* Rocky Mountain Forest and Range Experiment Station, Fort Collins, Colorado.
Organisms associated with Arceuthobium include birds, mammals, insects, arachnids, and fungi. Most of the literature, however, is observational or anecdotal and widely scattered. Scientific names of birds and mammals mentioned here are listed in the appendix.
Except for the dwarf mistletoes (with their explosive fruits) and a few terrestrial root parasites, most mistletoe seeds are primarily dispersed by birds (Kuijt 1969a). Nicholls and others (1984) identified several types of bird–dwarf mistletoe associations: (1) long-distance dispersal of seeds, (2) use of shoots and fruits for food, (3) use of shoots and witches’ brooms as foraging areas, and (4) use of witches’ brooms for cover and nesting. Potential indirect effects of bird–dwarf mistletoe interactions are largely unstudied. Such effects include, for example, utilization of dwarf mistletoe-killed trees and those with dead tops by cavity-nesting birds, and openings in stand structure caused by dwarf mistletoe infestations.
Birds have been implicated in long-distance dispersal of dwarf mistletoe seeds by several workers (Nicholls and others 1984, Weir 1916b, Zilka and Tinnin 1976). Kuijt (1963) discovered several isolated trees of Pseudotsuga menziesii infected by Arceuthobium douglasii in southern British Columbia that were about 80 km from the closest known source of infection. Weir (1916b) discovered seeds of A. laricis about 400 m from the closest infected larch trees. He surmised that the seeds were transmitted by high winds but mentioned that birds also may have been involved. Ireland (1926) found seeds of A. occidentale in an apple orchard about 1 km from the closest infested trees of Pinus sabiniana.
Only 3 studies quantify the frequency of isolated or "satellite" infection centers in otherwise mistletoe-free forests:
Although satellite centers are relatively scarce, the explosive mechanism of seed dispersal utilized by dwarf mistletoes enables them to intensify and spread rapidly from a newly established satellite center.
Nicholls and others (1984) made a thorough study of animal vectors of Arceuthobium americanum and reviewed the previous literature (table 8.1). They showed that animals, especially birds, act as long-distance dispersal agents of this dwarf mistletoe in Colorado. Unlike seeds of other mistletoes, those of Arceuthobium are destroyed if they are ingested (Hudler and others 1979). Thus, birds can only disperse seeds that accidentally adhere to their feathers and are subsequently deposited where infection is likely to occur (safe-site). Although such events are rare, a sufficient proportion of birds (27%) carried dwarf mistletoe seeds to make some such dispersal probable (Nicholls and others 1984). The gray jay was the most important seed vector for A. americanum, but other important resident species of birds were Steller’s jay, mountain chickadee, and dark-eyed junco. Because dwarf mistletoe fruits mature in late summer, migratory birds such as warblers, robins, and hermit thrushes can also play a significant role in long-distance dispersal (Nicholls and others 1984).
Punter and Gilbert (1989) studied animal dispersal in Arceuthobium americanum on Pinus banksiana in southern Manitoba. They found no seeds on small mammals but observed seeds on 5% of the birds captured in mist-nets; gray jays and dark-eyed juncos were most common. A brown creeper, a red-breasted nuthatch, and a Swainson’s thrush also carried dwarf mistletoe seeds.
Various bird species are implicated as dispersal agents for several dwarf mistletoe species. Gray jays are apparently the most important vectors for Arceuthobium pusillum in Picea mariana and for A. americanum in Pinus contorta. Steller’s jays disperse several dwarf mistletoe species in the Pacific Northwest; nuthatches and chickadees are important for long-distance dispersal of A. vaginatum subsp. cryptopodum in Colorado (table 8.1). Birds, particularly the mistle thrush, have been suggested as long-distance vectors of A. oxycedri in France (Gerber and Cotte 1908) and Pakistan (Zakaullah and Badshah 1977), but quantitative data are lacking. Gorrie (1929) suggests that tits and finches are the primary long-distance dispersal agents of A. minutissimum in India.
