Hemlock woolly adelgid (Adelges tsugae) infestation affects water and carbon relations of eastern hemlock (Tsuga canadensis) and Carolina hemlock (Tsuga caroliniana)

New Phytologist

Volumn 199, Issue 2, 2013, Pages 452-463

  Domec, Jean Christophe ^a,b   Rivera, Laura N ^b   King, John S ^b   Peszlen, Ilona ^b   Hain, Fred ^b   Smith, Benjamin ^b   Frampton, John ^b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Carbon isotope; Hydraulic conductivity; Mortality; Soil plant atmosphere model; Stomatal conductance; Traumatic resin canals; Water potential; Wood anatomy

Indexed keywords

CARBON; NITROGEN; WATER;

ANATOMY; CARBON ISOTOPE; CONIFEROUS TREE; ECOLOGICAL IMPACT; GAS EXCHANGE; HYDRAULIC CONDUCTIVITY; INSECT; INVASIVE SPECIES; MORTALITY; PARASITE INFESTATION; PEST DAMAGE; PEST SPECIES; PHYSIOLOGICAL RESPONSE; PRIMARY PRODUCTION; STOMATAL CONDUCTANCE; WATER UPTAKE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CIRCADIAN RHYTHM; HEMIPTERA; HISTOLOGY; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT STEM; PLANT STOMA; SEASON; TSUGA; WOOD; XYLEM;

ANIMALS; CARBON; CARBON ISOTOPES; CIRCADIAN RHYTHM; HEMIPTERA; MODELS, BIOLOGICAL; NITROGEN; PLANT DISEASES; PLANT LEAVES; PLANT STEMS; PLANT STOMATA; SEASONS; TSUGA; WATER; WOOD; XYLEM;

ADELGES TSUGAE; ADELGIDAE; CONIUM; HEXAPODA; TSUGA; TSUGA CANADENSIS; TSUGA CAROLINIANA;

EID: 84879694206     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12263     Document Type: Article

References (77)

