Arceuthobium tsugense (Viscaceae): four subspecies with contrasting morphologies and host distributions
DOI:
https://doi.org/10.17348/jbrit.v11.i2.1076Keywords:
hemlock dwarf mistletoe, Arceuthobium, mountain hemlock, noble fir, pacific silver fir, western hemlockAbstract
There have been four subspecies of hemlock dwarf mistletoe (Arceuthobium tsugense: Viscaceae) described by various investigators of this complex group of parasitic flowering plants: subsp. tsugense, subsp. amabilae, subsp. contortae, and subsp. mertensianae. As suggested by their subspecific epithets, these taxa differ in their host affinities; parasitizing different and the same hosts to varying degrees. Although these taxa also have morphological differences, their classifica-tion has been under debate for many years. Therefore, we compared the morphological characteristics of each subspecies using both univariate and multivariate statistical analyses in order to better assess their differences. Because some investigators have grouped hemlock dwarf mistletoe with western dwarf mistletoe (A. campylopodum), we also compared the subspecies of hemlock dwarf mistletoe with western dwarf mistletoe. Our morphometric analyses demonstrated that all of the subspecies are morphologically distinct from western dwarf mistletoe and that subsp. contortae is the most morphologically differentiated of the subspecies. Overlap in the morphological characters across two of the other three subspecies was evident; yet, subsp. amabilae and subsp. mertensianae were also consistently delimited using female and male plant morphologies. Statistical comparisons of female or male plants via standard and stepwise discriminant function analyses demonstrated that without consideration of host plant, female and male A. tsugense subsp. tsugense are morphologically similar to corresponding plants of subsp. amabilae and mertensianae but not subsp. contortae or A. campylopodum.
References
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Filip, G.M., J.S. Hadfield, & C. Schmitt. 1979. Branch mortality of true firs in west-central Oregon associated with dwarf mistletoe and canker fungi. Pl. Dis. Rep. 63:189?193.
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Hawksworth, F.G. 1987. Taxonomy of hemlock dwarf mistletoe. In: S. J. Cooley, ed. Proceedings of the 34th Western International Forest Disease Work Conference. USDA Forest Serv., Forest Health Management, Portland, Oregon, U.S.A. Pp. 45–46.
Hawksworth, F.G. & D. Wiens. 1972. Biology and classification of dwarf mistletoes (Arceuthobium). Agric. Handb. 401, USDA Forest Serv., Washington, D.C., U.S.A.
Hawksworth, F.G. & D. Wiens. 1996. Dwarf mistletoes: Biology, pathology, and systematics. Agric. Handb. 709, USDA Forest Serv., Washington, D.C., U.S.A.
Hawksworth, F.G., D. Wiens, & D.L. Nickrent.1992. New western North American taxa of Arceuthobium (Viscaceae). Novon 2:204–211. doi:10.2307/3391549
Hennon, P.E., J.S. Beatty, & D. Hildebrand. 2001. Hemlock dwarf mistletoe. Forest Insect and Disease Leaflet 135, USDA Forest Serv., Pacific Northwest Region, Portland, Oregon, U.S.A.
Hildebrand, D.M. 1995. Arceuthobium tsugense hemlock dwarf mistletoe. A species of special concern? USDA Forest Serv., Pacific Northwest Region, Portland, Oregon, U.S.A.
Hunt, R.S. & R.B. Smith. 1978. Natural infection of two new hosts by hemlock dwarf mistletoe in British Columbia. Canad. Pl. Dis. Surv. 58:31–32.
Kenaley, S.C., R.L. Mathiasen, & C.M. Daugherty. 2016. Morphological evidence for continued species recognition among white pine dwarf mistletoes (Viscaceae): Arceuthobium apachecum, A. blumeri, A. californicum, A. cyanocarpum, and A. monticola. J. Bot. Res. Inst. Texas 10:361?383.
Kuijt, J. 1956. A new record of dwarf mistletoe on lodgepole and western white pine. Madroño 13:170?172.
Kuijt, J. 1969. A systematic study of branching patterns in dwarf mistletoe (Arceuthobium). Mem. Torrey Bot. Club 22:1–38.
