The hosts of dwarf mistletoes are ranked as "principal," "secondary," "occasional," and "rare." Potential hosts that are not parasitized are designed as "immune". These susceptibility classifications are defined in table 6.1, and were devised by Hawksworth and Wiens (1972). They were based on an "infection index" defined by percentage classes of infected trees (for each host species) within 6 m of a heavily parasitized host. Infection indices are meaningful only in stands with trees older than 30 years.
The susceptibility classification (table 6.1) is not a measure of the frequency with which a host species may be infested over its geographical distribution. For example, Pinus cembroides is designated as a principal host of Arceuthobium divaricatum, even though the two species occur together only in the Davis Mountains of west Texas. In this region, however, P. cembroides is as susceptible as the other pinyons that act as principal hosts in other portions of this dwarf mistletoe’s distribution.
Some variation in susceptibility is to be expected over the geographical distribution of a host species, as well as in certain habitats (see chapter 7). Such differences could reflect variation in the host, parasite, or environment (Wiens 1961). Nonetheless, the host relationships of each dwarf mistletoe species are sufficiently consistent to make the rankings meaningful.
The principal hosts of both New World and Old World dwarf mistletoes tend to be restricted to a single genus or for Pinus to a single subgenus (figs. 6.1 and 6.2). Only Arceuthobium microcarpum, A. laricis, and A. tsugense have principal hosts that belong to different genera (respectively, Picea and Pinus; Larix and Tsuga; and Abies, Pinus, and Tsuga).
The susceptibility of natural hosts is listed by Arceuthobium taxa in table 6.2 and by host taxa in table 6.3. Host susceptibility classification is usually based on direct field observations; for those cases where data are lacking, we classified taxa on the basis of our field experience. The absence of field studies precludes the preparation of a susceptibility classification for the Old World species.
The susceptibility classes were based on the most common situation encountered for a particular host–parasite combination. For example, in the San Bernardino Mountains near Snow Valley, California, Arceuthobium campylopodum severely parasitizes Pinus coulteri; at lower elevations, however, the mistletoe severely parasitizes P. attenuata and only occasionally infects P. coulteri. Therefore, even though P. coulteri is sometimes heavily infested by A. campylopodum, it is a secondary host in most situations and is classified as such. Fortunately, this kind of variation is rare, and most host taxa readily fall into a single susceptibility class for an associated dwarf mistletoe taxa.
As shown in table 6.3, some host taxa are parasitized by a number of dwarf mistletoes: 9 taxa infect Pinus durangensis; 7 parasitize P. cooperi, P. contorta var. latifolia, P. engelmannii, and P. monticola; and 6 infect P. arizonica var. arizonica, P. teocote, and P. pseudostrobus.
Some dwarf mistletoes are highly host specific—Arceuthobium apachecum is restricted to Pinus strobiformis, A. bicarinatum to P. occidentalis, and A. guatemalense to P. ayacahuite. Other dwarf mistletoes, however, have broader host ranges—A. laricis, which principally parasitizes Larix occidentalis, also occurs on Abies, Picea, Pinus, and Tsuga. Arceuthobium douglasii primarily parasitizes Pseudotsuga menziesii although it infects Abies and Picea rarely.
A number of species of Arceuthobium infect nearly all western true firs (Abies) to some extent. However, Abies is the principal host of only 3 dwarf mistletoe species—A. abietinum in the western United States and northern Mexico, A. abietis-religiosae in central Mexico, and A. tsugense in the coastal north Pacific region. There is a single collection by Weir (ILL) of an Arceuthobium on the rare bristlecone fir, Abies bracteata, of the Santa Lucia Mountains, California. The mistletoe species is most likely A. occidentale, which typically parasitizes Pinus sabiniana, but the specimen is poorly documented and so fragmented that positive identification is impossible.
All North American spruces—except the Mexican species Picea chihuahuana and P. mexicana (Martínez 1963) and the recently described P. martinezii—are hosts for Arceuthobium. Two dwarf mistletoe species are principal parasites of spruce: (1) A. pusillum on Picea mariana, P. glauca, and P. rubens in the Great Lakes region, New England, and eastern Canada; and (2) A. microcarpum on Picea engelmannii and P. pungens in Arizona and New Mexico. Picea sitchensis is rarely parasitized by A. tsugense subsp. tsugense (Laurent 1966, Mathiasen 1994).
