The dwarf mistletoes are serious pathogens of coniferous forest trees in many parts of the Northern Hemisphere, particularly in western North America. These widespread parasites retard growth of infected trees and cause extensive timber losses through direct and indirect mortality. In addition, the dwarf mistletoes reduce seed production and wood quality of the host plants, particularly in Abies and Tsuga. Infections by dwarf mistletoe also can provide entrance points for decay fungi.
In many parts of western North America, particularly in the central Rocky Mountains and the Southwest, the dwarf mistletoes are the most damaging pathogens of coniferous forest trees (Hawksworth and Shaw 1984). The extent of economic losses caused by dwarf mistletoes has been estimated at about 11.3 million cubic meters of wood annually (or about 3 billion board feet) in the western United States (Drummond 1982) and 3.8 million cubic meters in western Canada (Sterner and Davidson 1982). No information is available on losses in Latin America or Asia. It is difficult to calculate an actual dollar loss, but it is certainly several billion dollars annually.
The commercially important trees that are most seriously damaged in the western United States are Pinus ponderosa, P. contorta, P. jeffreyi, Pseudotsuga menziesii, Abies magnificae, A. concolor, Larix occidentalis, and Tsuga heterophylla. In parts of the Great Lakes region and New England, damage is severe on Picea mariana, P. glauca, and P. rubens. In Canada, the most seriously affected trees are Pinus contorta, P. banksiana, Tsuga heterophylla, Larix occidentalis, and Picea mariana.
Dwarf mistletoes also are the most serious parasites of conifers in Mexico, where at least 30 species of pines, as well as firs and Douglas-fir, are affected (Hawksworth 1991a). Although no economic data are available on losses outside the United States and Canada, dwarf mistletoes are known to have serious effects on forest production not only in Mexico, but also in Guatemala and Belize (our observations), the Dominican Republic (Etheridge 1971), India (Bagchee 1952, Bakshi and Puri 1971), Pakistan (Zakaullah 1988), and China (Tong and Ren 1980).
Dwarf mistletoe infections ultimately reduce a tree’s growth rate in both height and diameter, but only after the upper half of the tree’s crown is parasitized. Growth rate of the host then declines rapidly as the severity of infestation in the upper half of the crown increases (Hawksworth 1961a). Severe dwarf mistletoe infection will eventually kill the host. The time required for the parasite to kill a tree, however, varies considerably and depends on many factors, including
Just how dwarf mistletoes affect the growth and physiology of their host trees is not fully understood (chapter 9). Presumably, they alter the tree’s metabolic balance so that water, minerals, and various assimilates are appropriated by the parasite and infected parts of the lower crown at the expense of healthy parts of the crown. An infected branch thus becomes a nutrient sink. Radial growth of infected branches is greatly enhanced, as opposed to uninfected branches in the same whorl (Korstian and Long 1922, Hawksworth 1961a). Infected branches also tend to outlive adjacent uninfected branches. As progressively more nutrients are appropriated to infected branches, the vigor of the crown declines, and the tree ultimately dies.
Several systems for quantifying the severity of dwarf mistletoe infestation have been proposed (Hawksworth 1977, Dooling 1978). Some of these systems have as few as 4 classes, and others have as many as 18. Most of the early systems used subjective, undefined ratings such as "light," "medium," or "heavy." In an attempt to develop a less subjective system that would be applicable to several host–parasite combinations, the 6-class dwarf mistletoe rating system (DMR) was developed in the early 1950’s (Hawksworth and Lusher 1956, Hawksworth 1961a). Hawksworth (1977) gives details on the 6-class DMR system, including its uses and limitations.
In the 6-class system (fig. 12.1), the live crown is visually divided into thirds, and each third is rated as 0 for no mistletoe visible, 1 for light mistletoe infection (less than half of the branches infected), or 2 for heavy mistletoe infection (more than half of the branches infected). Ratings for each third are then added to obtain a total for the tree. For example, a tree heavily infected in the lower one-third of the crown, lightly infected in the middle one-third, and not infected in the upper third would be rated: 2 + 1 + 0 = class 3. A tree heavily infected in each third would be class 6. In this system, infections on the main stem are not considered, unless they are the only infections on the tree, which would be rated as class 1. An average stand or plot rating (stand DMR) is obtained by computing the mean rating of all live infected and noninfected host trees by species. This calculation may need adjustment depending on how trees are sampled (Filip and others 1993). Another statistic useful for describing infestation severity is the dwarf mistletoe index (DMI), the average DMR rating of live infected trees only (Geils and Mathiasen 1990). Because the 6-class system is easy to apply and ratings on the same tree by different observers are comparable, it has become the standard for quantifying the severity of dwarf mistletoe infection (Dooling 1978).