Birds are very important for dispersal of dwarf mistletoe species that typically occur in isolated trees or in the tops of otherwise uninfected trees. This pattern is characteristic of the following dwarf mistletoes:
Except for Arceuthobium verticilliflorum, seeds of these species are effectively dispersed by explosive fruit, although birds likely augment mistletoe spread. Because the large fruits of A. verticilliflorum are not explosively discharged, birds probably are the primary vectors of this species; their activity probably accounts for the widespread distribution of this mistletoe in the open-canopy stands where it commonly occurs. Dispersal agents for A. verticilliflorum have not been determined, but we suspect the gray silky-flycatcher because it feeds on the fruits of other mistletoes (particularly Phoradendron spp.) and is common in pine forests of the Sierra Madre Occidental (Sutton 1951).
Birds in the United States that utilize dwarf mistletoes for food are summarized in table 8.2. Weir (1916b) noted house sparrows feeding on fruits of Arceuthobium campylopodum in Idaho, and Hawksworth (1961a) observed evening grosbeaks taking ripe fruits of A. vaginatum subsp. cryptopodum in Arizona. Phainopeplas feed on ripe fruits of A. occidentale in the Sierra Nevada foothills (W. J. Hawksworth, personal communication). The Antillean euphonia eats large quantities of A. bicarinatum fruits in the Dominican Republic (Etheridge 1971); tits and finches forage on fruits of A. minutissimum in India (Gorrie 1929). The song thrush ingests fruits of A. oxycedri in France (Gerber and Cotte 1908), and the mistle thrush feeds on this dwarf mistletoe in Pakistan (Zakaullah and Badshah 1977). In general, feeding on dwarf mistletoe shoots and fruits is uncommon for birds other than the euphonia in the Dominican Republic and the gray silky-flycatcher in Mexico.
A number of reports document feeding by grouse on dwarf mistletoes (table 8.2). Most of these reports are simply observational, but Severson (1986) notes that although blue grouse feed primarily on foliage of Pseudotsuga menziesii, 2 to 8% of the bird’s diet is composed of Arceuthobium douglasii. The importance of such large birds as grouse for establishment of new mistletoe populations is unknown. Although ingested seeds would be rendered inviable, Zilka (1973) suggests that grouse roosting high in tree crowns would carry seeds externally that, once dislodged, would be washed down to young host shoots susceptible to infection.
The dense and abnormally branched witches’ brooms caused by dwarf mistletoe infection are commonly utilized by some birds for nesting sites. The often large systemic witches’ brooms in Pseudotsuga menziesii that result from infection by Arceuthobium douglasii are often used as nesting platforms by several owls and accipiters (table 8.3). Approximately 25 to 30% of these raptors normally nest in witches’ brooms. In eastern Oregon, however, 19 of 20 nests of long-eared owls were found in witches’ brooms (Bull and others 1988). Ravens on the east side of the Cascades in Washington nest in witches’ brooms (S. Martin, personal communication). Witches’ brooms induced by A. douglasii are also commonly used for roosting cover by grouse (Martinka 1972, Stauffer and Peterson 1986, Weir 1916b). At least 10 passerine species have been found nesting in witches’ brooms of various dwarf mistletoes (table 8.4).
Bennetts (1991) and Bennetts and Hawksworth (1992) studied relationships in central Colorado between infestations by Arceuthobium vaginatum subsp. cryptopodum in stands of Pinus ponderosa and the population dynamics of various bird species. The abundance of dwarf mistletoe in a stand was directly correlated with species diversity and bird density. They also demonstrated a strong positive correlation between incidence of dwarf mistletoe and the number of snags used by cavity-nesting birds. Severs and others (1991) reported a nearly three-fold increase in the density of cavity-nesting birds in stands severely infested by dwarf mistletoes over the density in comparable but uninfested stands.
Literature involving mammal–dwarf mistletoe associations has been discussed in detail by Hawksworth (1975), Nicholls and others (1984), and Tinnin and others (1982).
