Vascular Epiphytes: General Biology and Related Biota (Cambridge Tropical Biology Series)

CAMBRIDGE TROPICAL BIOLOGY SERIES EDITORS: Peter S. Ashton Arnold Arboretum, Harvard University Stephen P. Hubbell Princeton University Daniel H. Janzen University of Pennsylvania Adrian G. Marshall University ofAberdeen Peter H. Raven Missouri Botanical Garden P. B. Tomlinson Harvard Forest, Harvard University

Vascular epiphytes

Vascular epiphytes General biology and related biota

DAVID H. BENZING Oberlin College

The right of the University of Cambridge to print anil sell all manner of books was granted by Henry VIII in 1534. The University has printed and published continuously since 1584.

CAMBRIDGE UNIVERSITY PRESS Cambridge New York Port Chester Melbourne Sydney

Published by the Press Syndicate of the University of Cambridge The Pitt Building, Trumpington Street, Cambridge CB2 1RP 40 West 20th Street, New York, NY 10011, USA 10 Stamford Road, Oakleigh, Melbourne 3166, Australia ©Cambridge University Press 1990 First published 1990 Library of Congress Cataloging-in-Publication

Data

Benzing, David H. Vascular epiphytes. (Cambridge tropical biology series) Bibliography: p. 1. Epiphytes. I. Title. QK922.B46 1990 582.5

88-35353

British Library Cataloguing in Publication Data Benzing, David H. Vascular epiphytes (Cambridge tropical biology series) 1. Epiphytes I. Title 581.5'24 ISBN 0-521-26630-0 hard covers Transferred to digital printing 2003

To A. S. Renfrow, for her skilled contribution and remarkable dedication to the production of this monograph and to most of my other publications and studies of epiphyte biology.

Contents

Preface Abbreviations Glossary

page xi xiii xiv

1 Epiphytism: a preliminary overview Historical notes Character and importance of epiphytic vegetation The geologic record of epiphytism Global occurrence Systematic occurrence Epiphytism as a coherent ecological category The epiphytic habitat Classification of epiphytes Continuously supplied versus pulse-supplied epiphytes

1 1 2 3 26 27 27 29 31 42

2 Photosynthesis Photosynthetic pathways Photosynthesis in nonfoliar organs Adaptations to specific exposures Shade acclimatization Optical and morphological enhancement of photosynthesis Leaf variegation and shoot architecture Vertical stratification Ancestral habitats Evergreenness/sclerophylly

44 44 58 61 63 64 65 71 77 79

3 Water balance Water use and conservation: defense against drought Water balance categories Moisture procurement Adaptive uniqueness vn

80 80 87 99 107

viii 4

5

6

7

Contents Mineral nutrition

112 112 114 117 125 147 150

Reproduction and life history

Breeding systems Movement of diaspores Germination Orchids and mycotrophy Survivorship Life-history characteristics

152 152 158 169 173 174 178

Mistletoes Systematics and biogeography Vegetative morphology Pollination Dispersal Germination and establishment Hemiparasitism: its variable nature Water balance Mineral nutrition Water versus nitrogen as the growth-limiting resource Evolution of aerial parasitism Host-mistletoe specificity Host-mistletoe crypsis Mistletoes as pathogens

184 184 185 189 190 191 194 194 197 200 201 202 205 207

Ecology

210 210

Nutritional categories Factors influencing nutrient supply, demand, and use Nutrient sources in forest canopies Nutritional modes Vegetative reduction Recapitulation

Host specificity Circumscribing, labeling, and documenting the epiphyte community Community composition Succession Relationships with canopy fauna Evolution of ant-epiphyte associations Phytotelm epiphytes Expanding the definition of tropical forest soil

219 222 224 229 238 241 246

Contents Epiphyte phytotelmata Stranglers and other primary hemiepiphytes Effects of epiphytes on associated vegetation Broader effects of epiphyte nutrition on the forest

ix 247 253 254 265

8 Epiphyte occurrence Distribution: taxonomic and geographic Reasons for the neotropical bias A more pervasive impetus for radiation Regional and smaller-scale determinants of distribution Predisposition and phylogenetic constraints Historical basis for canopy dwelling Envoi

271 271 273 282 285 299 302 311

References Author index Subject index Taxonomic index

313 333 339 346

Preface

There are about 25,000 vascular species sharing the peculiar habit of rooting in tree crowns rather than on the ground, yet only an occasional epiphyte the wide-ranging Spanish moss, for example - has attracted much scientific curiosity. Uncounted thousands of animal populations (mostly insects) regularly associate with these plants, sometimes because there are no alternatives for lodging, food, or other critical resources. Vascular epiphytes remain best known to horticulturists and systematists; the how and why of their growth in nature under such novel conditions have been mostly ignored. Other ecological groups such as carnivores, halophytes, mangroves, and parasites have been thoroughly covered in monographs despite their smaller numbers, more restricted distribution, and limited literature base. Also underrepresented is information on epiphyte-dependent fauna and effects on supporting trees. But times are changing. Improved climbing techniques allow extended observation and collection of representative fauna. Portable equipment for measuring such plant phenomena as gas exchange has opened the upper canopy to sophisticated analyses. Clearing land for roads, while destroying woodland, has fostered research in the field; so has establishment of permanent field stations, particularly in the neotropics. Results are heartening; what for many years was only a trickle of papers on nontaxonomic aspects of epiphyte biology and forest canopy fauna now approaches a flood. Three international symposia devoted to epiphytes have been held in just the past four years. What is needed now for the student and nonspecialist alike is a comprehensive and, it is hoped, provocative volume that distills the primary literature as well as the considerable body of unpublished data on epiphytism and interactions between canopy flora and co-occurring biota. There are several ways to produce this product. I have chosen to focus on functional aspects of arboreal life, and examples were chosen without regard to systematics. However, the extensive indexes are designed to provide the specialist easy access to ants, Bromeliaceae, mistletoes, Orchidaceae, residents of phytotelmata, and pteridophytes. Three strictly botanical topics are emphasized: (1) aspects of the forest canopy that most constrain its resident flora; (2) corresponding adaptations in that flora; and (3) occurrence and diversity XI

