Impacts of dwarf mistletoe on the physiology of host Tsuga heterophylla trees as recorded in tree-ring C and O stable isotopes

Tree Physiology

Volumn 34, Issue 6, 2014, Pages 595-607

  Marias, Danielle E ^a   Meinzer, Frederick C ^b   Woodruff, David R ^b   Shaw, David C ^a   Voelker, Steven L ^c   Brooks, J Renée ^d   Lachenbruch, Barbara ^a   Falk, Kristen ^a   McKay, Jennifer ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b PACIFIC NORTHWEST RESEARCH STATION   (United States)

^c SOUTHERN OREGON UNIVERSITY   (United States)

^d U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Effective path length; Mesophyll conductance

Indexed keywords

BASAL AREA; CARBON ISOTOPE; CONIFEROUS TREE; GAS EXCHANGE; GROWTH RESPONSE; HOST-PARASITE INTERACTION; ISOTOPIC RATIO; OXYGEN ISOTOPE; PARASITIC PLANT; PHYSIOLOGICAL RESPONSE; PLANT WATER RELATIONS; STABLE ISOTOPE; STOMATAL CONDUCTANCE;

CARBON; OXYGEN; WATER;

EVAPOTRANSPIRATION; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; MESOPHYLL CELL; METABOLISM; PARASITOLOGY; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT STEM; TREE; TSUGA; UNITED STATES; VISCACEAE;

CARBON; CARBON ISOTOPES; HOST-PARASITE INTERACTIONS; MESOPHYLL CELLS; OXYGEN; OXYGEN ISOTOPES; PHOTOSYNTHESIS; PLANT DISEASES; PLANT LEAVES; PLANT STEMS; PLANT TRANSPIRATION; TREES; TSUGA; VISCACEAE; WASHINGTON; WATER;

EID: 84904335544     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tpu046     Document Type: Article

References (73)

1. Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Funct Plant Biol 34: 83-94.
2. Barbour MM, Farquhar GD (2000) Relative humidity-And ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves. Plant Cell Environ 23: 473-485.
3. Barbour MM, Walcroft AS, Farquhar GD (2002) Seasonal variation in δ 13C and δ 18O of cellulose from growth rings of Pinus radiata. Plant Cell Environ 25: 1483-1499.
4. Barnard HR, Brooks JR, Bond BJ (2012) Applying the dual-isotope conceptual model to interpret physiological trends under uncontrolled conditions. Tree Physiol 32: 1183-1198.
5. Bell TL, Adams MA (2011) Attack on all fronts: functional relationships between aerial and root parasitic plants and their woody hosts and consequences for ecosystems. Tree Physiol 31: 3-15.
6. Bickford CP, Kolb TE, Geils BW (2005) Host physiological condition regulates parasitic plant performance: Arceuthobium vaginatum subsp. cryptopodum on Pinus ponderosa. Oecologia 146: 179-189.
7. Brooks JR, Coulombe R (2009) Physiological responses to fertilization recorded in tree-rings: isotopic lessons from a long-Term fertilization trial. Ecol Appl 19: 1044-1060.
8. Brooks JR, Mitchell AK (2011) Interpreting tree responses to thinning and fertilization using tree-ring stable isotopes. New Phytol 190: 770-782.
9. Brooks JR, Meinzer FC, Warren JM, Domec JC, Coulombe R (2006) Hydraulic redistribution in a Douglas-fir forest: lessons from system manipulations. Plant Cell Environ 29: 138-150.
10. Cernusak LA, Pate JS, Farquhar GD (2004) Oxygen and carbon isotope composition of parasitic plants and their hosts in southwestern Australia. Oecologia 139: 199-213.
11. Cernusak LA, Ubierna N, Winter K, Holtum JAM, Marshall JD, Farquhar GD (2013) Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytol 200: 950-965.
12. Chhikara A, Ross Friedman CM (2008) The effects of male and female Arceuthobium americanum (lodgepole pine dwarf mistletoe) infection on the relative positioning of vascular bundles, starch distribution, and starch content in Pinus contorta var. latifolia (lodgepole pine) needles. Botany 86: 539-543.
13. Cook ER (1985) A time series approach to tree-ring standardization. Ph.D. dissertation, University of Arizona, Tucson AZ, 171 p.
14. Cook ER, Holmes RL (1986) User's manual for 0orogram ARSTAN. Laboratory of Tree-Ring Research, University of Arizona, Tucson, AZ.
15. Craig H, Gordon LI (1965) Deuterium and oxygen-18 variation in the ocean and the marine atmosphere. In: Tongiorgi E (ed) Proceedings of a conference on stable isotopes in oceanographic studies and paleotemperatures. Spoleto, Italy, pp 9-130.
16. Cuntz M, Ogee J, Farquhar GD, Peylin P, Cernusak LA (2007) Modelling advection and diffusion of water isotopologues in leaves. Plant Cell Environ 30: 892-909.
17. Dongmann G, Nurnberg HW, Forstel H, Wagener K (1974) On the enrichment of H218O in the leaves of transpiring plants. Radiat Environ Biophys 11: 41-52.
18. Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon-water relations. Academic Press, San Diego, pp 47-70.
19. Farquhar GD, O'Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9: 121-137.
20. Farquhar GD, Hubick KT, Condon AG, Richards RA (1989a) Carbon isotope fractionation and plant water-use efficiency. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research. Springer, Berlin, pp 21-40.
21. Farquhar GD, Ehleringer JR, Hubick KT (1989b) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40: 503-537.
22. 2. Plant Cell Environ 35: 611-625.
23. Flanagan LB, Marshall JD, Ehleringer JR (1993) Photosynthetic gas exchange and the stable isotope composition of leaf water: comparison of a xylem-Tapping mistletoe and its host. Plant Cell Environ 16: 623-631.
24. 2: current knowledge and future prospects. Plant Cell Environ 31: 602-621.
25. 2: An unappreciated central player in photosynthesis. Plant Sci 193-194: 70-84.
26. Geils BW, Collazo IV (2002) Loranthaceae and Viscaceae in North America. In: Geils BW, Tovar JC, Moody B (eds) Mistletoes of North American Conifers. General Technical Report RMRS GTR-98. USDA Forest Service, pp 1-5.
27. Haavik LJ, Stephen FM, Fierke MK, Salisbury VB, Leavitt SW, Billings SA (2007) Dendrochronological parameters of northern red oak infested with red oak borer. For Ecol Manag 255: 1501-1509.
28. Hawksworth, FG, Wiens D (1996) Dwarf mistletoes: biology, pathology and systematics. Agriculture Handbook 709. USDA Forest Service, Washington, DC, 410 p.
29. Helliker BR, Richter SL (2008) Subtropical to boreal convergence of tree-leaf temperatures. Nature 454: 511-514.
30. Hennon PE, Beatty JS, Hildebrand D (2001) Hemlock dwarf mistletoe. Forest Insect and Disease Leaflet 135. USDA Forest Service, Forest Health Protection, Pacific Northwest Region, Portland, OR, USA.
31. Holmes RL (1983) Computer-Assisted quality control in tree-ring dating and measurement. Tree Ring Bull 43: 69-78.
32. Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24: 113-121.
33. Hull RJ, Leonard OA (1964) Physiological aspects of parasitism in mistletoes (Arceuthobium and Phoradendron). I. The carbohydrate nutrition of mistletoe. Plant Physiol 39: 996-1007.
34. Kahmen A, Simonin K, Tu KP, Merchant A, Callister A, Siegwolf R, Dawson TE, Arndt SK (2008) Effects of environmental parameters, leaf physiological properties and leaf water relations on leaf water δ18O enrichment in different Eucalyptus species. Plant Cell Environ 31: 738-751.
35. Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology. Springer, New York, USA.
36. Leavitt SW, Danzer SR (1993) Methods for batch processing small wood samples to holocellulose for stable-carbon isotope analysis. Anal Chem 65: 87-89.
37. Leavitt SW, Long A (1982) Evidence for 13C/12C fractionation between tree leaves and wood. Nature 298: 742-744.
