Bryophyte Ecology (ver Jul 2020) [4]

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About the Author e Janice Glime is Professor Emerita in the Department of Biological Sciences at Michigan Technological University, Houghton, Michigan, USA. She has a Bachelor of Science degree in elementary education from Frostburg State University, Maryland, USA (1962), a Master of Science in botany from West Virginia University (1964), and a Doctor of Philosophy in botany from Michigan State University (1968). She specialized in teaching freshmen in general biology and botany, and has taught ecology, evolution, systems ecology, and bryology. She is past President of the International Association of Bryologists (IAB) and is the manager of Bryonet-L, the IAB email discussion group on bryophytes. She has published over 100 papers, mostly on b1yophyte ecology, is author of the book The Elfin World of Mosses and Live1worts of Isle Roya{e and the Upper Peninsula of Michigan, co-author with Dinesh Saxena of Uses of Bryophytes, and editor of Methods in Bryofogy. Her primary research interests are on aquatic bryophytes and on the interactions of bryophytes and on the interactions of bryophytes with other organisms.

About the Book For more than ten years I have been working on a book on bryophyte ecology and was joined by Heinjo During, who has been very helpful in critiquing multiple versions of the chapters. But as the book progressed, the field of bryophyte ecology progressed faster. No chapter ever seemed to stay finished, hence the decision to publish online. Furthermore, rather than being a textbook, it is evolving into an encyclopedia that would be at least three volumes. Having reached the age when I could retire whenever I wanted to, I no longer needed be so concerned with the publish or perish paradigm. In keeping with the sharing nature of bryologists, and the need to educate the non-bryologists about the nature and role of bryophytes in the ecosystem, it seemed my personal goals could best be accomplished by publishing online. This has several advantages for me. I can choose the format I want, I can include lots of color images, and I can post chapters or parts of chapters as I complete them and update later if I find it important. Throughout the book I have posed questions. I have even attempt to offer hypotheses for many of these. It is my hope that these questions and hypotheses will inspire students of all ages to attempt to answer these. Some are simple and could even be done by elementary school children. Others are suitable for undergraduate projects. And some will take lifelong work or a large team of researchers around the world. Have fun with them!

The Format The decision to publish Bryophyte Ecology as an ebook occurred after I had a publisher, and I am sure I have not thought of all the complexities of publishing as I complete things, rather than in the order of the planned organization. But I wanted to reach a worldwide audience that included not only professional bryologists, but beginners, non-bryologist ecologists, teachers, naturalists, anyone who wanted to know something about bryophytes. Many of these people would never be willing or able to pay the cost of such a book in print copy. And the cost of the numerous color plates would be prohibitive. Some chapters have been easier for me to do and some will simply need help from others. The "book" will actually be multiple volumes, with the first being physiological ecology, but including an introduction to the broad classification of phyla and classes, morphology, structures, and life cycles. Communities, habitats, roles, interactions, and methods, among others, are in various stages of completion. Large chapters and those with many images difficult to download, so chapters are broken into smaller segments that I shall call subchapters. Sections, chapters, and subchapters will not always be posted in order, so each begins new pagination. Where possible, I will try to number sections of a chapter continuously. New chapters will be added as they are ready but may not cover all planned topics at the onset. Bryologists are encouraged to send me text or images for consideration, or to volunteer to write a chapter. I am considering making this like an online journal with reviewers, but that needs more planning and is likely to make style and nomenclature inconsistent. Your thoughts on the idea would be appreciated.

Acknowledgments The contributors to this book are far too numerous to mention all of them by name. To my graduate students and students of bryology, I owe a debt of gratitude for their enthusiasm for this project and for helping me to write for a somewhat less than professional and experienced audience by critically reviewing early chapters. To the members of Bryonet, I thank you not only for your wonderful contributions through Bryonet, but for the promptness with which I receive help for my many requests for images, information, ideas, and publications, reminding me over and over what a wonderful group of people comprise bryology. From Heinjo During I received numerous helpful suggestions and encouragement to keep going. As my co-author he obtained a contract with Cambridge, which we later abandoned. In the end, he modestly withdrew from authorship, claiming to have made no contribution, but his contributions in reading my chapters have been invaluable. Irene Bisang, as my co-author on the Sexual Strategies chapter update, kept me organized, and I still feel her presence and advice as I work on other chapters. To many persons I owe an immense debt of gratitude for permission to use their images. Without this wide array of choices, the book would have been of incredibly dull appearance on the web, and much less instructive. But most of all, I owe the beauty of the book to Michael Lüth, who gave me blanket permission to use as many of his wonderful images as I wished. They have provided more than half the bryophyte images used and put my own early photographic efforts to shame. Finally, I acknowledge the support of the Botanical Society of America, the International Association of Bryologists, and most of all, the Department of Biological Sciences of Michigan Technological University for sponsorship of the web version of the book. To my department chair, John Adler, I appreciate his cooperation and support in publishing this as an online book instead of a printed one. To Emil (Tiger) Groth, I owe the web layout and all the web activity needed to place the book there in an accessible and searchable form. And to Annelise Doll and the E. R. Lauren Library staff, we all owe gratitude for selecting this book for Digital Commons and for doing her best to meet all my requests, assuring that this book will be preserved for posterity.

Glime, J. M. and Chavoutier, L. 2017. Glossary. In: Glime, J. M. Bryophyte Ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Last updated 16 July 2020 and available at .

G-1

GLOSSARY JANICE GLIME AND LEICA CHAVOUTIER

1n: having only one set of chromosomes 2n: having two sets of chromosomes

2,4-D: 2,4-dichlorophenoxyacetic acid; herbicide that mimics IAA 6-methoxybenzoxazolinone (6-MBOA): glycoside derivative; insect antifeedant; can stimulate reproductive activity in some small mammals that eat them by providing growth substances >>: much greater ♀: sign meaning female, i.e. bearing archegonia ♂: symbol meaning male

A α-amylase: enzyme that hydrolyses alpha bonds of large, alphalinked polysaccharides, such as starch and glycogen, yielding glucose and maltose A horizon: dark-colored soil layer with organic content and minerals intermixed ABA: abscisic acid; plant hormone (growth regulator) associated with water stress, drought hardening, growth inhibition, stomatal closing, and seed dormancy in some plants; known from mosses abandoned land: land having previous human use abaxial: referring to lower surface of leaf; facing away from stem of plant

Abbreviations aff.: related to agg.: aggregate, designating group of species which are difficult to distinguish from one another auct.: Latin abbreviation for auctor, meaning author c.: Latin circa, meaning around, about cf.: Latin confer, compare with cfr. (c. fr.): Latin cum fructibus, meaning with sporophytes cm: centimeter det.: Latin determinavit, meaning determined by e.g.: Latin exempli gratia, meaning for example fo.: Latin forma, meaning form ibid.: Latin ibidem, meaning in the same book i.e.: Latin id est meaning that is IPL: inner peristomial layer leg.: Latin legit, meaning collected by µm: micrometer; micron; length unit = 1/1 000 mm. n: chromosome number (haploid). op. cit.: Latin opus citatum, meaning mentioned, cited above OPL: meaning outer peristomial layer PPL: meaning primary peristomial layer s.d.: Latin sine die, meaning without date sensu: Latin sensu, meaning in the sense (of) s.l.: Latin sensu lato, meaning in broad sense s.n.: Latin sine numero, meaning without number

s.s.: Latin sensu stricto, meaning strict sense sp.: species spp.: more than one species ssp.: subspecies var.: variety