xii

Preface

among the epiphytes. Following a preliminary overview, focus will center on photosynthesis, water balance, mineral nutrition, and reproduction. Next, the epiphytes' effects on hosting trees and the ways in which they utilize and serve other life forms are highlighted. Finally, epiphyte occurrence will be considered from ecological, geographic, and historical perspectives. Speculation is unavoidable where there are gaps in our understanding of many of the subjects covered here; it is nevertheless my hope that the reader will not be irritated by guesswork but rather will regard it as a stimulus to further research. For more than 20 years, my interest in epiphytes has been variously assisted and promoted by numerous colleagues, students, and institutions. Travel to tropical habitats and laboratory research on bromeliads and orchids were made possible by grants and contracts from the National Science Foundation, the National Geographic Society, the National Park Service, and Oberlin College. Biologists who have been particularly helpful in providing information on specific plant groups or on other subjects included in this volume are Joe Arditti, Bradley Bennett, Cathy Burt, Diane Davidson, Calaway Dodson, Murray Evans, Susan Gardner, Alan Gentry, Amy Jean Gilmartin, Camilla Huxley, John Longino, Harry Luther, Michael Madison, Craig Martin, Nalini Nadkarni, Mauritzio Paoletti, Alec Pridgeon, Jack Putz, Suzanne Renner, Russ Sinclair, Ben and Debbie Stinner, Warren Ullum, John Utley, and Norris Williams. Oberlin College students have helped conduct many of my investigations on epiphyte structure and function. Especially noteworthy were the contributions of Andrew Bent, Ray Broggini, Chris Dahle, Rick Davidson, Karen Henderson, Page Owen, Will Pockman, Joanne Sulak, and John Titus. David Bermudes, Janice Derr, Ned Friedman, and Jeff Seemann not only provided valuable assistance while undergraduates at Oberlin but continue as collaborators from other institutions. Special thanks are owed to Calaway Dodson, David Miller, and Michael Zimmerman who read chapters and provided valuable input; also to Michael Madison and Barry Tomlinson for their critical reviews of the entire manuscript.

Abbreviations

Amax ATP C3 C4 CAM Chi Ca C; CS AH + 5nC MPa MUE NADP PAR PEPc PPFD PPNUE PS RH rm RPP RuBPc/o RWC ST TR ^crit ^L ^P ^s VAM WUE WVPD Xlll

maximum photosynthetic capacity adenosine triphosphate see R P P the Hatch and Slack photosynthetic pathway Crassulacean acid metabolism chlorophyll partial pressure of carbon dioxide outside the leaf concentration of carbon dioxide inside the leaf continuously supplied diurnal change in titratable acidity carbon isotope ratio; 13C enrichment in parts per thousand megapascals mineral use efficiency nicotinamide adenine dinucleotide phosphate photosynthetically active radiation phosphoenolpyruvate carboxylase photosynthetic photon flux density potential photosynthetic nitrogen use efficiency pulse-supplied relative humidity Malthusian coefficient reductive pentose phosphate or C3 pathway ribulose phosphate carboxylase/oxygenase relative water content as percentage of saturation spirally thickened (idioblasts) transpiration ratio leaf water potential at stomatal closure bulk leaf water potential turgor solute potential vesicular-arbuscular mycorrhizas water use efficiency water vapor pressure deficit

Glossary

Accidental epiphyte: A typically terrestrial species with occasional members that grow to maturity anchored in a tree crown. Allelopathy: The process whereby one plant inhibits or kills another through the production of toxic compounds. Allogamy: Seed production resulting from pollen flow between different plants. Anemochory: The dispersal of seeds by wind. Ant-fed ant-house epiphyte: A species that produces hollow organs (domatia) specifically for housing ant colonies. Ant nest-garden epiphyte: A species that regularly and often exclusively roots in arboreal ant nests. Atmospheric epiphyte: A species directly dependent on the atmosphere for moisture and nutrient ions (e.g., xerophytic Tillandsia). Autogamy: Seed production resulting from self-pollination. Axenic: Applied to tropical trees that by nature do not support epiphytes. Bromelioid: An adjective applied to taxa assigned to subfamily Bromelioideae of Bromeliaceae. CAM-cycling: A photosynthetic syndrome characterized by diurnal CO2 fixation and nocturnal recapture of respired CO2. CAM-idling: A photosynthetic syndrome characterized by continuous stomatal closure and energy maintenance through internalized CO2 recycling; a common stress response of CAM plants. Carton: The material constructed of plant fiber, seeds, feces, and diverse other materials by ants to produce their nests and enclosed runways. Chasmogamy: The condition allowing pollen transport to and from an opened flower. Clade: A group of species that share a single ancestral lineage. Cladogenesis: The process of creating two species from one; the splitting of a single lineage into two. Cleistogamy: The condition of a flower that sets seed without presenting anthers or stigma to pollinators. CS epiphyte: An epiphyte with relatively continuous access to external supplies of moisture and nutritive ions. XIV

Glossary

xv

Decarboxylase: An enzyme that catalyzes the release of CO2 from an organic acid. Deciduous: An adjective describing leaves that abscise in less than one year. Domatium: A plant cavity regularly occupied by ants. Epiparasite: A parasite that taps its host via a fungal intermediate. The term is also used to describe vascular parasites that attack other parasitic plants. Epiphyll: A nonvascular plant that inhabits the surfaces of foliage. Epivelamen: The delicate layer of cells forming the outer boundary of some velamentous roots. Eutroph: A plant native to fertile substrata. Evergreen: An adjective describing green organs - usually foliage - that remain functional for at least a full year. Everwet forest: A forest that receives enough rainfall through the year to support predominantly drought-sensitive vegetation (includes rain forest). Exodermis: The specialized outer cell layer of the root cortex that is especially well developed in epiphytic Orchidaceae. Facultative CAM: Carbon fixation via CAM or C3 photosynthesis depending on environmental conditions. Facultative epiphyte: A species that regularly grows epiphytically and rooted in earth-soil, often emphasizing one or the other habit in a particular habitat. Glycophyte: A plant that does not accumulate high concentrations of sodium chloride. Guild: A group of co-occurring but not necessarily related species that utilize one or more common resources. Halophyte: A plant native to saline habitats. Haustorium: The invasive appendage of a parasitic plant. Hemiepiphyte: A plant that maintains vascular connection with earth-soil over part of its life. The epiphytic stage may occur early (primary hemiepiphyte) or later (secondary hemiepiphyte). Hemiparasite: An haustorial parasite with significant photosynthetic capacity. Histosol: A soil composed primarily of organic matter (e.g., peat). Homoeosis: Assumption by one member of a series of a form or structure characteristic of another member of the series. Homoiohydry: The condition of maintaining tissue hydrature relatively independent of ambient humidity. Homoptera: The taxonomic order of arthropods including plant-sucking forms exemplified by aphids and scale insects.