Although effects of dwarf mistletoes on tree vigor (as exhibited by thin, off-color foliage) are obvious in most severely infested stands, they are difficult to quantify. The most comprehensive report is the now classic study by Korstian and Long (1922) of Arceuthobium vaginatum subsp. cryptopodum on Pinus ponderosa in northern Arizona. They measured needle length, length of needle-bearing stems, number of needles, and photosynthetic surface on uninfected trees and comparable trees with various amounts of dwarf mistletoe infection (table 12.1). They found significant effects, particularly for heavily infected trees, in which average needle length was reduced by 30%, length of needle-bearing stems by 50%, leaf surface by 85%, and number of needles per tree by 80%. They also observed that infected trees had yellow-green foliage, whereas uninfected trees had olive-green foliage.
Andrade and Cibrián (1981) found a significant reduction in needle length on Pinus hartwegii heavily infected by Arceuthobium globosum subsp. grandicaule and A. vaginatum subsp. vaginatum in central Mexico—needles on uninfected trees averaged 14.8 cm long, whereas those of heavily infected trees averaged 9.4 cm, a reduction of 36%.
Weir (1918a) measured lateral and terminal buds of young Pseudotsuga menziesii trees in Montana that were uninfected or heavily infected with Arceuthobium douglasii. Terminal buds on uninfected trees averaged 12 x 4 mm compared with 8 x 3 mm for heavily infected trees. Uninfected trees had an average of 157 lateral buds (mean size 7 x 3 mm) compared to 108 (5 x 3 mm) for heavily infected trees.
Hawksworth (1961a) rated 1,600 Pinus ponderosa trees in southern New Mexico for crown vigor (on a 3-class scale) and severity of dwarf mistletoe infection (6-class DMR system). Vigor of the upper crown third was rated "good" for trees with normal needle color and density, "fair" for trees with intermediate needle color and density, or "poor" for trees with off-color needles and thin crowns. In a 55-year-old stand, 61% of the DMR class 6 trees were rated as poor, compared to 24% for DMR class 5 trees, and 2% for all other DMR infection classes, including noninfected trees. In a mature stand, 28% of the DMR class 6 trees were rated as poor, compared to 12% in DMR class 5 trees, and 3% for all other DMR infection classes.
Hawksworth and Johnson (1989a) conducted similar analyses for 2,600 mature Pinus contorta trees in Colorado and Wyoming infected by Arceuthobium americanum, but used Taylor’s (1939) 4-class vigor rating system. This system rates trees as most vigorous (class A: crown dense, full, of good color, and pointed) to least vigorous (class D: crown thin, open, off-color, and rounded). Only 20% of the trees in DMR classes 0 to 3 were in vigor class D, but this increased to about 27% for DMR class 4 and 5 trees, and up to 66% for DMR class 6 trees.
Schaffer and others (1983a) measured pulsed electrical resistance of trunk sapwood for Pinus contorta trees in various DMR classes and rated crown vigor with a 3-class system (Hawksworth 1961a and described above for P. ponderosa in New Mexico). Electrical resistance was found to be inversely correlated with crown vigor class:
| "Good" | 16.3 ± 0.4 k-ohms |
| "Fair" | 21.9 ± 1.2 k-ohms |
| "Poor" | 30.0 ± 3.6 k-ohms |
However, only trees in DMR class 6 had a significantly higher electrical resistance than trees in other DMR classes (including class 0, uninfected).
Mortality rates of infected seedlings are high, particularly those with main-stem infections. Weir (1916b) studied a 0.4-ha stand of 480 young Pinus ponderosa trees near Spokane, Washington; 245 (51%) of these trees were infected by Arceuthobium campylopodum and 49 (10%) had been killed by dwarf mistletoe. Roth (1971), also studying A. campylopodum, observed about 50% mortality among infected seedlings after 12 years. The surviving but infected trees were only about half as tall as uninfected trees.