abiosis: absence or lack of life; nonviable state abiotic: referring to non-living and including dust and other particles gained from atmosphere, organic leachates from bryophytes (and host trees for epiphytes), decaying bryophyte parts, and remains of dead inhabitants; usually includes substrate abortive: having development that is incomplete, abnormal, stopped before maturity abscisic acid: ABA; plant hormone (growth regulator) abscission: process where plant organs are shed; e.g. deciduous leaves in autumn absent: missing abundance: numerical representation of species; measure of amount of given species in sample local abundance is relative representation of species in particular ecosystem, usually measured as number of individuals found per sample relative species abundance is calculated by dividing number of species from one group by total number of species from all groups acaulescent: provided with very short stem ACC: acetyl-CoA carboxylase; ethylene precursor; biotindependent enzyme that catalyzes irreversible carboxylation of acetyl-CoA to produce malonyl-CoA through its two catalytic activities, biotin carboxylase (BC) and carboxyltransferase (CT) accession number: number assigned to specimen when it is entered into herbarium record accessory pigment: pigment that captures light energy and passes it to chlorophyll a accidentally foliicolous: accidentally, not normally, growing on leaves acclimation: gradual and reversible adjustment of organism to environmental fluctuations; e.g. adjustment to winter cold or summer heat; compare to adaptation, which is persistent genetic change that provides organism with better ability to survive its environmental conditions accrescent: continuing to grow after reproduction accumulation enrichment factor: amount of metal in plants divided by its stream water concentration -aceae: suffix denoting family in Plant Kingdom acellular: not divided into multiple cells

G-2

Glossary

acetylcholine: chemical formed by choline and acetyl group; neurotransmitter in nervous system used to transmit nerve impulses achlorophyllous: lacking chlorophyll acicole: growing on or among needles of conifers acid: substance with pH less than 7.0 acid flush: concentrated pollutants released rapidly during snow melt acid precipitation: precipitation having pH less than 5.4 acidicline: preferring weakly acidic substratum acidophile: plant growing best on acidic substrate acidophilous: growing on acidic substrates acrocarp: moss species that produces sporophyte at apex of stem or main branch acrocarpous: gametophyte producing sporophyte at apex of stem or main branch; generally upright mosses with terminal sporangia, usually unbranched or sparsely branched acrogynous: in many leafy liverworts, sporophyte growing at top of stem (from apical cell), e.g. Mesoptychia collaris [ant. anacrogynous] acropetal: referring to movement of substance from base to apex; of growth, outward toward shoot (or root) apex [ant. basipetal] acrotelm: living layer of peat actinomorphic: having radial symmetry, like spokes of wheel activation conditions: conditions of sufficient moisture and light for germination acuminate tip: prolonged tip adaptation: genetic change, arrived at through process of natural selection, which enables organism to compete more effectively under given set of conditions (L. adaptare = to fit in); compare to acclimation, gradual and reversible adjustment of organism to environmental fluctuations adaxial: on side toward axis (stem) of plant, such as upper surface of leaf [ant. abaxial] adenine: nitrogenous base; one member of base pair adeninethymine in DNA adherent: strongly attached to substratum e.g. Frullania dilatata adhesion tube: in Collembola, attachment to abdomen that may be used for cleansing body and as means of transferring drops of water from surface of body to mouth where they are then absorbed; previously thought to provide adherence adhesive organ: structure by which some nematodes adhere to bryophytes adhesive peg: structure of fungus that contacts rotifer or other entrapped organism, stimulating fungus to release glue from its trap adnate: said of two fused structures, e.g. peristome and epiphragm of Atrichum undulatum adsorption: fixation of elements on surface adventitious: growing on atypical place, e.g. adventitious rhizoids on costa in Conardia compacta adventitious root: root that arises from stem or other non-root axis point, as seen in corn adventive: introduced aerenchyma: in some thallose liverworts, loose parenchyma, with empty spaces between groups of cells aerobiology: study of airborne microorganisms, pollen, spores, and seeds, especially as agents of infection; form of passive transport aerohaline: subject to influence of salty sea spray

aerohygrophyte: plant growing in habitats having high air humidity aerophyte: plant growing on aerial parts of another aestivation: state of animal dormancy, similar to hibernation, but taking place in summer rather than winter Afro-alpine: high mountains of Ethiopia and tropical East Africa, which represent biological 'sky islands' with high level of endemism Afromontane: subregions of Afrotropical realm, one of Earth's eight biogeographic realms, covering plant and animal species found in mountains of Africa and southern Arabian Peninsula aggregate: clustered together; group of species which are difficult to distinguish from one another aggressive mimicry: form of mimicry in which predators, parasites, or parasitoids share similar signals, using harmless model, allowing them to avoid being correctly identified by their prey or host; e.g. playing dead Agral 600: horticultural wetting agent agroforest: land use management forest in which trees or shrubs are grown around or among crops or pastureland air chamber: in some thallose liverworts, specialized aircontaining cavity air layering: method of propagating plant by girdling or cutting part way into stem or branch and packing area with moist medium, as Sphagnum moss, stimulating root formation so that stem or branch can be removed and grown as independent plant air pore: in some thallose liverworts, opening of air-chamber alanine: non-polar amino acid that is relatively insoluble in water; defense compound that enables plants to withstand various stresses such as hypoxia, waterlogging, and drought alar cell: cell at basal angle of moss leaf, usually different in size and shape from other leaf cells -ales: suffix applied to order of plants or algae (e.g. Dicranales, Orthotrichales) alginate: viscous gum; general term for salts of alginic acid, especially sodium but also calcium or barium ions; composed of guluronic and mannuronic acids alkaline: rich in bases, having pH of more than 7 alkalinity: capacity of water to resist changes in pH that would make water more acidic; equivalent sum of bases that are titratable with strong acid alkaloid: basic organic compound containing nitrogen; toxic allele: particular form of gene allelopathic: having ability to inhibit growth of another organism through secondary metabolite allelopathy: condition in which one organism makes environment chemically unsuitable to another through secondary metabolism; type of chemical warfare in plants allochthonous: originating from elsewhere allopatric: said of two species which have separate (nonoverlapping) areas of distribution allopolyploidy: type of polyploidy (multiple sets of chromosomes) in which chromosome complement consists of more than two copies, with chromosomes derived from different species, producing hybrid species alluvium: deposit of clay, silt, sand, and gravel left by flowing water in river valley or delta, usually as fertile soil alpestrine: subalpine; growing to tree line alpha amylase: enzyme that hydrolyses alpha bonds of large, alpha-linked polysaccharides, such as starch and

