This file was created by scanning the printed publication. Errors identified by the software have been corrected; however, some errors may remain. CHAPTER 1 Introduction

Arceuthobium () is a clearly defined ent. Control of dwarf in some areas has group of small (generally less than 20 cm high), vari­ been hampered by inadequate knowledge of the iden­ ously colored (yellow, brown, black, or red) flowering tity of the parasite involved and the relationship to its that are aerial parasites only on members of the host(s). and . The dwarf mistletoes, as has been classically included in the they are commonly known, are of unusual biological subfamily Viscoideae of the . Van interest because they are the most evolutionarily spe­ Tieghem (1895) considered Arceuthobium so distinct cialized of the Viscaceae. Some of the features from related genera that he proposed its classification that make Arceuthobium unique among mistletoes as a separate family positioned phylogenetically include: between the Viscaceae and the . This pro­ Extreme reduction in size-Arceuthobium posal, however, has never been followed. The sub­ minutissimum with flowering shoots only several families Loranthoideae and Viscoideae are now gener­ millimeters high is among the smallest of dicotyle­ ally agreed to warrant family status (Barlow 1964, donous plants. Thorne 1992). Members of these groups differ in floral Evolution of species that regularly cause systemic morphology, floral anatomy, pollen characteristics, patterns of witches' broom formation­ embryology, and chromosome size and numbers , A. pusillum, and (Calder 1983). The previously supposed similarities A. minutissimum. between the two groups are largely the result of evo­ lutionary convergence for the aerial parasitic habit and Development of a highly effective mechanism of dispersal by birds, rather than the consequence explosive ( of virtually all of a common phyletic origin. We, therefore, accept other aerial mistletoes are dispersed by birds). full family status for both groups. Occurrence of bicolored . Engler and Krause (1935) classified Arceuthobium Stems with variant (anomalous) patterns of sec­ as a monogeneric tribe in the Viscoideae. They placed ondary growth. , , and in Sessile, ring-like anthers surrounded by a sterile the tribe Phoradendreae and separated Korthalsella in central column that in Arceuthobium ameri­ subtribe Korthalsellinae and Phoradendron in sub­ canum and A. pusillum are capable of opening tribe Phoradendrinae. Regardless of its relationship and closing in response to environmental to other Viscaceae, Arceuthobium has clearly defined changes. limits, and its generic status has never been ques­ Geographical distribution that encompasses both tioned. Kuijt (1970) suggested that the genus is sepa­ the New and Old Worlds. rable into two natural groups on the basis of branch­ ing habit (verticillate versus flabellate).

The dwarf mistletoes are of immense economic The New World has a greater number of species importance because they are the single-most destruc­ (34) than the Old World (8). In the Old World, two tive pathogen of commercially valuable coniferous species are recently described from China (Arceu­ timber trees in several regions of Mexico, western thobium tibetense and A. sichuanense). Another two Canada, western United States, and parts of species, A. azoricum and A. juniperiprocerae, have (Bakshi and Puri 1971, Hawksworth and Shaw 1984, been segregated from the widely distributed species Zakaullah and Badshah 1977). A.oxycedri. In the New World, dwarf mistletoes are found from southeastern Alaska, northern Canada, With the increasing recognition of dwarf mistle­ and Newfoundland through most of the western toes as destructive parasites on commercially impor­ United States and Mexico to Central America (Honduras), tant forest trees, the need for additional systematic and with an extreme outlying population on the island of other biological studies on the group became appar- Hispaniola (see fig. 5.2).