Red squirrels and flying squirrels are known to carry seeds of Arceuthobium pusillum in Picea mariana stands in Minnesota (Hudler and others 1974, Ostry and others 1983). In the first year of their studies, 20 seeds were found on mammals and birds—including 1 on a red squirrel and 10 on flying squirrels. In the following year, 25 seeds were found—all on red squirrels. Lemons (1978) studied the role of red squirrels as seed vectors of A. campylopodum in central Oregon. He found no seeds on squirrels in stands of Pinus ponderosa where dwarf mistletoe infestation was low, but about 50% of squirrels carried mistletoe seeds in severely infested stands. He observed that squirrels carried seeds for distances up to 150 m. Because squirrels groom seeds from their fur soon after becoming attached, he doubted they were important for establishment of new and distant infection centers.
The seed vectors of Arceuthobium americanum on Pinus contorta in Colorado were studied by Nicholls and others (1987b, 1989). Seeds were discovered on 4 species of mammals—least chipmunk (24 of 254 animals with seeds), golden-mantled ground squirrel (3 of 20 animals with seeds), red squirrel (1 of 15 animals with seed), and American marten (1 of 1 animal with seed). Although chipmunks and ground squirrels carried the most seeds, they are unlikely to initiate new infection centers because they spend most of their time on or near the ground and are therefore unlikely to deposit those seeds at infection safe-sites. Red squirrels are more effective animal vectors because they frequent tree crowns; but they have relatively small home ranges and are less likely than birds to effect long-distance dispersal.
Taylor (1935) studied porcupines in Arizona and discussed the possibility that they might disperse Arceuthobium vaginatum subsp. cryptopodum. Porcupines definitely feed on dwarf mistletoe shoots (see below), but we question the importance their role as an effective vector because (1) outer twigs with needles (safe-sites) are too small to support such large animals, and (2) resinous wounds on older tissues (where porcupines frequent) are unlikely infection courts (Hawksworth 1961a).
In Manitoba, Punter and Gilbert (1989) trapped 193 mammals in Pinus banksiana stands infested by Arceuthobium americanum; none of the animals (including least chipmunk, red-backed vole, deer mouse, and Franklin’s ground squirrel) carried dwarf mistletoe seeds. Urban (1968) implicated various rodent species in the dispersal of A. cyanocarpum in the open stands of P. flexilis at Craters of the Moon National Monument in southern Idaho.
Various mammals utilize dwarf mistletoe shoots as a dietary supplement, but none are dependent on them as a primary food source.
The red squirrel is the most thoroughly studied of all the mammals that forage on trees infected with dwarf mistletoe. It is most commonly associated with Arceuthobium americanum on Pinus contorta in British Columbia (Baranyay 1968, Wood and others 1985), Montana (U.S. Department of the Interior 1970), Wyoming (Wagner 1968), and Colorado (unpublished data). Small branches 6 to 13 mm in diameter are nipped off and the cortex consumed; in all areas observed, squirrels select mistletoe-infected twigs over uninfected twigs. In British Columbia, 90% of the mistletoe-infected branches over a 30-ha area were gnawed (Wood and others 1985). One of the earliest reports of dwarf mistletoes in North America mentions that this squirrel fed on A. campylopodum in the "Oregon Territory" (Hooker 1847). Rodents, presumably tree squirrels, in California feed on dwarf mistletoe cankers in true firs (Scharpf 1982).
Abert squirrels in northern Arizona feed nearly exclusively on the bark of young twigs of Pinus ponderosa (Keith 1965). Keith observed that these squirrels also feed on the inner bark of twigs infected by Arceuthobium vaginatum subsp. cryptopodum by removing the mistletoe shoots and outer bark, and consuming inner bark and associated endophytic system of dwarf mistletoe. Shaw and Hennon (1991) found that 22% of the infections caused by A. tsugense on young Tsuga heterophylla in southeast Alaska had been chewed by rodents. Wass (1976) reported rodent chewing on A. tsugense infections on P. contorta in British Columbia and noted their absence on similarly infected T. heterophylla. States and others (1988) found that foraging times of Abert squirrels on dwarf mistletoe and associated structures varied by season—1% in spring, 3% in summer, 5% in autumn, and 12% in winter. Stephenson (1975) reported that squirrels in Arizona consumed dwarf mistletoe shoots and fruits throughout the year, but mistletoe comprised less than 4% of the total diet. In southeastern Utah, however, dwarf mistletoe was rarely used for food (Patton and Vahle 1986).
