Plants on plants – the biology of vascular epiphytes

Fascinating Life Sciences Gerhard Zotz Plants on Plants The Biology of Vascular Epiphytes Fascinating Life Sciences This interdisciplinary series brings together the most essential and captivating topics in the life sciences They range from the plant sciences to zoology, from the microbiome to macrobiome, and from basic biology to biotechnology The series not only highlights fascinating research; it also discusses major challenges associated with the life sciences and related disciplines and outlines future research directions Individual volumes provide in-depth information, are richly illustrated with photographs, illustrations, and maps, and feature suggestions for further reading or glossaries where appropriate Interested researchers in all areas of the life sciences, as well as biology enthusiasts, will find the series’ interdisciplinary focus and highly readable volumes especially appealing More information about this series at http://www.springer.com/series/15408 Gerhard Zotz Plants on Plants – The Biology of Vascular Epiphytes Gerhard Zotz Institute of Biology and Environmental Sciences University of Oldenburg Oldenburg, Germany ISSN 2509-6745 ISSN 2509-6753 (electronic) Fascinating Life Sciences ISBN 978-3-319-39236-3 ISBN 978-3-319-39237-0 (eBook) DOI 10.1007/978-3-319-39237-0 Library of Congress Control Number: 2016951311 # Springer International Publishing Switzerland 2016 This work is subject to copyright All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed The use of general descriptive names, registered names, trademarks, service marks, etc in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made Cover illustration: Cover photo shows epiphytic Fascicularia bicolor in a temperate rainforest near Huinay (Chile), courtesy of Simon Pfanzelt Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer International Publishing AG Switzerland Preface Epibiota, organisms which live on other living things, are a fascinating facet of life on earth A barnacle on a blue whale, a tiny diatom on a huge kelp, a liverwort on a palm leaf in the understory of a rainforest, and a huge tank bromeliad in the outer crown of a giant tree have quite a few things in common, but there are also a large number of distinctions My initial plan was to write a book with a very broad taxonomic scope, covering at least the phenomenon of epiphytism in terrestrial, i.e., non-marine and non-limnetic, systems This would have resulted in the treatise of epiphytic vascular plants, lichens, mosses, liverworts, and (terrestrial) algae such as Trentepohlia sp It took a few months for me to realize that covering the biology of vascular epiphytes in the desired depth would already be enough of a challenge for a single person Hence, I narrowed the scope to the biology of the approximately 28,000 species of vascular plants which always or primarily occur on other plants The reader will see that this does not mean, however, that I am ignoring nonvascular epiphytes or other canopy-living organisms As much as possible, I tried to identify open research questions and to connect the particular case of vascular epiphytes to general biological principles, hoping that this will make stimulating reading both for the advanced graduate student, who is, e.g., looking for an interesting project, and for the senior scientist turning to epiphytes because there may be a connection with the organisms he or she is studying The final product of my efforts may also be seen as the successor of a book that has been the reference for those with a genuine interest in vascular epiphytes for more than a quarter century, David H Benzing’s seminal “Vascular epiphytes,” which was published in 1990 I can only hope that my book will be as stimulating and useful a resource as David’s book has been for me and many others for the last decades Initially planning to write in “dry” scientific prose, I soon decided to include personal comments on desirable directions and to be rather explicit in pointing out particular areas that I consider understudied A provocative