Glossary

glycogen, yielding glucose and maltose; substance that helps some rotifers identify plant substrate alpha diversity: mean species diversity in sites or habitats at local scale, i.e. local species diversity alpine: habitat above treeline of mountain alternation of generations: alternating cycle of sporophyte (2n) and gametophyte (1n) generations altimontane: montane grasslands, shrublands, and woodlands alveola (pl. alveolae): more or less polygonal surface depression alveolate: with depressions on surface Amass: leaf mass per area Amax: maximum assimilation ambush predator: sit and wait predator, often having camouflage amensalism: interaction in which one species is harmed by other while other is neither harmed nor benefitted ametabiotic: describes metabolic state of life entered by organism in response to adverse environmental conditions such as desiccation, freezing, or oxygen deficiency; all measurable metabolic processes stop, preventing reproduction, development, and repair; cryptobiotic ametabolic state: state of life entered by organism in response to adverse environmental conditions such as desiccation, freezing, or oxygen deficiency; cryptobiotic state in which all measurable metabolic processes stop, preventing reproduction, development, and repair; including tardigrades, free-living nematodes, and rotifers; having no obvious metamorphosis amictic: non-sexual, as in some rotifers, with asexual reproduction recurring until conditions are favorable amidon: macromolecule composed of glucose constituents; starch; (L. amylum = complex carbohydrate) amoeboflagellate: in some slime molds, diploid cell stage that includes flagellated cells and amoeboid cells that develop directly into plasmodium amorphous: without definite form amphibious: capable of living in or out of water amphigastrium (pl. amphigastria): underleaves of leafy liverworts; few mosses where upper or lower leaves are differentiated from lateral leaves and smaller, as in Racopilum amphispory: spore size frequencies and mean spore size frequencies grouped around 2 mean sizes in varying ratios; small spore fraction is aborted amphithecium (pl. amphithecia): outer layer of embryonic capsule that gives rise to capsule tissues amphitropical: distributed on both sides of tropics amplexus: mating stage in which male amphibian grasps female with his front legs prior to depositing sperm on her eggs amyloid: waxy translucent substance of various complex proteins in combination with polysaccharides and staining blue with iodine (like starch) deposited in tissues in different disease processes and tissue degeneration; builds up inside tissue in amorphous way amyloplast: colorless plastid that forms starch granules in plants; statolith; might play role in gravitropism anabiosis: temporary state of suspended animation or greatly reduced metabolism anacrogynous: designating sporophyte growing in lateral position on stem, branch or thallus (e.g., thallose liverworts like Pellia endiviifolia)

G-3

anadromous: referring to fish living in ocean and migrating up freshwater streams to spawn anaerobic: without oxygen anagenesis: species formation without branching of evolutionary line of descent anagenetic speciation: speciation on islands through gradual change from founder population analogous: said of structures not having common phylogenetic origin but having similar function anastomosis: condition of union of one structure with another, usually crisscrossing; interconnecting; may be applied to irregularly divided peristome teeth (e.g. endothecium of Anthelia juratzkana) or river with islands and meanders anchor ice: submerged ice anchored to bottom of stream or other water body ancophile: plant living in canyon forests ancophilous: living in canyon forests Andreaeobryopsida: class of mosses in Bryophyta Andreaeopsida: class of mosses in Bryophyta androcyte: cell that will give rise to antherozoid androecial branch: specialized branch bearing antheridia and bracts androecium (pl. androecia): male inflorescence; antheridia and surrounding bracts androgametophyte: male gametophyte androgynogametophyte: autoicous or synoicous gametophyte androgynous: male and female organs in same inflorescence, monoicous anemochorous: wind-dispersed anemochory: dispersal by wind, such as spore, gemma, or other propagule angle of incidence: angle formed between direction of light and vertical (difference from straight on), so low sun has higher angle of incidence, thus small leaf angle (approaching vertical) creates effect of large angle of incidence anhydrobiosis: dormant state; strategy of surviving dehydrated state or extreme temperature conditions; reviviscence anion: negatively charged ion anisogamy: size, shape, or behavioral differences in gametes anisophyllous: having two types of leaves on same stem; stem leaves and branch leaves morphologically different, as in Sphagnum [ant. isophyllous] anisosporous: having bimodal distribution of spore sizes with smaller spores generally producing males anisospory: condition having bimodal distribution in spore size; genetically determined condition of two spore sizes anisotropic dispersal: directional dispersal annotinous: with yearly growths annual: plant that germinates, reproduces, and dies all within one year [ant. perennial]; see Mägdefrau life forms annual shuttle: species that requires small disturbances that last 1-2 years; survive severe stress periods annular: ring-shaped annulus: zone of differentiated cells between capsule urn and operculum, facilitating opening of capsule anoxybiosis: biological response triggered by lack of oxygen in which organism takes in water and becomes turgid and immobile, possibly form of cryptobiosis; used by tardigrades to survive unfavorable conditions

G-4

Glossary

antagonistic: interaction in which one species benefits at expense of another anterior: dorsal, abaxial [ant. posterior] anterior whiplash flagellum: thin whiplike structure on front end of cell (L. flagellum = whip) antheraxanthin: bright yellow accessory pigment found in many organisms that perform photosynthesis; xanthophyll cycle pigment, oil-soluble alcohol within xanthophyll subgroup of carotenoids; in pathway to making ABA antheridiophore: specialized antheridium-bearing branch antheridium (pl. antheridia): male gametangium found in all sexual plants except seed plants; sperm container, multicellular globose to broadly cylindric stalked structure producing sperm antherozoid: spermatozoid, male gamete Anthocerotophyta: phylum of hornworts, characterized by thallose gametophyte with hornlike sporophyte having continued growth at its base anthocyanin: water-soluble blue, purple, or red flavonoid pigment found in cell vacuole of plants, especially flowers and autumn leaves; in bryophytes, usually based on 3desoxyanthocyanidins located in cell wall anthracine: coal black anthropochorous: dispersal of propagules associated with human activities anthropogenic: relative to ecosystem, resulting from action of humans antical: relative to surface of thallus, upper side [ant. postical] antifeedant: compound that discourages herbivory antifreeze protein (AFP): protein that prevents freezing antrorse: forward, upward, toward tip, e.g. antrorse teeth in Dichodontium pellucidum [ant. retrorse] aperturate: with opening aperture: opening, hole, orifice apex: tip; end farthest from point of attachment or from base of organ (L. apex = point) aphyllous: without leaves apical: at tip or apex apical cell: single meristematic cell at apex of shoot, thallus, or other organ that divides repeatedly apical dominance: phenomenon whereby main, central stem of plant is dominant over other side branches, typically by supressing their growth apiculate: with short and abrupt point apiculus (pl. apiculi): short point, e.g. leaf tip of Entodon concinnus apogamous: condition of producing sporophyte without union of gametes apogamy: asexual multiplication, without fusion of gametes [syn. apomixis] apomixis: asexual multiplication, without fusion of gametes [syn. apogamy] apophysis: strongly differentiated sterile neck at base of capsule, e.g. Splachnum rubrum [syn. hypophysis] apoplast: capillary spaces in cell wall apoplastic: outside cell membrane, such as cell walls and dead cells; used to describe water transport between cells aposematic mimicry: resemblance to organisms with behavior or morphology serving to warn or repel