xvi

Glossary

Hypodermis: A subepidermal zone of usually achlorophyllous, thin-walled, collapsible water storage cells in leaves. Iteroparity: The type of reproductive timing illustrated by plants that fruit repeatedly rather than once. Lineage: The unbroken succession of generations that constitutes the history of a taxon through geologic time. Mist epiphyte: A species equipped to live where moisture is often available as mist. Mistletoe: A woody hemiparasite of tree branches. Monocarpy: The type of life cycle characterized by a single reproductive effort just before death. Mycotroph: A plant with fungus-assisted nutrition (e.g., orchid seedlings) but excluding species with typical mycorrhizas. Myrmecochory: The dispersal of seeds by ants. Myrmecophyte: A plant that is regularly associated with ant colonies and utilizes that symbiosis to some degree. Nitrogenase: The enzyme complex responsible for reducing N2 to organic nitrogen. Nutritional piracy: The process whereby epiphytes intercept nutrients moving between the supporting tree crown and the forest floor. Oligotroph: A plant native to nutrient-deficient substrata. Paedomorphy: Exhibition of adult traits that reflect juvenile conditions in an ancestor. Peloton: A dense mass of collapsed chitinous walls of an invading fungus that characterizes infected plant cells of aging orchid mycorrhizas. Phorophyte: A support for vascular epiphytes. Phylloclade: A branch that resembles, and functions like, a leaf. Phytoalexin: Low-molecular-weight, toxic organic compounds synthesized in certain plant tissues in response to infection by pathogenic microbes. Phytotelmata: Natural plant cavities that hold water and support resident aquatic organisms. Phytotelm plant: A plant that produces phytotelmata. Pluvial forest: Continuously wet forest that receives rainfall exceeding 5000 mm/yr (includes rain forest). Pneumathode: A localized zone in the rhizodermis of a velamentous root that repels moisture and apparently promotes ventilation of the root interior. Poikilohydry: The condition of maintaining tissue water content at levels strongly influenced by ambient humidity. PS epiphyte: A pulse-supplied epiphyte with only sporadic access to external supplies of moisture and required nutritive ions.

Glossary

xvii

Reproductive index: The proportion of the mature plant body committed to seeds and associated reproductive tissue. Ruderal: A fast-maturing plant native to temporary but resource-rich habitats. Sciophyte: A plant tolerant of deep shade. Sclerophylly: The condition describing evergreen foliage containing much sclerified tissue. Seasonal forest: Forest occurring in areas characterized by enough seasonal variation in rainfall to require plant tolerance for moderate to severe drought. Shootless orchid: A species with much reduced vegetative shoots and green roots that have replaced foliage as photosynthetic organs (members of subtribe Sarcanthinae). Spathe: A sheathing bract or pair of bracts enclosing an inflorescence. Strangler: A primary hemiepiphyte that produces a robust root system that eventually provides self-support and may kill the host tree (e.g., Ficus). Suspended humus: The mantle of degrading vegetation and living plants that covers bark and serves as a rooting medium for epiphytes native to humid forests. Synusia: A group of co-occurring plants of the same life form. Tillandsioid: An adjective applied to taxa assigned to subfamily Tillansioideae of Bromeliaceae. Tilosome: A fibrous outgrowth produced by velamen cells positioned above transfer cells in the aerial roots of some orchids and other monocots. Transfer cell: A cell specialized to perform solute transport and absorption (e.g., passage cells of the root exodermis and endodermis). Transpiration ratio: A coefficient produced by dividing the mass of water lost in transpiration by the simultaneous gain in weight attributable to photosynthesis. Trash-basket epiphyte: A species that creates relatively dry collections of intercepted litter in catchments fashioned of roots or leaves (e.g., Catasetum, Platycerium). Trophic myrmecophyte: See ant-fed ant-house epiphyte. Velamen: A spongy, multilayered rhizodermis composed of dead cells that surround the cortex of aerial and some terrestrial roots, particularly those of orchids. Vivipary: The germination of an embryo before the enclosing seeds are shed; the term is sometimes also used to describe the proliferation of asexual progeny on an inflorescence.

Epiphytism: a preliminary overview

Historical notes Columbus is credited with the first recorded comment on canopy-adapted vegetation; he wrote that tropical trees "have a great variety of branches and leaves, all of them growing from a single root" (Gessner 1956). The earliest known picture of an epiphyte - or, for that matter, reference to American botany - appears in The Badianus Manuscript, a Mexican herbal of 1552, written and probably illustrated by the Aztec Indian physician Martinus de la Cruz and translated into Latin by his Indian colleague Juannes Badianus at the College of Santa Cruz (Emmart 1940). The subject was Vanilla fragrans, a vining hemiepiphytic orchid. The fruit of this species (tlilxochitl in Aztec, meaning "black flower") was an ingredient in the doctor's prescription for "The Traveler's Safeguard," a mixture of pulverized herbs wrapped in a magnolia leaf and hung around the neck so that the voyager could "catch and inhale the very redolent odor . . . " By the eighteenth century, ships' captains and explorers the world over were carrying ornamental plants, epiphytes included, back to Europe. Within decades, a brisk trade had developed; many additional aroids, bromeliads, cacti, orchids, and ferns were imported. Showiness, small size, and easy culture encouraged fads that drove prices to exorbitant levels and prompted more than one collector to lie about where he found his specimens. But scientific interest in these plants did not keep pace; other groups such as carnivores, halophytes, ruderals, and succulents are far better known today. A. F. W. Shimper's monograph Die epiphytische Vegetation Amerikas was a noteworthy exception. This treatise (1888) and related works (e.g., 1884, 1903) published over a long career were major contributions to the study of epiphytes, and in fact remain arguably the most comprehensive treatment to date. Schimper's skillful accounts of fascinating and unusual adaptations in several epiphytic taxa contain remarkable insight for that time. Over the next 75 years, occasional papers covered the functional and ecological aspects of epiphytism: absorption by certain bromeliad leaf trichomes (Mez 1904); fauna and nutrition of tank bromeliads (Picado 1913);