Introduction 1 Chapter 1

Species diversity is greatest in northwestern examined the specimens at the major herbaria in Mexico and the western United States, where 28 of the and . 34 New World species occur. The six New World Our goal was to develop a natural and useful clas­ species outside this area are Arceuthobium bicarina­ sification of dwarf mistletoes based on a broad eclectic tum on Hispaniola; A. aureum, A. guatemalense, A. approach involving morphology, ecology, physiology, hawksworthii, and A. hondurense in Central America; biochemistry, and genetics. Other features of evolu­ and A. pusillum in southeastern Canada, the Great tionary interest included biogeography, paleobotany, Lakes region, and the northeastern United States. reproduction, and life cycles. Finally, to provide utility Twenty species occur in Mexico, and eight of these are for practicing foresters, discussions of pathological found also in the western United States. Nineteen effects on host trees and control measures were species occur in the United States, five of which also included. occur in Canada (A. americanum, A. douglasii, A. lari­ cis, A. pusillum, and A. tsugense). Arceuthobium dou­ A glossary of some of the less familiar terms and glasii has the widest distribution in the New World. special usages is included, as well as lists of scientific This is distributed from southern British and common names of species mentioned in the text. Columbia, Canada, southward throughout most of the western United States to southern Durango, Mexico. Taxonomic History The first dwarf mistletoe described, Arceuthobium Objectives and Scope oxycedri, was originally included in (Clusius Our initial interest in Arceuthobium was to clarify 1576). It was later segregated from Viscum by the confusion surrounding the A. campylopodum Hoffman (1808) as RazoumoJskya. Arceuthobium was complex (see Hitchcock and Cronquist 1964), which first proposed as a genus by Marschall von Bieberstein centered primarily around Gill's (1935) designation of (1819), and it was generally used until the early 1900's. host-forms in this group. However, when we discov­ The Vienna Botanical Congress in 1905 conserved ered the rich dwarf mistletoe flora in Mexico Arceuthobium over Razo umoJskya. Because the (Hawksworth and Wiens 1965, 1977, 1980, 1989), we American Code emphasized strict priority, however, expanded our investigations to include a comprehen­ most botanists in the United States continued to use sive treatment of the entire genus .. We have since stud­ RazoumoJskya. Arceuthobium finally displaced ied naturally occurring populations of all 38 known RazoumoJskya as a result of the 1930 Cambridge New World taxa, as well as 4 of the 8 known Old Botanical Congress and Gill's (1935) taxonomic revi­ World species. Beginning in 1962, our field studies of sion of the species in the United States. Arceuthobium have taken us over 800,000 kilometers Humboldt and Bonpland's collection of a dwarf by foot, hoof, wheel, and wing throughout North mistletoe on Cofre de Perote (Veracruz, Mexico, 1804) America, Central America, the Caribbean, the Azores, was apparently the first in the New World. This speci­ Europe, North and East , and the . men was designated as the type for Arceuthobium The more than 3,000 dwarf mistletoe specimens vaginatum described in 1806 by Willdenow (as we have collected in our field work, plus many early Viscum vagina tum). In 1826, David Douglas (1914) U.S. Department of Agriculture collections by]. R. discovered two dwarf mistletoes on his botanical 'Weir, G. G. Hedgcock,]. S. Boyce, andL. S. Gill, are explorations of the Pacific Northwest: A. campylopodum filed at the USDA Forest Service's Mistletoe Herbarium (on ) andA. americanum (onP. con­ at Fort Collins, Colorado. They provide the basis for torta). William Hooker (1847) first discussed the tax­ our taxonomic understanding of the genus. onomy of Arceuthobium in North America north of Duplicates of our collections are deposited in various Mexico and compared Douglas' specimens and anoth­ North American herbaria, particularly those of the er by Drummond (of A. americanum) with the University of Colorado (Boulder), Missouri Botanical European A. oxycedri, but he detected no differences Garden (St. Louis), U.S. National Museum except for color variations. George Engelmann was (Washington, DC), and Instituto de Biologia of the the first to publish (in Gray 1850) a formal description Universidad Nacional Autonoma de Mexico, Escuela of a dwarf mistletoe found in the United States Nacional de Ciencias Biologias of the Instituto (A. americanum). As the taxonomic architect of the Politecnico Nacional, and Instituto Nacional de genus in North America, Engelmann (associated with Investigaciones Forestales y Agropecuarias (Mexico the Missouri Botanical Garden) named most of the City). In addition to our own collections, we have