aposematism: warning coloration; advertising by animal to potential predators that it is not worth attacking or eating; may indicate poisonous or bad taste or carnivorous attack aposporous: producing gametophyte from sporophyte tissue without meiosis apparency: hypothesis predicts that apparent plants (i.e., most easily found in vegetation) would be most commonly eaten by herbivores, including humans; grouping of plants, including bryophytes, that are most conspicuous photosynthetic food items available apparent plants: conspicuous plants, easily found by herbivores apparent quantum yield: measure of how many molecules of certain substance such as H2O2, dissolved inorganic carbon, etc. can be produced per photon absorbed by, for example, colored dissolved organic matter appressed: referring to leaves lying closely or flat against stem or plant to substrate [Frullania dilatata] aquatic: pertaining to water habitat arabinoglucan: new polysaccharide from mosses, made of glucose and arabinose; has potential medicinal value arabinose: monosaccharide sugar containing five carbon atoms, and including aldehyde (CHO) functional group arable land: land used for or suitable for growing crops arachidonic acid: polyunsaturated, essential fatty acid that makes membranes more pliable in cold arachnoid: covered with fine and tangled hairs, e.g. Marchantia polymorpha ssp. montivagans archegoniophore arboreal: living in trees arbuscular hypha (pl. hyphae): mycorrhizal filament characterized by formation of unique structures, arbuscules, and vesicles by fungi of phylum Glomeromycota arbuscule: finely branched organ produced by endomycorrhizal fungi inside host cells; interface at which fungus and plant exchange phosphorus and photosynthates archegoniophore: specialized archegonia-bearing branch archegonium (pl. archegonia): multicellular egg-containing structure that later houses embryo; female gametangium; flask-shaped structure consisting of stalk, venter, and neck present in Bryophyta and all tracheophytes except flowers archesporium: layer of cells which give rise to spores Arctic: present in areas around North pole arctic-alpine: distribution in arctomontane: distribution in Arctic region and montane areas in lower latitudes; climatic type of Arctic and high elevations area: region of distribution arenicolous: growing on sand areola (pl. areolae): small, angular or polygonal surface area differentiated on thallus and overlying chamber, forming pattern or network, as in Conocephalum areolate: divided into chambers areolation: cellular network of leaf or thallus argillicolous: growing on clay soils arginine: highest nitrogen to carbon ratio among 21 proteinogenic amino acids; amino acid with basic group, alkaline in solution; water soluble; major storage and transport form for organic nitrogen in plants arid: having little or no rain arista: awn; hair point, e.g. leaf tip of Syntrichia caninervis aristate: ending in awn, e.g. Syntrichia ruralis leaves

Glossary

arthrodontous: having lateral walls of peristome teeth eroded with uneven thickenings (arthro = jointed; don = tooth), e.g. peristome of Orthotrichum cupulatum ascending: pointing obliquely upward, away from substrate Ascomycota: phylum of fungi commonly known as sac fungi because spores are produced in sacs called asci aseptic: free of disease-causing microorganisms asexual: referring to reproduction without union of gametes, such as gemmae in Marchantia asl: above sea level aspartate: amino acid with higher molecular weight and protonated -NH+3 aspect: compass direction slope faces astomous: without stomata (capsule); capsule that doesn't open ATP: adenosine triphosphate; energy-storing compound atratous: turning black Aufwuchs: German word for small organisms living firmly attached to substratum, but not penetrating it; see also periphyton auricle: earlike lobe, sometimes at base of moss leaf or liverwort underleaf; in Blasia houses Cyanobacterial partner auroxanthin: diepoxy carotenoid pigment known in Fontinalis austral: of Southern Hemisphere author(s): name(s) of bryologist(s) (sometimes abbreviated) who contributed to taxonomic description and nomenclature of taxon autoclave: oven-like equipment capable of high temperatures for heat sterilization autogamy: within one gametophytic self-fertilization autohydrolysis: hydrolysis (molecule of water ruptures one or more chemical bonds) of peptide or enzyme catalyzed by itself autoicous: having male and female reproductive organs in separate clusters (different branches) on same plant autolysis: release of enzymes when cells die, causing cells to break down quickly; common in many insects autopolyploidy: all chromosomes derived from same species, frequently same individual; in bryophytes, having more than 1 set of homologous chromosomes in gametophyte autotomy: self-amputation; behaviour whereby animal sheds or discards one or more of its own appendages, usually as selfdefense mechanism to elude predator's grasp or to distract predator and thereby allow escape autotropism: tendency of plant organs to grow in straight line when not influenced by external stimuli auxin: plant growth-regulating hormone, usually referring to hormone indoleacetic acid (IAA); influences cellular elongation, among other things avoidance strategy: adaptations that permit organism to alter factor so that it is no longer significantly damaging, such as minimizing hydrodynamic forces by adaptive life form awn: hair-point, e.g. leaf tip of Cirriphyllum piliferum axenic: pure (sterile) culture, without other organisms axial strand: column formed of elongated cells and located in center of some stems or thalli; central strand in mosses axil: angle formed where leaf joins stem axillary: forming in axis between stem and leaf axis: main stem axopod: sticky pseudopod on some Protozoa

G-5

B B horizon: dark soil layer of accumulated transported silicate, clay, minerals, iron, and organic matter, having blocky structure Baas-Becking hypothesis: everything is everywhere, but, the environment selects; applied to small organisms and propagules such as spores bacterivore: consumes primarily bacteria Baermann funnel: apparatus for extracting turbellarians (as well as nematodes, copepods, and tardigrades) from bryophytes; cheese cloth, muslin, or tissue paper is placed in funnel to hold sample, usually supported by piece of screening; water is run through sample with rubber tubing clamped at end of funnel; sample sits overnight or longer, then water is released from funnel and collected; first few drops will have concentration of nematodes, which are heavier than water Baker's law: loss of dispersal power and bias toward selfcompatibility after immigration to islands ballooning: phenomenon in which spider ascends to something taller, like fence, points its spinnerets upward, then secretes thread, then jumps or is blown with thread serving as anchor bana: low Amazon caatinga tall bana: type of low caatinga with trees over 10 m tall low bana: type of low caatinga with maximum tree height typically less than 5 m open bana: in central low caatinga where trees are even shorter and very widely spaced bank: land along side body of water scientific unit of measurement of pressure; 1 bar  1 atmosphere of pressure (0.986923 tam)  14.503 psi = 750 mm Hg = 99.992 kPa barbate: with tufts of long hairs, beard-like bark: outermost layer of stems and roots of woody plants; surrounding wood of tree or shrub basal cells: group of cells located at base, in proximal part of leaf basal membrane: short cylinder at base of peristome (single peristome) or at base of endostome (double peristome) supporting segments and cilia basic: alkaline, containing base, having pH higher than 7 Basidiomycota: phylum of fungi; fungi composed of hyphae and reproducing sexually by formation of specialized clubshaped end cells called basidia that normally bear external meiospores (usually four) basionym: original name on which current taxon name is based basipetal: referring to movement of substance from apex to base; tissue or organ developing or maturing from apex toward base [ant. acropetal] basiphile: preferring basic habitats (limestone, sandstone, chalk, dolomite, etc.) [ant. acidophile] Batesian mimicry: mimicry in which one organism resembles toxic or otherwise dangerous organism, but is not dangerous itself beaded stream: pools connected by narrow channels behavioral drift: occurring at particular time of day or night; may result from crowding, competition, need for food, predation, making new case, or attempting to reach land at emergence time beneficial acclimation hypothesis (BAH): hypothesis that predicts animals will have their best performance at temperature to which they are acclimated benthic: living on bottom of body of water bar:

G-6

Glossary

Bergmann's rule: within broadly distributed taxonomic clade, populations and species of larger size are found in colder environments, while populations and species of smaller size are found in warmer regions; usually applied to endotherms Berlese funnel: apparatus using light and/or temperature gradient that separates mobile organisms such as arthropods and annelids from litter or bryophytes in funnel; organisms collected in preservative (usually alcohol) below funnel beta diversity: ratio between regional and local species diversity bet hedger: organism that uses combination of two or more strategies, thus never having optimal adaptations to extremes but being prepared to lesser degree for most circumstances; plant that seems to have both good sexual reproduction and means of vegetative reproduction, e.g. bryophyte that produces frequent capsules but also produces gemmae, as in Tetraphis pellucida and Marchantia polymorpha bicostate: with two nerves bicuspidate: with two points, e.g. leaves of Cephalozia lunulifolia Bidder's organ: structure on male toads that can become ovary under right conditions bidentate: with two teeth (different from double teeth) biennial: cycle of two season’s duration (generally less than two years) bifarious: on two opposite rows, distichous biflagellate: having two flagella; functions in cell motility bilobate: divided into two lobes or segments, e.g. Lophocolea bidentata binding site: site for attachment, usually referring to ions; can occur on cell walls, soil particles, glass containers, etc. binocular: having two eyepieces binomial: expression used to designate species; formed of two Latin terms: generic and specific term; by convention this binomial is written in italics because it is foreign word bioassay: use of living organism for assessing effects of biologically active substances biocoenosis: association of different organisms living together in habitat; biotic community (or biocenosis) along with its physical environment (or biotope) biomass: quantitative estimate of total mass of organisms or parts being considered biotope: ensemble of physical, chemical and climatic conditions of habitat; biotope plus biocenosis form ecosystem twice pinnately branched, e.g. Thuidium bipinnate: tamariscinum bipolar: said of species found in both polar regions biramous: divided into two branches, e.g. pincers on end of crab claw or divided antenna bird cliffs: steep cliffs with numerous small shelves that serve as nesting locations for bird colonies bisexual: having both sexes on same individual; monoicous (gametophyte) or monoecious (sporophyte of tracheophytes) bistratose: having two layers of overlapping cells, as in some moss leaves bivoltine: producing two broods per season blade: portion of leaf excluding stalk (Plagiomnium) bloom: powder covering some capsules or leaves, e.g. leaves of Saelania glaucescens bog: acidic, wet area in which nutrients are received by rainfall and groundwater flow is negligible; consists mostly of decaying moss and other plant material; characterized by low nutrients

bog moss: usually meaning Sphagnum bole: main trunk of tree bonkei: tray landscape, typically made with bryophytes bonsai: dwarfed ornamental tree, often with mosses at base border: land at edge of habitat; in bryophytes, edge; margin (cells of different shape, size, or color than other cells of structure), e.g. leaf of Mnium thomsonii boreal: pertaining to north; life zone bounded on south by growth-season accumulated temperature above 6.1ºC of 5538ºC and mean daily temperature of 18ºC for six hottest weeks (L. boreas = north) boreal forest: predominantly conifer forest extending across northern North America and parts of Europe and Asia BOREAS: climate model for boreal region botryoid: like bunch of grapes, e.g. oil bodies of Calypogeia suecica boundary layer resistance: boundary layer is that layer of fluid in immediate vicinity of bounding surface; boundary layer resistance is resistance to movement of CO2, heat, and other substances through that thin layer brachycyte: short cell; seen on protonemata treated with ABA brachypterous: short-winged bract: modified leaf associated with gametangium or gemmaecup bracteole: modified underleaf associated with gametangium in liverworts branch: lateral subdivision of stem or axis Braun-Blanquet method: method uses cover-abundance scale to describe vegetation; these levels are divided into cover classes, typically using 5-7 categories:

1 2 3 4 5 6 7

10% eufoliicolous: true leaf-dwelling euhydrobiont: living in water eukaryotic: having nucleus euryoecious: able to live in variety of conditions eutrophic: relative to habitat rich with mineral nutrients and so supporting dense population [ant. oligotrophic] eutrophication: process characterized by excessive plant and algal growth due to increased availability of one or more

G-15

limiting growth factors needed for photosynthesis, such as sunlight, carbon dioxide, and nutrient fertilizers evacuolate: lacking vacuoles evanescent: relative to rib which ends just before apex of leaf, fading, disappearing evaporative cooling: process in which evaporation of water removes heat from system; can occur at plant, animal, or ecosystem level evapotranspiration: loss of water through evaporation from among plants and from plants themselves (transpiration) evenness: similarity of frequencies of different units (species) making up population or sample evergreen: condition where plant remains green and retains its leaves for full year or longer; persistent; green year-round everything is everywhere: Baas-Becking hypothesis that everything is everywhere, but, environment selects; applied to small organisms and propagules such as spores evolution: series of genetic changes (changes that are heritable) that causes organisms to change through time (L. evolutio = unrolling) evolutionary drivers: selection pressures EX: extinct (IUCN) ex: in case of validation after formation of name, e.g. Straminergon stramineum (Dicks. ex Brid.) Hedenäs ex-: prefix meaning "sans," "non" excavate: hollowed, concave exchange site: location on plant cell wall or soil particle where ions are traded, such as replacement of hydrogen from COOH by Ca+2; when charge of new ion is greater than that of one it replaces, it is shared by more than one exchange site exchanger: organism capable of replacing one ion for another, usually replacing hydrogen with cation such as Ca+2 excurrent: relative to rib, beyond apex of leaf, e.g. leaf costa of Fissidens taxifolius exine: outer layer of spore exogenous: growing or originating from outside organism, e.g. fungus can be source of IAA for protonema exogenous: generated by outside source; external origin exohydric: having water transport essentially external by surface flow; including capillary flow between leaves or though surface papillae exoskeleton: rigid external covering for body in some invertebrate animals, especially arthropods, providing both support and protection; e.g. in crayfish exosporic: condition in which first mitotic division occurs outside spore after rupture of spore wall, typical of most bryophytes exostome: outer peristome of arthrodontous capsule, e.g. outer peristome of Orthotrichum striatum exothecial: relative to exothecium, outer capsule wall exothecium: relative to capsule, outermost layer exotic: foreign; introduced from foreign country (L. exoticus = foreign) explant: portion of plant transplanted to artificial medium explerent: life strategy for non-competitive species that fills spaces between others exposed feeder: organism that feeds at exposed surface exserted: relative to capsule that far exceeds perichaetial leaves, e.g. capsules of Orthotrichum anomalum exsiccatum (pl. exsiccata): distributed and labelled reference specimen

G-16

Glossary

extant: existing today [ant. extinct] extensin: glycoprotein thought be involved in cell wall extension extern: relative to surface of leaf, dorsal face, abaxial face extirpation: local extinction extinct: no longer present on Earth [ant. extant] extinction rate: rate of disappearance of species extracellular: on outside of cell extremophile: organism with optimal growth in environmental conditions considered extreme and challenging for carbonbased life form with water as solvent to survive extrorse: turned outwards exuvia (pl. exuviae): cast-off outer skin of tardigrade or arthropod after molt

F ♀: sign meaning female, in bryophytes bearing archegonia face: side facies: general appearance (habit of species), or appearance of plant community dominated by taxon or small number of taxa Factor H: adenine derivative hormone stimulant for inhibiting caulonema growth and promoting formation of gametophore buds in bryophytes facultative: not occurring regularly; occurring optionally in response to circumstances rather than by nature; for example, terrestrial but occasionally surviving in water facultative aquatic: having some degree of tolerance to desiccation and xerophytic conditions facultative diapause: resting period that can change based on conditions facultative epiphyte: organism that lives on trees, but lives on other substrates as well falcate: sickle-shaped falcate-secund: sickle-shaped and turned towards only one side of stem falcation: condition of being curved like sickle, e.g. leaves of many Dicranum species fallow land: plowed and harrowed but left unsown for period false anisospory: condition of having small, non-viable spores found among dimorphic spores in certain species of bryophytes due to factors such as spore abortion; non-genetic condition of more than one spore size false leaf trace: in bryophytes, extension into cortex from leaf but not connected with central strand of stem; found in Mniaceae and Splachnaceae family: subdivision of order – next major classification level; ending in "aceae" fan: life form found on vertical substrate, usually where there is lots of rain; creeping, with branches in one plane and leaves usually flat; e.g. Neckeraceae, Pterobryaceae, Thamnobryum, some Plagiochila; see Mägdefrau life forms farinaceous: farinose, covered with white bloom fascicle: small tuft or cluster of fibers, leaves, branches, or flowers; in Sphagnum, clump of branches on stem fasciculate: arranged in fascicles fastigiate: with branches erect, nearly parallel and nearly same length fault: break in rocks that make up Earth's crust, rocks on each side have moved past each other feces: excrement; waste material discharged from gut