Chipmunks eat the fruits and seeds of Arceuthobium campylopodum in Washington (Broadbooks 1958), those of an unidentified mistletoe in northern Idaho (Wicker 1967a), and those of A. americanum in Colorado (Nicholls and others 1984). Dwarf mistletoes, however, are probably not an important element in their overall diet.
Taylor (1935) commented that some porcupines in the Southwest are "excessively fond" of Arceuthobium vaginatum subsp. cryptopodum and prefer this plant to pine needles and inner bark during certain seasons. Winter foraging on dwarf mistletoe was restricted to only 20% of the porcupine population, but those individuals that did feed on mistletoe, did so extensively. In winter, spring, and summer, 20 to 25% of stomach contents was mistletoe shoots; in autumn, the amount rose to 65%. Certain trees of Pinus ponderosa in Colorado that are infested with A. vaginatum subsp. cryptopodum are also especially attractive to porcupines in winter; the ground under these trees is often littered with hundreds of porcupine fecal pellets comprised of fragments of dwarf mistletoe shoots. Johnson and Carey (1979) noted that, in one area of northern Colorado, dwarf mistletoe shoots made up about 25% of the porcupine fecal pellets. In the Pacific Northwest, A. campylopodum is such an attractive food for porcupines in autumn and winter that shoots of this dwarf mistletoe are used for bait to trap the animals (Hooven 1971, Lawrence 1957).
Deer forage opportunistically on dwarf mistletoes. Although shoots are high in nutritive value (Urness 1969), they are usually inaccessible. Shoots of Arceuthobium vaginatum subsp. cryptopodum have a digestibility ratio of about 50% and are high in nutrients—45 to 55% acid-detergent fiber, 0.15 to 0.25% phosphorus, and 5 to 7% crude protein (Urness 1969). Hawksworth (1961b) observed mule deer in northern Arizona feeding on shoots of A. vaginatum subsp. cryptopodum in green logging slash. Other observations of mule deer in several studies (Currie and others 1977) showed that this dwarf mistletoe contributed less than 1% to the total diet. Dried mistletoe shoots that had fallen to the ground were only eaten in April and constituted about 2.5% of that month’s diet. Wright and Arrington (1950), in their study on mule deer of the northern Kaibab Plateau, reported that A. vaginatum subsp. cryptopodum contributed from a trace to 54% of the diet (overall average <1%). Leach (1956) and Leach and Hiele (1957) observed that A. campylopodum occurred in the stomach contents of California mule deer 10 to 25% of the time, but contributed only 1 to 2% of the volume consumed. Craighead and others (1973) report that A. americanum on Pinus contorta is an important, high-protein, winter food for elk in thermal areas of Yellowstone National Park.
Farentinos (1972) found that, in Colorado, 10 of 40 nests of Abert squirrels were in witches’ brooms of Pinus ponderosa induced by Arceuthobium vaginatum subsp. cryptopodum. Dwarf mistletoe was rare on the study site, and all large witches’ brooms observed were utilized as nesting sites. Similar observations were reported near Allenspark, Colorado (Pollock 1981).
Red squirrels in Colorado nest in witches’ brooms of Pinus contorta caused by Arceuthobium americanum (Hatt 1943). Patton and Vahle (1986) reported that 35% of red squirrel nests in an Arizona mixed conifer forest were found in witches’ brooms. Nesting sites for red squirrels in eastern Oregon were found in brooms of P. ponderosa induced by A. campylopodum (Lemons 1978).