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Mathiasen, R. 1982. Taxonomic studies of dwarf mistletoes (Arceuthobium spp.) parasitizing Pinus strobiformis. Great Basin Nat. 42:120–127.
Mathiasen, R.L. 1994. Natural infection of new hosts by hemlock dwarf mistletoe. USDA Forest Serv., Res. Note RM-RN-530, Rocky Mtn. Res. Sta., Ft. Collins, Colorado, U.S.A.
Mathiasen, R.L. 1996. Dwarf mistletoes in forest canopies. N. W. Sci. 70 (Special Issue):61–71.
Mathiasen, R.L. 1998. Comparative susceptibility of conifers to larch dwarf mistletoe in the Pacific Northwest. Forest. Sci. 44:559–568.
Mathiasen, R.L. 2007. A new combination for Hawksworth’s dwarf mistletoe. Novon 17:217–221.
Mathiasen, R.L. 2008. New combinations for Arceuthobium aureum (Viscaceae) in Mexico and Central America. Novon 18:501–507.
Mathiasen, R.L. 2011. Susceptibility of conifers to three dwarf mistletoes in the Klamath-Siskiyou Mountains. W. J. Appl. Forest. 26:13?18.
Mathiasen, R.L. & C.M. Daugherty. 2005. Comparative susceptibility of conifers to western hemlock dwarf mistletoe in the Cascade Mountains of Washington and Oregon. W. J. Appl. Forest. 20:94?100.
Mathiasen, R.L. & C.M. Daugherty. 2007. Arceuthobium tsugense subsp. amabilae, a new subspecies of hemlock dwarf mistletoe (Viscaceae) from Oregon. Novon 17:222–227. doi:10.3417/1055-3177(2007)17[222:ATSAAN]2.0.CO;2
Mathiasen, R.L. & C.M. Daugherty. 2008. Distribution of red fir and noble fir in Oregon based on dwarf mistletoe host specificity. N. W. Sci. 82:108–119.
Mathiasen, R.L. & C.M. Daugherty. 2009. Arceuthobium abietinum subspecies wiensii, a new subspecies of fir dwarf mistletoe (Viscaceae) from northern California and southern Oregon. Madroño 56:118?126.
Mathiasen, R.L. & C.M. Daugherty. 2010. Susceptibility of Brewer spruce (Picea breweriana) to dwarf mistletoes (Arceuthobium spp., Viscaceae). N. W. Sci. 84:295?301.
Mathiasen, R.L. & C.M. Daugherty. 2013. Additional morphological measurements of Arceuthobium littorum and A. occidentale (Viscaceae). Phytologia 95:70–78.
Mathiasen, R.L. & F.G. Hawksworth. 1988. Dwarf mistletoes on western white pine and whitebark pine in northern California and southern Oregon. Forest. Sci. 34:429–440.
Mathiasen, R.L. & S.C. Kenaley. 2015a. A morphometric analysis of the dwarf mistletoes in the Arceuthobium campylopodum-occidentale complex (Viscaceae). Madroño 62:1–20.
Mathiasen, R.L. & S.C. Kenaley. 2015b. A morphometric analysis of Arceuthobium campylopodum, A. laricis, and A. tsugense (Viscaceae). Phytologia 97:200–218.
Mathiasen, R.L. & S.C. Kenaley. 2016. The classification of California Viscaceae: An alternative perspective. Madroño 63:8–33. doi: 10.3120/0024-9637-62.1.1
Mathiasen, R.L. & S.C. Kenaley. 2017. Contrasting perspectives on the measurements and taxonomy of Arceuthobium: A long standing controversy. Phytologia 99:95–110.
Mathiasen, R.L., S.C. Kenaley, & C.M. Daugherty. 2016. A morphometric analysis of Arceuthobium campylopodum and Arceuthobium divaricatum (Viscaceae). Aliso 34:9–23.
Moreno-Letelier, A. & D. Piñero. 2009. Phylogeographic structure of Pinus strobiformis Engelm. across the Chihuahuan Desert filter-barrier. J. Biogeogr. 36:121–131.