fecundity: number of offspring produced by organism during its lifetime fecundity-advantage model: need of species needs to produce large number of eggs feldmark: plant community characteristic of sites where plant growth is severely restricted by extremes of cold and exposure to wind, typical of alpine tundra and sub-Antarctic environments female: organism that produces egg femur (pl. femora): third segment of leg fen: minerotrophic peatland or moss-dominated ecosystem that gets its nutrients primarily from ground water or surface water; poor fens have low nutrient content, intermediate fens are characterized by intermediate nutrient levels, and rich fens have highest nutrient levels among these habitats; this term has been variously defined in different countries with older North American literature including poor fens as bogs fenestrate: pierced, perforated with openings like windows, e.g. peristome of Grimmia crinitoleucophaea ferredoxin: iron-sulfur protein needed for conversion of nitrogen oxides to NH4+ ferricrete: hard, erosion-resistant layer of sedimentary rock, usually conglomerate or breccia, cemented together by iron oxides ferrugineous, ferruginous: rust colored fertile: producing sex organs (antheridia, archegonia), bearing sporophytes [ant. sterile] fertilization: fusion of gametes resulting in formation of zygote; act of adding nutrients by applying fertilizer to improve plant growth ferulic acid: phenolic compound and major constituent of fruits and vegetables with strong antioxidant and antiinflammatory properties; only released after severe hydrolysis; present in shoots but absent in young capsules of Mnium hornum fibrilla (pl. fibrillae): thickened bands across hyaline cells of Sphagnum, strengthen cell walls; fibril fibrillose: with fibrils, e.g. leaf hyaline cells of Sphagnum field: area of open land, especially one planted with crops or pasture fine adjustment: knob on microscope used for fine-tuning focus; used with high magnifications; see coarse adjustment fire place: construction in which to build fire fistulated: having passageway cut from rumen to outside flank: in some thallose liverworts, zone between median groove and margin of thallus, e.g. thallus of Riccia flavonoids: group of plant pigments that absorb UV light fleshy: soft and thick floristic list: list of species present on site flagellate: possessing flagellum flagelliform: whiplike, gradually tapering from base to tip of branch flagellum (pl. flagella): slender, whip-like appendage that enables cells to move through liquids; differs from cilia in having only one or two per cell; found on most sperm; as propagule, slender branches with reduced leaves that occur in axils of upper leaves – basal portion multicellular, separating them from caducous branchlets flavonoid: group of plant pigments that absorb UV light and include anthocyanins

Glossary

flotation: separation technique requires that density of flotation liquid be greater than that of arthropods but less than that of debris or bryophytes fluorescence: emission of light by substance that has absorbed light or other electromagnetic radiation of different wavelength; due to excited electrons returning to ground state; visible or invisible radiation emitted by certain substances as result of incident radiation of shorter wavelength such as X-rays or ultraviolet light flush: area where water from underground flows out onto surface to create area of saturated ground, rather than welldefined channel; piece of boggy ground, especially where water frequently lies on surface; swampy place; pool of water in field maximum fluorescence of dark adapted material; Fm: fluorescence resulting from flashing bright light on leaf in dark fo.: abbreviation meaning "forma" fogging: technique used for killing insects that involves using fine pesticide spray which is directed by blower fog-stripping: condensing water vapor from frequent fog and mist; often primary means for bryophytes to obtain water in cloud forest foliicolous: growing on leaves [syn. epiphyllous] foliose: leaf-like, leafy foot: basal portion of most bryophyte sporophytes, embedded in gametophyte foot candle: intensity of light from one candle on square foot of surface one foot from candle foot gland: in some rotifers, gland on foot to secrete glue footpath: narrow path suitable for walking foraging: in bryophytes, use of horizontal growth that permits mosses or liverworts to take wider advantage of nutrients and light forb: non-grass herbaceous flowering plant forest: wooded habitat forest gap: opening in forest canopy, often due to fallen tree forest track: something resembling large wooded area, especially in density form: lowest level of classification (below variety), often determined by environment founder principle: small population becomes separated to new location, representing only small portion of variability of species; loss of genetic variation in new population established elsewhere by very small number of individuals from larger population; in bryophytes, includes arrival of only one sex to colonize particular location fount: spring or fountain fountain: natural spring of water fovea: spore ornamentation, depression like golf-ball foveolate: pitted FPOM: fine particulate organic matter fragmentation: breaking into fragments (pieces) frank water: obvious pools of water, as opposed to water adhering to moss frass: excrement of insect larvae; insect feces; fine powdery refuse or fragile perforated wood produced by activity of boring insects freeze avoidance: survival strategy that prevents body fluids (especially arthropods) from freezing at temperatures well below 0°C

G-17

freeze tolerance: ability of plants to withstand subzero temperatures through formation of ice crystals in xylem and intercellular space, or apoplast, of their cells freezing longevity: length of time bryophyte can remain frozen and survive fresh: fresh state; in presence of sufficient moisture freshet: flood of river from heavy rain or melted snow; rush of fresh water flowing into sea freshwater: not salt water frieze: as endive salad, e.g. thallus of Anthoceros agrestis fringe: margin lined with cilia frondose: habit that is densely branched, fern-like frost tolerance: lowest temperature at which no more than defined percent (typically 50%) suffer irreversible damage in net photosynthetic activity relative to unfrozen plants fructification: in slime molds, process of forming sporangia; analogy to vascular plants, synonymous term with sporophyte; used for bryophytes, but considered by some authors as unsuitable for bryophytes fruit inappropriate term by some authors, meaning sporophyte fugacious: fleeting fugitive: life strategy of species that lives in unpredictable environment; generally stays only 1-2 years while habitat remains suitable at site and produce small spores that permit them to be dispersed easily fulvous: reddish yellow functional grouping: species having similar roles in ecosystem fungus (pl. fungi): kingdom and common name for group of non-photosynthetic organisms; sometimes placed in kingdom Mycota; formerly classified as plants, but food reserves, cell wall components, and other biochemical differences have caused biologists to re-classify them into their own kingdom funiform: like rope furcula: forked appendage at end of abdomen in springtail, by which insect jumps furfuraceous: covered with scales furrow: groove, e.g. in thallus of Riccia sorocarpa furrowed: sulcate, grooved fuscous: dark brown and somber color fusiform: elongated, spindle-shaped; tapering at both ends Fv: variable fluorescence of dark-adapted material; difference between maximum and minimum fluorescence Fv/Fm: in photosystem II, variable vs maximum fluorescence; measure of chlorophyll fluorescence; measurement ratio that represents maximum potential quantum efficiency of Photosystem II if all capable reaction centers are open; . Accessed 2 March 2020 via GBIF.org. ITIS. 2020a. Marsupella boeckii. Accessed 17 February 2020 at . ITIS. 2020b. Marsupella emarginata. Accessed 17 February 2020 at .

ITIS. 2020c. Nardia assamica. Accessed 11 June 2020 at .