1. Arthur FH, Hain FP. 1986. Water potential of Fraser fir infested with balsam woolly adelgid (Homoptera: Aldegidae). Environmental Entomology 15: 911-913.
2. Balch RE, Clark J, Bonca JM. 1964. Hormonal action in production of tumours and compression wood by an aphid. Nature 202: 721-722.
3. Barataud F, Moyne C, Bréda N, Granier A. 1995. Soil water dynamics in an oak stand. Plant and Soil 172: 29-43.
4. Bosc A, de Grandcourt A, Loustau D. 2003. Variability of stem and branch maintenance respiration in a Pinus pinaster tree. Tree Physiology 23: 227-236.
5. Breda N, Huc R, Granier A, Dreyer E. 2006. Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Annals of Forest Science 63: 625-644.
6. Broeckling CD, Salom SM. 2003. Volatile emissions of eastern hemlock, Tsuga canadensis, and the influence of hemlock woolly adelgid. Phytochemistry 62: 175-180.
7. Cochard H, Coll L, Le Roux X, Améglio T. 2002. Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiology 128: 282-290.
8. Coley PD, Bryant JP, Chapin FS III. 1985. Resource availability and plant anti-herbivore defense. Science 230: 895-899.
9. Coops NC, Ferster CJ, Waring RH, Nightingale J. 2009. Comparison of three models for predicting gross primary production across and within forested ecoregions in the contiguous United States. Remote Sensing of Environment 113: 680-690.
10. Craig H. 1957. Isotopic standards for carbon and oxygen and correlation factors for mass spectrometric analysis of carbon dioxide. Geochimica et Cosmochimica Acta 12: 133-149.
11. Daley MJ, Phillips NG, Pettijohn JC, Hadley JC. 2007. Water use by eastern hemlock (Tsuga Canadensis) and black birch (Betula lenta): implications of effects of the hemlock woolly agelgid. Canadian Journal of Forest Research 37: 2031-2040.
12. Dang QL, Margolis HA, Sy M, Coyea MR, Collatz GJ, Walthall CL. 1997. Profiles of photosynthetically active radiation, nitrogen and photosynthetic capacity in the boreal forest: implications for scaling from leaf to canopy. Journal of Geophysical Research Atmosphere 102: 28845-28859.
13. Domec J-C, King JS, Noormets A, Treasure EA, Gavazzi MJ, Sun G, McNulty SG. 2010. Hydraulic redistribution of soil water by roots affects whole stand evapotranspiration and net ecosystem carbon exchange. New Phytologist 187: 171-183.
14. Domec J-C, Noormets A, King JS, Sun G, McNulty SG, Gavazzi M, Boggs J, Treasure E. 2009a. Decoupling the influence of leaf and root hydraulic conductances on stomatal conductance and its sensitivity to vapor pressure deficit as soil dries in a drained loblolly pine plantation. Plant, Cell & Environment 32: 980-991.
15. Domec J-C, Warren JM, Meinzer FC, Lachenbruch B. 2009b. Safety factors for xylem failure by implosion and air-seeding within roots, trunks and branches of young and old conifer trees. IAWA Journal 30: 101-120.
16. Ehleringer JR. 1993. Carbon and water relations in desert plants: an isotopic perspective. In: Ehleringer JR, Hall AE, Farquhar GD, eds. Stable isotopes and plant carbon-water relations. San Diego, CA, USA: Academic Press, 155-172.
17. Evans AM, Gregoire TG. 2007. Geographically variable model of hemlock woolly adelgid spread. Biological Invasions 9: 369-382.
18. Evans JR, Seemann JR. 1989. The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences, and control. In: Briggs WR, ed. Photosynthesis. Plant biology 8. New York, NY, USA: Alan R. Liss Inc., 183-205.
19. Farquhar GD, O'Leary MH, Berry JA. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9: 121-137.
20. Field C, Mooney HA. 1986. The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ, ed. On the economy and form of plant function. Cambridge, UK: Cambridge University Press, 25-55.
21. Fitzpatrick MC, Preisser EL, Porter A, Elkinton JS, Ellison AM. 2012. Modeling range dynamics in heterogeneous landscapes: invasion of the hemlock woolly adelgid in eastern North America. Ecological Applications 22: 472-486.
22. Ford CR, Vose JM. 2007. Tsuga canadensis (L.) Carr. mortality will impact hydrological processes in southern Appalachian forest ecosystems. Ecological Applications 17: 1156-1167.
23. Gonda-King L, Radville L, Preisser E. 2012. False ring formation in eastern hemlock branches: impacts of hemlock woolly adelgid and elongate hemlock scale. Environmental Entomology 41: 523-531.
24. Guswa AJ, Spence CM. 2012. Effect of throughfall variability on recharge: application to hemlock and deciduous forests in western Massachusetts. Ecohydrology 5: 563-574.
25. Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA. 2001. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126: 457-461.
26. 2. Plant, Cell & Environment 15: 271-282.
