Abstract
Much research has focused on effects of plant parasites on host-plant physiology and growth, but little is known about effects of host physiological condition on parasite growth. Using the parasitic dwarf mistletoe Arceuthobium vaginatum subsp. cryptopodum (Viscaceae) and its host Pinus ponderosa, we investigated whether changes in host physiological condition influenced mistletoe shoot development in northern Arizona forests. We conducted two studies in two consecutive years and used forest thinning (i.e., competitive release) to manipulate host physiological condition. We removed dwarf mistletoe shoots in April, before the onset of the growing season, and measured the amount of regrowth in the first season after forest thinning (Study I: n=38 trees; Study II: n=35 trees). Thinning increased tree uptake of water and carbon in both studies, but had no effect on leaf N concentration or δ13C. Mistletoe shoot growth was greater on trees with high uptake of water and carbon in thinned stands than trees with low uptake in unthinned stands. These findings show that increased resource uptake by host trees increases resources to these heterotrophic dwarf mistletoes, and links mistletoe performance to changes in host physiological condition.
Similar content being viewed by others
References
Adams HD, Kolb TE (2004) Drought responses of conifers in ecotone forests of northern Arizona: tree ring growth and leaf δ13C. Oecologia 140:217–225
Allen MF (1991) The Ecology of Mycorrhizae. Cambridge University Press, New York
Alosi MC, Calvin CL (1985) The ultrastructure of dwarf mistletoe (Arceuthobium spp.) sinker cells in the region of the host secondary vasculature. Can J Bot 63:889–898
Ayers MP, Lombardero MJ (2000) Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci Total Environ 262:263–286
Bannister P, King WM, Strong GL (1999) Aspects of water relations of Ileostylus microanthus (Hook. f.) Tieghem, a New Zealand mistletoe. Ann Bot 84:79–86
Baranyay JA, Smith JA (1972) Dwarf mistletoes in British Columbia and recommendations for their control. Report BC-X-72.Canadian Forestry Service, Pacific Forest Research Centre Victoria, BC, 18 p
Bennetts RE, Hawksworth FG (1992) The indirect effects of dwarf mistletoe on bird communities in Colorado ponderosa pine forests. In: Muir JA comp (ed) Proceedings of the 39th Annual Western International Forest Disease Work Conference. August 5–9, 1991. British Columbia Ministry of Forests, Silviculture Branch, Victoria, pp 14–17
Bond BJ, Farnsworth BT, Coulombe RA, Winner WE (1999) Foliage physiology and biochemistry in response to light gradients in conifers with varying shade tolerance. Oecologia 120:183–192
Brooks JR, Flanagan LB, Varney GT, Ehleringer JR (1997) Vertical gradients in photosynthetic gas exchange characteristics and refixation of respired CO2 within boreal forest canopies. Tree Physiol 17:1–12
Buchmann N, Kao WY, Ehleringer J (1997) Influence of stand structure on carbon-13 of vegetation, soils, and canopy air within deciduous and evergreen forests in Utah, United States. Oecologia 110:109–119
Colorado Plateau Stable Isotope Laboratory (2005) http://www4.nau.edu/cpsil/. Cited 27 March 2005
Conklin DA (2003) Comparison of dwarf mistletoe behavior and stand development in treated and untreated areas: 10-year monitoring on Jarita Mesa. USDA Forest Service, Southwestern Region Forestry and Forest Health Report R3-03-02. Albuquerque, NM, 11 p
Covington W, Fule P, Moore M, Hart S, Kolb T, Mast J, Sackett S, Wagner M (1997) Restoring ecosystem health in ponderosa pine forests of the Southwest. J For 95:23–29
Davidson NJ, True KC, Pate JS (1989) Water relations of the parasite:host relationship between the mistletoe Amyema linophyllum (Fenzl) Tieghem and Casuarina obesa Miq. Oecologia 80:321–330
Davies DM, Graves JD (1998) Interactions between arbuscular mycorrhizal fungi and the hemiparasitic angiosperm Rhinanthus minor during co-infection of a host. New Phytol 139:555–563
