THE GEOBIOLOGY AND ECOLOGY OF METASEQUOIA

TOPICS IN GEOBIOLOGY

Series Editors: Neil H. Landman, American Museum of Natural History, New York, New YorkDouglas S. Jones, University of Florida, Gainesville, Florida

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The Geobiology and Ecologyof Metasequoia

Edited by

BEN A. LePAGEURS Corporation,335 Commerce Drive, Suite 300Pennsylvania, 19034 U.S.A.

CHRISTOPHER J. WILLIAMSDepartment of Earth and EnvironmentFranklin and Marshall CollegeP.O. Box 3003Lancaster, Pennsylvania 17604, U.S.A.

and

HONG YANGDepartment of Science and TechnologyBryant University1150 Douglas PikeSmithfield, Rhode Island02917, U.S.A.

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Cover illustration:Trees of Metasequoia glyptostroboides growing along banks of the Yujiang River and base ofthe mountains in the Shiziba Valley, Hubei Province, China. Photography by Ben A. LePage,URS Corporation, Fort Washington, Pennsylvania.

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Table of Contents

Contributors xi

1. Ben A. LePage, Hong Yang and Midori Matsumoto TheEvolution and Biogeographic History of Metasequoia 3

2. Arata Momohara Paleoecology and History of Metasequoia inJapan, with Reference to its Extinction and Survival in East Asia 115

3. Suzanna L. Richter and Ben A. LePage A High-ResolutionPalynological Analysis, Axel Heiberg Island, Canadian High Arctic 137

4. Herbert W. Meyer Metasequoia in the Oligocene Bridge CreekFlora of Western North America: Ecological Implications and theHistory of Research 159

5. Judy Barrett Litoff Gunther’s Travels: The Odyssey ofMetasequoia Seeds from the 1920s? 187

6. Qin Leng Cuticle Analysis of Living and Fossil Metasequoia 197

7. Karimah Schoenhut Ultrastructural Preservation in MiddleEocene Metasequoia Leaf Tissues from the Buchanan LakeFormation 219

8. Hong Yang Biomolecules from Living and Fossil Metasequoia:Biological and Geological Applications 253

9. Christopher J. Williams Ecological Characteristics ofMetasequoia glyptostroboides 285

10. David R. Vann Physiological Ecology of Metasequoiaglyptostroboides Hu et Cheng 305

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11. Richard Jagels and Maria A. Equiza Competitive Advantagesof Metasequoia in Warm High Latitudes 335

12. John Kuser Selecting and Propagating New Cultivarsof Metasequoia 353

13. Christophe Nugue Cultivars of Metasequoia glyptostroboides 361

14. Gaytha A. Langlois A Conservation Plan for Metasequoia in China 367

Index 419

Maria A. Equiza, University of Maine, Department of Forest EcosystemScience, Orono, Maine, 04469, USA

Richard Jagels, University of Maine, Department of Forest EcosystemScience, Orono, Maine, 04469, USA; Richard Jagels@umenfa.maine.edu

John Kuser, Department of Ecology, Evolution and Natural Resources, CookCollege, Rutgers University, New Brunswick, New Jersey, 08901-8551,USA

Qin Leng, Nanjing Institute of Geology and Palaeontology, ChineseAcademy of Sciences, Nanjing 210008 & State Key Laboratory ofPalaeobiology and Stratigraphy, Nanjing, 210008, China; leng@nigpas.ac.cn

Gaytha A. Langlois, Department of Science and Technology, BryantCollege, 1150 Douglas Pike, Smithfield, Rhode Island, 02917, USA;langlois@bryant.edu

Ben A. LePage, URS Corporation, 335 Commerce Drive, Suite 300, FortWashington, Pennsylvania, 19034, USA; Ben LePage@URSCorp.com

Judy Barrett Litoff, Bryant College, Department of History and SocialSciences, 1150 Douglas Pike, Smithfield, Rhode Island, 02917, USA;jlitoff@bryant.edu

Midori Matsumoto, Department of Earth Sciences, Chiba University,Yayoi-cho 1-33, Inage-ku, Chiba 263, Japan; midori@earth.s.chiba-u.ac.jp

Herbert W. Meyer, Florissant Fossil Beds National Monument, UnitedStates National Park Service, P.O. Box 185, 15807 Teller County Road 1,Florissant, Colorado, 80816, USA; herb Meyer@nps.gov

Arata Momohara, Faculty of Horticulture, Chiba University, 648 Matsudo,Chiba, 271-8510, Japan; arata@midori.h.chiba-u.ac.jp

Christophe Nugue, National Collection CCVS of Metasequoia, 15 AvenueJacques Chastellain, Apt. 176, Rouen, 76100, France;Metasequoia.cn@wanadoo.fr

Suzanna L. Richter, Department of Earth and Environmental Science,University of Pennsylvania, 240 South 33rd Street, Philadelphia,Pennsylvania, 19104, USA; richter2@sas.upenn.edu

Karimah Schoenhut, URS Corporation, 335 Commerce Drive, Suite 300,Fort Washington, Pennsylvania, 19034, USA;karimahSchoenhut@alumni.upenn.edu

x

David R. Vann, Department of Earth and Environmental Science, Universityof Pennsylvania, 240 South 33rd Street, Philadelphia, Pennsylvania, 19104,USA; drvann@sas.upenn.edu

Christopher J. Williams, Department of Earth and Environment, Franklinand Marshall College, PO Box 3003, Lancaster, Pennsylvania, 17604, USA;cwillia@fandm.edu

