Biology and Classification of DWARF MISTLETOES (Arceuthobium) by Frank G. Hawksworth Rocky Mountain Forest and Range Experiment Station Fort Collins, Colorado and Delbert Wiens Department of Biology University of Utah Salt Lake City, Utah Agriculture Handbook No. 401 Library of Congress Catalog Card Number 72-609841 Forest Service United States Department of Agriculture Washington, D.C. February 1972 For sale by the Superintendent of Documents U.S. Government Printing Office Washington, D.C, 20402—Price $4.50 CONTENTS DEDICATION v Chemical Characters 49 ACKNOWLEDGMENTS vi Methods 51 Results 52 ABSTRACT viii Discussion and Conclusions 55 INTRODUCTION 1 NUMERICAL ANALYSES 56 Objectives and Scope 1 Methods 56 Taxonomic History 2 Results _:_ 60 GENERALIZED LIFE CYCLE 3 COLLECTING AND CURATING BIOGEOGRAPHY 7 TECHNIQUES 61 FORMAL TAXONOMY 62 Paleobotany 7 Generic Description 62 Paleogeography 8 Subgeneric Classification and Natural Keys to Extant Distribution 9 Ranges of the Genus and Species 9 the Species 26 Extension of Dwarf Mistletoe Ranges 11 Subgenus Arceuthohium 64 Relation of Parasite to Host Distribution 12 Subgenus Vaginata 64 Artificial Key to the New World Species of Sympatry 13 Arceuthohium 67 HOST RELATIONSHIPS 16 Artificial Key to the Old World Species of Natural Hosts 16 Arceuthohium 70 Extra-Limital and Unnatural Hosts _ 25 New World Taxa 90 Nonhosts 25 1. A rceuthohium ahietinum 90 Host-Parasite Relationships 25 a. f. sp. concoloris 90 Host Reactions 26 b. f. sp. magnificae 93 Effects on Hosts 28 2. A rceuthohium ahietis-religiósae 93 MECHANISMS AND TRENDS OF EVOLU- 3. A rceuthohium americanum 96 TION 28 4. Arceuthohium. apachecum 101 The Genetic System and Recombination 5. A rceuthohium hicarinatum 104 Potential 28 6. Arceuthohium hlumeri 104 Progressive Evolution and Adaptive Radiation. _ 36 7. Arceuthohium californicum 106 Absence of Hybridization and Polyploidy 36 8. Arceuthohium campylopodum 110 Evolutionary Patterns and Taxonomic Structure 37 9. A rceuthohium cyanocarpum 114 Evolutionary Trends 37 10. A rceuthohium divaricatum 117 SYSTEMATIC^ OF ARCEUTHOBIUM 40 11. Arceuthohium douglasii 120 Taxonomic Considerations 40 12. Arceuthohium gillii 124 Problems in Classification 40 a. Subspecies gillii 126 Subspecific Classification 42 b. Subspecies nigrum 128 CRITERIA FOR CLASSIFICATION 42 13. Arceuthohium glohosum 129 Morphological Characters 42 14. Arceuthohium guatemalense 132 Plant Size and Habit 42 15. Arceuthohium hondurense 135 Shoots 43 16. Arceuthohium laricis 135 Inflorescence 45 17. A rceuthohium microcarpum 138 Buds and Flowers 45 18. Arceuthohium occidentale 141 Anthers - 45 19. Arceuthohium pusillum 145 Fruit 45 20. Arceuthohium ruhrum 148 Palynological Characters 45 21. Arceuthohium strictum 149 Cytogenetical Characters 47 22. Arceuthohium tsugense 153 Physiological Characters 48 23. A rceuthohium vaginatum 156 Phenology 48 a. Subspecies vaginatum 157 Hosts 49 b. Subspecies cryptopodum 159 Witches' Brooms 49 c. Subspecies durangense 163 24. Arceuthohium verticilliflorum 163 LITERATURE CITED 172 Old World Taxa 166 APPENDIX 182 25. Arceuthohium chínense 166 Glossary 182 26. Arceuthohium minutissimum 167 Scientific and Common Tree Names 184 27. Arceuthohium oxycedri 167 Specimens Examined 186 28. Arceuthohium pini 169 Herbaria 186 Rejected Species 170 New World Taxa 186 MAJOR CONCLUSIONS 170 Old World Taxa 227 SUGGESTIONS FOR FURTHER RESEARCH _ 171 Exsiccatae. Index to Numbered Collections _ _ _ _ 228 IV DEDICATION This work is dedicated to the memory of Dr. Lake S. Gill (1900- 1969), Forest Pathologist with the U.S. Department of Agriculture from 1923 to 1960. Dr. GilFs classic paper ^'Arceuthobium in the United States'' (1935) was the first comprehensive treatment of the North American dwarf mistletoes, and since its appearance has been the authoritative publication on the genus. Through his continued research and missionary zeal, Dr. Gill, more than any other man, was responsible for the present awareness of Arceuthobium as economically important forest pathogens. He demon- strated that dwarf mistletoes were not merely curiosities, but caused significant mortality and reduction of growth rates in western conifers. Dr. Gill followed our work with interest and encouraged our efforts. We discussed many aspects of the study with him, but his death on July 5, 1969 precluded his seeing the final manuscript. His enthusiasm and interest was a constant source of encouragement for those with whom he worked. The use of trade, firm, or corporation names in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement of any product by the U.S. Department of Agriculture to the exclusion of others which may be suitable. ACKNOWLEDGMENTS We want to thank the curators of