Muir, J.A. & B.W. Geils. 2002. Management strategies for dwarf mistletoes: Silviculture. In B.W. Geils, J. Cibrián Tovar, & B. Moody (tech. coords.). Mistletoes of North American conifers. Gen. Tech. Rep. RMRS-GTR-98, USDA Forest Serv., Rocky Mtn. Res. Sta., Ogden, Utah, U.S.A. Pp. 83–94.
Muir, J.A. & P.E. Hennon. 2007. A synthesis of the literature on the biology, ecology, and management of western hemlock dwarf mistletoe. USDA Forest Serv., Gen. Tech. Rep. PNW-GTR-718, Pacific N. W. Res. Sta., Portland, Oregon, U.S.A.
Nickrent, D.L. 2012. Justification for subspecies in Arceuthobium campylopodum (Viscaceae). Phytoneuron 51:1–11.
Nickrent, D.L. 2016. Viscaceae Batch—Christmas Mistletoe Family. In: Flora of North America. Volume 12. Flora of North America Editorial Committee, eds. Oxford University Press, New York, New York, U.S.A. Pp. 422?440.
Nickrent, D.L., M.A. García, M.P. Martín, & R.L. Mathiasen. 2004. A phylogeny of all species of Arceuthobium (Viscaceae) using nuclear and chloroplast DNA sequences. Amer. J. Bot. 91:125–138. doi:10.3732/ajb.91.1.125
Nickrent, D.L. & A.L. Stell. 1990. Electrophoretic evidence for genetic differentiation in two host races of hemlock dwarf mistletoe (Arceuthobium tsugense). Biochem. Sys. Ecol. 18:267–280.
Norton, D.A. & M.A. Carpenter. 1998. Mistletoes as parasites: Host specificity and speciation. Tree 13:101–105.
Quinn, G.P. & M.J. Keough. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UK. doi:10.1017/CBO9780511806384
Rancher, A.C. 2002. Methods of multivariate analysis. Second edition. John Wiley and Sons, Inc., New York, NY. doi:10.1002/0471271357
Reif, B.P., R.L. Mathiasen, S.C. Kenaley, & G.J. Allan. 2015. Genetic structure and morphological differentiation of three Western North American dwarf mistletoes (Arceuthobium: Viscaceae). Syst. Bot. 40:191–207. doi:10.1600/036364415X686503
Scott, J.M. & R.L. Mathiasen. 2009. Bristlecone pine dwarf mistletoe: Arceuthobium microcarpum subsp. aristatae (Viscaceae), a new subspecies of western spruce dwarf mistletoe from northern Arizona. J. Bot. Res. Inst. Texas 3:13–22.
Shaw, C.G. 1982. Mountain hemlock is an occasional host for hemlock dwarf mistletoe in Alaska. Pl. Dis. 66:852–854.
Smith, R.B. 1969. Assessing dwarf mistletoe on western hemlock. Forest. Sci. 15:277–285.
Smith, R.B. 1974. Infection and development of dwarf mistletoes on plantation-grown trees in British Columbia. Report BC-X-97, Canad. Forest. Serv., Pacific Forestry Res. Centre, Victoria, B.C., Canada.
Smith, R.B. & E.F. Wass. 1976. Field evaluation of ecological differentiation of dwarf mistletoe on shore pine and western hemlock. Canad. J. Forest Res. 6:225–228.
Smith, R.B. & E.F. Wass. 1979. Infection trials with three dwarf mistletoe species within and beyond their known ranges in British Columbia. Canad. J. Pl. Path. 1:47–57.
Southwest Environmental Information Network. 2017. Available on-line at http://swbiodiversity.org/portal/index.php. (Accessed 15 April 2017).
Wass, E.F. 1976. Ecological study of shore pine stands infested with dwarf mistletoe on southeastern Vancouver Island. Report BC-X-142. Canad. Dept. Environ., Pacific Forestry Res. Centre, Victoria, B.C., Canada.
Wass, E.F. & R.L. Mathiasen. 2003. A new subspecies of Arceuthobium tsugense (Viscaceae) from British Columbia and Washington. Novon 13:268–276.
Weir, J.R. 1915. A new host for a species of Razoumofskya. Phytopath. 5:73.
Weir, J.R. 1916. Mistletoe injury to conifers in the Northwest. USDA Bull. 360.