Hong Yang, Department of Science and Technology, 1150 Douglas Pike,Smithfield, Rhode Island, 02917, USA; hyang@bryant.edu

Contributors

This volume of the Topics in Geobiology series offers original contributionsfrom the 1st International Metasequoia Symposium, which was held on the cam-pus of the China University of Geosciences in Wuhan, Hubei Province fromAugust 5–7, 2002 and included a field trip to the native habitat of Metasequoia.The goal of this symposium was to provide an international forum where scien-tists who were actively involved in the study of fossil and living Metasequoiacould unite to exchange ideas, assess the current state of knowledge and iden-tify new research directions within a sound scientific framework. To this end,51 participants from 4 countries were in attendance. The conference featured21 contributed oral and 3 poster presentations. Presentations were organizedaround several themes: history and conservation of Metasequoia, paleobiologyand ecology of Metasequoia, and modern ecology of Metasequoia. We arepleased that all of these themes are represented in the peer-reviewed contribu-tions of this volume.

Renewed interest in the evolutionary history of Metasequoia indicated theneed to establish a multi-disciplinary working group of scientists to initiatenew and rigorous studies of this genus. This volume is an outgrowth of thisworking group. For scientists and the general public alike, few trees have fueledour curiosity and fascination, as have the redwoods for their size, longevity andtheir evolutionary history. Among the redwoods, Metasequoia glyptostroboidesHu et Cheng (Hu & Cheng, 1948) or the Dawn redwood, is probably one ofthe most interesting species, even though it is a more recent addition to thefamily. The dawn redwood was known initially only as a fossil and was firstdescribed in the scientific literature in 1941 by the Japanese paleobotanist,Shigeru Miki. Eight years later, the Chinese botanists Hu and Cheng unveileda tree to the world that local residents of the Xiahoe Valley in southeast China

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xii Contributors

called the Shui-Sha (Water Fir) and was morphologically identical to the fossilsof Metasequoia that Miki had previously described.

Over the last 60 years, both the biology and paleobiology of the genus havebeen studied. Information regarding different features of the living species,ranging from morphology to genetics, has been accumulated. Hundreds ofpublications have appeared in which Metasequoia has been reported as a majoror minor constituent of the fossil floras. Consequently, its fossil record is wellknown and indicates that the genus was widely distributed throughout the mid-and high-latitude regions of North America and Eurasia from early Late Creta-ceous (ca. 100 million years ago) to Pliocene/Pleistocene time. The spatial andtemporal distribution patterns indicate that Metasequoia was perhaps one ofthe most successful trees that occupied the temperate regions of the mid- andhigh-latitudes. At times Metasequoia was part of the broad-leaved temperateforests, while in others, large tracts of lowland swamp forests, consisting almostexclusively of Metasequoia are known to have existed, especially in the polarregions.

Today the genus has a distribution that is geographically restricted to twosmall disjunct regions in southeast China, with one of the two only representedby an isolated tree. Although Metasequoia was an important conifer through-out the mid- and high-latitudes forests of the Northern Hemisphere in the past,details of its modern ecological and physiological attributes are still poorlyunderstood and scientific papers dealing with ecological aspects of the livingrepresentatives are few and often anecdotal. The primary objective of nearly allof the early expeditions led by western scientists to the native range of Metase-quoia was to procure seeds and live plant material to prevent the extinctionof this species. In contrast, there has been only limited study of Metasequoiaecology within its native habitat (e.g., Chu & Cooper, 1950). In fact, given itsextensive fossil record we may know more about the paleoecology of Metase-quoia than we do about the ecology of the extant species. With the constructionof the Three Gorges Dam Project nearby, the habitat of living Metasequoiawithin the Xiahoe Valley may yet experience another dramatic change in theyears to come. Thus, the need to compile known ecological information as wellas documenting the existing status of the living species is urgent.

This book represents a distillation of the collective efforts and results of sev-eral Metasequoia specialists and enthusiasts. It is probably the most up-to-dateand comprehensive reference source for the genus and the authors have soughtto incorporate obscure, hard-to-get and non-English reference sources. Thetopics and scope of this book should be of interest to a wide audience includ-ing botanists, geologists, paleobotanists, biogeographers, foresters, ecologists,paleoecologists, ecophysiologists, geochemists, climate modelers, geneticists,naturalists, science historians, and not the least, gardeners. A brief summary ofeach contribution follows.

Contributors xiii

B.A. LePage, H. Yang and M. Matsumoto provide a comprehensiveoverview of the spatial and temporal distribution patterns of fossil Metase-quoia in the Northern Hemisphere beginning in the early Late Cretaceous untilthe Pliocene-Pleistocene. The wide distribution of the genus indicates that itwas capable of adapting and growing under a wide range of climatic and envi-ronmental conditions, including those unique to the polar latitudes. AlthoughMetasequoia was a prominent constituent of the broad-leaved deciduous foreststhroughout the Northern Hemisphere, the genus appears to have been precludedfrom occupying Europe. Increasing global aridity, cooling and competition forspace and resources from representatives of the Pinaceae appear to have con-tributed to the reduced distribution and abundance of the genus during theNeogene. The results of this study also indicate that with few exceptions, thegenus has remained unchanged morphologically for 100 million years and pro-vides another spectacular example of morphological stasis in the plant fossilrecord.