ITIS. 2020d. Nardia scalaris. Accessed 11 June 2020 at .

ITIS. 2020e. Harpanthus flotovianus. Accessed 11 June 2020 at .

ITIS. 2020f. Eremonotus myriocarpus. Accessed 11 June 2020 at .

ITIS. 2020g. Jungermannia atrovirens. Accessed 11 June 2020 at .

ITIS. 2020h. Jungermannia exsertifolia. Accessed 11 June 2020 at . ITIS. 2020i. Jungermannia exsertifolia subsp. cordifolia. Accessed 11 June 2020 at . ITIS 2020j. Jungermannia pumila. Accessed 11 June 2020 at . ITIS 2020k. Saccogyna viticulosa. Accessed 11 June 2020 at .

Chapter 1-4: Aquatic and Wetland: Marchantiophyta, Order Jungermanniales – Jungermanniineae

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Wagner, D. H. 2018. Mesoptychia gillmanii. Species Fact Sheet. Oregon/Washington Bureau of Land Management, 6 pp. Wagner, D. H., Christy, J. A., and Larson, D. W. 2000. Deepwater bryophytes from Waldo Lake, Oregon. Lake Reservoir Mgmt. 16: 91-99. Wang, B. and Qiu, Y. L. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299-363. Wang, S., Li, R. J., Zhu, R. X., Hu, X. Y., Guo, Y. X., Zhou, J. C., Lin, Z.-M., Zhang, J.-Z., Wu, J.-Y., Kang, Y.-Q., MorrisNatschke, S. L., Lee, K.-H., Yuan, H.-Q., and Lou, H.-X. 2014. Notolutesins A–J, dolabrane-type diterpenoids from the Chinese liverwort Notoscyphus lutescens. J. Nat. Prod. 77: 2081-2087. Warmers, U. and König, W. A. 1999. Sesquiterpene constituents of the liverwort Calypogeia fissa. Phytochemistry 52: 695704. Warmers, U., Wihstutz, K., Bülow, N., Fricke, C., and König, W. A. 1998. Sesquiterpene constituents of the liverwort Calypogeia muelleriana. Phytochemistry 49: 1723-1731. Watson, L. and Dallwitz, M. J. 2019. The liverwort genera (Bryophyta: Hepaticae and Anthocerotae) of Britain and Ireland. 5th Version. Accessed 4 March 2020 at . Watson, W. 1919. The bryophytes and lichens of fresh water. J. Ecol. 7: 71-83. Weber, D. P. 1976. The Bryophytes of Cataracts Provincial Park, Newfoundland. M.S. thesis, Department of Biology, Memorial University of Newfoundland, 85 pp. West, G. 1910. An epitome of a comparative study of the dominant phanerogamic and higher cryptogamic flora of aquatic habit, in seven lake areas of Scotland. In: Sir J. Murray. Bathymetrical Survey of the Scottish Fresh-water Locks, Conducted under the Direction of Sir John Murray… and Laurence Pullar… During the Years 1897 to 1909. Report on the Scientific Results. Edinburgh, Challenger Office, pp. 156-190. Wickens, G. E. 2001. Useful ferns, bryophytes, fungi, bacteria and viruses. In: Economic Botany. Chapt. 18. Principles and Practices. Springer, New York, pp. 347-372. Wilkinson, S. M. and Ormerod, S. J. 1994. The effect of catchment liming on bryophytes in upland Welsh streams, with an assessment of the communities at risk. Aquat. Conserv.: Marine Freshwat. Ecosyst. 4: 297-306. Williams, H. and Cain, R. F. 1959. Additions to the Hepaticae of Ontario. Bryologist 62: 145-148. Wittlake, E. B. 1950. Bryophytes of Spy Rock Hollow. J. Ark. Acad. Sci. 3: 39-40. Zechmeister, H. and Mucina, L. 1994. Vegetation of European springs: High‐rank syntaxa of the Montio‐Cardaminetea. J. Veg. Sci. 5: 385-402. Zhu, R. L., Wang, D., Xu, L., Shi, R. P., Wang, J., and Zheng, M. 2006. Antibacterial activity in extracts of some bryophytes from China and Mongolia. J. Hattori Bot. Lab. 100: 603615. Zubel, R. 2008. Does Jungermannia exsertifolia subsp. cordifolia (Marchantiophyta, Jungermanniaceae) occur in the Polish Carpathians? In: Stebel, A. and Ochyra, R. (eds.). Bryophytes of the Polish Carpathians. Sorus, Poznań, pp. 267-270. Zubel, R. 2009. New interesting localities of Cladopodiella fluitans and Geocalyx graveolens (Marchantiophyta, Jungermanniales) in SE Poland against the background of their distribution in the country. Ann. UMCS Biol. 64: 6773.

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Chapter 1-4: Aquatic and Wetland: Marchantiophyta, Order Jungermanniales – Jungermanniineae

Glime, J. M. 2020. Stream Physical Factors Affecting Bryophyte Distribution. Chapt. 2-1. In: Glime, J. M. Bryophyte Ecology. Volume 4. Habitats and Roles. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Last updated 21 July 2020 and available at .

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CHAPTER 2-1 STREAM PHYSICAL FACTORS AFFECTING BRYOPHYTE DISTRIBUTION

TABLE OF CONTENTS Factors Affecting Bryophyte Presence ................................................................................................................................... 2-1-2 Stability and Stream Order ..................................................................................................................................................... 2-1-5 Substrate ................................................................................................................................................................................ 2-1-6 Substrate Type ............................................................................................................................................................... 2-1-6 Rock Size ....................................................................................................................................................................... 2-1-8 Substrate Stability ........................................................................................................................................................ 2-1-12 Erosion ................................................................................................................................................................. 2-1-14 Stability, Bryophytes, and Macroinvertebrates .................................................................................................... 2-1-14 Step Pools............................................................................................................................................................. 2-1-15 Disturbance Factors ............................................................................................................................................................. 2-1-15 Flow ............................................................................................................................................................................. 2-1-17 Abrasion and Scouring ................................................................................................................................................. 2-1-20 Drag Coefficients ......................................................................................................................................................... 2-1-21 Flooding ....................................................................................................................................................................... 2-1-21 Bankfull Discharge ...................................................................................................................................................... 2-1-23 Regulated Rivers .......................................................................................................................................................... 2-1-24 Drought and Desiccation .............................................................................................................................................. 2-1-24 Depth............................................................................................................................................................................ 2-1-25 Siltation ........................................................................................................................................................................ 2-1-26 Pasture and Plantations ................................................................................................................................................ 2-1-27 Clear-cutting ................................................................................................................................................................ 2-1-27 Forest Buffers....................................................................................................................................................... 2-1-28 Effects on Streams and Riparian Zones................................................................................................................ 2-1-28 Time Lags ............................................................................................................................................................ 2-1-29 Ice and Snow ................................................................................................................................................................ 2-1-29 Anchor Ice.................................................................................................................................................................... 2-1-30 Summary .............................................................................................................................................................................. 2-1-31 Acknowledgments ............................................................................................................................................................... 2-1-31 Literature Cited .................................................................................................................................................................... 2-1-31

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Chapter 2-1: Stream Physical Factors Affecting Bryophyte Distribution

CHAPTER 2-1 STREAM PHYSICAL FACTORS AFFECTING BRYOPHYTE DISTRIBUTION

Figure 1. Tolliver Falls 7 January 1961, Swallow Falls Park, Maryland, USA. The stream remains open even though the ground is buried in snow. The leafy liverwort Scapania undulata is common in the falls. Photo by Janice Glime.