Wellwood, R.W. 1956. Some effects of dwarf mistletoe on western hemlock. Forest. Chron. 32:282–296.
Etheridge, D.E. 1973. Wound parasites causing tree decay in British Columbia. Forest Pest Leaflet 62, Canad. Forest. Serv., Dept. of Environ., Pacific Forestry Res. Centre, Victoria, B.C., Canada.
Filip, G.M., J.S. Hadfield, & C. Schmitt. 1979. Branch mortality of true firs in west-central Oregon associated with dwarf mistletoe and canker fungi. Pl. Dis. Rep. 63:189?193.
Frankis, M. 2009. The high elevation white pines of Mexico and the adjacent SW USA. Pinus L. subgenus Strobus Lemmon, Pinaceae. Int. Dendrol. Soc. Yearb. 2008:64–72.
Gill, L.S. 1935. Arceuthobium in the United States. Trans. Conn. Acad. Arts Sci. 32:111–245.
Hawksworth, F.G. 1977. The 6-class dwarf mistletoe rating system. Gen. Tech. Rep. RM-48, USDA Forest Serv., Rocky Mtn. For. and Range Exp. Sta., Ft. Collins, Colorado, U.S.A.
Hawksworth, F.G. 1987. Taxonomy of hemlock dwarf mistletoe. In: S. J. Cooley, ed. Proceedings of the 34th Western International Forest Disease Work Conference. USDA Forest Serv., Forest Health Management, Portland, Oregon, U.S.A. Pp. 45–46.
Hawksworth, F.G. & D. Wiens. 1972. Biology and classification of dwarf mistletoes (Arceuthobium). Agric. Handb. 401, USDA Forest Serv., Washington, D.C., U.S.A.
Hawksworth, F.G. & D. Wiens. 1996. Dwarf mistletoes: Biology, pathology, and systematics. Agric. Handb. 709, USDA Forest Serv., Washington, D.C., U.S.A.
Hawksworth, F.G., D. Wiens, & D.L. Nickrent.1992. New western North American taxa of Arceuthobium (Viscaceae). Novon 2:204–211. doi:10.2307/3391549
Hennon, P.E., J.S. Beatty, & D. Hildebrand. 2001. Hemlock dwarf mistletoe. Forest Insect and Disease Leaflet 135, USDA Forest Serv., Pacific Northwest Region, Portland, Oregon, U.S.A.
Hildebrand, D.M. 1995. Arceuthobium tsugense hemlock dwarf mistletoe. A species of special concern? USDA Forest Serv., Pacific Northwest Region, Portland, Oregon, U.S.A.
Hunt, R.S. & R.B. Smith. 1978. Natural infection of two new hosts by hemlock dwarf mistletoe in British Columbia. Canad. Pl. Dis. Surv. 58:31–32.
Kenaley, S.C., R.L. Mathiasen, & C.M. Daugherty. 2016. Morphological evidence for continued species recognition among white pine dwarf mistletoes (Viscaceae): Arceuthobium apachecum, A. blumeri, A. californicum, A. cyanocarpum, and A. monticola. J. Bot. Res. Inst. Texas 10:361?383.
Kuijt, J. 1956. A new record of dwarf mistletoe on lodgepole and western white pine. Madroño 13:170?172.
Kuijt, J. 1969. A systematic study of branching patterns in dwarf mistletoe (Arceuthobium). Mem. Torrey Bot. Club 22:1–38.
Kuijt, J. 2012. Viscaceae. In: Baldwin, B.G., D. Goldman, D.J. Keil, R. Patterson, T.J. Rosatii, & D.H. Wilken, eds. The Jepson manual: Vascular plants of California. University of California Press, Berkeley, California, U.S.A. Pp. 600–603.
Mathiasen, R. 1982. Taxonomic studies of dwarf mistletoes (Arceuthobium spp.) parasitizing Pinus strobiformis. Great Basin Nat. 42:120–127.
Mathiasen, R.L. 1994. Natural infection of new hosts by hemlock dwarf mistletoe. USDA Forest Serv., Res. Note RM-RN-530, Rocky Mtn. Res. Sta., Ft. Collins, Colorado, U.S.A.
Mathiasen, R.L. 1996. Dwarf mistletoes in forest canopies. N. W. Sci. 70 (Special Issue):61–71.