Recent stratigraphic and paleoenvironmental data have enabled A. Momo-hara to reconstruct the regional ecology and discuss the processes that led tothe extinction of Metasequoia in Japan and its survival in China. A thoroughevaluation of fossil Metasequoia in Japan and eastern Asia indicates that thegenus was a common constituent in the wide sedimentary basins that were asso-ciated with contiguous fluvial flood plain ecosystems. Orogenic and volcanicactivities in Japan influenced local topography in the adjoining or adjacentfloodplains and may have influenced the distribution of Metasequoia duringthe mid-to late Neogene. The extinction of the last remaining populations ofMetasequoia from Japan during the early Pleistocene and its re-appearance inChina during the Holocene is discussed.

S.L. Richter and B.A. LePage present the results of a high-resolution paly-nological study on a siltstone unit located between two prominent coals repre-senting Metasequoia-dominated swamp forests from the middle Eocene (ca. 45million years old) Buchanan Lake Formation at Napartulik, Axel Heiberg Is-land, Nunavut, Canada. The pollen and spore microflora provides evidenceof successional processes and indicates that the local vegetation respondedto climatic and environmental changes. Furthermore, the pollen data indicatethat the local floodplain vegetation was part of a larger, dynamic floral mosaicwithin a regional polar broad-leaved deciduous forest community and that pe-riods of prolonged environmental stasis were generally limited to the swampforest communities. Catastrophic flooding appears to have been a major distur-bance factor throughout the landscape and fern spikes record at least two majorflooding events.

H.W. Meyer examines the evolution of Metasequoia and the broad-leaveddeciduous vegetation that became widespread in the Northern Hemisphere fol-lowing the Eocene-Oligocene climatic cooling. He begins with an historical

xiv Contributors

overview of Chaney’s concepts of the composition and biogeographic historyof North American fossil forests prior to and after the discovery of livingM. glyptostroboides in China. Using the early Oligocene Bridge Creek floraof the John Day Formation in Oregon, USA as a model, Meyer suggests thatthe Mixed Mesophytic Forest originated through various responses of individ-ual species during the Eocene-Oligocene transition, including 1) extinction orextirpation, 2) pre-adaptation or evolution in place, 3) dispersal from higherelevations, or 4) dispersal from higher latitudes.

J.B. Litoff recounts the story of how Wilhelm Gunther (1893–1983), aGerman national who lived and worked in China between 1914 and 1941,acquired seeds in the late 1920s that decades later would be identified as thoseof M. glyptostroboides. Drawing from historical and contemporary photographsas well as interviews with Gunther’s daughters, this essay unravels the odysseyof these M. glyptostroboides seeds that possibly predate the discovery of thenative population in China.

The discovery of Uneven and Even Type cuticle in native populations ofM. glyptostroboides has prompted Q. Leng to conduct a re-evaluation of the tax-onomic utility of cuticle characters in both living and fossil Metasequoia. Theresults of her study indicate that the Even Type cuticle appears to be restrictedto a single tree located in Paomu Village, Hunan Province, China, whereasthe Uneven Type cuticle is widely distributed in the main M. glyptostroboidespopulations. More importantly, all of the fossil Metasequoia leaves examinedpossess the Even Type, suggesting that the Even Type is the ancestral char-acter state for the genus. This finding bears significant implications for theevolution and paleogeography of this genus, as well as the conservation of thisendangered species.

K. Schoenhut examined mummified leaflets of middle Eocene Metasequoiafrom the Upper Coal member of the Buchanan Lake Formation at Napartulikon Axel Heiberg Island. She utilized transmission electron microscopy (TEM)to quantitatively and qualitatively assess the extent of sub-cellular preservation.The presence of organelles such as chloroplasts and chloroplast constituentswere tallied on a per cross-section basis and by performing a nested multivariateanalysis of variance, significant differences in leaf preservation were observedbetween individual leaflets as well as leaves between vertical intervals. Wherediscernible, thylakoid features were used to classify the fossil leaflets as origi-nating from high or low-light environments. The results indicate that between67 and 78% of the leaflets were classified as ‘shade-types.’

Biomolecules from living and fossil Metasequoia have allowed H. Yang toprovide insight into the biological and geological history of the genus, as wellas its phylogeny and evolution, population genetics and molecular taphon-omy. The chemistry of labile biomolecules and nucleotide sequences from

Contributors xv

M. glyptostroboides reconfirm the systematic position of Metasequoia as thesister taxon to Sequoia Endlicher and Sequoiadendron J. Buchholz, which formthe subfamily Sequoioideae. Relative rate testing based on different gene se-quences suggests an evolutionary rate slow down in the Sequoioideae lineage,while non-sequence based studies indicate a low overall genetic diversity anda lack of spatial genetic structure in the native Chinese populations. Molecularand biochemical investigations of the ancient biomolecules from well-preservedTertiary fossil Metasequoia remains reveal that labile biomolecules such as car-bohydrates and cutin acids that are normally absent from the Cenozoic fossilrecord are preserved. Comparative geochemical and SEM analyses of thesechemically unstable biomolecules and suggests that they may carry importantstructural functions to support the integrity of plant fossil morphology.

C.J. Williams provides a comprehensive update on the ecology and cli-matic conditions under which M. glyptostroboides grows in its native habitatin China as well as those growing in cultivation. The results indicate that theChinese population grows under a narrow range of climatic and environmentalconditions. The trees growing in cultivation however indicate that M. glyp-tostroboides is capable of growing across a gradient of 16.3◦C of mean annualtemperature and 2360 mm of mean annual precipitation. No cultivated M. glyp-tostroboides are known to exist without supplemental water in areas that receiveless than ca. 500 mm of mean annual precipitation. Analysis of growth perfor-mance of M. glyptostroboides through time indicates that trees from differentseedlots grown in common garden experiments remain static in their rela-tive growth rates through time. A mixture of environmental factors may alterM. glyptostroboides growth form. Most notably, shrubby varieties are knownfrom a mixture of cold climates, but are not always found in extremely coldareas.

