B. W. Geils ID. Wiens Chapter F. G. Hawksworth 3 Phoradendron in Mexico and the United States The generally familiar mistletoes are the leafy Phoradendron that typically infest hardwood trees and are placed at doorways for winter celebrations. Several of these mistletoes, however, more resemble the dwarf mistletoes by their apparently leafless stems and presence on conifers; but their large, fleshy berries that are attractive to birds clearly identify them as Phoradendron, “the tree thief.” For several reasons, the conifer-infecting Phoradendron (the group reviewed here) have not gotten the level of attention from forest managers that the Arceuthobium have. Phoradendron most typically cause slight damage to junipers in Southwestern woodlands. But these mistletoes include a number of different species, range from Oregon to Mexico, infect a variety of hosts, and provide an interesting model of host–parasite interactions. Along with the other mistletoes, the taxonomy, biology, physiol- ogy, and ecology of the Phoradendron are reviewed by Gill and Hawksworth (1961) and Kuijt (1969a). Foresters have long been interested in the Phoradendron on incense cedar (Meinecke 1912). USDA Forest Service Gen. Tech. Rep. RMRS-GTR-98. 2002 19 Geils, Wiens, and Hawksworth Phoradendron in Mexico and the United States Picture guidebooks are available by Walters (1978) for perennial, but plants of all ages are subject to mortal- the Southwest and by Scharpf and Hawksworth (1993) ity by extreme low temperatures (Wagener 1957). for the Pacific States. General summaries of informa- tion including control are provided by Hawksworth Host–Parasite Physiology and Scharpf (1981), Hernandez (1991), and Vega (1976). The taxonomy of the Phoradendron on coni- The physiology of Phoradendron is generally re- fers was first monographed by Trelease (1916) and viewed by Fisher (1983), Knutson (1983), and Kolb then revised by Wiens (1964). Confusion over the (2002) as typical for most mistletoes (but different position and ranking of several taxa (Hawksworth from that of the dwarf mistletoes). Many details of the 1979) and recent evidence from molecular systemat- nitrogen, carbon, and water relations of the “xylem- ics (Ashworth 2000) suggest the group requires an- tapping” Phoradendron juniperinum are elucidated in other taxonomic monograph. a series of recent ecophysiology studies (Ehleringer and others 1986, Marshall and Ehleringer 1990, Marshall and others 1993, 1994). The mistletoes do fix Life History and Biology __________ some carbon but get much from their host; mistletoes transpire a lot of water (all from their host); and they The Phoradendron have a typical mistletoe life cycle get a lot of nitrogen from the host, as the inevitable characterized by bird dispersal of sticky seeds, inter- consequence of the physiological relation (Marshall nal parasitism of a woody host, and aerial shoots for and others 1994). Lei (1997) concludes that heavy flower and fruit production. Phoradendron biology, mistletoe infection increases host-plant water stress reproduction, and parasitism have received intense and reduces vigor, viability, and reproductive success study from ecological and evolutionary perspectives. of the host in favor of the mistletoe. McHenry (1934) reports that Phoradendron at the Grand Canyon kills Life Cycle juniper. Hawksworth and Wiens (1966) indicate that The most detailed but still comprehensive study and junipers may also form witches’ broom in response to review of a Phoradendron life cycle is that by Felix infection. (1970a) for the mistletoe on Abies concolor. A number of bird species feed on the mistletoe fruits and disperse Host–Parasite Ecology seeds by excreting or regurgitating them. The most Numerous authors have studied the effects of important birds for effective dispersal include cedar Phoradendron parasitism on population dynamics and waxwings, euphonias, silky flycatcher, bluebirds, interactions with other species. Hreha and Weber thrushes, robins, and solitaires (see Sutton 1951, Gill (1979) compare pinyon dwarf mistletoe (Arceuthobium 1990). Seeds pass quickly, and because birds perch in divaricatum) and juniper mistletoe (Phoradendron trees, seeds are deposited at suitable sites for infection juniperinum) at the South Rim of the Grand Canyon, (often the top or warm side of a potential host, com- reporting more infection in bigger (older) trees, a lack monly one already infected). Germinating seeds pro- of infestation in recently burned (young) areas, and duce a radicle, holdfast, and penetrate the host branch general stability in the populations. They consider the usually near a needle (Ruhland and Calvin 2001). The pinyon dwarf mistletoe the more detrimental because endophytic system consists of longitudinal strands