Weir (1918a) measured heights of 4- to 10-year-old Pinus ponderosa trees near Spokane, Washington, and found those infected with Arceuthobium campylopodum were 30 to 40% shorter than uninfected trees. Knutson and Toevs (1972) noted that 2-year-old seedlings infected with this dwarf mistletoe were reduced in height and had shorter roots and less root volume than comparable uninfected seedlings. Seedling infection can be especially high in some stands. For example, Scharpf and Vogler (1986) reported that in the Laguna Mountains of southern California, 77% of the P. jeffreyi seedlings about 15 years old were infected by A. campylopodum, mostly on the main stem.
There is considerable literature on the pathological effects of different dwarf mistletoes on various hosts, particularly with respect to mortality and growth in diameter, height, and volume. Pertinent literature for North America was summarized by Hawksworth and Shaw (1984) and Hawksworth and others (1992a). Only a few representative examples are provided here.
Reduction in diameter growth is related primarily to infection severity but is also a function of the host–parasite combination. Usually, the effect is not measurable until severity of infection reaches DMR class 3 (table 12.2). As infection increases above this threshold, growth rates decline rapidly. Generally, reduction measured as 10-year periodic diameter increment is 10% for class 4 trees, 30% for class 5 trees, and 50% or more for class 6 trees (Hawksworth and others 1992c, Wicker and Hawksworth 1988).
Information on height growth is more difficult to obtain than for diameter growth, and fewer data are available. In general, effects of dwarf mistletoes on height growth are similar to those for diameter growth, but height reductions are usually slightly greater and are detectable earlier. In Pinus hartwegii infected by two species of Arceuthobium near Chapingo, Mexico, diameter growth was reduced by 19% but height was reduced by 29% (Andrade and Cibrián 1981). Some studies quantifying effects of dwarf mistletoes on height growth are summarized in table 12.3.
Reductions in stem volume reflect a combined effect of reduced growth in both diameter and height. Thus, losses in volume are proportionately greater than for those in diameter or height alone. Several studies show that severely infested stands produce only one-half to one-third the merchantable volume of timber expected from uninfected stands on comparable sites (Shubert and others 1993).
Although volume growth losses in surviving trees are important for many host–parasite combinations, mortality is a more serious component of timber loss for other combinations. Increased mortality rates within dwarf mistletoe-infested stands were summarized by Hawksworth and others (1992c) (table 12.4). Some North American host–parasite combinations in which elevated tree mortality is particularly important are listed in table 12.5. In addition, Arceuthobium minutissimum increases mortality rates of Pinus wallichiana in the western Himalayas (Zakaullah 1988).
Mortality rates are significantly higher in multiple-age stands with trees less than 25 cm in diameter than in older stands with larger trees. This was demonstrated for stands of Pinus ponderosa infested by Arceuthobium vaginatum subsp. cryptopodum in Arizona (Hawksworth and Geils 1990) and stands of Pseudotsuga menziesii infested by A. douglasii in the Southwest (Mathiasen and others 1990).
Effects of dwarf mistletoes on old-growth stands have received relatively little study. Previously, emphasis has been primarily on harvesting old-growth stands and regenerating the areas with mistletoe-free stands. With an increasing emphasis toward preserving old-growth forests, however, information on the effects of pathogens in such stands is becoming more important. By inducing formation of witches’ brooms and causing topkill and mortality of host trees, dwarf mistletoes affect the species composition, vertical crown structure, and spacing of trees within infested stands. These direct effects, in turn, have numerous consequences on the physical structure and functioning of the ecosystem. For example, the brooms provide forage, nesting, and cover for birds and mammals, but also increase the likelihood of ground fires becoming crown fires. Canopy gaps caused by mistletoe-induced mortality increase within-stand diversity but also reduce the interior-forest area. These ecological effects are complex and provided a fascinating area for future research.
Roth (1954) made an intensive survey of Arceuthobium campylopodum in a 259-ha stand of old-growth Pinus ponderosa in central Oregon. Dwarf mistletoe occurred on 105 ha or 41% of the area surveyed. Within the infested area, infection level was rated as very light on 58% of the area, light on 29%, intermediate on 12%, and heavy to very heavy on only 1%. Dwarf mistletoes generally exhibited a patchy distribution as the result of many interacting factors, including steepness of slope, aspect, fire history, and stand structure.