D.R. Vann examines the modern species’ autecology, focusing on gas ex-change relations, to address the role of physiological constraints in rangecontraction over time. Examination of CO2 uptake and transpiration in re-sponse to light, temperature, humidity and CO2 concentration indicate thatM. glyptostroboides is drought-intolerant, adapted to low light levels and rela-tively cool climates, as might be expected in foggy coastal or riparian habitats.Gas-exchange relations of the modern species are sufficiently flexible to ex-plain the presence of fossil Metasequoia at all known sites and imply that thespecies has not undergone any major adaptive changes in its core physiologicalprocesses.

R. Jagels and M. Equiza examine the mechanical/hydraulic stem attributes,leaf-level water-use-efficiency and photobiology of M. glyptostroboides, Se-quoia sempervirens (D. Don) Endlicher, Taxodium distichum (L.) Richard,Glyptostrobus pensilis (Staunton ex D. Don) K. Koch and Larix laricina

xvi Contributors

(Du Roi) K. Koch to consider the question of competitiveness of differenttree species growing at the polar latitudes during the early Tertiary. The resultsindicate that T. distichum would have been limited primarily by a significantdecrease in photosynthetic efficiency when growing under continuous light. Se-quoia sempervirens should have been highly competitive, but was likely limitedby its evergreen habit. Glyptostrobus pensilis would have been restricted to mi-nor component status by its slow growth rate and short stature and althoughL. laricina demonstrated improved water-use-efficiency under continuous light,it had a less-competitive photobiology than Metasequoia and sequestered moreresources into its stem biomass.

The Ryder’s Lane Plantation at Rutgers University was established byJ. Kuser after receiving a seedlot collection of M . glyptostroboides from Chinain 1990. In this paper Kuser provides an overview of the best method to propa-gate cuttings, hormone treatments and the best time of year to propagate cuttingsof M. glyptostroboides. Furthermore, a brief discussion of three new cultivarsawaiting introduction is provided.

C. Nugue provides a comprehensive overview of the known varieties ofM. glyptostroboides that have either been described in the literature, are com-mercially available or in the process of being developed for commercial distri-bution.

G. Langlois presents a number of models that have been used previouslyfor resource protection, including the program challenges and successes for theredwood forests in California, rainforests in Central and South America, coralreefs in Australia and the Giant panda in China. A Metasequoia Conserva-tion Plan is discussed and tools for assessing the effectiveness of conservationprograms are suggested.

It is our hope that through our continuing efforts and increased involve-ment of Metasequoia specialists and enthusiasts that the International Metase-quoia Conference will convene again. By uniting Metasequoia researchers fromacross the globe and providing a forum for the dissemination of research find-ings the conference can contribute meaningfully to the ongoing conservationand research efforts focused on this unique species.

We would like to thank the contributors to this volume. Without their en-thusiasm this volume would have never come to fruition. We would also liketo extend our gratitude to the Chinese National Science Foundation, ChinaUniversity of Geosciences, Administration of Xingdoushan Natural Reserve,Andrew W. Mellon Foundation, Bryant College and Chinese PaleontologicalAssociation for funding. Thanks are due to the following manuscript reviewersfor their helpful comments and suggestions: Pim van Bergen, David Cantrill,Geoffrey Creber, David Creech, Clyde Hunt, Steven Manchester, Thanh-ThuyNguyen, Jon Parker, Dana Royer, Ken’ichi Saiki, Shinya Sugita and CatherineYansa. Thanks are also due to Michael Leslie, Michael Leslie Photography for

Contributors xvii

his assistance in preparing a number of the photographs used in this volume. Aspecial debt of gratitude is also extended to Xulong Lai, Tao Li, Guilin Sheng,Shujuan Yang and Xiugao Zhou, China University of Geosciences, who borethe brunt of organizing the conference.

Ben A. LePage1

Christopher J. WilliamsHong Yang

1 We would also like to add that all royalties from this volume will be donated to the Xiaohe MetasequoiaConservation Station conservation fund so that basic, but much needed equipment can be purchased.

Detailed Table of Contents

Part I • Fossil Metasequoia and History

Chapter 1 • The Evolution and Biogeographic History ofMetasequoia 3

Ben A. LePage, Hong Yang and Midori Matsumoto

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42. Taxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63. Morphological Stasis and Genetic Variation . . . . . . . . . . . . . . . . . . . 84. Distribution of Metasequoia glyptostroboides . . . . . . . . . . . . . . . . . . 105. Phytogeography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 116. Putative Metasequoia Remains from Europe . . . . . . . . . . . . . . . . . . . 237. Orogenies and Ecological Competition . . . . . . . . . . . . . . . . . . . . . . . . 248. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

10. Appendix A . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3411. Appendix B . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57

11.1. Russia and Former Countries of the USSR . . . . . . . . . . . . . 5711.2. Greenland . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6111.3. Spitsbergen/Faroe Island . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6211.4. Arctic Canada . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6311.5. Sakhalin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6411.6. China . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6511.7. Alaska . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6611.8. Canada . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6911.9. USA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72

11.10. Korea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7911.11. Japan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80

11.11.1. Hokkaido . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8011.11.2. Honshu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81

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11.11.3. Shikoku . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9311.11.4. Kyushu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