it more readily kills its host. Juniper mistletoe often and sinkers (Calvin and others 1991, Felix 1970a). has a patchy distribution, with some trees heavily Once aerial shoots are produced, the Phoradendron infested. Gregg (1991) concludes the critical difference does photosynthesize, but it is a parasite (see below) between infested and uninfested sites is the need for a not a simple epiphyte. Plants are either male or dependable moisture supply to maintain the high female. Although Dawson and others (1990a) report a demand of infected trees. Moisture stress in firs in- male-bias and provide hypotheses why there might be fected by Phoradendron is associated with reduced such a bias, Daughtery and Mathiasen (1999) find the resistance and increased successful attack by the fir sex ratio is one to one. Flower production and repro- engraver (Felix 1970a, Ferrell 1974). Gehring and duction is typical, except that natural hybridization Whitham (1992) report that on droughty sites, juniper occurs but rarely (Wiens and Dedecker 1972). Fruits severely infested by mistletoe have lower rates of are produced several years after infection; older plants beneficial mycorrhiza infection, and female junipers produce more and larger fruits (Dawson and Ehleringer are more seriously affected than male junipers. An- 1991, Dawson and others 1990a, 1990b). Although the other three-way, conditional interaction is described shapes of shoots and leaves of Phoradendron might by van Ommeren and Whitham (2002) for juniper, mimic their host, the biology behind the appearance is mistletoe, and their avian dispersers. Although mistle- unclear (Atsatt 1993b). Endophytic systems are toe has a negative impact on the health of infected 20 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-98. 2002 Phoradendron in Mexico and the United States Geils, Wiens, and Hawksworth trees, mistletoe provides a more dependable food source height, nodes constricted, lacking epicortical roots; than juniper for the shared avian dispersers of each phyllotaxy opposite or decussate; inflorescence a spike; species’ seeds. By considering dispersal and reproduc- perianth generally three-parted and persistent; an- tive success in the interaction model, they conclude thers small, sessile and bilocular; fruit a berry, 3 to 6 that the net effect of mistletoe parasitism, depending mm, single color of white, pink, or reddish. A genus of on populations, shifts between favoring the mistletoe about 200 species in temperate and tropical America. to favoring the juniper. Type species: Phoradendron californicum Nuttall. The Phoradendron also exhibit a curious phenom- The genus Phoradendron, the largest genus of mistle- enon whereby a mistletoe is parasitized by another toes, is in serious need of definitive taxonomic study. mistletoe of the same or different species (Hawksworth Trelease (1916) is the first monographic study of the and Wiens 1966, Wiens and Calvin 1987). Although genus, but Wiens (1964) revises many of Trelease’s several of the conifer-infecting Phoradendron may be taxa that occur on conifers (see table 3-1). This tax- infected by other Phoradendron mistletoes (Felix onomy is further reconsidered by Hawksworth and 1970b), the occurrence is too rare to effect a significant Wiens (1993a, 1993b) for the flora of California, Ne- biological control. vada, and Arizona. Other floristic treatments with keys and illustrations include Hitchcock and others (1964) for the Pacific Northwest, McMinn (1939) for Description of Genus ____________ California, Standley (1920) for Mexico, and Wiggins Phoradendron (1980) for Baja California. Kuijt (1996) questions the Mistletoe, injerto significance and interpretation of many of the tradi- Shrubby parasite of trees and other woody plants tional morphological features used for the taxonomy of (fig. 3-1), woody at base, glabrous or hairy; shoots Phoradendron. Ashworth (2000) provides much in- cylindrical, green or less often reddish, 20 cm in sight to the relations among these mistletoes using techniques of molecular systematics. Most of the taxa of Phoradendron that parasitize conifers are in the section Pauciflorae as described by Wiens (1964). Ashworth (2000) reports that these taxa (see table 3-1), delimited by morphological features, also form a single, related cluster based on molecular features. Phoradendron rhipsalinum is also a parasite of conifers but is apparently more closely related to a number of Phoradendron that typically infect hard- woods. A few other Phoradendron reportedly occur on conifers, but these are either rare cases or possibly misidentifications. Usual conifer host genera are Abies, Calocedrus, Cupressus, Juniperus, Taxodium (table 3-2). Martínez (1948) illustrates Phoradendron velutinum C on Pinus leiophylla