Epiphytism: a preliminary overview

water balance in orchid roots, particularly the role of the velamen-exodermis complex (Haberlandt 1914); osmotica in epiphyte versus host foliage (Harris and Lawrence 1916; Harris 1918); autecology of the epiphytic fern Polypodium polypodioides (Fig. 1.6; Pessin 1925); and an overview of New Zealand's canopy-adapted flora (Oliver 1930). Richards (1952) covered epiphytes in The Tropical Rain Forest, and Curtis (1952) cited 170 references on epiphytism in his reviews of common life systems in plants. Other classic writings include Went's (1940) attempt to explain the factors responsible for host selection, and the identification by Sanford (1969, 1974) and Johansson (1974) of the influence of climate on orchid distribution in Nigeria. Broader coverages are those of Gessner (1956) on water economy and Madison's (1977) overview. Benzing and Seemann (1978) and Benzing (1983, 1984) considered interactions between epiphytes and their supports and dependent fauna - subjects that provide the second focus for this monograph. A recent surge of reports on epiphyte biology reflects increased interest in tropical forests and an improved climate for biological research in parts of Latin America, Malaysia, Singapore, and several other strategically located areas. Journals now contain papers on physiology, functional anatomy, life history, associated biota, and the effects of epiphytes on nutrient cycling in hosting ecosystems. Character and importance of epiphytic vegetation

Epiphytes are responsible for much of the biotic diversity that makes humid tropical forests the most complex of all the world's terrestrial ecosystems (Gentry and Dodson 1987a). Canopy-based species constitute fully one third - perhaps up to 50% - of the total vascular flora in some pluvial neotropical forests (Fig. 8.4). In addition, the capacity of these sites to accommodate fauna, including the majority of a suspected 30,000,000 insect species worldwide (Erwin 1983), can be attributed in significant measure to the shelter and sustenance provided by epiphytic vegetation. Effects on community dynamics are no less impressive. Green biomass (and presumably photosynthetic capacity as well) of nonvascular and higher plants anchored in tree crowns can rival - probably even exceed - that of phorophytes. Epiphytes display various mechanisms, some novel, for countering drought and acquiring essential ions; such specialization is unexcelled in the plant world. Some animals are preyed upon, others become symbiotic mutualists; outof-the-ordinary substrata are utilized. Of all wide-ranging plant groups, the tropical forest canopy supports one of the least studied and most important.

The geologic record of epiphytism A few days' exploration can still yield undescribed epiphytes, primarily in Orchidaceae but also in such sizable families as Araceae and Gesneriaceae. The geologic record of epiphytism Paleontologists have found little evidence of pre-Cenozoic or even early- to mid-Tertiary epiphytism. Araceae and several other families that today contain many epiphytes were well differentiated by the end of the Eocene, but no fossil remains can be unquestionably assigned to their canopy-based lineages. Except for a few doubtful Eocene fossils from southern Europe, Orchidaceae have not been reported in pre-Quaternary sediments (Schmid and Schmid 1977). Tillandsia-like pollen has been reported for the Panamanian Eocene (A. Graham pers. comm.), but there is no way to determine the habits of the bromeliads that produced it. Animal dispersal in so many epiphyte-containing angiosperm families also indicates that tree crowns were colonized only recently by flowering plants. Fleshy fruit, and the bats, birds, and mammals that eat it, first became diverse and abundant in the Paleocene/Eocene (Tiffney 1984). Involvement of early pteridophytes and primitive seed plants in epiphytism is even more obscure. Petrified stems of arborescent lycopods, calamites, and other potential pre-Cretaceous hosts show penetration by alien roots, but these intrusions probably occurred after death; the invading axes appear to belong to other terrestrials. The absence of verified epiphytic angiosperms in ancient geologic deposits and their concentration today in a few large advanced families point to a recent massive expansion (Table 1.1). The present active state of evolution of many tropical orchid clades and other species-rich, canopy-based genera (e.g., Anthurium, Rhododendron, Drymonia, Peperomia, Tillandsia; Table 1.2), as well as their concentration in geologically young montane habitats, suggests that much epiphyte diversity dates from the Pliocene/Pleistocene. Canopy colonization was also limited before the rise of Magnoliophyta because this division had to supply most of the substrata. The broadleaf forests at low humid latitudes, where so many epiphytes anchor today, began to develop near the Cretaceous/Tertiary boundary. That was only about 65 million years ago after a shift toward wetter climate fostered extensive multistratal vegetation. Early angiosperms were small and probably restricted to savanna, riverine, and other disturbed habitats. Extant relatives provide a little insight on the nature of early conifers as arboreal habitats: A few modern taxa {Taxodium and some Pinus spp.) support heavy epiphyte

Epiphytism: a preliminary overview

Table 1.1. The systematic distribution of vascular epiphytes Taxa Division Pteridophyta Class Filicopsida Subclass Polypodiidae Order Ophioglossales Family Ophioglossaceae Genus Ophioglossum L. Order Polypodiales Family Schizaeaceae Genus Schizaea J. Sm. Family Hymenophyllaceae Genus Hymenophyllum J. Sm. Trichomanes L. Family Vittariaceae Genus Ananthacorus Underw.& Maxon Anetium (Kunze) Splitg. Antrophyum Kaulf. Hecistopteris J. Sm. Monogramma Schkurh. Polytaenium Desv. Scoliosorus Moore Vaginularia Fee Vittaria J. Sm. Family Dennstaedtiaceae Genus Lindsaea Dryander ex J. Sm. Oenotrichia Copel. Family Dryopteridaceae Genus Arthropteris J. Sm. Dryopteris Adans. Elaphoglossum Schott Lastreopsis Ching Lomariopsis Fee Oleandra Cav. Polystichum Roth Psammiosorus C. Christ. Rumohra Raddi Teratophyllum Holtt. Family Aspleniaceae Genus Asplenium L. Family Davalliaceae Genus Araiostegia Copel. Davallia J. Sm. Davallodes (Copel.) Copel. Humata Cav. Nephrolepis Schott Parasorus Alderwerelt Scyphularia Fee Trogostolon Copel. Family Blechnaceae Genus Stenochlaena J. Sm.