12. References for Metasequoia-Bearing Fossil Sites . . . . . . . . . . . . . . . 94

Chapter 2 • Paleoecology and History of Metasequoia in Japan,with Reference to its Extinction and Survival in EastAsia 115

Arata Momohara

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1162. Occurrence and Paleoecology of Metasequoia in the Late

Cretaceous and Paleogene Floras in and Around Japan . . . . . . . . . . 1183. Geographical Changes in the Distribution of Metasequoia During

the Neogene and Early Pleistocene . . . . . . . . . . . . . . . . . . . . . . . . . . . 1214. Extinction and Survival of Metasequoia in East Asia . . . . . . . . . . . . 1315. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1346. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134

Chapter 3 • A High-Resolution Palynological Analysis, AxelHeiberg Island, Canadian High Arctic 137

Suzanna L. Richter and Ben A. LePage

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1382. Study Area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1393. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1414. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1435. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147

5.1. Geology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1475.2. Palynofloral Assemblages and Paleoenvironmental

Reconstruction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1485.2.1. Zone I . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1485.2.2. Zone II . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1505.2.3. Zone III . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1505.2.4. Zone IV . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1515.2.5. Zone V . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1525.2.6. Zone VI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152

6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1537. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1538. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1549. Appendix A . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156

Chapter 4 • Metasequoia in the Oligocene Bridge Creek Flora ofWestern North America: Ecological Implications andthe History of Research 159

Detailed Table of Contents xxi

Herbert W. Meyer

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1602. Metasequoia in the Bridge Creek Flora . . . . . . . . . . . . . . . . . . . . . . . . 1613. History of Study, Early Interpretations, and the Bearing of the

Discovery of Extant Metasequoia on Interpretations ofPaleocommunities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164

4. Ecological Setting and Conservation of the Modern MetasequoiaForest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169

5. Ecological Setting and Climate of the Oligocene Bridge CreekFlora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173

6. The Eocene-Oligocene Transition: Climate Change and theDevelopment of Mixed Mesophytic Forest . . . . . . . . . . . . . . . . . . . . . 175

7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1828. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1839. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183

Chapter 5 • Gunther’s Travels: The Odyssey of MetasequoiaSeeds from the 1920s? 187

Judy Barrett Litoff

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1882. Gunther in China . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1883. Gunther in America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1904. Gunther’s Metasequoia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1915. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1946. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194

Part II • Cuticle, Ultrastructure and Biomolecules

Chapter 6 • Cuticle Analysis of Living and Fossil Metasequoia 197

Qin Leng

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1982. Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2003. Cuticle of Living Metasequoia glyptostroboides . . . . . . . . . . . . . . . . 2014. Cuticle of Fossil Metasequoia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2065. Evolutionary Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2076. Conclusions and Prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2117. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2138. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213

Chapter 7 • Ultrastructural Preservation in Middle EoceneMetasequoia Leaf Tissues from the Buchanan LakeFormation 219

xxii Detailed Table of Contents

Karimah Schoenhut

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2202. Methods and Materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2223. Qualitative Observations on Fossil Leaf Ultrastructure . . . . . . . . . . 2254. Condition of Preserved Chloroplasts and Components . . . . . . . . . . . 2275. Negative Staining of the Chloroplast Membranes . . . . . . . . . . . . . . . 2296. Quantitative Analysis of Chloroplast Preservation . . . . . . . . . . . . . . 2327. Implications of Quantitative Analysis . . . . . . . . . . . . . . . . . . . . . . . . . 2408. Patterns of Degradation: Senescence versus Trauma Induced

Detachment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2409. Mechanism of Preservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243

10. Sun/Shade Classification of Fossil Leaflets . . . . . . . . . . . . . . . . . . . . 24510.1. Results of Sun/Shade Classification Analysis . . . . . . . . . . . 24510.2. Discussion of Sun/Shade Classification . . . . . . . . . . . . . . . . 247

11. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25012. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250

Chapter 8 • Biomolecules from Living and Fossil Metasequoia:Biological and Geological Applications 253

Hong Yang

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2542. Biomolecules and Applied Technology . . . . . . . . . . . . . . . . . . . . . . . . 2553. DNA and Proteins from Metasequoia glyptostroboides . . . . . . . . . . 258

3.1. Molecular Phylogeny and Evolution . . . . . . . . . . . . . . . . . . . 2583.2. Population Genetics and Conservation . . . . . . . . . . . . . . . . . 260

4. Biochemistry of Ancient Biomolecules from Fossil Metasequoia . 2624.1. Polysaccharides and Bound Fatty Acids . . . . . . . . . . . . . . . . 2624.2. Source and Role of Labile Biomolecules . . . . . . . . . . . . . . . 2654.3. Lipids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2664.4. Bound Alkanes and Alkenes . . . . . . . . . . . . . . . . . . . . . . . . . . 268

5. Fossil Taphonomy and Paleoenvironmental Applications . . . . . . . . 2695.1. Molecular Taphonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2695.2. Paleophysiological and Paleoclimatic Signals . . . . . . . . . . . 270

6. General Implications and Conclusions . . . . . . . . . . . . . . . . . . . . . . . . 2717. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2728. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2739. Appendix A . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280

Part III • Ecology and Ecophysiology

Chapter 9 • Ecological Characteristics of Metasequoiaglyptostroboides 285

Christopher J. Williams

Detailed Table of Contents xxiii

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2862. Habitat and Native Range . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287

2.1. Climate of Native Range . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2892.2. Geographic Distribution of Cultivated Metasequoia . . . . . 291