Farentinos RC (1972) Nests of the tassel-eared squirrel. J Mammal 53:900–903
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Mol Biol 40:503–537
Feeney SR, Kolb TE, Covington WW, Wagner MR (1998) Influence of thinning and burning restoration treatments on presettlement ponderosa pines at the Gus Pearson Natural Area. Can J For Res 28:1295–1306
Fessenden JE, Ehleringer JR (2003) Temporal variation in δ13C of ecosystem respiration in the Pacific Northwest: links to moisture stress. Oecologia 136:129–136
Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, London, pp 25–55
Fisher JT (1983) Water relations of mistletoes and their hosts. In: Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sydney, pp 161–184
Flanagan LB, Ehleringer JR (1998) Ecosystem-atmosphere CO2 exchange: interpreting signals of change using stable isotope ratios. Trends Ecol Evol 13:10–14
Garnett GN (2002) Wildlife use of witches’ brooms induced by dwarf mistletoe in ponderosa pine forests of northern Arizona. MS thesis, Northern Arizona University
Godfree RC, Tinnin RO, Forbes RB (2002) Relationships between Arceuthobium americanum and the structure of Pinus contorta var. murrayana stands in central Oregon. Plant Ecol 165:69–84
Hawksworth FG (1977) The 6-class dwarf mistletoe rating system. General Technical Report RM-48. USDA Forest Service, Rocky Mountain Forest and Range Experimental Station, Fort Collins, 7 p
Hawksworth FG, Shaw CG (1984) Damage and loss caused by dwarf mistletoes in coniferous forests of western North America. In: Wood RKS, Jellis GJ (eds) Plant diseases: Infection, damage, and loss. Blackwell, Oxford, pp 285–297
Hawksworth FG, Weins D (1996) Dwarf mistletoes: biology, pathology, and systematics. Agriculture Handbook 709, USDA Forest Service, Washington DC
Hawksworth FG, Geils BW (1990) How long do mistletoe-infected ponderosa pines live? W J App For 5:47–48
Hawksworth FG, Geils BW (1996) Biotic associates. In: Hawksworth FG, Weins D (eds) Dwarf mistletoes: biology, pathology, and systematics. USDA Forest Service, Washington DC, pp 73–90
Hegyi F (1974) A simulation model for managing jack-pine stands. In: Fries J (ed) Growth models for tree and stand simulation. Royal College of Forestry Stockholm, Stockholm, pp 74–90
Hull RJ, Leonard OA (1964a) Physiological aspects of parasitism in mistletoes (Arceuthobium and Phoradendron) I. The carbohydrate nutrition of mistletoe. Plant Physiol 39:996–1007
Hull RJ, Leonard OA (1964b) Physiological aspects of parasitism in mistletoes (Arceuthobium and Phoradendron) II. The photosynthetic capacity of mistletoe. Plant Physiol 39:1008–1017
Huynh H, Feldt LS (1970) Conditions under which mean square ratios in repeated measurements designs have exact F distribution. J Am Stat Assoc 65:1582–1589
Kaye JP, Hart SC (1998) Restoration and canopy-type effects on soil respiration in a ponderosa pine-bunchgrass ecosystem. Soil Sci Soc Am J 62:1062–1072
Keith JO (1965) The Abert squirrel and its dependence on ponderosa pine. Ecology 46:150–163
Kolb PF, Robberecht R (1996) Pinus ponderosa seedling establishment and the influence of competition with the bunchgrass Agropyron spicatum. Int J Plant Sci 4:509–515
Kolb TE (2002) Ecophysiology of parasitism in the plant kingdom. In: Lopez Saez JA, Rodriguez PC, Saez L (eds) Plantas Parasitas de la Peninsula Iberica e Islas Baleares (Guide on Parasitic Plants of the Iberian Peninsula and the Balearic Islands). MundiPrensa, Madrid
Kolb TE, Holmberg KM, Wagner MR, Stone JE (1998) Regulation of ponderosa pine foliar physiology and insect resistance mechanisms by basal area treatments. Tree Physiol 18:375–381
Kolb TE, Stone JE (2000) Differences in leaf gas exchange and water relations among species and tree sizes in an Arizona pine-oak forest. Tree Physiol 20:1–12
Lamont B (1983) Mineral nutrition of mistletoes. In: Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sydney, pp 185–203
Latham P, Tappeiner J (2002) Response of old-growth conifers to reduction in stand density in western Oregon forests. Tree Physiol 22:137–146