Witches’ brooms of Pinus contorta induced by Arceuthobium americanum are frequently used by the American marten for nesting sites in California (Spencer 1987), Montana (Burnett 1981), and Wyoming (Campbell 1979, Hauptman 1979, Buskirk and others 1987). In northeastern Oregon, witches’ brooms of Pseudotsuga menziesii caused by A. douglasii are often used by porcupines in winter for protection from snow and wind (Smith 1982). Flying squirrels on the east side of the Cascades in Washington also frequently utilize witches’ brooms induced by A. douglasii for cover and nesting sites (S. Martin, personal communication). Lemons (1978) reports that witches’ brooms of Pinus ponderosa caused by A. campylopodum are used as nesting sites by flying squirrels and bushy-tailed woodrats in eastern Oregon.
The indirect effects of dwarf mistletoe infection on stand opening—the production of dead branches and dying trees—have been studied in relation to abundance of mammals in Pinus ponderosa infested with Arceuthobium vaginatum subsp. cryptopodum. In certain years, dwarf mistletoe-infested stands in northern Arizona received significantly more use by mule deer than stands without dwarf mistletoe, but no long-term preferences were observed (Clary and Larson 1971). Both mule deer and elk in Colorado used infested stands more frequently than uninfested stands (Bennetts and others 1991).
The literature on insect–dwarf mistletoe associations was summarized by Stevens and Hawksworth (1970, 1984). They recognized 3 major types of association: (1) pollination (chapter 3), (2) predation of shoots, fruits, and seeds (this chapter), and (3) invasion of insects into trees weakened by dwarf mistletoe infection (chapter 12).
Many diverse species of insects feed on dwarf mistletoe shoots, fruits, and seeds (Stevens and Hawksworth 1970, 1984). Most are generalist feeders that only forage on dwarf mistletoes incidentally and opportunistically. For example, the grasshopper Melanoplus devastator, which usually feeds on herbaceous vegetation, destroyed more than 90% of the shoots of Arceuthobium campylopodum in a California plantation of Pinus jeffreyi (Scharpf and Koerber 1986). Also, the harvester ant, Atta mexicana, which is a generalist feeder, utilized shoots of Arceuthobium durangense in Sinaloa, Mexico (Nickrent 1988).
A number of insect species, including members of the Lepidoptera, Hemiptera, Coleoptera, and Thysanoptera, feed exclusively on dwarf mistletoes.
The thicket hairstreak butterfly, Mitoura spinetorum (Lycaenidae), is highly prized by butterfly collectors, and larvae are obligate feeders on dwarf mistletoe (fig. 8.1). The species occurs from southern British Columbia to central Mexico (Shields 1965). Larvae have been collected from 10 species of Arceuthobium (Stevens and Hawksworth 1970) and probably occur on all North American species. Larvae are common enough in certain years to exert a minor degree of biological control but are usually too rare to significantly affect dwarf mistletoe populations. A related species, M. johnsonii, occurs on both subspecies of hemlock dwarf mistletoe—A. tsugense subsp. mertensianae in California and A. tsugense subsp. tsugense from Oregon to southern British Columbia (McCorkle 1962). McCorkle (Anonymous 1982) found in Oregon that 28 larvae completely destroyed 74% of 144 shoots of A. tsugense subsp. tsugense.
The most destructive larvae that feed on dwarf mistletoe are Dasypyga alternosquamella (Pyralidae) and Filatima natalis (Gelechidae) (Heinrich 1921). Little is known of the biology of these species, but both are apparently widespread in western North America and occur on several species of Arceuthobium. Dasypyga alternosquamella in British Columbia is extremely destructive to shoots of A. americanum (Reich 1992). Larvae of either species can destroy an entire crop of mistletoe shoots by mining larger shoots and consuming smaller shoots.