Eight dwarf mistletoe species occur primarily on the North American white pines (subgenus Haploxylon)—Arceuthobium apachecum on Pinus strobiformis; A. blumeri on P. ayacahuite var. brachyptera and P. strobiformis; A. californicum on P. lambertiana; A. cyanocarpum on P. albicaulis, P. aristata, P. flexilis, and P. longaeva; A. divaricatum on numerous pinyons; A. guatemalense on P. ayacahuite var. ayacahuite; A. monticola on P. monticola; and A. pendens on several pinyons. Pinus chiapensis, a species indigenous to Guatemala and southern Mexico, is the only North American white pine not known to be parasitized by Arceuthobium.
The hard pines (subgenus Diploxylon) are by far the most common hosts of North American dwarf mistletoes. Twenty-three of the 39 North American taxa are primary parasites of these pines, and 6 other species occur at least rarely on them.
Usually a dwarf mistletoe species parasitizes 1, sometimes 2, or rarely 3 host species in the same stand. We have observed only 3 instances where a particular dwarf mistletoe species parasitized 4 different host species within a stand:
Trees of various species have been inoculated with, and have occasionally become colonized by, dwarf mistletoe species that do not occur naturally within the range of the host species (extra-limital hosts). In some instances, trees co-occurring with a particular dwarf mistletoe are immune to natural infection but can be artificially inoculated. For example, Weir (1918a) inoculated and established Arceuthobium campylopodum on Abies concolor. Even though this species is frequently associated with A. campylopodum in nature, no natural infections have been found. Numerous examples of successful artificial inoculation are reported in table 6.4. Most such experiments have been conducted in unnatural environments, and life cycle data based on such artificial inoculations may be misleading. For example, when Arceuthobium cyanocarpum was grown on Pinus strobiformis in a greenhouse, dwarf mistletoe plants exhibited accelerated growth and produced shoots within 5 months and flowers within 7 months (Hawksworth, unpublished data). In nature, A. cyanocarpum does not produce shoots until 2 or 3 years following infection and flower production requires 4 or 5 years.
The susceptibility of a host species to natural infection by a dwarf mistletoe species with which it does not naturally occur is sometimes economically important (table 6.5). For example, Graham and Leaphart (1961) reported that Pinus sylvestris cultivated in Washington was so severely parasitized by Arceuthobium laricis that they recommended this species should not be planted where A. laricis is present.
Because dwarf mistletoes parasitize so many western conifer species, it is of interest to know which are not hosts. We list here the few members of the Pinaceae from the western United States and Mexico that have not been found to be naturally infected by Arceuthobium. Some of these species, however, could be hosts because many Arceuthobium collections from Mexico do not identify the host species. Of the 14 species of pine listed below, 6 are pinyons (indicated by asterisks).
True firsAn interesting feature of parasitism by Arceuthobium is the existence of a kind of "competitive host exclusion" between different mistletoe species (Hawksworth 1969). If a species of Arceuthobium that typically infests a certain host species is present in an area, then other dwarf mistletoe species only rarely infest that host species; if the principal parasite of that host species is not present, however, then another dwarf mistletoe species present in the area is likely to infest the host species. Several examples of host exclusion are found in the Colorado Front Range, where Pinus contorta is typically the principal host of A. americanum and P. ponderosa is typically the principal host of A. vaginatum subsp. cryptopodum. Infection of P. ponderosa trees by A. americanum was only 13% in stands where both mistletoe species were present, but 64% in stands where A. vaginatum subsp. cryptopodum was absent (Hawksworth 1969). The converse situation also occurs with respect to infection of P. contorta trees by A. vaginatum subsp. cryptopodum and A. americanum (Hawksworth 1969). Other examples involve the combination of A. americanum (principal host P. contorta) with A. cyanocarpum (principal host P. flexilis) in Colorado (Hawksworth and Wiens 1972) and A. occidentale (principal host P. sabiniana) with A. campylopodum (principal hosts P. ponderosa and P. jeffreyi) in California. Wiens (1961) also noted such competitive host exclusion in mistletoes of the genus Phoradendron parasitizing junipers near Sedona, Arizona (P. juniperinum and P. densum). The mechanism that controls this phenomenon constitutes a fascinating subject for additional research.