Genera* 92/239 90/235 88/233 1/3 1/3 87/224 1/4 2/2 9/9

2/18 10/55

1/7 8/9

1/9

Species* 2,593/9,000 2,388/7,749 2,380/7,740 8/56 8/56 8/30 2,372/7,565 2/170 2/30 400/600 250/300 150/300 112/112 1/1 1/1 40/40 1/1 2/2 10/10 1/1 6/6 50/50 3/370 2/150 1/4 292/1,920 15/15 1/150 250/500 1/35 1/45 20/40 1/160 1/1 1/2 1/9 400/675 400/650 139/150 12/12 40/40 11/11 50/50 15/20 1/1 8/8 2/2 1/175 1/5

The geologic record of epiphytism

Table 1.1. (cont.) Genera"

Taxa

Family Polypodiaceae Genus Acrosorus Copel. Aglaomorpha Schott Amphoradenium Desv. Anarthropteris Copel. Arthromeris (Moore) J. Sm. Belvisia Mirbel Calymmodon Presl Campyloneurum Presl Christiopteris Copel. Colysis Presl Crypsinus Presl Dendroconche Copel. Diblemma J. Sm. Dictymia J. Sm. Drymotaenium Makino Drynaria (Bory) J. Sm. Drynariopsis (Copel.) Ching Eschatogramme Trev. Goniophlebium (Bl.) Presl Grammatopteridium Alderwerelt Grammatis Sw. Holcosorus Moore Holostachyum (Copel.) Ching Lecanopteris Reinw. Lemmaphyllum Presl Leptochilus Kaulf. Loxogramme (Bl.) Presl Marginariopsis C. Christ. Merinthosorus Copel. Microgramma Presl Microsorium Link Nematopteris Alderwerelt Neocheiropteris C. Christ. Neurodium Fee Niphidium J. Sm. Oleandropsis Copel. Oreogrammatis Copel. Paragramma (Bl.) Moore Paraleptochilus Copel. Photinopteris J. Sm. Platycerium Desv. Pteo/?6>///s/Kunth in HBK

Polypodiopteris Reed Polypodium L. Prosaptia Presl Pteropsis Desv. Pycnoloma C. Christ. Pyrrosia Mirbel

53/65

Species0 1,023/1,100 5/5 4/4 6/6 1/1 6/9 15/15 25/25 25/25 4/4 2/30 40/40 2/2 1/1 3/3 2/2 20/20 1/1 4/4 20/20 2/2 400/400 3/3 1/1 15/15 4/4 1/1 25/25 1/1 2/2 13/13 40/40 1/1 3/3 1/1 4/4 1/1 1/1 2/2 2/2 1/1

15/15 10/10 3/3 140/150 20/20

6/6 3/3 100/100

t>

Epiphytism: a preliminary overview

Table l.l.(cont) Genera0

Taxa Scleroglossum Alderwerelt Selliguea Bory Solanopteris Copel. Thayeria Copel. Thylacopteris Kunze ex Mett. Subclass Psilotidae Order Psilotales Family Psilotaceae Genus Psilotum Sw. Tmesipteris Bernh. Class Lycopodiopsida Order Lycopodiales Family Lycopodiaceae Genus Lycopodium L. Order Selaginellales Family Selaginellaceae Genus Selaginella Beauv. Division Cycadophyta Class Cycadopsida Order Cycadales Family Zamiaceae Genus Zamia L. Division Gnetophyta Class Gnetopsida Order Gnetales Family Gnetaceae Genus Gnetum L. Division Magnoliophyta Class Magnoliopsida Subclass Magnoliidae Order Magnoliales Family Winteraceae Genus Drimys J. R. & G. Forst. s.l. Order Piperales Family Piperaceae Genus Peperomia Ruiz & Pav.

2/2 2/2 2/2 2/4 1/2 1/2 1/1 1/1 2/10 2/10 2/10 2/7 1/3 1/3 1/1 1/1 782/11,836 262/9,409 4/496 1/177 1/7 2/20 2/10

Piper L.

Order Ranunculales Family Ranunculaceae Genus Thalictrum L. Subclass Hamamelidae Order Urticales Family Moraceae Genus Antiaropsis K. Schum. Coussapoa Aubl. Ficus L. Pourouma Aubl. Family Urticaceae Genus Elatostema Gaudich.

1/148 1/50 8/174 7/112 4/40

3/45

Species* 6/6 4/5 4/4 1/1 2/2 8/9 8/9 8/9 2/2 6/7 205/1,251 200/401 200/401 200/400 5/700 5/700 5/700 2/155 2/155 2/155 2/125 2/35 3/66 3/66 3/30 3/30 3/30 20,859/221,868 4,251/167,893 717/11,761 6/2,948 6/100 6/70 710/1,782 710/3,100 700/1,000 10/2,000 1/3,148 1/2,000 1/150 563/3,373 562/2,130 522/1,000 1/1 20/45. 500/800 1/50 40/700 10/200

The geologic record of epiphytism

Table 1.1. (cont.) Taxa Pilea Lindl. Procris Comm. ex Juss. Order Myricales Family Myricaceae Genus Myrica L. Subclass Caryophyllidae Order Caryophyllales Family Cactaceae Genus Aporocactus Lem. Cryptocereus Alex. Disocactus Lindl. Eccremocactus Britton & Rose Epiphyllum Haworth Heliocereus (Berg.) Britton & Rose Hylocereus (Berg.) Britton & Rose Lymanbensonia Kimm. Mediocactus Britton & Rose Nopalxochia Britton & Rose Pfeiffera Salm-Dyck Rhipsalis Gaertn. Schlumbergera Lem. Selenicereus (Berg.) Britton & Rose Strophocactus Britton & Rose Weberocereus Britton & Rose Werckleocereus Britton & Rose Wilmattea Britton & Rose Family Caryophyllaceae Genus Arenaria L. Stellaria L. Subclass Dilleniidae Order Theales Family Marcgraviaceae Genus Marcgravia L. Marcgraviastrum Bedell, ined. Norantea Aubl. Ruyschia Jacq. Sarcopera Bedell, ined. Schwartzia Veil. Souroubea Aubl. Family Clusiaceae Genus Clusia L. Clusiella Planch. & Triana Havetiopsis Planch. & Triana Odematopus Planch. & Triana Quapoya Aubl. Renggeria Meisn. Order Malvales Family Elaeocarpaceae Genus Sericolea Schlecht.