Leonard OA, Hull RJ (1965) Translocation relationships in and between mistletoes and their hosts. Hilgardia 37:115–153
Linhart YB, Snyder MA, Gibson JP (1994) Differential host utilization by two parasites in a population of ponderosa pine. Oecologia 98:117–120
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
Lorimer CG (1983) Test of age-independent competition indices for individual trees in natural hardwood stands. For Ecol Manag 6:343–360
Marshall JD, Dawson TE, Ehleringer JR (1994) Integrated nitrogen, carbon, and water relations of a xylem-tapping mistletoe following nitrogen fertilization of the host. Oecologia 100:430–438
Mathiasen R (1996) Dwarf mistletoes in forest canopies. Northwest Sci 70:61–71
McDowell N, Brooks JR, Fitzgerald SA, Bond BJ (2003) Carbon isotope discrimination and growth response of old Pinus ponderosa to stand density reductions. Plant Cell Environ 26:631–644
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
Meyer CL, Sisk TD, Covington WW (2001) Microclimatic changes induced by ecological restoration of ponderosa pine forests in northern Arizona. Restor Ecol 9:443–452
Miller G, Ambos N, Boness P, Reyher D, Robertson G, Scalzone K, Steinke R, Subirge T (1995) Terrestrial ecosystem survey of the Coconino National Forest. USDA Forest Service, Southwestern Region, 405 p
Miller JR, Tocher RD (1975) Photosynthesis and respiration of Arceuthobium tsugense (Loranthaceae). Am J Bot 62:765–769
Mooney KA (2003) Promylea lunigerella glendella Dyar (Pyralidae) feeds on both conifers and parasitic dwarf mistletoe (Arceuthobium spp.): one example of food plant shifting between parasitic plants and their hosts. J Lepidopterists Soc 57:47–53
Moore MM, Casey CA, Bakker JD, Springer JD, Fulé PZ, Covington WW, Laughlin DC (2005) Herbaceous response to restoration treatments in a ponderosa pine forest, 1992–2004. Rangeland Ecol Manage (in press)
Mueller RC (2004) Dwarf mistletoe infection on pinyon pine: Environmental stress, host vigor, and ectomycorrhizae. MS thesis, Northern Arizona University
Nyland RD (2002) Silviculture, McGraw-Hill Series in Forest Resources, 2nd edn. McGraw-Hill, New York
Pennings SC, Callaway RM (2002) Parasitic plants: parallels and contrasts with herbivores. Oecologia 131:479–489
Quick CR (1964) Experimental herbicidal control of dwarfmistletoe on some California conifers. Research Note PSW-47. USDA Forest Service, Pacific Southwest Forest and Range Experimental Station, Berkeley, 9 p
Quraishi MA, Khalique A, Perveen S, Akhtar P (1977) Water relations of dwarf mistletoe (Arceuthobium oxycedri M. Bieb) in relation to that of its host (Juniperus excelsa M. Bieb). Pak J For 27:198–202
Rediske JH, Shea KR (1961) The production and translocation of photosynthate in dwarfmistletoe and lodgepole pine. Am J Bot 48:447–452
Rey L, Sadik A, Fer A, Renaudin S (1991) Trophic relations of the dwarf mistletoe Arceuthobium oxycedri with its host Juniperus oxycedri. J Plant Physiol 138:411–416
Roth LF, Barrett JW (1985) Response of dwarf mistletoe-infested ponderosa pine to thinning: 2. Dwarf mistletoe propagation. USDA Forest Service, Res Pap PNW-331. Portland, 20 p
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
Salonen V, Setala H, Puustinen S (2000) The interplay between Pinus sylvestris, its root hemiparasite, Melampyrum pretense, and ectomycorrhizal fungi: Influences on plant growth and reproduction. Ecoscience 7:195–200
SAS Institute Inc. (2002) JMP Statistics and Graphics Guide Version 5. SAS Institute Inc., Cary
Scharpf RF (1972) Light affects penetration and infection of pines by dwarf mistletoe. Phytopathol 62:1271–1273
Schulze ED, Ehleringer JR (1984) The effect of nitrogen supply on growth and water-use efficiency of xylem-tapping mistletoes. Planta 162:268–275
Schulze E-D, Lange OL, Ziegler H, Gebauer G (1991) Carbon and nitrogen isotope ratios of mistletoes growing on nitrogen and non-nitrogen fixing hosts and on CAM plants in the Namib desert confirm partial heterotrophy. Oecologia 88:457–462
