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Diversity, Ecology, and Conservation of Truffle Fungi in Forests of the Pacific Northwest

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Diversity, Ecology, and Conservation of Truffle Fungi in Forests of the Pacific Northwest United States Department of Agriculture Diversity, Ecology, and Forest Service Conservation of Truffle Pacific Northwest Research Station Fungi in Forests of the General Technical Report PNW-GTR-772 April 2009 Pacific Northwest James M. Trappe, Randy Molina, Daniel L. Luoma, D E E P R A U R T LT MENT OF AGRICU Efren Cázares, David Pilz, Jane E. Smith, Michael A. Castellano, Steven L. Miller, and Matthew J. Trappe Authors James M. Trappe is a professor, Department of Forest Science, Oregon State University, 321 Richardson Hall, Corvallis, OR 97331; he prepared sections on history of truffle science in the Pacific Northwest (PNW), evolution, and diversity of truffles. Randy Molina is a research botanist (retired), U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Forestry Sciences Laboratory, 629 SW Main, Suite 400, Portland, OR 97205; he prepared sections on introductory concepts, mycorrhizal symbiosis and specificity, fungal rarity, management principles, and historical contributions of James Trappe to truffle science in the PNW. Daniel L. Luoma is an assistant professor, Department of Forest Science, Oregon State University, 321 Richardson Hall, Corvallis, OR 97331; he prepared sections on community ecology, mycophagy, silvicultural effects, and inventory methods. Efren Cázares is an affiliate faculty member, Department of Forest Science, Oregon State University, 321 Richardson Hall, Corvallis, OR 97331; he prepared sections on genera descriptions. David Pilz is an affiliate faculty member, Department of Forest Science, Oregon State University, 321 Richardson Hall, Corvallis, OR 97331; he prepared sections on culinary truffles. Jane E. Smith is a research botanist and Michael Castellano is a research forester, U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Forestry Sciences Laboratory, 3200 SW Jefferson Way, Corvallis, OR 97331; Smith prepared ecosystem functions, fire ecology, and habitat restoration, and Castellano helped with genera descriptions and prepared many of the truffle figures used in the publication and the CD-ROM. Steven L. Miller is professor and Department Head, Department of Botany, University of Wyoming, 114 Aven Nelson Building, Laramie, WY 82071; he prepared the first draft of keys to genera. Matthew J. Trappe is a research assistant, Department of Environmental Sciences, Oregon State University, 2046 Cordley Hall, Corvallis, OR 97331. Cover art: This photographic collage displays the species diversity, ecosystem function, human use, and beauty of truffle fungi in the Pacific Northwest. Clockwise: High magnification of Hysterangium spp. truffle attached via an umbilical-like fungal cord (rhizomorph) to ectomycorrhizae on Douglas-fir roots (photo by B. Zak). Northern flying squirrel eating a truffle (photo by Jim Grace). Surface and interior tissue of the ascomycete truffle Hydnotrya cubispora (photo by Michael Castellano). Basket of commercially harvested Oregon black truffles, Leucangium carthusianum, displayed at the Orgeon Truffle Festival in Eugene, 2007; a chocolate truffle candy is also shown in the upper left of basket (photo by David Pilz). Bright lemon-yellow truffles of the basidiomycete Rhizopogon truncatus found under pines in southwest Oregon (photo by Randy Molina). Abstract Trappe, James M.; Molina, Randy; Luoma, Daniel L.; Cázares, Efren; Pilz, David; Smith, Jane E.; Castellano, Michael A.; Miller, Steven L.; Trappe, Matthew J. 2009. Diversity, ecology, and conservation of truffle fungi in forests of the Pacific Northwest. Gen. Tech. Rep. PNW-GTR-772. Portland, OR: U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station. 194 p. Forests of the Pacific Northwest have been an epicenter for the evolution of truffle fungi with over 350 truffle species and 55 genera currently identified. Truffle fungi develop their reproductive fruit-bodies typically belowground, so they are harder to find and study than mushrooms that fruit aboveground. Nevertheless, over the last five decades, the Corvallis Forest Mycology program of the Pacific Northwest Research Station has amassed unprecedented knowledge on the diversity and ecol- ogy of truffles in the region. Truffle fungi form mycorrhizal symbioses that benefit the growth and survival of many tree and understory plants. Truffle fruit-bodies serve as a major food souce for many forest-dwelling mammals. A few truffle spe- cies are commercially harvested for gourmet consumption in regional restaurants. This publication explores the biology and ecology of truffle fungi in the Pacific Northwest, their importance in forest ecosystems, and effects of various silvicul- tural