2 Introduction Chapter 1

American species of Arceuthobium during the latter Job Kuijt (1955, 1960a, 1960b, 1963, 1964) rejected half ofthe 19th century (Gray 1850, Watson 1880). Gill's host-form concept for Arceuthobium campy­ lopodum and A. vaginatum and considered each as a Between 1910 and 1920, G. G. Hedgcock and]. R. single variable species. He also concluded, as did Gill Weir of the Division of Forest Pathology (Department of Agriculture) independently initiated studies on the (1935), that A. bicarinatum of Hispaniola should be included in A. campylopodum. and host relationships of Arceuthobium in the United States. Both published a number of articles Hawksworth and Graham (1963) first discussed on dwarf mistletoes, but for unknown reasons their the difficulties of applying Gill's host-form concept to taxonomic conclusions remained unpublished as man­ the dwarf mistletoes that parasitize Picea in the west­ uscripts on fil~ Vvith the USDA Forest Service, Fort ern United States. They concluded that many of Gill's Collins, Colorado. This was unfortunate, because "forms" in the Arceuthobium campylopodum complex Hedgcock had a keen understanding of the genus. For could be distinguished morphologically and should be example, he first recognized that the dwarf mistletoe accorded higher taxonomic rank. on Pinus lambertiana (our A. californicum) was dis­ Hawksworth and Wiens (1964) described a new tinct from A. cyanocarpum, and that A. campylopodum species, (a parasite of Pinus leio­ was distiriguishable from A. occidentale. Hedgcock phylla var. chihuahuana in southern Arizona and (1915) published a host list of Arceuthobium for the northern Mexico) that had been previously confused United States and later reported some new hosts of with the more widespread A. vaginatum subsp. cryp­ A. campylopodum and A. occidentale resulting from topodum (a parasite of P. ponderosa). Hawksworth artificial inoculations (Hedgcock and Hunt 1917). and Wiens (1965) published the first comprehensive Weir (1918a) artificially inoculated various hosts study of the genus in Mexico and described five addi­ with several species of dwarf mistletoes in the tional taxa. Wiens (1968) analyzed the chromosome Northwest under both field and greenhouse condi­ numbers in Arceuthobium and organized the species tions, and he discussed the taxonomic implications of into distinct flowering groups. Next, Hawksworth and the results. He began a systematic treatise on Wiens (1970a) published a subgeneric classification of American dwarf mistletoes but never completed the the genus with descriptions of four new species and work. He did, however, publish observations of hosts two new combinations from Mexico, Guatemala, and associated with several dwarf mistletoes (Weir 1915a, the United States. We then reviewed the biology and 1915b, 1916c, 1917, 1918b). classification of the entire genus (Hawksworth and Wiens 1970b) and published our monograph on Aven Nelson of the University of Wyoming Arceuthobium 2 years later (Hawksworth and Wiens described two new dwarf mistletoes: Arceuthobium 1972). cyanocarpum in Wyoming (Coulter and Nelson 1909) andA. blumeri in Arizona (Nelson 1913). Karl von Following the publication of our monograph, we Tubeuf (1919) published a review of the genus based segregated two species from the widely distributed on available literature, his extensive knowledge of A. : A. azoricum from the AZores oxycedri, and results of a brieftrip in 1913 to the west­ and A. juniperiprocerae from East Africa (Hawks­ ern United States. Unfortunately, this work did little to worth and Wiens 1976). Shortly thereafter, we resolve taxonomic relationships. Heil (1923), another described three additional taxa from Mexico and German worker, describedA. abietis-religiosae, a para­ Guatemala (Hawksworth and Wiens 1977). This was site of Abies in central Mexico. followed by a study of the flavonoid chemistry of the genus (Crawford and Hawksworth 1979) and descrip­ Following Nelson's and Tubeuf's studies, taxo­ tion of another new species (A. pendens) on pinyons nomic understanding of the genus did not advance from central Mexico (Hawksworth and Wiens 1980). until a revision of the species in the United States was Mark and Hawksworth (1981) analyzed the branching published in 1935 by L. S. Gill while employed by the patterns in two California dwarf mistletoes. An update U.S. Department of Agriculture. Gill re-evaluated and review of the taxonomy of the genus was complet­ Engelmann's taxonomic conclusions, recognized ed by Hawksworth and Wiens (1984). Are-evaluation flowering periods as an important taxonomic charac­ of the classification of the dwarf mistletoes on Tsuga ter, and reduced the rank of several closely related was then undertaken (Hawksworth 1987a), and the species to host-forms of Arceuthobium campylopo­ taxonomy and evolution of the genus was reviewed by dum and A. vaginatum. Although Gill clearly estab­ Hawksworth (1987b). Clarification of the host rela­ lished a taxonomic framework for the genus, he con­ tionships of three dwarf mistletoes that parasitize sidered his work to be provisional "pending a com­ white in northern California and southern plete revision of the genus based on further field and experimental evidence." Introduction 3 Chapter 1