Genera*

1/3 1/3 20/500 20/458 18/115

2/75 60/1,460 13/176 7/7

6/50

3/225 1/10

Species" 20/400 10/20 1/50 1/50 1/35 152/10,864 152/9,464 150/1,500 6/6 1/2 7/7 3/3 21/21 5/5 18/20 1/1 2/2 1/1 1/1 58/65 6/6 13/17 1/1 3/3 2/2 1/1 2/2,000 1/250 1/150 925/24,643 181/3,385 89/122 50/55 10/15 1/2 7/7 4/10 8/14 9/19 92/1,200 85/145 3/7 1/5 1/10 1/3 1/3 6/3,300 1/400 1/20

Epiphytism: a preliminary overview

Table 1.1. (cont) Taxa

Genera* Family Bombacaceae Genus Ceiba Mill. Spirotheca Ulbrich Order Nepenthales Family Nepenthaceae Genus Nepenthes L. Order Violales Family Begoniaceae Genus Begonia L. Order Ericales Family Epacridaceae Genus Prionotes R. Br. Family Ericaceae Genus Agapetes D. Don ex G. Don Anthopterus W. J. Hook. Anthopteropsis A. C. Sm. Calopteryx A. C. Sm. Cavendishia Lindl. Ceratostema Juss. Costera J. J. Sm. Demosthenesia A. C. Sm. Didonica Luteyn & Wilbur Dimorphanthera F. Muell. Diogenesia Sleum. Diplycosia Bl. Disterigma Niedenzu ex Drude Gaultheria Kalm ex L. Gonocalyx Planch. & Lind. ex A. C. Sm. Killipiella A. C. Sm. Lateropora A. C. Sm. Lyonia Nutt. Macleania W. J. Hook. Mycerinus A. C. Sm. Oreanthes Benth. Orthaea Kl. Pellegrinnia Sleum. Pernettyopsis King & Gamble Plutarchia A. C. Sm. Psammisia Kl. Rhododendron L. Rusbya Britton Satyria Kl. Semiramisa Kl. Siphonandra Kl. Sphyrospermum Poepp. & Endl. Themistoclesia Kl. Thibaudia Ruiz & Pav. Cft/cya Wilbur & Luteyn Vaccinium L.

2/25

Species* 5/200 1/10

4/4 1/8 1/1

1/276 1/4

37/174 1/30 36/122

6/193 6/75 6/75 30/4,818 30/1,000 30/900 673/4,044 1/400 1/1

672/3,500 60/80 3/6 1/1 1/2

75/100 16/23 8/8

6/11 2/2

25/71 5/13 61/98 15/30 8/200 6/8 2/2 2/3

1/35 25/45 1/3 4/4

20/31 1/4 1/1

6/12 25/55 112/850 1/1

20/23 2/4 1/1

18/22 22/31 20/60 1/1

95/450

The geologic record of epiphytism

Table 1.1. (cont.) Taxa Order Ebenales Family Sapotaceae Genus Bumelia Sw. Order Primulales Family Myrsinaceae Genus Cybianthus Mart. Embelia Burm. Grammadenia Benth. Myrsine L. Subclass Rosidae Order Rosales Family Cunoniaceae Genus Ackama A. Cunn. Weinmannia L. Family Pittosporaceae Genus Pittosporum Banks ex Soland. Family Grossulariaceae Genus Phyllonoma Willd. ex Schult. Family Crassulaceae Genus Echeveria DC. Kalanchoe Adans. Sedum L. Family Saxifragaceae Genus Hydrangea L. Quintinia A. DC. Family Rosaceae Genus Pyrus L. Order Myrtales Family Alzateaceae Genus Alzatea Family Myrtaceae Genus Mearnsia Merr. Metrosideros Banks ex Gaertn. Family Onagraceae Genus Fuchsia Family Melastomataceae Genus Adelobotrys DC. Anerincleistus Korth. Backeria Bakh. f. Blakea P. Br. Calvoa J. D. Hook Catanthera F. Muell. Clidemia D. Don Creochiton Bl. Dalenia Korth. Dicellandra J. D. Hook. Diplectria Reichb. Dissochaeta Bl. Graffenrieda DC.

Genera* 1/87 1/70 4/64 4/30

68/3,194 10/317 2/25

Species" 1/1,752 1/800 1/60 28/2,100 28/1,000 5/40 5/130 6/15 12/200 791/57,047 21/6,696 3/350 1/3

1/9

1/25 3/25

2/40 1/100 37/445 1/1

2/140

2/170 5/200 5/150 1/350 1/8

5/900 2/150 1/200 2/600 4/700 2/80 2/20 3/3,000 3/30 671/7,205 1/1 1/1

7/3,000 4/7

1/17 33/180

3/60 15/675 15/100 648/4,770 21/25 1/1 2/2

98/100 4/18 16/16 11/145 4/6 2/2 1/3 4/4

20/20 2/40

10

Epiphytism: a preliminary overview

Table l.l.(cont) Genera*

Taxa Gravesia Naud. Hypenanthe Bl. Kendrickia J. D. Hook. Leandra Raddi Macrolenes Naud. ex Miq. Medinilla Gaudich. Miconia Ruiz & Pav. Monolena Triana Myrianthemum Gilg Neodissochaeta Bakh. f. Omphalopus Naud. Ossaea DC. Pachycentria Bl. Phainantha Gleason Plethiandra J. D. Hook. Pleiochiton Naud. Pogonanthera Bl. Preussiella Gilg Topobea Aubl. Triolena Naud. Order Cornales Family Cornaceae Genus Griselinia G. Forst. Order Celastrales Family Celastraceae Genus Euonymus L. Microtropis Wall. Family Aquifoliaceae Genus //ex L. Order Rhamnales Family Vitaceae Genus Pterisanthes Bl. Tetrastigma Planch. Order Sapindales Family Aceraceae Genus Acer L. Family Burseraceae Genus Dacryodes Vahl Family Anacardiaceae Genus Spondias L. Order Geraniales Family Balsaminaceae Genus Impatiens L. Order Apiales Family Araliaceae Genus Didymopanax Decne. & Planch. Motherwellia F. Muell. Oreopanax Decne. & Planch. Pentapanax Seem. Polyscias J. R. & G. Forst Pseudopanax C. Koch