3. Life History . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2934. Growth Rates and Tree Form . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2965. Reaction to Competition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3006. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3017. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3018. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 302

Chapter 10 • Physiological Ecology of Metasequoiaglyptostroboides Hu et Cheng 305

David R. Vann

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3062. Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3083. Gas Exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 308

3.1. Response to Light Intensity . . . . . . . . . . . . . . . . . . . . . . . . . . . 3093.1.1. Carbon Dioxide . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3093.1.2. Transpiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311

3.2. Response to Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3123.2.1. Respiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3133.2.2. Transpiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315

3.3. Response to Relative Humidity of Air . . . . . . . . . . . . . . . . . 3163.4. Response to CO2 Concentration in Air . . . . . . . . . . . . . . . . 317

4. Other Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3184.1. Pigments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3194.2. Water Relations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3204.3. Winter Tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3214.4. Secondary Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 321

5. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3225.1. Paleoecological and Evolutionary Aspects . . . . . . . . . . . . . . 323

5.1.1. Evolutionary Stasis . . . . . . . . . . . . . . . . . . . . . . . . . 3235.1.2. Species Migration . . . . . . . . . . . . . . . . . . . . . . . . . . 3255.1.3. High-Latitude Survival . . . . . . . . . . . . . . . . . . . . . 3265.1.4. Evolution of Deciduousness . . . . . . . . . . . . . . . . . 327

6. Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3297. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330

Chapter 11 • Competitive Advantages of Metasequoia in WarmHigh Latitudes 335

Richard Jagels and Maria A. Equiza

xxiv Detailed Table of Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3362. Competition Criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3383. Mechanical/Hydraulic Attributes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3394. Water use Efficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3415. Photobiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3436. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3447. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3468. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 346

Part IV • Cultivars and Horticulture

Chapter 12 • Selecting and Propagating New Cultivars ofMetasequoia 353

John Kuser

1. Origins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3532. Cultivar Selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3543. Propagation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3574. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3595. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3606. Literature Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 360

Chapter 13 • Cultivars of Metasequoia glyptostroboides 361

Christophe Nugue

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3612. Metasequoia glyptostroboides Varieties . . . . . . . . . . . . . . . . . . . . . . . 3623. Putative Cultivars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3654. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3655. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 365

Chapter 14 • A Conservation Plan for Metasequoia in China 367

Gaytha A. Langlois

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3682. History of Metasequoia glyptostroboides . . . . . . . . . . . . . . . . . . . . . . 3693. General guidelines for Resource Protection . . . . . . . . . . . . . . . . . . . . 3704. Specific Challenges of Preserving Metasequoia glyptostroboides

Forests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3715. Preservation of the California Redwood Forests . . . . . . . . . . . . . . . . 3726. Preservation Issues in California . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3757. Preservation Strategies for California Redwoods . . . . . . . . . . . . . . . . 3778. Essentials of a Metasequoia Conservation Plan . . . . . . . . . . . . . . . . . 381

Detailed Table of Contents xxv

8.1. Site Identification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3828.2. Management Scheme for Project Oversight . . . . . . . . . . . . . 3828.3. Formal Proposal for Metasequoia Protection . . . . . . . . . . . . 3838.4. Communication Network for Metasequoia Conservation . 3838.5. Partnership Collaboratives for Setting Up the Protected

Reserve . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3848.6. Education Program to Accompany the Metasequoia Con-

servation Plan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3858.7. Scientific Research Plan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3858.8. Permit Program for Scientists and Bioresource Specialists 3868.9. Expand and Update the Metasequoia Field Research Sta-

tion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3868.10. Effective Marketing Program for Metasequoia Conserva-

tion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3868.11. Phasing of Implementation of Metasequoia Conservation

Plan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3888.12. Non-Profit Organization (NGO) for Metasequoia Conser-

vation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3898.13. Funding for the Metasequoia Conservation Plan . . . . . . . . 3898.14. Assessment Tools for Evaluating the Conservation Plan . . 390

9. Other Successful Conservation Programs—What Lessons can beLearned? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3909.1. Lessons Learned from Efforts to Preserve Rainforests . . . . . . 3919.2. Lessons Learned from Australian Efforts to Preserve the

Great Barrier Reef . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3969.3. Recent Efforts in China to Address Environmental Protection

and to Preserve Giant Panda Habitat . . . . . . . . . . . . . . . . . . . . . 3999.4. Lessons Learned from China’s Efforts to Preserve the Giant

Panda . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40310. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40411. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40412. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40413. Appendix A . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41014. Appendix B . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41215. Appendix C . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41416. Appendix D . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41517. Appendix E . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41618. Appendix F . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 417

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419

PART I

Fossil Metasequoia and History

Chapter 1

The Evolution and BiogeographicHistory of Metasequoia

BEN A. LePAGE1, HONG YANG2 and MIDORI MATSUMOTO3

1URS Corporation, 335 Commerce Drive, Suite 300, Fort Washington, Pennsylvania, 19034,USA; 2Department of Science and Technology, Bryant University, 1150 Douglas Pike,Smithfield, Rhode Island, 02917, USA; 3Department of Earth Sciences, Chiba University,Yayoi-cho 133, Inage-ku, Chiba 263, Japan.

