. Wood Sci. Technol. 12: 37-48.
61. Bonello, P., T. R. Gordon, D. A. Herms, D. L. Wood, and N. Erbilgin. 2006. Nature and ecological implications of pathogen-induced systemic resistance in conifers: a novel hypothesis. Physiol. Mol. Plant P. 68: 95-104. (Pubitemid 46274153)
62. Butin, E., E. Preisser, and J. Elkinton. 2007. Factors affecting settlement rate of the hemlock woolly adelgid, Adelges tsugae, on eastern hemlock, Tsuga canadensis. Agric. For. Entomol. 9: 215-219. (Pubitemid 47074992)
63. Cherubini, P., B. L. Gartner, R. Tognetti, O. U. Braker, W. Schoch, and J. L. Innes. 2003. Identi+cation, measurement and interpretation of tree rings in woody species from mediterranean climates. Biol. Rev. 78: 119-148. (Pubitemid 36253948)
64. Copenheaver, C. A., E. A. Pokorski, J. E. Currie, and M. D. Abrams. 2006. Causation of false ring formation in Pinus banksiana: a comparison of age, canopy class, climate and growth rate. For. Ecol. Manag. 236: 348-355. (Pubitemid 44803100)
65. Cornelissen, T., D. Negreiros, and G. Fernandes. 2002. Plant resistance against gall-forming insects: the role of hypersensitivity. In M. Wagner, K. Clancy, F. Lieutier and T. Paine (eds.), Mechanisms and deployment of resistance in trees to insects. Kluwer Academic, Boston, MA. 137-152.
66. Fernandes, G. W. 1990. Hypersensitivity: a neglected plantresistance mechanism against insect herbivores. Environ. Entomol. 19: 1173-1182.
67. Gómez, S., C. Orians, and E. Preisser. 2012. Exotic herbivores on a shared native host: tissue quality after individual, simultaneous, and sequential attack. Oecologia DOI: 10.1007/s00442-00012-02267-00442.
68. Heath, M. C. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44: 321-334. (Pubitemid 32143033)
69. Heijari, J., A. M. Nerg, J. K. Holopainen, and P. Kainulainen. 2010. Woodborer performance and wood characteristics of drought-stressed Scots pine seedlings. Entomol. Exp. Appl. 137: 105-110.
70. Hoffer, M., and J. C. Tardif. 2009. False rings in jack pine and black spruce trees from eastern Manitoba as indicators of dry summers. Can. J. For. Res./Rev. Can. Rech. For. 39: 1722-1736.
71. Hollingsworth, R., and F. Hain. 1991. Balsam woolly adelgid (Homoptera: Adelgidae) and spruce-+r decline in the southern Appalachians: assessing pest relevance in a damaged ecosystem. Fla. Entomol. 74: 179-187.
72. Hollingsworth, R., and F. Hain. 1992. Balsam woolly adelgid(Homoptera: Adelgidae) effects on wood and bark structure of Fraser +r and silver +r. Environ. Entomol. 21: 1103-1109.
73. Kaplan, I., R. Halitschke, A. Kessler, S. Sardanelli, and R. F. Denno. 2008. Effects of plant vascular architecture on aboveground-belowground-induced responses to foliar and root herbivores on Nicotiana tabacum. J. Chem. Ecol. 34: 1349-1359.
74. Karban, R., and I. T. Baldwin. 1997. Induced response to herbivory. University of Chicago Press, Chicago, IL.
75. Levin, D. A. 1973. Role of trichomes in plant defense. Q. Rev. Biol. 48: 3-15.
76. Liu, X., C. E. Williams, J. A. Nemacheck, H. Wang, S. Subramanyam, C. Zheng, and M. S. Chen. 2010. Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiol. 152: 985-999.
77. McClure, M. 1978. Seasonal development of Fiorinia externa, Tsugaspidiotus tsugae (Homoptera: Diaspididae), and their parasite, Aspidiotiphagus citrinus (Hymenoptera: Aphelinidae): importance of parasite-host synchronism to the population dynamics of two scale pests of hemlock. Environ. Entomol. 7: 863-870.
78. McClure, M. 1980. Competition between exotic species: scale insects on hemlock. Ecology 61: 1391-1401.
79. McClure, M. 1988. The armored scales of hemlock, pp. 45-65. In A. Berryman (ed.), Dynamics of forest insect populations: patterns, causes, implications. Plenum, New York.
80. McClure, M. 1989. Evidence of a polymorphic life cycle in the hemlock woolly adelgid Adelges tsugae (Homoptera: Adelgidae). Ann. Entomol. Soc. Am. 82: 50-54.
81. McClure, M. 1991. Density-dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae) on Tsuga canadensis. Environ. Entomol. 20: 258-264.
82. McClure, M., and C. Cheah. 1999. Reshaping the ecology of invading populations of hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae), in Eastern North America. Biol. Invasions 1: 241-254.