Species* 13/110 4/4 1/1

4/200 20/20 300/400 11/1,000 6/15 1/1

10/10 1/1

2/100 8/8 4/4 6/6 7/7 1/1 2/2

1/16 1/11 3/119 2/50 1/4

2/67 2/11 3/500 1/2

1/18 1/70 1/25 1/2

11/370 9/70

59/60 2/18 3/140 3/100 3/6

4/2,149 3/800 2/175 1/70 1/400 1/400 4/1,670 4/700 2/20 2/90 3/5,346 1/112 1/110 1/600 1/50 1/600 1/12 5/2,154 5/451 5/450 80/3,700 78/700 1/40 1/1

1/120 2/15 5/80 2/6

The geologic record of epiphytism

11

Table l.l.(cont) Taxa Scheflera J. R. & G. Forst. Sciadophyllum P. Br. Tupidanthus J. D. Hook & Thorns. Family Apiaceae Genus Hydrocotyle L. Myrrhidendron Coulter & Rose Subclass Asteridae Order Gentianales Family Loganiaceae Genus Desfontainia Ruiz & Pav. Fragraea Thunb. Family Gentianaceae Genus Leiphaimos Cham. & Schlecht. Macrocarpaea Gilg Voyria Aubl. Family Apocynaceae Genus Mandevilla Lindl. Family Asclepiadaceae Genus Ceropegia L. Conchophyllum Bl. Cynanchum L. Dischidia R. Br. Dischidiopsis Schlecht. Heynella Backer Hoya R. Br. Marsdenia R. Br. Order Solanales Family Solanaceae Genus Dyssochroma Miers Ectozoma Miers Hawkesiophyton A. T. Hunz. Juanulloa Ruiz & Pav. Lycianthes Hassl. Markea L. C. Rich. Merinthopodium Donn. Sm. Rahowardiana D'Arcy Schultesianthus A. T. Hunz. Solandra Sw. Solanum L. Trianaea Planch. & Linden Order Lamiales Family Verbenaceae Genus Clerodendrum L. Order Scrophulariales Family Scrophulariaceae Genus Wightea Wall. Family Gesneriaceae Genus Aeschynanthus Jack Agalmyla Bl. Alloplectus Mart.

Genera0

Species0 60/200 5/30

2/300

1/1

2/3,000 1/100 1/5

102/3,585 14/547 2/20 3/75

1/200 8/250

1,103/60,205 163/5,502 21/500 1/5

20/35 4/1,000 1/40 2/35 1/8

1/2,000 1/114 137/2,000 3/160 1/10 2/150 60/90 9/9 1/1

12/182 12/85

60/200 1/10 56/5,099 56/2,800 2/2 1/1 3/3

10/10 2/200 8/8 5/5 1/1 5/5

1/10 15/1,700 3/3

1/403 1/100 37/758 1/190 30/120

2/7,805 2/2,600 2/400 615/11,465 3/4,000 3/3

560/2,500 80/80 15/15 25/65

12

Epiphytism: a preliminary overview

Table 1.1. (cont.) Genera*

Taxa Alsobia Hanst. Asteranthera Hanst. Boea Comm. ex Lam. Capanea Planch. Codonanthe (Mart.) Hanst. Codonanthopsis Mansf. Columnea L. Cyrtandra J. R. & G. Forst Dalbergaria Tussac Dichrotrichum Reinw. Didymocarpus Wall. Drymonia Mart. Fieldia A. Cunn. Heppiella Regel Loxostigma C. B. Cl. Lysionotus G. Don Mitraria Cav. Monopyle Benth. Nematanthus Schrader Neomortonia Wiehler Paradrymonia Hanst. Pentadenia (Planch.) Hanst. Rufodorsia Wiehler Sarmienta Ruiz & Pav. Sinningia Nees Streptocarpus Lindl Trichantha W. J. Hook. Family Acanthaceae Genus Glockeria Nees Louteridium S. Watson Family Bignoniaceae Genus Gibsoniothamnus L. O. Wms. Schlegelia Miq. Family Lentibulariaceae Genus Pinguicula L. Utricularia L. Order Campanulales Family Campanulaceae Genus Burmeistera Karst. & Triana Canarina L. Centropogon Presl Clermontia Gaudich. Cyanea Gaudich. Order Rubiales Family Rubiaceae Genus Amaracarpus Bl. Balmea Martinez Coprosma J. R. & G. Forst. Cosmibuena Ruiz & Pav. Didymochlamys J. D. Hook

2/250 2/100 2/5 5/93 5/70

25/451 25/450

Species* 2/2 1/1 2/25 8/11 17/17 3/3 70/70 10/600 65/65 4/4 1/120 100/110 1/1 1/23 3/4 2/2 1/1 1/23 26/26 3/3 8/28 23/24 4/4 1/1 3/60 10/132 70/70 8/2,500 1/10 7/7 29/800 11/11 18/18 15/200 2/60 12/150 24/2,490 24/2,000 5/82 1/3 7/300 10/27 1/60 223/6,503 223/6,500 3/60 1/1 6/90 6/15 2/2

13

The geologic record of epiphytism

Table l.l.(cont) Genera0

Taxa Hillia Jacq. Hydnophytum Jack Lecananthus Jack Lucinaea DC. Malanea Aubl. Manettia Mutis ex L. Myrmecodia Jack Myrmedoma Becc. Myrmephytum Becc. Nertera Banks & Soland. Ophiorrhiza L. Posoqueria Aubl. Proscephaleium Korth. Psychotria L. Randia L. Ravnia Oerst. Relbunium Benth. & J. D. Hook. Schradera Vahl Squamellaria Becc. Timonius DC. Order Asterales Family Asteraceae Genus Anaphylis DC.

20/20 75/80 1/2

15/25 2/27 5/130 40/45 2/2 2/2

6/12 5/150 1/15 1/1

7/700 2/250 4/4

2/30 12/15 2/2

8/1,100 8/1,100

£>a/z//tf Cav.

Eupatorium L. (s.l.) Liabum Adans. Pseudogynoxys (Greenm.) Cabrera Rensonia S. F. Blake Senecio L. Tuberostylis Steetz

Class Liliopsida Subclass Arecidae Order Cyclanthales Family Cyclanthaceae Genus Asplundia Harling Dicranopygium Harling Evodianthus Oerst. Ludovia Brongn. Sphaeradenia Harling Stelestylis Drude Thoracocarpus Harling Order Pandanales Family Pandanaceae Genus Pandanus L. Order Arales Family Araceae Genus Amydrium Schott Anthurium Schott Epipremnum Schott Monstera Adans.