Hawksworth and others (1992c) examined the distribution of Arceuthobium americanum and its effects on basal area growth and mortality in three 2.02-ha plots in 300-year-old Pinus contorta stands in Colorado. From 34 to 60% of the area was infested, and no isolated infection centers occurred. This pattern was in marked contrast to nearby 70-year-old stands, which had an average of 1.4 isolated infection centers per ha (Nicholls and others (1987a). Mortality levels on infested plots were 1.7 times greater than levels on uninfested plots. Basal area growth was significantly reduced (about 30%) only in the most heavily infected trees (DMR class 6). This reduction in basal area growth is considerably less than that in younger infested stands of Pinus contorta: 6% reduction for DMR class 4 trees, 20% for DMR class 5 trees, and 42% for DMR class 6 trees. The study suggests that old-growth P. contorta trees tolerate dwarf mistletoe infection with significantly less effect than do younger trees.
Cone and seed production of heavily infected trees are generally reduced, but there are few quantitative studies. Cone production on dwarf mistletoe witches’ brooms is usually markedly reduced (Weir 1916b, Kuijt 1960b). However, Bonga (1964) noted mature cones with viable seeds on a witches’ broom caused by Arceuthobium pusillum on Picea mariana in New Brunswick. We also have observed cones on systemic witches’ brooms in Pinus contorta and Pseudotsuga menziesii, but these cones and seeds are smaller than normal.
Pearson (1912) studied seed germination of Pinus ponderosa trees in Arizona infected by Arceuthobium vaginatum subsp. cryptopodum. Germination of seed was 61% from infected trees and to 78% from uninfected trees. Korstian and Long (1922) studied these species in the same area and reported that production of viable seeds was not significantly reduced for lightly infected trees but was reduced by about 60% for moderately infected trees and 75% for heavily infected trees. Munns (1919) found that P. jeffreyi trees infected by A. campylopodum had seeds that were about half the normal weight, had a 20% lower germination rate, and produced less vigorous seedlings than those from uninfected trees. Reid and others (1991), however, observed no effect on cone production on Pinus rudis infected by A. vaginatum subsp. vaginatum.
Schaffer and others (1983b), working in the Rocky Mountains, reported that cone size, seed size, and seed germination of Pinus contorta trees were negatively correlated with the severity of infestation by Arceuthobium americanum. In Oregon, Wanner (1986) reported that cone length, number of seeds per cone, seed weight, and calories per seed of P. contorta were significantly reduced from normal for moderately and heavily infected trees. However, he found no relationship between severity of dwarf mistletoe infection and seed viability. In fact, 1-year survival of seedlings was significantly higher in heavily infested stands; this increased survival was attributed to better seedbed conditions provided by the higher amounts of woody litter that negated effects of reduced seed production in heavily infested stands.
Picea mariana infected by Arceuthobium pusillum in Newfoundland showed 10 to 22% loss of cone production and 25% reductions in seed production (Singh 1981). Further studies by Singh and Carew (1989) showed that infected trees had 10 to 24 fewer cones per tree than uninfected trees, 8 to 30 fewer seeds per cone, 8 to 29% lighter seeds, and 18 to 63% lower germination rates.
Hawksworth and Zakaullah (1985) found a strong correlation between the severity of infection by Arceuthobium minutissimum and cone production of Pinus wallichiana in Pakistan. Cone production was rated on a 4-class scale: 0 for trees with no cone crop; 1 for trees with cone crop less than normal and restricted to less than half of the upper crown; 2 for trees with cone crop less than normal but distributed over more than half of the upper crown; and 3 for tree with a normal cone crop. The average ratings for trees in each DMR class were then determined:
| 6-class DMR system |
Number of trees |
Cone production rating |
|---|---|---|
| 0 | 22 | 2.9 |
| 1 | 3 | 2.3 |
| 2 | 11 | 2.3 |
| 3 | 17 | 2.2 |
| 4 | 16 | 1.6 |
| 5 | 37 | 0.8 |
| 6 | 47 | 0.04 |
Trees in DMR class 6 produced practically no cones; trees in class 5 produced fewer and markedly smaller cones than those on uninfected and lightly infected trees.