The plant bug Neoborella tumida (Miridae) feeds on several species of dwarf mistletoes in the western United States and Mexico (Knight 1925, Stevens and Hawksworth 1970). Neoborella tumida is notable for its size and color mimicry of dwarf mistletoe fruits. Three other species of Neoborella that apparently also feed exclusively on dwarf mistletoes have been described from the western United States and Canada (Herring 1972, Kelton and Herring 1978). Platylygus mexicanus is reported from Durango, Mexico, on a "mistletoe" (presumably Arceuthobium nigrum) of Pinus leiophylla (Kelton and Knight 1970).
The spittle bug Clastoptera distincta (Cercopidae) is widespread on Arceuthobium vaginatum subsp. cryptopodum in Arizona, New Mexico, and southern Colorado, but it apparently does little damage. The spittle bug is also common in northern Arizona on A. abietinum f. sp. concoloris.
The twig beetle Pityophthorus arceuthobii (Scolytidae) is apparently restricted to dwarf mistletoes in central Mexico. These beetles mine large shoots (frequently >3 cm at base) of both subspecies of Arceuthobium globosum (subsp. globosum and subsp. grandicaule) (Wood 1971, unpublished data). This twig beetle may also occur on other large-stemmed Mexican dwarf mistletoes such as A. vaginatum subsp. vaginatum and A. durangense.
Several species of thrips (Thripidae) are commonly associated with Arceuthobium (Stevens and Hawksworth 1970, 1984). Thrips are plant feeders, but the severity of their effects on dwarf mistletoe populations is not known. Most dwarf mistletoe-associated thrips have broad host ranges, but at least the species Frankliniella hawksworthii feeds exclusively on dwarf mistletoe (O’Neill 1970).
Several species of mites (Mesostigmata and Trombiformes) occur on dwarf mistletoes (Stevens and Hawksworth 1970), but their effects are unknown. Most dwarf mistletoe-associated mites have broad host ranges, but at least 4 species appear to be exclusively associated with dwarf mistletoes—Typhlodromus arceuthobius (Pytoseiidae) on Arceuthobium campylopodum and A. occidentale in California (Kennett 1963); T. pusillus on A. pusillum in eastern Canada (Kennett 1963); Paraphytopus arceuthobii (Eriophiidae) on flowers of A. campylopodum and A. occidentale in California (Keifer 1952); and Brevipalpus porca (Tenuipalpidae) on several dwarf mistletoes in California, Arizona, Utah, and New Mexico (Pritchard and Baker 1958).
Spiders associated with dwarf mistletoes in northern Colorado were studied by Jennings and others (1989). They found 22 species in 18 genera associated with 3 species of dwarf mistletoe, but none was restricted to them. Of the 118 individuals collected, 65% were hunters and 35% were web spinners. The spider fauna varied considerably among Arceuthobium americanum, A. cyanocarpum, and A. vaginatum subsp. cryptopodum, but differences were apparently associated with their host trees (Pinus contorta, P. flexilis, and P. ponderosa, respectively) rather than with the dwarf mistletoe. Many of the spiders had Arceuthobium pollen adhering to their body setae, but it is unlikely that spiders are effective pollinators. Spiders may, in fact, hinder pollination by ensnaring pollen grains in their webs (Baker and others 1985, Jennings and others 1989) or by capturing pollinating insects.
Many fungi are associated with dwarf mistletoes. They frequently kill shoots, fruits, and seeds directly; they may indirectly kill shoots by destroying the outer host cortex of a branch or by killing the entire branch. Heart rot fungi may also invade dwarf mistletoe swellings on the trunks of fir or hemlock trees (chapter 12).
Several fungi infect shoots and fruits of Arceuthobium (Gilbert 1984, Kuijt 1963, Hawksworth and others 1977, Wicker and Shaw 1968). Many of these are saprophytic or weakly parasitic, but at least 8 species are parasitic and apparently restricted to Arceuthobium (table 8.5). Fungi that parasitize dwarf mistletoe- infected trees also may infect the dwarf mistletoe. For example, the brown felt blight fungus, Herpotrichia juniperi, which infects Abies magnificae in California, also parasitizes A. abietinum f. sp. magnificae (Scharpf 1986).