Mathiasen, R.L. 1998. Comparative susceptibility of conifers to larch dwarf mistletoe in the Pacific Northwest. Forest. Sci. 44:559–568.
Mathiasen, R.L. 2007. A new combination for Hawksworth’s dwarf mistletoe. Novon 17:217–221.
Mathiasen, R.L. 2008. New combinations for Arceuthobium aureum (Viscaceae) in Mexico and Central America. Novon 18:501–507.
Mathiasen, R.L. 2011. Susceptibility of conifers to three dwarf mistletoes in the Klamath-Siskiyou Mountains. W. J. Appl. Forest. 26:13?18.
Mathiasen, R.L. & C.M. Daugherty. 2005. Comparative susceptibility of conifers to western hemlock dwarf mistletoe in the Cascade Mountains of Washington and Oregon. W. J. Appl. Forest. 20:94?100.
Mathiasen, R.L. & C.M. Daugherty. 2007. Arceuthobium tsugense subsp. amabilae, a new subspecies of hemlock dwarf mistletoe (Viscaceae) from Oregon. Novon 17:222–227. doi:10.3417/1055-3177(2007)17[222:ATSAAN]2.0.CO;2
Mathiasen, R.L. & C.M. Daugherty. 2008. Distribution of red fir and noble fir in Oregon based on dwarf mistletoe host specificity. N. W. Sci. 82:108–119.
Mathiasen, R.L. & C.M. Daugherty. 2009. Arceuthobium abietinum subspecies wiensii, a new subspecies of fir dwarf mistletoe (Viscaceae) from northern California and southern Oregon. Madroño 56:118?126.
Mathiasen, R.L. & C.M. Daugherty. 2010. Susceptibility of Brewer spruce (Picea breweriana) to dwarf mistletoes (Arceuthobium spp., Viscaceae). N. W. Sci. 84:295?301.
Mathiasen, R.L. & C.M. Daugherty. 2013. Additional morphological measurements of Arceuthobium littorum and A. occidentale (Viscaceae). Phytologia 95:70–78.
Mathiasen, R.L. & F.G. Hawksworth. 1988. Dwarf mistletoes on western white pine and whitebark pine in northern California and southern Oregon. Forest. Sci. 34:429–440.
Mathiasen, R.L. & S.C. Kenaley. 2015a. A morphometric analysis of the dwarf mistletoes in the Arceuthobium campylopodum-occidentale complex (Viscaceae). Madroño 62:1–20.
Mathiasen, R.L. & S.C. Kenaley. 2015b. A morphometric analysis of Arceuthobium campylopodum, A. laricis, and A. tsugense (Viscaceae). Phytologia 97:200–218.
Mathiasen, R.L. & S.C. Kenaley. 2016. The classification of California Viscaceae: An alternative perspective. Madroño 63:8–33. doi: 10.3120/0024-9637-62.1.1
Mathiasen, R.L. & S.C. Kenaley. 2017. Contrasting perspectives on the measurements and taxonomy of Arceuthobium: A long standing controversy. Phytologia 99:95–110.
Mathiasen, R.L., S.C. Kenaley, & C.M. Daugherty. 2016. A morphometric analysis of Arceuthobium campylopodum and Arceuthobium divaricatum (Viscaceae). Aliso 34:9–23.
Moreno-Letelier, A. & D. Piñero. 2009. Phylogeographic structure of Pinus strobiformis Engelm. across the Chihuahuan Desert filter-barrier. J. Biogeogr. 36:121–131.
Muir, J.A. & B.W. Geils. 2002. Management strategies for dwarf mistletoes: Silviculture. In B.W. Geils, J. Cibrián Tovar, & B. Moody (tech. coords.). Mistletoes of North American conifers. Gen. Tech. Rep. RMRS-GTR-98, USDA Forest Serv., Rocky Mtn. Res. Sta., Ogden, Utah, U.S.A. Pp. 83–94.
Muir, J.A. & P.E. Hennon. 2007. A synthesis of the literature on the biology, ecology, and management of western hemlock dwarf mistletoe. USDA Forest Serv., Gen. Tech. Rep. PNW-GTR-718, Pacific N. W. Res. Sta., Portland, Oregon, U.S.A.