statement here and there is arguably a way to stimulate interesting science If you disagree about a particular point of view, let me know—and let’s start a discussion about the best way to move forward Oldenburg, Germany February 2016 Gerhard Zotz v ThiS is a FM Blank Page Acknowledgments Science is a social endeavor Hence, this single-author monograph is not the isolated achievement of one person but builds on the work of many others I have tried to acknowledge this contribution of others with numerous citations, which in the end yielded a substantial citation list However, it is simply impossible to cite all papers that contributed in one way or the other to this book in a comprehensive way My personal collection of publications that contain information on vascular epiphytes sums up to almost 7000 papers, books, book chapters, theses, or reports I apologize if your paper is not cited—I had to make a choice This does not suggest any underlying judgment of quality or importance In addition, I had countless conversations with colleagues and students on my favorite subject over the last two decades, which helped to form the ideas and conclusions of this book I also use unpublished information For example, Cat Cardelu´s (Colgate, USA), Michael Kessler (ETH, Switzerland), and Nico Bl€uthgen (Darmstadt, Germany) provided extensive datasets on nutrient concentrations Wolfgang Wanek (Vienna, Austria) shared unpublished data on nutrient uptake and Peter Hietz (Vienna, Austria) unpublished biomass data Finally, I thank Rhett Harrison (Kunming, PR China) for sharing insights into the biology of hemiepiphytes A number of colleagues (Dirk Albach, Jose-Luis Andrade, Catherine Cardelu´s, Helena Einzmann, Peter Hietz, Michael Kessler, Holger Kreft, Thorsten Kr€omer, Glenda Mendieta Leiva, Heidi Meudt, Ana Silvia Moreira, Simon Pfanzelt, Alfredo Salda~ na, Katrin Wagner, and Wolfgang Wanek) read drafts of individual chapters and I am grateful for their suggestions and frank criticism Others helped out with specific information on canopy anurans, euglossine bees, or C4 photosynthesis (Shawn McCracken, David Roubik, and Rowan Sage) Having said this, I am solely responsible for any factual mistakes or interpretations you may disagree with I am happy to take any criticism I thank Herta Sauerbrey (University Oldenburg) and Angel Aguirre (Smithsonian Tropical Research Institute—STRI) for all the help in procuring literature over many years Dirk Albach, Peter Bak, Wilhelm Barthlott, Kevin Burns, Damian Catchpole, Gerhard Gottsberger, Michael Kessler, Moritz Klinghardt, Bejat McCracken, Ana Silvia Moreira, Steve Pearce, Rick Riefner, David Roubik, Steven Sylvester, and Christian Ziegler generously offered vii viii Acknowledgments photographs Laura Kuijpers, Christian K€onig, and Holger Kreft helped with the geographical data and the preparation of the global distribution figures Katrin Wagner supplied modified versions of graphs of previous publications Vera Mageney and Dirk Albach helped with the figure on the relationship of pseudobulbs, epiphytism, and phylogeny in the Epidendroideae Joachim Beyschlag provided a graph illustrating the potential of Y-Plant Last but not least, I also want to acknowledge the financial support by a number of institutions that made it possible for me to work on the biology of epiphytes for so many years, most prominently the DFG, but also the DAAD, STRI in Panama, the Jubilaăumsstiftung in W€urzburg, Germany, and the Freiwillige Akademische Gesellschaft in Basel, Switzerland A Comment on Plant Names Accepted species names are not constant but rather frequently change with taxonomic revisions For consistency, I only use names that are currently accepted in the online database “The Plant List” (accessed December 2015), even when other names were used in the original publications The following list compares the currently accepted names with those in the original publications Name used in original publication Didymopanax pittieri Epidendrum macrostachyum Ficus stupenda Guzmania minor Laelia cinnabarina Lecanopteris sinuosa Oncidium enderianum Pitcairnia