Sphaeria arceuthobii, long known as Wallrothiella arceuthobii, was recently transferred by Barr and others (1986) to Caliciopsis. Sphaeria arceuthobii was originally described by Peck (1875) as a parasite of Arceuthobium pusillum in New York and subsequently was found in northern Michigan (Wheeler 1900), but no additional records of the fungus on A. pusillum have been reported. The biology of Caliciopsis was studied by Weir (1915a), Dowding (1931b), Wicker and Shaw (1968), Kuijt (1969b), Parker (1970), and Knutson and Hutchins (1979). The fungus infects stigmas during anthesis; later, stigmas and apical portions of the fruit are replaced by a black mycelial stroma. Normal fruit development is prevented and infected fruits fail to produce seed (fig. 8.2).
Caliciopsis arceuthobii is restricted to spring-flowering species of dwarf mistletoe (table 8.6) and is common on Arceuthobium douglasii, frequent on A. americanum, and rare on A. vaginatum subsp. cryptopodum (Hawksworth 1961b). In certain years, the fungus destroys more than 90% of the fruits of A. douglasii (Weir 1915c, Hawksworth and others 1977).
An 1,100-km disjunction (fig. 8.3) exists between populations of Caliciopsis arceuthobii in Oregon, Washington, and Idaho and those in Colorado, Arizona, New Mexico, and Mexico (Hawksworth and others 1977). We have been unsuccessful in spite of considerable effort over many years to collect the fungus within this distributional gap, and now believe it is a real discontinuity. Comparative studies on the biology and morphology of the northern and southern populations are needed. Wood (1986) gives a distribution map of C. arceuthobii in British Columbia.
Colletotrichum gloeosporioides is the most lethal and widespread pathogen of Arceuthobium. Weir recognized the fungus before 1920 as a serious parasite of dwarf mistletoes in the Pacific Northwest (Wicker and Shaw 1968). The biology and pathology of C. gloeosporioides were described in detail by Parmeter and others (1959). Infection first appears as small brown to black necrotic lesions on mistletoe shoots; lesions enlarge, coalesce, and ultimately cause dieback of shoots (fig. 8.4). The fungus affects most western species of dwarf mistletoe (table 8.6). Several observers report locating areas where a large portion of shoots have been killed by this pathogen. In California, Parmeter and others (1959) observed more than half of the shoots of A. abietinum killed; in Washington, Wicker (1967a) noted 24% of the shoots of A. campylopodum diseased; and in Alberta, Muir (1977) found more than half of the shoots of A. americanum affected. Muir (1967) and Wood (1986) describe the distribution of the fungus in western Canada; the distribution in the United States appears in figure 8.5.
Cylindrocarpon gillii was studied in detail by Ellis (1946), but it was recognized as a serious shoot parasite of Arceuthobium by Weir before 1920 (Wicker and Shaw 1968). In fact, Weir described it as "Fusarium campylopodii sp. nov." in an unpublished manuscript. Ellis (1939) also originally thought that it was a Fusarium, but after detailed study he transferred it to Septogloeum (Ellis 1946). Muir (1973) classified it as Cylindrocarpon. Early infection of mistletoe shoots by C. gillii is characterized by small, yellowish white lesions. These lesions enlarge, coalesce, erupt through the epidermis, and expose conspicuous masses of white spores; shoot tissues distal to lesions die. The fungus is widespread and parasitizes most species of Arceuthobium in the western United States and western Canada (fig. 8.6 and table 8.6; Wood 1986). There are, however, few collections from Idaho, Montana, Nevada, or Wyoming. Mielke (1959) attempted to introduce the fungus on A. americanum in southern Idaho, but the population of the parasite became extinct within about 3 years.