Infection by dwarf mistletoes also affects the merchantability of wood by producing larger knots, developing abnormal grain, and reducing strength. The anatomy of dwarf mistletoe-infected wood is characterized by shorter, distorted tracheids and increased ray volume (Srivastava and Esau 1961b, Piirto and others 1974, Cibrián and others 1980). In old-growth Larix occidentalis, distorted wood grain, heavy pitch infiltration, insect frass, and associated decay markedly reduce merchantability of wood around trunk burls (Weir 1916a).
Wellwood (1956a, 1956b) reported that sapwood of Tsuga heterophylla trees infested by Arceuthobium tsugense had a lower moisture content and lower specific gravity than comparable uninfected wood. However, Hawksworth (1961a) observed that sapwood of Pinus ponderosa infected by A. vaginatum subsp. crytopodum had a higher moisture content and higher specific gravity than uninfected wood from the same trees. Knutson (1970) studying stem wood of P. ponderosa infected by A. campylopodum, found no difference in moisture content or specific gravity of wood at the infection site or immediately above it. Below the infection site, however, there was significantly higher moisture content and lower specific gravity. He concluded that stem infections impede normal movement of water and metabolites through sapwood.
Piirto and others (1974) observed that wood of Pinus contorta infected by Arceuthobium americanum had a higher specific gravity, a higher percentage of alcohol-benzene extractives, greater longitudinal shrinkage, and a lower percentage of latewood than comparable uninfected wood. Furthermore, infected wood was weaker in all strength tests—modulus of elasticity, modulus of rupture, and work to proportional limit. Finally, not only was wood from infected zones lower in strength, but wood from other parts of an infected tree was also adversely affected.
Infection by Arceuthobium vaginatum subsp. cryptopodum had little effect on bolts of Pinus ponderosa that were used for posts and treated with preservatives. In fact, wood from infected trees had slightly greater preservative penetration and retention than uninfected wood, but the differences were not significant (USDA Forest Service 1954).
The cumulative effects of dwarf mistletoe infection on lumber or pulp quality are usually negligible on Pinus contorta in British Columbia (Dobie and Britneff 1975), Abies concolor in California (Wilcox and others 1973), and Tsuga heterophylla in British Columbia (Hunt 1971) and Washington (Hadfield 1981). Presumably, most of the mistletoe-infected wood is near the outside of the trunk and removed when the logs are squared for sawing into cants or lumber.
Dwarf mistletoe infections of the main trunk and adjacent limbs of fir, larch, or hemlock trees frequently provide infection courts for decay fungi. This is usually not the case, however, for pine, spruce, or Douglas-fir trees, presumably because of their more resinous nature. In Tsuga heterophylla from Oregon and Washington, Englerth (1942) reported that nearly a third of the decay entered through dwarf mistletoe stem infections and adjacent swollen limbs. Several decay fungi are associated with dwarf mistletoe cankers in T. heterophylla in British Columbia; the most common is Fomitopsis pinicola (Etheridge 1973).
Dwarf mistletoe stem cankers on fir trees generally provide entrance courts for decay fungi only if the bark has died and sloughed off and the wood is exposed (Aho 1982, Aho and Roth 1978, Kimmey and Bynum 1961). Living bark is not affected. Trunk decay in Abies concolor is essentially limited to the zone of the swelling (Aho 1982). Studies by Parmeter and Scharpf (1982) indicate that for well-managed, young-growth stands of true fir in California, decay associated with stem infections should not lead to serious timber losses.
Weir (1916b) examined 540 dwarf mistletoe-infected Larix occidentalis in northern Idaho and found that 278 of 600 (46%) dwarf mistletoe-induced burls were infected by wood decay fungi, primarily Phellinus pini, Fomitopsis officinalis, and Laetiporus sulphureus. However, Weir (1916a) observed little decay associated with dwarf mistletoe burls in L. occidentalis in eastern Oregon.
Tree mortality may involve a complex of interacting pathological, entomological, and environmental factors. For example, Byler (1978) showed that interactions among several agents were involved in mortality of Pinus coulteri and P. jeffreyi in the Laguna Mountains of California: root pathogens alone were involved in 24% of the mortality, dwarf mistletoe alone in 32%, both pathogens jointly in another 28%, and other pest complexes in 16%.