Species*

1/150 20/20,000 20/20,000 1/35 1/20 7/1,200 2/90 1/21 1/1

5/2,000 2/2

520/2,427 21/329 7/10 7/10

16,608/53,975 1,439/6,461 86/200 86/200 60/90 5/50 1/1 3/3

15/40 1/3 1/3

13/116 13/110

1/3 1/1

4/732 4/732 4/550 1,349/2,529 1,349/2,500 4/4

750/1,000 15/15 29/30

14

Epiphytism: a preliminary overview

Table 1.1. (cont.) Taxa Pedicellarum Hotta Philodendron Schott Pothos L. Remusatia Schott Rhaphidophora Hassk. Rhodospatha Poepp. Scindapsus Schott Stenospermation Schott Syngonium Schott Subclass Commelinidae Order Commelinales Family Rapateaceae Genus Epidryos Maguire Stegolepis Kl. ex Koern. Family Commelinaceae Genus Campelia L. C. Rich. Cochliostema Lem. Cyanotis D. Don. Order Cyperales Family Cyperaceae Genus Cephalocarpus Nees Cyperus L. Pseudoeverardia Gilly Family Poaceae Genus Microlaena R. Br. Tripogon Roem. & Schult. Subclass Zingiberidae Order Bromeliales Family Bromeliaceae Genus Acanthostachys Link. K1.& Otto Aechmea Ruiz & Pav. Araeococcus Brongn. Billbergia Thunb. Brocchinia Schult.f. Bromelia L. Canistrum E. Morr. Catopsis Griseb. Glomeropitcairnia Mez Guzmania Ruiz & Pav. Hohenbergia Bak. Hohenbergiopsis L. B. Sm. & R. Read Lymania R. Read Mezobromelia L. B. Sm. & R. Read Navia J. H. Schult. Neoregelia L. B. Sm. Nidularium Lem. Pitcairnia L'Herit. Protea Brongn. & C. Koch Pseudaechmea L. B. Sm. & R. Read Quesnelia Gaudich

Genera*

Species0 1/1

300/350 50/75 1/4

10/703 5/71 2/16

100/100 14/20 20/30 30/30 35/35 15/14,977 10/1,004 6/100 3/3

3/50

3/23 4/700 1/3 2/2

5/570 3/70

1/50 5/12,000 3/4,000 1/7

1/550 2/500 33/134 26/45 26/45

1/1

2/8,000 1/10 1/20 1,170/4,520 1,144/2,500 1,144/2,500 2/2

120/150 4/4

45/50 3/18 3/40 3/7

20/20 2/2

120/140 20/40 1/1 4/4 4/4

2/60 65/75 15/22 75/280 5/7 1/1

6/12

The geologic record of epiphytism

15

Table l.l.(cont.) Taxa Ronnbergia E. Morr. & Andre Streptocalyx Beer Tillandsia L. Vriesea Lindl. Wittrockia Lindl. Order Zingiberales Family Zingiberaceae Genus Alpinia Roxb. Brachychilum (R. Br. ex Wall.) Petersen Burbidgea J. D. Hook. Hedychium Koen. Riedelia Oliv. Family Costaceae Genus Cost us L. Family Marantaceae Genus Maranta L. Subclass Liliadae Order Liliales Family Liliaceae Genus Astelia Banks & Soland. Clivia Lindl. Collospermum Skotts. Curculigo Gaertn. Cyrtanthus Ait. Dianella Lam. Hippeastrum Herb. Pamianthe Stapf Rhodocodon Baker Smilacina Desf. Family Agavaceae Genus Agave L. Yucca L. Family Smilacaceae Genus Lapageria Ruiz & Pav. Luzuriaga Ruiz & Pav. Family Dioscoreaceae Genus Dioscorea L. Order Orchidales Family Burmanniaceae Genus Burmannia L. Family Orchidaceae Genus Abdominea J. J. Sm. Acampe Lindl. Acineta Lindl. Acostaea Schltr. Acriopsis Reinw. ex Bl. Ada Lindl. Adenoncos Bl. Adrorhizon J. D. Hook. Aerangis Rchb. f.

Genera*

Species" 6/7

14/15 400/450 200/260 7/89 5/47

4/6

26/2,020 20/1,000 1/100 1/1 5/5

1/4

1/30 456/1,199 15/451 10/280

12/50 1/50 4/175 4/150 2/400 2/23 13,984/27,516 31/8,248 24/4,000 6/25 1/3 5/5

1/10 1/47 2/30 2/75 1/3 1/8

2/18 2/12

4/25 3/600 1/300 2/40 3/300 1/1 2/3

1/6

441/748 1/20 440/725

1/630 1/600 13,953/19,268 2/130 2/57 13,951/19,128 2/2 6/6

10/10 8/8

12/12 9/9

17/17 1/1

60/60

16

Epiphytism: ii preliminary overview

Table 1 .1. (cont.) Genera*

Taxa Aeranthes Lindl. Aerides Lour. Aganisia Kaempf. ex Spreng. Aglossorhyncha Schltr. Agrostophyllum Bl. Alamania La LI. & Lex. Ambrella H. Perrier Ames i ella Schltr. ex Garay Amparoa Schltr. Ancistrochilus Rolfe Ancistrorhynchus Finet Andreettaea Luer Angraecopsis Krzl. Angraecum Bory Anguloa Ruiz & Pav. Ansellia Lindl. Anthosiphon Schltr. Antillanorchis Garay Appendicula Bl. Arachnis Bl. Armodorum Breda Arpophyllum La LI. & Lex. Artorima Dressl. & Poll. Ascocentrum Schltr. Ascochilopsis Carr Ascochilus Ridl. Ascoglossum Schltr. Aspasia Lindl. Barbosella Schltr. Barkeria Knowles & Westc. Barombia Schltr. Basiphyllaea Schltr. Batemannia Lindl. Beadlea Small Beclardia A. Rich Beloglottis Schltr. Benthamia A. Rich. Biermannia King & Pantl. Bifrenaria Lindl. Bogoria J. J. Sm. £