Because seeds infected by mold will not germinate, molds can markedly effect populations of Arceuthobium. For example, Wicker (1967b) planted seeds of 6 dwarf mistletoe species and found that 32 to 60% of the seeds were killed by molds during the first winter (September to April) and an additional 6 to 11% in the following spring (April to June). Many species of fungi, yeasts, and bacteria were isolated from mistletoe seeds in the field (Wicker 1974a); the most common genera found were Epicoccum, Stemphylium, Hormiscium, Phyllosticta, and Coniothyrium. Carpenter and others (1979) and Shaw and Loopstra (1991) noted the loss to fungi of seeds of A. tsugense planted on Tsuga heterophylla in the wet coastal environment.
Many fungi invade the already diseased inner bark of host branches infected by dwarf mistletoe (dwarf mistletoe cankers). Some of these kill infected branches or prevent shoot formation by the dwarf mistletoe.
The canker caused by Cytospora abietis is common on firs parasitized by Arceuthobium abietinum in California and Oregon (Wright 1942; Scharpf 1969c, 1980, 1983a, 1983b; Scharpf and Bynum 1975; Filip 1984, Filip and others 1979). The fungus kills infected branches, thereby giving trees a ragged appearance due to "flagging" of afflicted branches (see fig. 16.7). Although the fungus is primarily associated with dwarf mistletoe-infected branches, it does occur on branches weakened from other causes as well. In California, 22% of mistletoe-infected branches were parasitized by the fungus, compared to only 4% of the non-mistletoe-infected branches (Scharpf 1969c).
More than 20 fungal species in coastal British Columbia are associated with the cankers caused by Arceuthobium tsugense infection of Tsuga heterophylla (Baranyay 1966; Funk 1973, 1979, 1981; Funk and Baranyay 1973; Funk and Smith 1981). The high incidence of fungi on this dwarf mistletoe is presumably due to the wet, cool climate characteristic of hemlock forests where the mistletoe is found. The most important of these fungi, Nectria macrospora, substantially reduces dwarf mistletoe shoot and fruit production (Funk and others 1973, Smith and Funk 1980).
A pathogenic syndrome termed "resin disease" is common throughout the central and northern Rocky Mountains on Arceuthobium americanum (Mark and others 1976). Several weakly parasitic fungi, primarily Alternaria alternata and Aureobasidium pullans, invade the outer cortex of the host tissue (Pinus contorta) adjacent to the dwarf mistletoe canker. A necrophylatic periderm layer develops, outer host tissue dies, and although the host branch remains alive, dwarf mistletoe shoot production ceases. The syndrome is occasionally abundant in some areas, usually killing nearly all mistletoe shoots.
A rust fungus, Peridermium bethelii, is associated with Arceuthobium americanum on Pinus contorta (fig. 8.7). It is common in the Rocky Mountains from southern Alberta to central Colorado, and is known from a single locality on the eastern slope of the California Sierra Nevada (fig. 8.8 and Hawksworth and others 1983). Hyphae infect not only the mistletoes’ endophytic system but adjacent host tissues as well (Hawksworth and others 1983, Peterson 1966). Although the rust’s life cycle has not been elucidated, observations of its patchy distribution within infested stands suggest that it does not have an alternate host but rather is transmitted directly from mistletoe canker to mistletoe canker. Peridermium bethelii kills mistletoe-infested branches but is too uncommon to exert significant biological control.
Several additional species of canker fungi are associated with dwarf mistletoe. Nectria fuckeliana is a pathogen in California of Arceuthobium littorum on Pinus muricata and of A. abietinum f. sp. concoloris on Abies concolor (Byler and Cobb 1972). Filip and others (1979) report that Cytospora abietis, Cryptosporium pinicola, and Nectria macrospora in Oregon are associated with cankers caused by Arceuthobium abietinum on Abies grandis. Funk (1984) observes that Endothiella agregata is associated with cankers on Pinus contorta induced by Arceuthobium americanum in British Columbia. Sphaeropsis sapinea in California causes necrosis and death of branches of P. sabiniana and P. muricata infected by A. occidentale and A. littorum, respectively (Hunt 1969).