If a host is rarely parasitized by a species of Arceuthobium, parasitism is often an "all or nothing" phenomenon: that is, most trees of a rare host species are immune, but trees that are infected tend to be heavily infected. For example, Picea engelmannii is a rare host (<1% of trees infected) of A. americanum, but those trees that are parasitized typically bear hundreds of infections (Hawksworth and Graham 1963).
Some species that are exceedingly rare appear to have little resistance to dwarf mistletoe infection. For example, Pinus culminicola has one of the most restricted distributions of all pinyons, yet it is readily parasitized by Arceuthobium vaginatum subsp. vaginatum on Cerro Potosí, Mexico. Also, Picea breweriana is often heavily infested by A. abietinum f. sp. concoloris, A. monticola, and A. tsugense subsp. mertensianae where the host occurs with these dwarf mistletoes. No dwarf mistletoe occurs within the limited distribution of Pinus torreyana, but Kuijt (1960a) inoculated a tree of this species with A. occidentale and found it to be susceptible.
A number of inoculation experiments have shown that various species are not compatible hosts for particular dwarf mistletoes (table 6.6). Features of the dwarf mistletoe that often indicate host–parasite incompatibility are reduced (sometimes complete lack of) shoot development and unusually large swellings at the point of infection.
The first external symptom of dwarf mistletoe infection is usually a swelling of the host tissues. As an infection develops, swelling enlarges and eventually becomes fusiform. Typically, dwarf mistletoe infection leads to the production of the profusely branched, dense masses of distorted host branches called "witches’ brooms." Two basic types of witches’ brooms are formed (Kuijt 1960b, Hawksworth 1961a):
In general, the type of witches’ broom formation is characteristic of the parasite species rather than the host species; therefore broom type is an important taxonomic character in Arceuthobium. Although a dwarf mistletoe species that typically forms non-systemic brooms will rarely induce formation of a systemic broom, there is never any question regarding the basic type of witches’ broom produced.
Systemic witches’ brooms are consistently formed by Arceuthobium americanum, A. douglasii, A. guatemalense, A. minutissimum, and A. pusillum, and apparently by the Asian species A. chinense, A. sichuanense, and A. pini (Hawksworth and Wiens 1972, Kiu 1984b). Non-systemic witches’ brooms are much more common among trees parasitized by North American dwarf mistletoes. At the type locality of A. pendens, only staminate plants appeared to produce systemic infections; this particular form of sexual dimorphism deserves further study.
A few dwarf mistletoe taxa do not induce witches’ broom formation in their hosts—Arceuthobium aureum subsp. aureum (fig. 6.5) and A. globosum subsp. globosum. Although A. occidentale does not induce typical broom formation, it does promote some "broom-like" development in Pinus sabiniana (R. F. Scharpf, personal communication).
Arceuthobium americanum produces shoots only at the girdles and not on segments of Pinus contorta branches more than 5 years old (Kuijt 1960b). Similarly, our limited observations of systemic infections of A. abietis-religiosae on Abies religiosa suggest that here, also, the dwarf mistletoe shoots are produced only at girdles.
Within a particular host genus, the types of witches’ broom formed by a dwarf mistletoe species are generally similar (Weir 1916c, Hawksworth 1956a, Kuijt 1960b). For example, the witches’ brooms formed by Arceuthobium americanum on all pines are similar, but brooms on spruces are distinctly different from those on pines (Hawksworth and Graham 1963, Kuijt 1960b).
Although systemically infected branches are usually immune to additional infection, Muir (1968) reported several secondary infections of Arceuthobium americanum on a witches’ broom of Pinus banksiana. In Oregon, R. Tinnin (personal communication) has also observed secondary infections on witches’ brooms of P. contorta induced by A. americanum. Secondary infections are detectable by location of shoots, differences in shoot color, differences in sex, and the formation of swellings. We have also rarely observed secondary infections in the following parasite–host combinations:
Kuijt (1960b) reported that cones usually are not produced on witches’ brooms, particularly on systemic brooms. We have frequently observed cone formation on witches’ brooms of Pseudotsuga menziesii caused by Arceuthobium douglasii, however. Cones were about half normal size, and apparently contained viable seeds. Bonga (1964) noted fertile cones on an aberrant witches’ broom in Picea mariana caused by A. pusillum. Schaffer and others (1983) observed cones on several systemic witches’ brooms on Pinus contorta induced by A. americanum, but all the cones were sterile.