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42. Taxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63. Morphological Stasis and Genetic Variation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84. Distribution of Metasequoia Glyptostroboides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105. Phytogeography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 116. Putative Metasequoia Remains from Europe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237. Orogenies and Ecological Competition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 248. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289. References Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

10. Appendix A . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3411. Appendix B . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57

11.1. Russia and Former Countries of the USSR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5711.2. Greenland . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6111.3. Spitsbergen/Faroe Island . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6211.4. Arctic Canada . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6311.5. Sakhalin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6411.6. China . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6511.7. Alaska . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6611.8. Canada . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6911.9. USA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72

11.10. Korea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7911.11. Japan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80

11.11.1. Hokkaido . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8011.11.2. Honshu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81

The Geobiology and Ecology of Metasequoia, edited by Ben A. LePage, Christopher J.Williams and Hong Yang, c© Springer 2005.

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4 Ben A. LePage, Hong Yang and Midori Matsumoto

11.11.3. Shikoku . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9311.11.4. Kyushu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

12. References for Metasequoia-Bearing Fossil Sites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94

Abstract: The fossil record of Metasequoia Miki is extensive and demonstrates that the genuswas widely distributed throughout North America and Eurasia from the early Late Cretaceous tothe Plio-Pleistocene. The genus first appears in Cenomanian age deposits from western Canada,Alaska and the Arkagala and Koylma River basins in Russia and indicates that Metasequoia hadachieved a wide distribution early in its evolutionary history. Exchange of Metasequoia betweenAsia and North America probably occurred across Beringia, which had become functional atthe Albian-Cenomanian boundary (ca. 100 million years ago). However, if the inter-continentalexchange of the early representatives of this genus occurred prior to the establishment of Beringia,migration would have still been possible across the Spitsbergen Corridor, which was functionalduring the Early Cretaceous. By the early Tertiary, the distribution patterns do not appear tohave changed considerably from that seen during the Late Cretaceous, except that Metasequoiabecame a dominant constituent of the polar Broad-leaved Deciduous Forests. More importantly,the distribution of Metasequoia indicates that the genus grew and reproduced under a diverserange of climatic and environmental conditions throughout geologic time, including the cold andunique lighting conditions of the polar latitudes. Of particular interest is the apparent lack ofMetasequoia fossils in Europe despite the presence of two land bridges linking North Americaand Europe throughout the early Tertiary and the drying of the Turgai Straits that separatedeastern and western Asia up until Oligocene time. Metasequoia persisted in western Siberia andthe Canadian Arctic until late Pliocene time, and in western Georgia and Japan until the latePliocene-early Pleistocene. Following the apparent early Pleistocene extinction, Metasequoiare-appeared in southeastern China. The pronounced reduction in distribution during the Mioceneappears to be coupled with increasing global aridity and cooling and increased competition forresources and habitat from representatives of the Pinaceae. With few exceptions, the bulk of theMetasequoia fossils described in the literature indicate that the fossils assigned to M. occidentalisare indistinguishable from the living species. The remarkable morphological stasis observed inMetasequoia demonstrates that the genus has remained unchanged, at least morphologically,since the early Late Cretaceous.

Key words: China; Cretaceous; evolution; mycorrhiza; land bridges; Napartulik;orogeny; paleogeography; Shui-sha-ba Valley; systematics; taxonomy; Tertiary; TurgaiStait.

1. INTRODUCTION

Metasequoia Miki (Miki, 1941) is one of seven monospecific genera withinthe Taxodiaceae (now subsumed within the Cupressaceae), with Metasequoiaglyptostroboides Hu et Cheng (Hu & Cheng, 1948) occurring in small and pos-sibly relictual populations in Sichuan, Hubei and Hunan Provinces, China. Itoccurs as a constituent of the mixed mesophytic forests and grows at elevationsranging from 800 to 1,500 m (Fu & Jin, 1992). Metasequoia glyptostroboides

The Evolution and Biogeographic History of Metasequoia 5

grows on acidic alluvial soils in the mountain valleys where there is abundantmoisture, mean annual temperature (MAT) is about 13◦C, the coldest monthmean temperature ranges from –6.1 to 1.7◦C (absolute coldest –15.4◦C) andthe warmest month mean temperature ranges from 23.3 to 32.3◦C (absolutewarmest 35.4◦C) (Bartholomew et al., 1983; Fu & Jin, 1992). Rainfall is sea-sonal with a mean annual precipitation of about 1,300 mm (climate data fromLichuan [1959–1978]); Wang, 1961; Bartholomew et al., 1983; Fu & Jin, 1992).For a detailed discussion on the ecology and environment of M. glyptostroboidessee Williams (this volume).

Although M. glyptostroboides currently grows in a part of the world that ismoderately warm, it must be pointed out that the temperature conditions un-der which M. glyptostroboides grows today should probably not be consideredindicative of the temperatures or environmental conditions under which the an-cient representatives of the genus grew, or that M. glyptostroboides is incapableof growing under much colder conditions. Snow and freezing temperatureswere reported to occur regularly during the winter months by local residentsof Modaoxi (Modaoqi), which is located within the Shui-sha-ba (Chinese forMetasequoia) Valley where M. glyptostroboides is thought to occur naturally(LePage, personal communication with local residents, 2002). Metasequoiaglyptostroboides trees growing in Montreal, Canada and St. Petersburg, Russiafrequently experience winter temperatures as low as –30◦C to –40◦C (Williams,this volume; LePage, unpublished) and laboratory experiments have shown thatthe leaves and twigs are frost resistant to temperatures as low as –30◦C (Sakai &Larcher, 1987). Wang (1961) indicates that the genus probably had a muchmore extensive distribution during Recent time and grew under a wider rangeof environmental conditions than that indicated by the modern, geographicallyrestricted, native populations.