flavescens Pleopeltis polypoidoides Polypodium phvllitidis Polypodium crassifolium Psygmorchis pusilla Psygmorchis glossomystax Rhipsalis heteroclada Currently valid name Schefflera rodriguesiana Beclardia macrostachya Ficus crassiramea subsp stupenda Guzmania lingulata Cattleya cinnabarina Myrmecophila sinuosa Oncidium praetextum Pitcairnia albiflos Polypodium polypodioides Campyloneurum phyllitidis Niphidium crassifolium Erycina pusilla Erycina glossomystax Rhipsalis teres Family Araliaceae Orchidaceae Moraceae Bromeliaceae Orchidaceae Polypodiaceae Orchidaceae Bromeliaceae Polypodiaceae Polypodiaceae Polypodiaceae Orchidaceae Orchidaceae Cactaceae ix Epilogue: The Epiphyte Syndrome 11 One of the most important questions that I wanted to address in this book was “what makes an epiphyte an epiphyte”? The length of this treatise demonstrates that there is no simple answer to this question There is no single unique feature, neither anatomical, morphological, physiological, nor any other biological aspect that could be used to characterize vascular epiphytes and distinguish them unambiguously from soil-rooted flora However, throughout this monograph I tried to identify traits that are particularly common or rare among epiphytes These traits may be relevant for particular taxonomic groups with epiphytic members or for epiphytes in general Some differences have been highlighted from the start of the scientific study of this plant group (e.g., small seeds, Schimper 1888), others are relatively new discoveries (e.g., longevity of gametophytes, Watkins and Cardelus 2012), some were expected and are easy to explain (e.g., a relatively high proportion of CAM species), others are less obvious and disputed (e.g., possible differences in genome size, Leitch et al 2009; Chochai et al 2012) Considering the complex nature of the epiphytic habitat and the diverse taxonomic background of the participating flora, I would argue that the lack of a simple answer is not due to a lack of information, but a simple consequence of biology— there are many ways of being an epiphyte Still, plants which typically occur as epiphytes are not just a random selection of the plant kingdom, and the accompanying table (Table 11.1) compiles all major features that are arguably “distinctive” for epiphytes and may be used to define something one could call the “epiphyte syndrome.” Although none of the listed features is universal for all 28,000 known epiphytic taxa, this compilation should provide a useful reference for comparative studies Go! # Springer International Publishing Switzerland 2016 G Zotz, Plants on Plants – The Biology of Vascular Epiphytes, Fascinating Life Sciences, DOI 10.1007/978-3-319-39237-0_11 267 Gametophyte morphology Dimorphy of fertile and sterile fronds Growth form A/M Leaf succulence Mesophyll idioblasts Plant size Roots with photosynthesis Seeds Stem succulence Tilosomes Impounding tank A/M A/M A/M A/M A/M A/M Almost exclusively found in epiphytes Varied Green roots with photosynthetic machinery Generally small Similar to ground-rooted taxa Generally smaller Only in epiphytic taxa Frequently pending, unusual for terrestrial herbs More pronounced Sometimes pending More common among epiphytes Typical manifestation in epiphytes Common in epiphytic orchids, rare in terrestrials Strap-like or ribbon-like Bromeliaceae, Asteliaceae Orchids Orchids, ferns Cacti Orchids “Throughout epiphytic orchids” Orchids Orchids, cacti, ferns Orchids Ferns and fern allies Ferns Taxonomic group Orchids More continuous supply with water and nutrients Need for vertical dispersal Access to light Overcoming intermittent water supply Increase water-storage capability, prevent cellular collapse during desiccation Mechanical reasons Use of space Use of space Proposed explanation Dispersal Pridgeon et al (1983) Benzing (2000) Nieder and Barthlott (2001), Chap Many different sources Diverse sources Diverse sources Pridgeon (1993) Pridgeon (1993) Diverse sources Diverse sources Farrar et al (2008) Watkins et al (2016) Source Halle´ (1986) Stern et al (1993) Rockwood (1985) Contrasting evidence 