Shaw DC, Weiss SB (2000) Canopy light and the distribution of hemlock dwarf mistletoe (Arceuthobium tsugense [Rosendahl] G.N. Jones subsp. tsugense) aerial shoots in an old-growth Douglas-fir/western hemlock forest. Northwest Sci 74:306–315
Sheppard PR, Comrie AC, Packin GD, Angersbach K, Hughes MK (2002) The climate of the US Southwest. Climate Res 21:219–238
Simonin K, Kolb TE, Montes-Helu M, Koch G (2005) Restoration thinning and the influence of tree size and leaf area to sapwood area ratio on Pinus ponderosa Laws. water relations. Tree Physiol (in press)
Skov KR, Kolb TE, Wallin KF (2004) Tree size and drought affect ponderosa pine physiological response to thinning and burning treatments. For Sci 50:81–91
Snyder MA, Fineschi B, Linhart YB, Smith RH (1996) Multivariate discrimination of host use by dwarf mistletoe: Arceuthobium vaginatum subsp. cryptopodum: inter- and intraspecific comparisons. J Chem Ecol 22:295–305
Srivastava LM, Esau K (1961) Relation of dwarfmistletoe (Arceuthobium) to the xylem tissue of conifers. I. Anatomy of parasite sinkers and their connection with host xylem. Am J Bot 48:159–167
Stevens RE, Hawksworth FG (1970) Insects and mites associated with dwarf mistletoes. Research paper RM-59. USDA Forest Service Rocky Mountain Forest and Range Experiment Station, Fort Collins
Stewart GR, Press MC (1990) The physiology and biochemistry of parasitic angiosperms. Annu Rev Plant Physiol Mol Biol 41:127–151
Sutherland EK (1989) The effect of prescribed burning on southwestern ponderosa pine growth. PhD Dissertation, University of Arizona
Tinnin RO, Knutson DM (1999) Effects of Douglas-fir dwarf mistletoe on trees in thinned stands in the pacific northwest. For Sci 45:359–365
van Ommeren RJ, Whitham TG (2002) Changes in interactions between juniper and mistletoe mediated by shared avian frugivores: parasitism to potential mutualism. Oecologia 130:281–288
Wallin KF, Kolb TE, Skov KR, Wagner MR (2004) Seven-year results of thinning and burning restoration treatments on old ponderosa pines at the Gus Pearson Natural Area. Restor Ecol 12:239–247
Wanner JL, Tinnin RO (1989) Some effects of infection by Arceuthobium americanum on the population dynamics of Pinus contorta in Oregon. Can J For 19:736–742
Wanner JL, Tinnin RO (1986) Respiration in lodgepole pine parasitized by American dwarf mistletoe. Can J For Res 16:1375–1378
Waring RH, Silvester WB (1994) Variation in foliar δ13C values within the crowns of Pinus radiata trees. Tree Physiol 14:1203–1213
Watson DM (2001) Mistletoe — a keystone resource in forests and woodlands worldwide. Annu Rev Ecol System 32:219–2490
Western Regional Climate Center (2005) http://www.wrcc.dri.edu/index.html. Cited 27 March 2005
Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426
Acknowledgements
Funding was provided by Mission Research Program, School of Forestry, Northern Arizona University (McIntire-Stennis/AZ Bureau of Forestry) and the USDA Rocky Mountain Research Station JVA (RJVA 00-JV-11221006-210) between B. Geils and T. Kolb. We thank Shawn Faiella, Megan Van Horne, Michelle Schaffer, Natacha Guerard, and Dan Koepke for help in conducting the study, Becky Mueller, Kitty Gehring and two anonymous reviewers for their comments on the manuscript, and the NAU Centennial Forest and Coconino National Forest for use of study sites. The experiments described in this paper comply with the current laws of the United States, where the experiments were performed.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Lawrence Flanagan
Rights and permissions
About this article
Cite this article
Bickford, C.P., Kolb, T.E. & Geils, B.W. Host physiological condition regulates parasitic plant performance: Arceuthobium vaginatum subsp. cryptopodum on Pinus ponderosa . Oecologia 146, 179–189 (2005). https://doi.org/10.1007/s00442-005-0215-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-005-0215-0