38. Logan BA, Huhn ER, Tissue DT (2002) Photosynthetic characteristics of eastern dwarf mistletoe (Arceuthobium pusillum Peck) and its effects on the needles of host white spruce (Picea glauca [Moench] Voss). Plant Biol 4: 740-745.
39. Logan BA, Reblin JS, Zonana DS et al. (2012) Impact of eastern dwarf mistletoe (Arceuthobium pusillum) on host white spruce (Picea glauca) development, growth and performance across multiple scales. Physiol Plant 147: 502-513.
40. Marshall JD, Dawson TE, Ehleringer JR (1994a) Integrated nitrogen, carbon, and water relations of a xylem-Tapping mistletoe following nitrogen fertilization of the host. Oecologia 100: 430-438.
41. Marshall JD, Ehleringer JR, Schulze ED, Farquhar G (1994b) Carbon isotope composition, gas exchange and heterotrophy in Australian mistletoes. Funct Ecol 8: 237-241.
42. Martin TA, Hinckley TM, Meinzer FC, Sprugel DG (1999) Boundary layer conductance, leaf temperature and transpiration of Abies amabilis branches. Tree Physiol 19: 435-443.
43. McCarroll D, Loader NJ (2004) Stable isotopes in tree-rings. Quarternary Sci Rev 23: 771-801.
44. McDowell NG, Bond BJ, Hill LT, Ryan MG, Whitehead D (2011) Relationships between tree height and carbon isotope discrimination. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size-And age-related changes in tree structure and function. Springer, Dordrecht.
45. 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 Environ 27: 937-946.
46. Paw UKT, Gao W (1988) Applications of solutions to non-linear energy budget equations. Agric For Meteorol 43: 121-145.
47. Reblin JS, Logan BA, Tissue DT (2006) Impact of eastern dwarf mistletoe (Arceuthobium pusillum) infection on the needles of red spruce (Picea rubens) and white spruce (Picea glauca): oxygen exchange, morphology and composition. Tree Physiol 26: 1325-1332.
48. Roden JS, Ehleringer JR (2007) Summer precipitation influences the stable oxygen and carbon isotopic composition of tree-ring cellulose in Pinus ponderosa. Tree Physiol 27: 491-501.
49. Roden JS, Farquhar GD (2012) A controlled test of the dual-isotope approach for the interpretation of stable carbon and oxygen isotope ratio variation in tree-rings. Tree Physiol 4: 490-503.
50. Roden JS, Siegwolf R (2012) Is the dual-isotope conceptual model fully operational? Tree Physiol 32: 1179-1182.
51. Roden JS, Lin G, Ehleringer JR (2000) A mechanistic model for interpretation of hydrogen and oxygen isotope ratios in tree-ring cellulose. Geochim Cosmochim Acta 64: 21-35.
52. Sala A, Carey EV, Callaway RM (2001) Dwarf mistletoe affects whole-Tree water relations of Douglas fir and western larch primarily through changes in leaf to sapwood ratios. Oecologia 126: 42-52.
53. Sangüesa-Barreda G, Linares JC, Camarero JJ (2013) Drought and mistletoe reduce growth and water-use efficiency of Scots pine. For Ecol Manag 296: 64-73.
54. Santiago LS, Goldstein G, Meinzer FC, Fisher JB, Machado K, Woodruff D, Jones T (2004) Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140: 543-550.
55. 18O in cellulose of trees. Plant Cell Environ 20: 1543-1550.
56. Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon stable isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125: 350-357.
57. Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155: 441-454.
58. Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30: 1035-1040.
59. Shaw DC, Weiss SB (2000) Canopy light and the distribution of hemlock dwarf mistletoe aerial shoots in an old-growth Douglas-fir/western hemlock forest. Northwest Sci 74: 306-315.
60. Shaw DC, Watson DM, Mathiasen RL (2004) Comparison of dwarf mistletoes (Arceuthobium spp., Viscaceae) in the western United States with mistletoes (Amyema spp., Loranthaceae) in Australia -ecological analogs and reciprocal models for ecosystem management. Aust J Bot 52: 481-498.
61. Shaw DC, Chen J, Freeman EA, Braun DM (2005) Spatial and population characteristics of dwarf mistletoe infected trees in an old-growth Douglas-fir-western hemlock forest. Can J For Res 35: 990-1001.
62. Shaw DC, Huso M, Bruner H (2008) Basal area growth impacts of dwarf mistletoe on western hemlock in an old-growth forest. Can J For Res 38: 576-583.
63. Simard S, Morin H, Krause C, Buhay WM, Treydte K (2012) Tree-ring widths and isotopes of artificially defoliated balsam firs: a simulation of spruce budworm outbreaks in Eastern Canada. Environ Exp Bot 81: 44-54.
64. Song X, Barbour MM, Farquhar GD, Vann DR, Helliker BR (2013) Transpiration rate relates to within-And across-species variations in effective pathlength in a leaf water model of oxygen isotope enrichment. Plant Cell Environ 36: 1338-1351.
65. Stanton S (2007) Effects of dwarf mistletoe on climate response of mature ponderosa pine trees. Tree Ring Res 63: 69-80.
66. Sternberg L (1989) Oxygen and hydrogen isotope measurements in plant cellulose analysis. In: Linskens HF, Jackson JF (eds) Modern methods of plant analysis, vol 10: plant fibers. Springer, Berlin, pp 89-99.
67. 2 diffusion. J Exp Bot 57: 343-354.
68. Watson DM (2001) Mistletoe -A keystone resource in forests and woodlands worldwide. Annu Rev Ecol Evol Syst 32: 219-249.
69. Way D (2011) Parasitic plants and forests: a climate change perspective. Tree Physiol 31: 1-2.
70. Wilson CA, Calvin CL (1996) Anatomy of the dwarf mistletoe shoot system In: Hawksworth FG, Wiens D (eds) Dwarf mistletoes: biology, pathology, and systematics. USDA FS, Washington, DC, pp 95-111.
71. Woodruff DR, Meinzer FC, Lachenbruch B, Johnson DM (2009) Co-ordination of leaf structure and gas exchange along a height gradient in a tall conifer. Tree Physiol 29: 261-272.
72. Yakir D, DeNiro MJ (1990) Oxygen and hydrogen isotope fractionation during cellulose metabolism in Lemna gibba L. Plant Physiol 93: 325-332.
73. Zweifel R, Bangerter S, Rigling A, Sterck FJ (2012) Pine and mistletoes: how to live with a leak in the water flow and storage system? J Exp Bot 63: 2565-2578.