83. Miller-Pierce, M., D. Orwig, and E. Preisser. 2010. Effects of hemlock woolly adelgid and elongate hemlock scale on eastern hemlock growth and foliar chemistry. Environ. Entomol. 39: 513-519.
84. Mitchell, R. 1967. Translocation of dye in grand and subalpine +rs infested by the balsam woolly aphid. Paci+c Northwest Forest Range Experimental Station, Portland, OR.
85. NOAA. National Oceanic and Atmostpheric Administration. 2011. Weather observation station data records.(http://www4.ncdc.noaa.gov/cgi-win/wwcgi.dll? wwDI StnSrch StnID 20017291).
86. Ollerstam, O., and S. Larsson. 2003. Salicylic acid mediates resistance in the willow Salix viminalis against the gall midge Dasineura marginemtorquens. J. Chem. Ecol. 29: 163-174. (Pubitemid 36204930)
87. Orwig, D., D. Foster, and D. Mausel. 2002. Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. J. Biogeogr. 29: 1475-1488.
88. Preisser, E. L., and J. S. Elkinton. 2008. Exploitative competition between invasive herbivores bene+ts a native host plant. Ecology 89: 2671-2677.
89. Preisser, E. L., A. G. Lodge, D. A. Orwig, and J. S. Elkinton. 2008. Range expansion and population dynamics of co-occurring invasive herbivores. Biol. Invasions 10: 201-213.
90. Preisser, E. L., M. R. Miller-Pierce, J. Vansant, and D. A. Orwig. 2011. Eastern hemlock (Tsuga canadensis) regeneration in the presence of hemlock woolly adelgid (Adelges tsugae) and elongate hemlock scale (Fiorinia externa). Can. J. For. Res./Rev. Can. Rech. For. 41: 2433-2439.
91. Priya, P. B., and K. M. Bhat. 1997. Woodanatomical changes in juvenile teak due to insect defoliation. International Association of Wood Anatomists 18: 311-317. (Pubitemid 27441847)
92. Puritch, G. S. 1971. Water permeability of the wood of grand +r (Abies grandis (Doug.) Lindl.) in relation to infestation by the balsam woolly aphid, Adelges piceae (Ratz.). J. Exp. Bot. 23: 936-945.
93. Radville, L., A. Chaves, and E. L. Preisser. 2011. Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlock (Tsuga canadensis). J. Chem. Ecol. 37: 592-597.
94. Sakai, A. K., F. W. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, S. Baughman, R. J. Cabin, J. E. Cohen, N. C. Ellstrand, et al. 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32: 305-332. (Pubitemid 34043164)
95. SAS Institute. 2010. JMP userÕs guide computer program, version 9.0. SAS Institute, Cary, NC.
96. Sopow, S. L., J. D. Shorthouse, W. Strong, and D. T. Quiring. 2003. Evidence for long-distance, chemical gall inductionby an insect. Ecol. Lett. 6: 102-105. (Pubitemid 36463397)
97. Souto, D., T. Luther, and B. Chianese. 1996. Past and current status of hemlock woolly adelgid in eastern and Carolina hemlock stands, pp. 9-15. In S. Salom, T. Tignor, and R. Reardon (eds.), First hemlock woolly adelgid review, 1996, Morgantown, WV. United States Forest Service.
98. Spicer, R., and B. L. Gartner. 1998. Hydraulic properties of Douglas-+r (Pseudotsuga menziesii) branches and branch halves with reference to compression wood. Tree Physiol. 18: 777-784. (Pubitemid 28532086)
99. Traw, M. B., and T. E. Dawson. 2002. Differential induction f trichomes by three herbivores of black mustard. Oecologia 131: 526-532. (Pubitemid 36080232)
100. USFS]. United States Forest Service. 2008. Hemlock woolly adelgid distribution map. Forest Health Protection Service, Newtown Square, PA.
101. Walker-Lane, L. 2009. The effect of hemlock woolly adelgid infestation on water relations of Carolina and eastern hemlock. M.S. thesis., NC State University Raleigh NC.
102. Wimmer, R., G. Strumia, and F. Holawe. 2000. Use of false rings in Austrian pine to reconstruct early growing season precipitation. Can. J. For. Res./Rev. Can. Rech. For. 30: 1691-1697. (Pubitemid 32045054)
103. Wong, B. L., and A. A. Berryman. 1977. Host resistance to the +r engraver beetle. 3. Lesion development and containment of infection by resistant Abes grandis inoculated with Trichosporium symbiotcum. Can. J. Bot. 55: 2358-2365.
104. Young, R., K. Shields, and G. Berlyn. 1995. Hemlock woolly adelgid (Homoptera: Adelgidae): stylet bundle insertion and feeding sites. Ann. Entomol. Soc. Am. 88: 827-835.