practices on sustaining truffle populations. General management principles and considerations to sustain this valuable fungal resource are provided. Keywords: Mycorrhiza, mycophagy, small mammals, biodiversity, conservation, fungi, mushrooms, truffles. Summary Pacific Northwest (PNW) forests harbor over 350 truffle species in 55 genera. Unlike their mushroom cousins that fruit aboveground, most truffle species fruit below- ground (hypogeously) producing small, potato-like structures that bear the reproduc- tive spores. Truffles are thus more difficult to find than mushrooms; collectors must rake away some of the forest duff to reveal the truffle fruit-bodies that reside at the mineral soil-organic layer interface. As truffles mature, their aromas intensify and attract animals that excavate and eat them. As the animals digest the truffle tissues, the spores pass through the digestive track unharmed and are released in fecal pellets and dispersed throughout the forest. Many small mammals strongly depend on truf- fles as a major part of their diets. Most truffle species also form mutually beneficial symbioses with plant roots called ectomycorrhizae. Ectomycorrhizal fungi receive their primary energy source from host photosynthate (sugars) sent from leaves to roots; in return, the fungus takes up minerals and water from soil and transports them into the fine feeder roots for use by the host plant. Plants absolutely depend on this functioning symbiosis for their growth and survival in natural ecosystems. Approximately 120 plant species from 19 families and 41 genera are documented as ectomycorrhizal hosts in the PNW, with members of the Pinaceae, Fagaceae, Betulaceae, and Salicaceae acting as the major tree hosts. This rich assembledge of ectomycorrhizal hosts, together with diverse forest habitat and climatic conditions, has created a unique confluence of biological and environmental conditions for the explosive evolution and diversity of truffle species in the PNW. As ectomycorrhizal fungi, truffle species also perform many important ecosystem functions includ- ing organic matter decomposition, nutrient cycling and retention, soil aggregation, and transferring energy through soil food webs. These functions contribute to the overall health, resiliency, and sustainability of forest ecosystems. Conserving these fungal communities and maintaining their functions are keys to wise management of our forest resources. This publication summarizes the knowledge accumulated over the last five decades by the Forest Mycology Team, Corvallis, Oregon, on the diversity, ecology, and management of truffle fungi. Descriptions and keys to genera, and photos of over 130 species provide a practical means to identify and appreciate these diverse and cryptic species. Effects of various silvicultural practices on truffle populations and community dynamics are discussed, so that managers can under- stand how truffle species respond to disturbance. We provide 12 summary manage- ment principles and considerations to help managers integrate truffle conservation into sustainable ecosystem management plans. Although this review is specific to the Pacific Northwest, many of the ecological concepts and management principles are applicable to other forested regions of the world where truffles occur. Contents 1 Introduction 16 What Are Truffles? 17 Where Do We Find Truffles? 20 History of Truffle Science in the Pacific Northwest 29 Evolution of the Hypogeous Habit 29 Darwinian Theory, Molecular Phylogenetics, and Plate Tectonics 34 Diversity of Hypogeous Fungi in the Pacific Northwest 35 Naming Fungi 37 Species Richness in Relation to Habitat and Mycorrhizal Hosts 38 Diversity by Taxonomic Groups 42 Descriptions of Truffle Genera 102 Keys to Genera 110 Ecology of Truffles 110 Mycorrhizal Symbiosis 117 Specificity Between Fungus and Host 120 Community Ecology of Truffle Fungi 123 Ecosystem Functions of Truffle Fungi 123 Nutrient Cycling and Soil Structure 125 Mycorrhizal Networks 125 Soil Food Webs 126 Small Mammal Mycophagy 136 Silviculture, Mycorrhizae, and Truffles 136 Clearcutting 137 Thinning 137 Green-Tree Retention 138 Fire Effects and Site Preparation 139 Truffles and Coarse Wood Remnants 140 Implications for Wildlife 141 Spore Inoculation of Nursery Seedlings 142 Culinary Truffles 142 History 143 Truffle Gastronomy 145 Native Culinary Truffles of the Pacific Northwest 149 Harvesting and Management of Pacific Northwest Truffles 151 The Future 153 Conservation and Management of Truffle Fungi and the Fungal Resource 155 Understanding Fungal Rarity 157 Inventory, Sampling, and Detection Considerations 158 Protection and Restoration of Habitat 160 Summary of Management Principles and Considerations 164 Concluding Remarks 164 Acknowledgments 164 Metric Equivalents 165 Literature Cited 194 Appendix Diversity, Ecology, and
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