27. Havill NP, Montgomery ME, Yu G, Shiyake S, Caccone A. 2006. Mitochondrial DNA from hemlock woolly adelgid (Hemiptera: Adelgidae) suggests cryptic speciation and pinpoints the source of the introduction to eastern North America. Annals of the Entomological Society of America 99: 195-203.
28. Hill TC, Williams M, Moncrieff JB. 2008. Modelling feedbacks between a boreal forest and the planetary boundary layer. Journal of Geophysical Research 113: D15122.
29. Hollingsworth RG, Blum U, Hain FP. 1991. The effect of adelgid-altered wood on sapwood conductance of Fraser fir Christmas trees. IAWA Bulletin New Series 12: 235-239.
30. Hollingsworth RG, Hain FP. 1991. Balsam woolly adelgid (Homoptera: Adelgidae) and spruce-fir decline in the southern Appalachians: assessing pest relevance in a damaged ecosystem. Florida Entomologist 74: 179-187.
31. Hubbard RM, Ryan MG, Stiller V, Sperry JS. 2001. Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant, Cell & Environment 24: 113-121.
32. Hudgins JW, Christiansen E, Franceschi VR. 2004. Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: a phylogenetic perspective. Tree Physiology 24: 251-264.
33. Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC. 2009. Leaf hydraulic conductance, measured in situ, declines and recovers daily: leaf hydraulics, water potential and gas exchange in four temperate and three tropical tree species. Tree Physiology 29: 879-887.
34. Kizlinski ML, Orwig DA, Cobb RC, Foster DR. 2002. Direct and indirect ecosystem consequences of an invasive pest on forests dominated by eastern hemlock. Journal of Biogeography 29: 1489-1503.
35. Kolb KJ, Sperry JS. 1999. Transport constraints on water use by the Great Basin shrub, Artemisia tridentata. Plant, Cell & Environment 22: 925-935.
36. Krapfl KJ, Holzmueller EJ, Jenkins MA. 2011. Early impacts of hemlock woolly adelgid in Tsuga canadensis forest communities of the southern Appalachian Mountains. The Journal of the Torrey Botanical Society 138: 93-106.
37. Krekling T, Franceschi VR, Berryman AA, Christiansen E. 2000. The structure and development of polyphenolic parenchyma cells in Norway spruce (Picea abies) bark. Flora 195: 354-369.
38. Krokene P, Nagy NE, Krekling T. 2008. Traumatic resin ducts and polyphenolic parenchyma cells in conifers. In: Schaller A, ed. Induced plant resistance to herbivory. Dordrecht, Netherlands: Springer, 147-169.
39. Loustau D, Domec J-C, Bosc A. 1998. Interpreting the variations in xylem sap flux density within the trunk of maritime pine (Pinus pinaster Ait.): application of a model for calculating water flows at tree and stand levels. Annales des Sciences Forestieres 55: 29-46.
40. McClure MS. 1991. Density-dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae) on Tsuga canadensis. Environmental Entomology 20: 258-264.
41. McClure MS. 1996. Biology of Adelges tsugae and its potential for spread in the northeastern United States. In: Salom SM, Tigner TC, Reardon RC, eds. Proceedings of the first hemlock woolly adelgid review. Forest Health Technology Enterprise Team 96-10. Morgantown, WV, USA: USDA Forest Service, 9-15.
42. McDowell NG. 2011. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155: 1051-1059.
43. McDowell NG, Adams HD, Bailey JD, Kolb TE. 2007. The role of stand density on growth efficiency, leaf area index and resin flow in southwestern ponderosa pine forests. Canadian Journal of Forest Research 37: 343-355.
44. McDowell NG, Allen CD, Marshall L. 2010. Growth, carbon-isotope discrimination, and drought-associated mortality across a Pinus ponderosa elevational transect. Global Change Biology 16: 399-415.
45. Meinzer FC. 2002. Co-ordination of liquid and vapor phase water transport properties in plants. Plant, Cell & Environment 25: 265-274.
46. Meinzer FC, Woodruff DR, Shaw DC. 2004. Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection. Plant, Cell & Environment 27: 937-946.
47. Niinemets U, Tenhunen JD. 1997. A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant, Cell & Environment 20: 845-866.
48. Niinemets U, Tenhunen JD. 1998. An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance. Tree Physiology 18: 681-696.
49. Nolan WG, Smillie RM. 1976. Multi-temperature effects on Hill reaction activity of barley chloroplasts. Biochimica Biophysica Acta 440: 461-475.
50. Nuckolls AE, Wurzburger N, Ford CR, Hendrick RL, Vose JM, Kloeppel BD. 2009. Hemlock declines rapidly with hemlock woolly adelgid infestation: impacts on the carbon cycle of southern Appalachian forests. Ecosystems 12: 179-190.
51. Orwig DA, Foster DR, Mausel DL. 2002. Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. Journal of Biogeography 29: 1475-1487.
52. Pataki DE, Oren R, Phillips N. 1998. Responses of sap flux and stomatal conductance of Pinus taeda L. trees to stepwise reductions in leaf area. Journal of Experimental Botany 49: 871-878.