11 A/M A/M Inflorescence A/M A/M A/M Trait/feature Elaters Field A/M Table 11.1 Traits which are particularly frequent or rare, respectively, among vascular epiphytes 268 Epilogue: The Epiphyte Syndrome Germination Germination Germination and seedling development Vegetative growth Herbivory DEV DEV DEV Mycorrhiza Mycorrhiza CAM Cuticles INT INT PHYS PHYS INT DEV Velamen radicum Bladder-like traps Litter trapper A/M A/M A/M Overproportionally common compared to terrestrial plants Extremely impermeable to water Distinct communities Lower levels of colonization Generally low Extremely slow Speed of development from seed to seedling much faster (Almost) universal in epiphytic orchids, also some other taxa (e.g., some Anthurium), but occasionally in terrestrial orchids and other taxa Asymbiotic germination much easier Faster in epiphytic species Uniform and somewhat smaller traps More common among epiphytes than among soil-rooted plants Orchidaceae, Bromeliaceae Several Orchidaceae Bromeliaceae, Orchidaceae Bromeliaceae, Orchidaceae Ferns and lycophytes Cymbidium Cactaceae Cymbidium Orchidaceae, Araceae Orchids, aroids, ferns Utricularia Water economy Difficulty of establishment of mycorrhizal fungi in the canopy Environmental constraints Trade-off growth stress tolerance Low nutritional value Improved access to nutrients Martos et al (2012) Silvera et al (2009) Helbsing et al (2000) Schmidt and Zotz (2002, etc.) Winkler et al (2005) Kessler et al (2010) Paula and Ribeiro (2004) Chang et al (2005) Arditti (1992) Reifenrath et al (2006) Zona and Christenhusz (2015) Arditti (1992) (continued) 11 Epilogue: The Epiphyte Syndrome 269 Osmotic potential Roots Stomatal behavior and light flecks Water relations Gametophyte longevity Life history PHYS PHYS PHYS POP Long-lived perennials, very rarely annuals Drought avoider, rarely poikilohydric Long-lived, years to decades Slower photosynthetic response to lightflecks Less negative than in terrestrials in similarly dry habitats Separation of holdfast and absorptive function Typical manifestation in epiphytes Smaller Several Ferns Ferns Bromeliaceae, Araceae (nomadic vines) Ferns, figs, orchids Several Taxonomic group Orchidaceae Importance of water relations Proposed explanation Selection for small guard cell sizes “All or nothing” Zhang et al (2009a) and Zotz and Mikona (2003) Zhang et al (2009b) Watkins and Cardelus (2012) Diverse sources Source Leitch et al (2009) Zotz and Hietz (2001) Benzing (2000) Chase (1986) Contrasting evidence Chochai et al (2012) 11 Traits are sorted by categories: A/M anatomy and morphology, DEV development, PHYS physiology, POP population biology, INT interactions with other organisms POP PHYS Trait/feature Genome size Field PHYS Table 11.1 (continued) 270 Epilogue: The Epiphyte Syndrome References 271 References Arditti J (1992) Fundamentals of orchid biology Wiley-Liss, Inc., New York Benzing DH (2000) Bromeliaceae—Profile of an adaptive radiation Cambridge University Press, Cambridge Chang C, Chen YC, Yen HF (2005) Protocorm or rhizome? The morphology of seed germination in Cymbidium dayanum Reichb Bot Bull Acad Sin 46:71–74 Chase MW (1986) A monograph of Leochilus (Orchidaceae) Syst Bot Monogr 14:1–97 Chochai A, Leitch IJ, Ingrouille MJ, Fay MF (2012) Molecular phylogenetics of Paphiopedilum (Cypripedioideae; Orchidaceae) based on nuclear ribosomal ITS and plastid sequences Bot J Linn Soc 170:176–196 doi:10.1111/j.1095-8339.2012.01293.x Farrar DR, Dassler C, Watkins JE Jr, Skelton C (2008) Gametophyte ecology In: Ranker TA, Haufler CH (eds) Biology and evolution of ferns and lycophytes, vol Cambridge University Press, New York, pp 222–256 Halle´ N (1986) Les elateres des Sarcanthinae et additions aux Orchidaceae de la NouvelleCaledonie Bulletin du Museum national d’Histoire naturelle, Paris, 4e ser, 8, section B Adansonia 3:215–239 Helbsing S, Riederer M, Zotz G (2000) Cuticles of vascular epiphytes: efficient barriers for water loss after stomatal closure? Ann Bot 86:765–769 Kessler M, Jonas R, Cicuzza D, Kluge J, Pia˛tek K, Naks P, Lehnert M (2010) A survey of the mycorrhization of