the many herbaria in North America and Europe who allowed us to examine dwarf mistletoe specimens; and the many colleagues who have collected the specimens, reviewed the manuscript, suppHed photographs or drawings, assisted with numerical analyses and Chromatographie work, and performed innumerable other courtesies. Canada Honduras Joe A. Baranyay Robert Armour Jan M. Bonga Antonio Molina R. Job Kuijt Mexico Michael J. Larsen Rudolfo Salinas Quinard John G. Laut José de Jesus Valdivia Sanchez John A. Muir Francisco Muños Sandoval Richard B. Smith Netherlands John Gremmen United States John W. Andresen Lee W. Lenz Southern lUinois University Rancho Santa Ana Botanic Garden Lyman Benson Estella B. Leopold Pomona College U. S. Geological Survey, Denver Charles M. Drew C. V. Morton U. S. Navy, China Lake, Calif. U. S. National Museum George F. Estabrook J. R. Parmenter, Jr. University of Colorado University of Cahfornia Ari Ferro David J. Rogers University of Utah University of Colorado Henry S. Fleming Lewis F. Roth University of Colorado Oregon State University David W. French Richard Snyder University of Minnesota University of Utah Robert L. Gilbertson Frank H. Tainter University of Arizona University of Minnesota Sharon Harris R. K. Vickery, Jr. University of Utah University of Utah John H. Hart Edward G. Voss Michigan State University University of Michigan Hugh H. Iltis William A. Weber University of Wisconsin University of Colorado VI Personnel of The U.S. Department of Agriculture—Forest Service Gerald W. Anderson David A. Graham Paul C. Lightle James L. Stewart Ralph L. Anderson Donald P. Graham Elbert L. Little, Jr. John H. Thompson Stuart R. Andrews Thomas E. Hinds Douglas R. Miller Harvey V. Toko Wilmer F. Bailey Bohun B Kinloch ^ g Peterson Willis W. Wagener Donald H. Brown Donald M. Knutson T^ u ^ 17 c^ u f TV/T.I .. T \XT..\.. T. W. Childs Richard G. Krebill I^^^ert F. Scharpf Melvyn J. Weiss Oscar Dooling Thomas H. Laurent Keith R. Shea Ed F. Wicker Vll ABSTRACT Arceuthobium (dwarf mistletoes), a distinctive genus of the family Viscaceae, is parasitic on conifers of the Pinaceae in the Old and New Worlds and on Cupres- saceae in the Old World. Although conifer forests in many parts of the Northern Hemisphere are infected with dwarf mistletoes, those most seriously damaged are in North America. In this taxonomic revision, the 32 recognized taxa comprise 28 species, 5 sub- species, and 2 formae spéciales. Four taxa are known in the Old World; 28 in the New. In North America, Arceuthohium ranges from central Canada and south- eastern Alaska to Honduras and Hispaniola, but most species are found in western United States and Mexico. Only A. pusillum, a parasite of Picea, occurs in eastern North America. Taxonomic characteristics presented for each of the 32 taxa include : morphol- ogy and color of shoots, fruits, and flowers; pollen features; phenology of flowering and seed dispersal; hosts and host reactions; chromosomal features; and chroma- tography of shoot pigments. The classification system is based on extensive field studies of all known New World dwarf mistletoes in their natural state, examination of specimens at the major herbaria in North America and Europe, and computer analyses of all tax- onomic data collected. The system, the first below-genus classification of Arceuthohium, divides the genus into subgenera Arceuthohium and Vaginata, Subgenus Arceuthohium com- prises all four Old World species {A. chinense, A. minutissimum, A. oxycedri, and A. pini), and three New World species, but is not formally subdivided into sections. Subgenus Vaginata, exclusively New World, contains three sections: Vaginata, 6 taxa; Campylopoda, 17 taxa; and Minuta, 2 taxa. Section Campylopoda contains three series: Ruhra, 3 taxa; Campylopoda, 13 taxa; and Stricta, 1 taxon. Identifi- cation keys, artificial and natural, are provided. The detailed botanical description of each dwarf mistletoe includes its distinctive taxonomic features, hosts, a colored photograph, and a map of its geographic distribution. vni Biology and Classification of Dwarf Mistletoes {Arceuthohium) by Frank G. Hawksworth^ and Delbert Wiens^ INTRODUCTION The dwarf mistletoes {Arceuthohium) are^ a highly has clearly defined limits, and its generic status has specialized and clearly defined genus of aerial dicot- never been questioned. No formal subgeneric treat- yledonous parasites that occur on Pinaceae or ment of Arceuthohium has been published, although Cupressaceae. These mistletoes are small, leafless, Kuijt (1970) suggests that the genus is separable into glabrous, and are characterized by a number of two natural groups on the basis of branching habit. unusual features: explosive, bicolored fruits; ringlike