53. Puritch GS. 1971. Water permeability of the wood of Grand fir (Abies grandis (Doug.) Lindl.) in relation to infestation by the balsam woolly aphid, Adelges piceae (Ratz.). Journal of Experimental Botany 22: 936-945.
54. Puritch GS. 1977. Distribution and phenolic composition of sapwood and heartwood in Abies grandis and the effects of the balsam woolly aphid. Canadian Journal of Forest Research 7: 54-62.
55. Radville L, Chaves A, Preisser EL. 2011. Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlocks (Tsuga canadensis). Journal of Chemical Ecology 37: 592-597.
56. Reich PB, Grigal DF, Aber JD, Gower ST. 1997b. Nitrogen mineralization and productivity in 50 hardwood and conifer stands on diverse soils. Ecology 78: 335-347.
57. Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado J-L. 2008. Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecology Letters 11: 793-801.
58. Reich PB, Walters MB, Ellsworth DS. 1997a. From tropics to tundra: global convergence in plant functioning. Proceeding of the National Academy of Sciences, USA 94: 13730-13734.
59. Reid DEB, Silins U, Lieffers VJ. 2003. Stem sapwood permeability in relation to crown dominance and site quality in self-thinning fire origin lodgepole pine stands. Tree Physiology 23: 833-840.
60. Rhea LK. 2010. Implications of elevated atmospheric carbon dioxide and tropospheric ozone for water use in stands of trembling aspen and paper birch. PhD thesis, North Carolina State University, Raleigh, NC, USA.
61. Ritchie GA, Hinckley TM. 1975. The pressure chamber as an instrument for ecological research. Advances in Ecological Research 9: 165-254.
62. Ryan MG, Gower ST, Hubbard RM, Waring RH, Gholz HL, Cropper WP, Running SW. 1995. Woody tissue maintenance respiration of four conifers in contrasting climates. Oecologia 101: 133-140.
63. Sala A, Piper F, Hoch G. 2010. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist 186: 274-281.
64. Small MJ, Small CJ, Dreyer GD. 2005. Changes in a hemlock dominated forest following woolly adelgid infestation in southern New England. Journal of the Torrey Botanical Society 132: 458-470.
65. Sperry JS, Adler FR, Campbell GS, Comstock JP. 1998. Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant, Cell & Environment 21: 347-359.
66. Spicer R, Gartner BL. 1998. Hydraulic properties of Douglas-fir branches and branch halves with reference to compression wood. Tree Physiology 18: 777-784.
67. Tyree MT, Sinclair B, Lu P, Granier A. 1993. Whole shoot hydraulic resistance in Quercus species measured with a new high pressure flowmeter. Annales des Sciences Forestieres 50: 417-423.
68. Vose JM, Swank WT. 1994. Effects of long-term drought on the hydrology and growth of a white pine plantation in the southern Appalachians. Forest Ecology and Management 64: 25-39.
69. Waring RH, Landsberg JJ, Williams M. 1998. Net primary production of forests: a constant fraction of gross primary production? Tree Physiology 18: 129-134.
70. Waring RH, Pitman GB. 1985. Modifying lodgepole pine stands to change susceptibility to mountain pine-beetle attack. Ecology 66: 889-897.
71. Waring RH, Running S. 1998. Forest ecosystems, analysis at multiple scales. San Diego, CA, USA: Academic Press.
72. Williams M, Bond BJ, Ryan MG. 2001. Evaluating different soil and plant hydraulic constraints on tree function using a model and sap flow data from ponderosa pine. Plant, Cell & Environment 24: 679-690.
73. Williams M, Rastetter EB, Fernandes DN, Goulden ML, Wofsy SC, Shaver GR, Melillo JM, Munger JW, Fan S-M, Nadelhoffer KJ. 1996. Modelling the soil-plant-atmosphere continuum in a Quercus-Acer stand at Harvard Forest: the regulation of stomatal conductance by light, nitrogen and soil/plant hydraulic properties. Plant, Cell & Environment 19: 911-927.
74. Woodruff DR, McCulloh KA, Warren JM, Meinzer FC, Lachenbruch B. 2007. Impacts of tree height on leaf hydraulic architecture and stomatal control in Douglas-fir. Plant, Cell & Environment 30: 559-569.
75. Xiao J, Zhuang Q, Baldocchi DD, Law BE, Richardson AD, Chen J, Oren R, Starr G, Noormets A, Ma S et al. 2010. A continuous measure of gross primary production for the conterminous United States derived from MODIS and AmeriFlux data. Remote Sensing of Environment 114: 576-591.
76. Young RF, Shields KS, Berlyn GP. 1995. Hemlock woolly adelgid (Homoptera: Adelgidae): stylet bundle insertion and feeding sites. Annals of the Entomological Society of America 88: 827-835.
77. Zhang JW, Feng Z, Cregg BM, Schumann CM. 1997. Carbon isotopic composition, gas exchange, and growth of three populations of ponderosa pine differing in drought tolerance. Tree Physiology 17: 461-466.