The occurrence of fertile and vegetative remains of Metasequoia in the plantfossil record indicates that the genus possessed a much wider distribution thatextended well into the polar regions of the Northern Hemisphere throughout theMesozoic and Cenozoic (Figure 1-1; Appendix A; Florin, 1963; Yang, 1999,Yang & Jin, 2000). Moreover, such a wide distribution in space and in timeindicates that representatives of the genus probably grew under a diverse rangeof climatic and environmental conditions throughout geologic time. The lackof significant morphological diversification observed between living and fossilMetasequoia foliage and seed cones leaves little doubt of the accuracy of thefossil identifications. In fact, in almost every report where Metasequoia fossilshave been described, the authors point out that they are more or less identicalto living M. glyptostroboides. Nevertheless, the practice of erecting new namesfor fossil species of Metasequoia based on slight differences in the size andshape of the fossil remains, or geologic age has, and continues to pervade theliterature.

6 Ben A. LePage, Hong Yang and Midori Matsumoto

Figure 1-1. Mesozoic and Cenozoic chronostratigraphic chart. Redrawn and modified fromTaylor and Taylor (1993). Arrow at the Cenomanian indicates the first occurrence of fossilMetasequoia from Russia, Canada and Alaska.

In this paper, the evolution and biogeographic history of the genus are dis-cussed in light of the tectonic and climatic history of the Northern Hemisphere.Examination of the fossils reported in the literature indicate that most of thefossils conform morphologically to the living species M. glyptostroboides, pro-viding a spectacular example of morphological, and possibly genetic stasis overa geologically-long period of time.

2. TAXONOMY

The affiliation of M. glyptostroboides with the Taxodiaceae was clearlyestablished in the initial description of the fossil material (Miki, 1941) and

The Evolution and Biogeographic History of Metasequoia 7

was substantiated by later studies using living specimens (Hu & Cheng,1948). Shortly after the living trees were discovered in China, Stebbins (1948)performed the first chromosomal analysis. His work along with studies bySchlarbaum et al. (1983, 1984) indicated that M. glyptostroboides, (2n = 22) isclosely related to Sequoiadendron J. Buchholz (2n = 22) and Sequoia Endlicher(2n = 66; Figure 1-2). Further molecular studies on the phylogeny of the genususing proteins and nucleotide sequences re-affirmed this grouping and furtherpointed out that the three taxa formed a “redwood clade (or sequoiod clade)”(Price & Lowenstein, 1989; Brunsfeld et al., 1994). This phylogenetic place-ment was further supported by recent PCR-RFLP data (Tsumura et al., 1995)and multi-gene analyses (Kusumi et al., 2000) (for details see Yang, this vol-ume). Combining the molecular and morphological data, Gadek et al. (2000)adopted earlier suggestions (Pilger, 1926; Eckenwalder, 1976; Brunsfeld et al.,1994) that recognized elevation of these three genera to the intra-familial level,the Sequoioideae, within the family Cupressaceae (Figure 1-2).

Metasequoia is one of the most abundant and easily recognized plant fos-sils found in the Late Cretaceous and Tertiary fossil plant record of the North-ern Hemisphere (Chaney, 1951; Florin, 1963; Liu et al., 1999; Yang, 1999;Yang & Jin, 2000). Prior to the discovery and description of fossil Metase-quoia from the late Miocene and Pliocene of Japan (Miki, 1941; Momohara,this volume), most Metasequoia remains, commonly seed cones and leaves,were assigned to Glyptostrobus Endlicher, Sequoia, Taxites Brongniart or Tax-odium Richard (Appendix A). In his seminal paper, Chaney (1951) providedthe most up-to-date account of fossil Metasequoia in North America. He rec-ognized two fossil species that corresponded to different geologic ages andassigned fossil Metasequoia remains from Cretaceous deposits to M . cuneata(Newberry) Chaney and those from the Tertiary to M. occidentalis (Newberry)Chaney.

Following the establishment of the fossil genus Metasequoia more than 20names for extinct species of the genus were erected over the next 60 years(Liu et al., 1999, Appendix A). Recently, Liu et al. (1999) found that almostall of these species were based on slight differences in the size and shape ofthe leaves and seed cones, and that the morphological variation of the fossilremains seen among these 20+ species was part of the natural morphologi-cal variability inherent to M. occidentalis. Liu et al.’s (1999) morphometricanalyses led them to conclude that only two species of fossil Metasequoia, M.occidentalis and M. milleri Rothwell et Basinger could be recognized fromthe entirety of the fossil record of the genus. More recently, Stockey et al.(2001) recognized a third species, M. foxii Stockey, Rothwell et Falder fromPaleocene (late Tiffanian [Ti4]) Paskapoo Formation, Alberta, Canada. The es-tablishment of this new species was based on the examination of more than10,000 specimens.

8 Ben A. LePage, Hong Yang and Midori Matsumoto

Figure 1-2. Most parsimonious tree for genera of the Taxodiaceae and Cupressaceae s.s.by the maximum parsimony method based on sequences of the matK gene, chlL gene,trnL-trnF IGS region and trn intron. The number above each branch is the number of stepsseparating each node and the numbers below indicate the percent of bootstrap values esti-mated from 1000 bootstrap replicates. The tree is rooted with Cunninghamia. Tree length =645; Consistency index = 0.860; Retention index = 0.908. Redrawn and modified fromKusumi et al. (2000).

3. MORPHOLOGICAL STASISAND GENETIC VARIATION

The lack of considerable morphological variability and species diversityseen in the fossil record of Metasequoia since its appearance in the LateCretaceous is important. The longevity of biological species is estimated to be