With the exception of infection by secondary fungi (chapter 8), there are surprisingly few studies on the interactions of dwarf mistletoes and other pathogens. Chorover and McBride (1987) reported a significant correlation between infection of Pinus radiata by Arceuthobium littorum and Endocronartium harknessii near Cambria, California. Singh and Carew (1989) observed that decay fungi infecting Picea mariana parasitized by A. pusillum were generally the same species as those on uninfected trees, but their frequency on mistletoe-infected trees increased by as much as 40%. Severe mortality occurs in many P. banksiana stands in southern Manitoba in which both A. americanum and Armillaria sp. (a root disease pathogen) are involved. The basis for the association and the role of each pathogen in the complex are now being investigated (Heberson and Baker 1994).
Whether or not infection by dwarf mistletoes alone can kill trees, severe infection can clearly weaken trees enough that they are readily killed by secondary infestations of insects. The interrelationships between dwarf mistletoes and Scolytidae (bark beetles) as causes of tree mortality have been long debated (Stevens and Hawksworth 1970, 1984). In some associations the susceptibility of mistletoe-infected trees to infestation by bark beetles increases, in others there is little or no effect, and in some instances mistletoe-infected trees may even be less susceptible. Associations where susceptibility of dwarf mistletoe-infected trees to insect infestation appears to be increased include:
Some associations where susceptibility of dwarf mistletoe-infected trees to bark beetle infestation is apparently little affected:
An association where susceptibility of dwarf mistletoe-infected trees to bark beetles may be decreased:
The last association is not unexpected because Pinus contorta trees infected by dwarf mistletoe usually have thinner phloem than uninfected trees, and trees with thin phloem are less susceptible to bark beetle attack (Amman and McGregor 1985, Roe and Amman 1970). In Colorado, however, little correlation was observed between phloem thickness and severity of dwarf mistletoe infection (Hawksworth and others 1983).
Mortality in Pinus ponderosa in northern Arizona defoliated by Coloradia pandora (Saturniidae) was highest in trees most severely infected by Arceuthobium vaginatum subsp. cryptopodum (Wagner and Mathiasen 1985). Similarly, in British Columbia, Tsuga heterophylla trees free of dwarf mistletoe survived successive defoliations by Lambdina fiscellaria (Geometridae) much better than trees infected by A. tsugense (Buckland and Marples 1952). In the Pacific Northwest, Filip and others (1993) found that A. douglasii and Choristoneura occidentalis (Tortricidae) individually reduced diameter growth of Pseudotsuga douglasii, but no significant interactions were found.
Extremes in temperature and moisture can affect mortality rates of dwarf mistletoe-infected trees. Mortality rates are often highest following periods of drought, but there are few quantitative data. Childs (1960) noted that mortality of mistletoe-infected Pinus ponderosa branches was high following the severe drought of 1958-1959 in the Pacific Northwest. The most comprehensive studies of the interaction of drought and Arceuthobium campylopodum on mortality in P. ponderosa are by Page (1981) and Smith (1983) for the California drought of 1975-1977. After the drought, mortality of mistletoe-infected trees was more than four times higher than that of noninfected trees.
Arceuthobium campylopodum is common on Pinus ponderosa and P. jeffreyi in the San Bernardino Mountains of southern California where oxidant injury is severe on conifers; however, no direct effects of oxidant injury on dwarf mistletoe plants have been observed (Miller and White 1977). Any indirect effects of oxidants on dwarf mistletoe, e.g., selective killing of diseased hosts, has not been assessed. De Bauer and others (1987) suggested that air pollution near Mexico City may predispose P. hartwegii to dwarf mistletoe damage. The most striking example of the effects of an air pollutant on dwarf mistletoe distribution is in the areas exposed to high levels of sulfur dioxide that surround the early copper smelter at Anaconda, Montana (Scheffer and Hedgcock 1955). Both A. cyanocarpum on P. flexilis and A. americanum on P. contorta had previously been common there but are now rare or absent. We have found no living A. cyanocarpum in that area, and the closest known A. americanum is at least 10 km from the smelter site.