Oregon was completed by Mathiasen and Hawks­ wash that they believed gave them long, thick hair worth (1988). Two additional new species were (Turner and others 1980). described, and two new combinations were proposed Mistletoes are utilized for medicinal purposes by for Mexican dwarf mistletoes by Hawksworth and aboriginal peoples in many parts of the world, and the Wiens (1989). Hawksworth (1991a) reviewed the dwarf mistletoes are no exception (Moerman 1977). genus in Mexico and Central America. Three species California Indians prepared a decoction of Arceu­ from California and southern Oregon were described, thobium occidentale to treat stomach ache (Chestnut and the subspecies and host races of Arceuthobium 1902). Indians in Butte County, California, used an tsugense were characterized by Hawksworth and oth­ undetermined species of dwarf mistletoe for treating ers (1992b). Finally, differences between herbarium hemorrhage of the lungs and mouth, tuberculosis, collections of A. aureum subsp. aureum from emaciation, stomach ache, cough, colds, and rheuma­ Guatemala and Belize lead us to the discovery of tism (Taylor 1981). Bella Coola Indians of coastal A. hawksworthii (Wiens and Shaw 1994). British Columbia employed shoots of A. tsugense in Five dwarf mistletoes are now known from south­ the treatment of several of the same maladies (Smith western China (Kiu 1984b):Arceuthobium chinense, 1928). Navajo Indians of New Mexico and Arizona A. oxycedri, A. pini, A. sichuanense, and A. tibetense. used both A. divaricatu,m and A. vaginatum subsp. Kiu and Ren (1982) described A. tibetense, a parasite of cryptopodum for unspecified medicinal purposes Abies. Kiu (1984a) described A. pini var. sichuanense, (Vestal 1952, Wyman and Harris 1941). a parasite of Picea; and Hawksworth and Wiens (1993) Dwarf mistletoes were utilized in the treatment of raised it to specific rank. several ailments in Veracruz, Mexico (Chazaro and The recent investigations of electrophoretic char­ Oliva 1988), and Mannez (1959) reports that acteristics and DNA sequencing analyses of the genus is used for the treatment of by Daniel Nickrent and colleagues at the University of cough in Mexico. Sra. S. Gonzales of Villa Guerrero, Illinois and Southern Illinois University (Nickrent 1986, Durango, Mexico (personal communication, 1987), 1987; Nickrent and Butler 1990; Nickrent and Stell informed us that indigenous peoples in the vicinity of 1990; Nickrent and others 1984; Schuette 1992; Schuette Tepehuanes, Durango, used a decoction of A. vagina­ and Nickrent 1992) have provided exciting new tum subsp. .vaginatum for the treatment of rheuma­ insights into the evolutionary history of the group and tism and lung disorders and that A. globosum subsp. the relationships among the various taxa (chapter 15). globosum was utilized for the treatment of diarrhea and nervous, pulmonary, and rheumatic disorders. Arceuthobium globosum subsp. globosum is also Ethnobotanical and Medicinal burned as incense in religious ceremonies, but Sra. Gonzales did not know the basis for this practice. Uses Various mistletoes, especially , have An extensive folklore surrounds the European been studied for pharmaceutical purposes, but the mistletoe, Viscum album, in northern Europe and dwarf mistletoes have received relatively little atten­ England. As new lands were discovered and colo­ tion in this regard. Extracts of Old World Arceu­ nized by these Europeans, other Viscaceae such as thobium oxycedri have a hypotensive action similar to Phoradendron were encountered that resembled extracts of V album (Livon 1913); constituents of A. V album. Inevitably, the folklore associated with americanum show some anti-tumor activity (Sealwry V album was transferred to these plants (Calder 1983). and others 1959), Toxic proteins in V album and Because of their relative inconspicuousness and gen­ Phoradendron have been examined for cancer thera­ eral dissimilarity to Viscum and Phoradendron, little py (Luther and Becker 1987). Several dwarf mistletoes folklore, however, is associated with species of have also been tested for toxic proteins (A. ameri­ Arceuthobium. According to Fernald (1900), French canum, A. campylopodum, A. divaricatum andA. and English women in northern Maine used spruce vaginatum subsp. cryptopodum), but only A. ameri­ twigs infected with A. pusillum in their hair at the mid­ canum tested positive for toxic acetone precipitate. winter ball. He was unable to determine, however, if This indicates a moderate level of toxic proteins, but the had the traditional seasonal significance of too low to be considered for commercial use the European mistletoe. Young women of the (Samuelsson 1969). Recent tests for pharmacological­ Okanogan-Colville tribe of British Columbia and ly active lectins in several North American species of Washington boiled branches from witches' brooms of Arceuthobium taxa have all been negative (H. Fraanz, Douglas- infected with A. douglasii to make a hair personal communication, 1988).

4 Introduction Chapter 1

There are reports of minor uses of dwarf mistle­ toes as dye plants (Bliss 1980) and as pollen sources for honey bees in California (Coleman 1921) and Arizona (O'Neal and Waller 1984). The dwarf mistletoe, Arceuthobium oxycedriJ is a preferred food of sheep and goats in Mediterranean countries, the Near East, and in the Himalayas (Acatay 1954, Zakaullah and Badshah 1977). Acatay (1954) expressed concern over the for­ est damage caused by cutting down juniper trees to provide dwarf mistletoe fodder for sheep and goats. Various mistletoes are utilized as food for domestic animals in different parts of the world, and both the Viscaceae and Loranthaceae appear to have few chemical defenses against predation (Barlow and Wiens 1977).

Introduction 5