Southeast Asian ferns and lycophytes Plant Biol 12:788–793 doi:10.1111/j 1438-8677.2009.00270.x Leitch IJ, Kahandawala I, Suda J, Hanson L, Ingrouille MJ, Chase MW, Fay MF (2009) Genome size diversity in orchids: consequences and evolution Ann Bot 104:469–481 doi:10.1093/aob/ mcp003 Martos F, Munoz F, Pailler T, Kottke I, Gonneau C, Selosse M-A (2012) The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids Mol Ecol 21:5098–5109 doi:10.1111/j.1365-294X.2012.05692.x Nieder J, Barthlott W (2001) Epiphytes and their role in the tropical forest canopy In: Nieder J, Barthlott W (eds) Epiphytes and canopy fauna of the Otonga rain forest (Ecuador) Results of the Bonn—Quito epiphyte project, funded by the Volkswagen Foundation, vol Books on Demand, Bonn, pp 23–88 Paula CC, Ribeiro OBC (2004) Cultivo pra´tico de cacta´ceas, 1st edn UFV, Vic¸osa Pridgeon AM (1993) Systematic anatomy of Orchidaceae Recource or anachronism? In: Proceedings of the 14th world orchid conference, Glasgow, Glasgow, 1993 HMSO, Edinburgh, pp 84–91 Pridgeon AM, Stern WL, Benzing DH (1983) Tilosomes in roots of Orchidaceae: morphology and systematic occurrence Am J Bot 70:1365–1377 Reifenrath K, Theisen I, Schnitzler J, Porembski S, Barthlott W (2006) Trap architecture in carnivorous Utricularia (Lentibulariaceae) Flora 201:597–605 Rockwood LL (1985) Seed weight as a function of life form, elevation and life zone in neotropical forests Biotropica 17:32–39 Schimper AFW (1888) Die epiphytische Vegetation Amerikas Botanische Mitteilungen aus den Tropen, vol Gustav Fischer, Jena Schmidt G, Zotz G (2002) Inherently slow growth in two Caribbean epiphytic species: a demographic approach J Veg Sci 13:527–534 Silvera K, Santiago LS, Cushman JC, Winter K (2009) Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae Plant Physiol 149:1838–1847 doi:10.1104/pp.108.132555 Stern WL, Morris MW, Judd WS, Pridgeon AM, Dressler RL (1993) Comparative vegetative anatomy and systematics of Spiranthoideae (Orchidaceae) Bot J Linn Soc 113:161–197 doi:10.1111/j.1095-8339.1993.tb00336.x 272 11 Epilogue: The Epiphyte Syndrome Watkins JE Jr, Cardelus CL (2012) Ferns in an angiosperm world: cretaceous radiation into the epiphytic niche and diversification on the forest floor Int J Plant Sci 173:695–710 doi:10 1086/665974 Watkins JE Jr, Churchill AC, Holbrook NM (2016) A site for sori: ecophysiology of fertile-sterile leaf dimorphy in ferns Am J Bot 103:845–855 doi:10.3732/ajb.1500505 Winkler M, H€ulber K, Mehltreter K, Garcı´a-Franco JG, Hietz P (2005) Herbivory of epiphytic bromeliads, orchids and ferns, in a Mexican montane forest J Trop Ecol 21:147–154 Zhang Q, Chen J-W, Li B-G, Cao K-F (2009a) Epiphytes and hemiepiphytes have slower photosynthetic response to lightflecks than terrestrial plants: evidence from ferns and figs J Trop Ecol 25:465–472 doi:10.1017/S026646740900618X Zhang Q, Chen JW, Li BG, Cao KF (2009a) The effect of drought on photosynthesis in two epiphytic and two terrestrial tropical fern species Photosynthetica 47:128–132 doi:10.1007/ s11099-009-0020-9 Zona S, Christenhusz MJM (2015) Litter-trapping plants: filter-feeders of the plant kingdom Bot J Linn Soc 179:554–586 doi:10.1111/boj.12346 Zotz G, Hietz P (2001) The physiological ecology of vascular epiphytes: current knowledge, open questions J Exp Bot 52:2067–2078 Zotz G, Mikona C (2003) Photosynthetic induction and leaf carbon gain in the tropical understorey epiphyte, Aspasia principisa Ann Bot 91:353–359 Glossary Any glossary is subjective and incomplete However, I hope that most unfamiliar terms the reader may encounter in the main text are included I also encourage the reader to consult Moffett’s (2000) excellent review of the terminology used by researchers interested in the forest canopy and its biota Abaxial Accidental epiphyte Adaxial Aerenchyma allelopathy Allozyme Amphistomatic Anemochory Ant-house epiphyte Apomorphic Apoplast Aquaporin Assemblage Atmospheric/atmospheric epiphyte Autogamy The surface of a leaf that faces away from the stem, usually the lower surface A terrestrial species that occasionally can be found in tree crowns (