Nickrent, D.L. 2012. Justification for subspecies in Arceuthobium campylopodum (Viscaceae). Phytoneuron 51:1–11.
Nickrent, D.L. 2016. Viscaceae Batch—Christmas Mistletoe Family. In: Flora of North America. Volume 12. Flora of North America Editorial Committee, eds. Oxford University Press, New York, New York, U.S.A. Pp. 422?440.
Nickrent, D.L., M.A. García, M.P. Martín, & R.L. Mathiasen. 2004. A phylogeny of all species of Arceuthobium (Viscaceae) using nuclear and chloroplast DNA sequences. Amer. J. Bot. 91:125–138. doi:10.3732/ajb.91.1.125
Nickrent, D.L. & A.L. Stell. 1990. Electrophoretic evidence for genetic differentiation in two host races of hemlock dwarf mistletoe (Arceuthobium tsugense). Biochem. Sys. Ecol. 18:267–280.
Norton, D.A. & M.A. Carpenter. 1998. Mistletoes as parasites: Host specificity and speciation. Tree 13:101–105.
Quinn, G.P. & M.J. Keough. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UK. doi:10.1017/CBO9780511806384
Rancher, A.C. 2002. Methods of multivariate analysis. Second edition. John Wiley and Sons, Inc., New York, NY. doi:10.1002/0471271357
Reif, B.P., R.L. Mathiasen, S.C. Kenaley, & G.J. Allan. 2015. Genetic structure and morphological differentiation of three Western North American dwarf mistletoes (Arceuthobium: Viscaceae). Syst. Bot. 40:191–207. doi:10.1600/036364415X686503
Scott, J.M. & R.L. Mathiasen. 2009. Bristlecone pine dwarf mistletoe: Arceuthobium microcarpum subsp. aristatae (Viscaceae), a new subspecies of western spruce dwarf mistletoe from northern Arizona. J. Bot. Res. Inst. Texas 3:13–22.
Shaw, C.G. 1982. Mountain hemlock is an occasional host for hemlock dwarf mistletoe in Alaska. Pl. Dis. 66:852–854.
Smith, R.B. 1969. Assessing dwarf mistletoe on western hemlock. Forest. Sci. 15:277–285.
Smith, R.B. 1974. Infection and development of dwarf mistletoes on plantation-grown trees in British Columbia. Report BC-X-97, Canad. Forest. Serv., Pacific Forestry Res. Centre, Victoria, B.C., Canada.
Smith, R.B. & E.F. Wass. 1976. Field evaluation of ecological differentiation of dwarf mistletoe on shore pine and western hemlock. Canad. J. Forest Res. 6:225–228.
Smith, R.B. & E.F. Wass. 1979. Infection trials with three dwarf mistletoe species within and beyond their known ranges in British Columbia. Canad. J. Pl. Path. 1:47–57.
Southwest Environmental Information Network. 2017. Available on-line at http://swbiodiversity.org/portal/index.php. (Accessed 15 April 2017).
Wass, E.F. 1976. Ecological study of shore pine stands infested with dwarf mistletoe on southeastern Vancouver Island. Report BC-X-142. Canad. Dept. Environ., Pacific Forestry Res. Centre, Victoria, B.C., Canada.
Wass, E.F. & R.L. Mathiasen. 2003. A new subspecies of Arceuthobium tsugense (Viscaceae) from British Columbia and Washington. Novon 13:268–276.
Weir, J.R. 1915. A new host for a species of Razoumofskya. Phytopath. 5:73.
Weir, J.R. 1916. Mistletoe injury to conifers in the Northwest. USDA Bull. 360.
Wellwood, R.W. 1956. Some effects of dwarf mistletoe on western hemlock. Forest. Chron. 32:282–296.
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Published
2017-11-29
How to Cite
Mathiasen, R. L., & Kenaley, S. C. (2017). Arceuthobium tsugense (Viscaceae): four subspecies with contrasting morphologies and host distributions. Journal of the Botanical Research Institute of Texas, 11(2), 363–390. https://doi.org/10.17348/jbrit.v11.i2.1076
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SYSTEMATICS