In the early stages of my career, few purely ecological studies of aquatic bryophytes existed. At that time, an emphasis on pollution fawned studies on the uptake and binding of heavy metals and other pollutants. Since that time, many studies on the ecology and physiology of these aquatic species have emerged. These have helped us to understand the roles of various ecological factors that determine which bryophytes can occupy a particular location. This chapter will introduce those stream parameters that are able to affect the bryophyte populations. Aquatic, and especially stream, bryophytes must be able to survive both complete submersion and periods of desiccation and even high light when their substrate becomes exposed. This exposure can often be coupled with high temperatures that are more conducive to respiration than to photosynthesis. Acrocarpous mosses tend to dominate in the frequently exposed situations,

whereas pleurocarpous mosses have better survival where water is flowing most of the time, and especially during periods of rapid flow. Aquatic habitats provide adaptive challenges that can be quite different from those of terrestrial habitats. These have been adequately described in several books and publications on limnology and flowing waters (e.g. Margalef 1960; Ruttner 1963; Hynes 1970; Allan 1995). Streams, because of their flowing water and sometimes intermittent flow, can be even more challenging. Hence, the number of truly aquatic bryophytes in streams is relatively small.

Factors Affecting Bryophyte Presence In their study of 187 Portuguese water courses (mostly headwaters), Vieira et al. (2012a) assessed the effects of fluvial and geologic gradients among the streams,

Chapter 2-1: Stream Physical Factors Affecting Bryophyte Distribution

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focussing on type of river segment, micro-habitat, immersion level, water velocity, depth range, shading, rock types, and altitude. They identified 140 taxa (102 mosses, 37 liverworts, and 1 hornwort). They furthermore noted that water velocity, local incident light, and hydrologic zone explained the taxonomic groups, life forms, and life strategies present (Vieira et al. 2012b). The most common taxa in these streams were Racomitrium aciculare (Figure 2), Platyhypnidium lusitanicum (Figure 3), Hyocomium armoricum (Figure 4), Scapania undulata (Figure 5), and Fissidens polyphyllus (Figure 6), with Brachytheciaceae (Figure 3), Grimmiaceae (Figure 2), and Fissidentaceae (Figure 6) being the most frequent families.

Figure 4. Hyocomium armoricum, one of the common bryophytes in Portuguese streams. Photo by David T. Holyoak, with permission.

Figure 2. Racomitrium aciculare (Grimmiaceae), one of the common bryophytes in Portuguese streams. Photo by Michael Lüth, with permission.

Figure 5. Scapania undulata, one of the common bryophytes in Portuguese streams. Photo by Michael Lüth, with permission.

Figure 6. Fissidens polyphyllus, one of the common bryophytes in Portuguese streams. Photo by David T. Holyoak, with permission.

Figure 3. Platyhypnidium lusitanicum (Brachytheciaceae), one of the common bryophytes in Portuguese streams. Photo by David T. Holyoak, with permission.

Scarlett and O'Hare (2006) studied the community structure of stream bryophytes in rivers of England and Wales. They analyzed the 50 most common bryophytes, determining that Fontinalis antipyretica (Figure 7) and Platyhypnidium riparioides (Figure 8) were the dominant

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Chapter 2-1: Stream Physical Factors Affecting Bryophyte Distribution

species. They found the strongest environmental gradient to be the transition from the lowland chalk geology to those of steeply sloping, high altitude systems with less erodable rocks. This trend relates to substrate size, altitude of source, distance to source, and site altitude as important predictors of species richness (stepwise regression analysis, p 60% of total, mainly into aspartate, alanine, and glutamate) and organic acids (< 40%). Cratoneuron filicinum (Figure 41), a droughtsensitive species, and Syntrichia ruralis (Figure 24), a drought-tolerant species, fix CO2 non-autotrophically at a rate of about 1.2 and 2.2 µmol h-1 g-1 dry weight, respectively (Dhindsa 1985). During drying these two species differ in their responses. The dark CO2 fixation rate of S. ruralis does not diminish until the tissues lose about 60% of their original fresh weight. This dark fixation resumes immediately upon rehydration in this species, but not in C. filicinum. Nevertheless, even in S. ruralis, when dry plants are placed in nearly 100% relative humidity, the weight increases to only about 40% of the original hydrated weight and dark CO2 fixation returns to only about 60% of that in the fresh moss. Dhindsa suggested that the immediate availability of NADPH, produced from NADH during dark CO2 fixation, in drought-tolerant species may be important in repairing cellular damage through reductive biosynthesis of membrane components and other damaged cellular constituents.

Temperature Effects Chlorophyll content can serve as a surrogate for cell health. Hearnshaw and Proctor (1982) used chlorophyll content to determine the loss of viability in seven species [Anomodon viticulosus (Figure 44), Racomitrium aquaticum (Figure 45), R. lanuginosum (Figure 46), Tortella humilis (Figure 47), Andreaea rothii (Figure 48), Frullania tamarisci (Figure 49), and Porella platyphylla (Figure 7)] of bryophytes that were kept dry at temperatures ranging 20-100ºC from a few minutes to weeks or months. Although the different temperatures tended to affect all of them similarly, the time required for the same amount of damage differed widely. At 100ºC, the least resistant species suffered a 50% loss of chlorophyll in a few minutes or less. The more resistant species survived at 20 and 37ºC for weeks to months before experiencing 50% chlorophyll loss. Both Racomitrium species exhibited great tolerance at temperatures in the middle part of the range investigated, despite R. aquaticum occurring on moist, shaded rocks and R. lanuginosum occurring frequently in the tundra and tropical alpine areas, although these locations are frequently misty or humid.

Figure 44. Anomodon viticulosus, a xeric species. Photo by Hermann Schachner, through Creative Commons.

Figure 45. Racomitrium aquaticum, a species of wet habitats. Photo by Hugues Tinguy, through Creative Commons.

Figure 46. Racomitrium lanuginosum, a xeric moss. Photo by Hermann Schachner, through Creative Commons.

Chapter 2-6: Physiological Adaptations – Water, Light, and Temperature

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the water. These two processes affect mosses from different habitats differently. Peñuelas (1984b) found that aquatic moss species lost 50% of their chlorophyll in very few weeks of emersion, with pigments having OD430/OD665 being most sensitive. The phaeo-pigment proportion was sensitive to periods of rainfall and humidity. Cinclidotus fontinaloides (Figure 50) was the most tolerant species, Fontinalis antipyretica (Figure 12) the least. By contrast, all terrestrial mosses studied lost 50% of their chlorophyll content in the first week of immersion. Spitale (2009) even found that he could use pigments as indicators of the height above the water table, hence the moisture conditions, in spring systems.

Figure 47. Tortella humilis, a species of rock crevices near water. Photo by Bob Klips, with permission.

Figure 48. Andreaea rothii, a rock-dwelling xeric moss. Photo by David T. Holyoak, with permission.

Figure 50. Cinclidotus fontinaloides, a species of emergent rocks that is relatively tolerant of desiccation. Photo by Hermann Schachner, through Creative Commons.

Fatty Acid Responses

Figure 49. Frullania tamarisci, a moss that can be exposed to a wide range of humidities. Photo by Tim Waters, through Creative Commons.

Pigment Responses Like emigration and immigration, emersion is the process of exiting and immersion is the process of entering

Stewart and Bewley (1982) found that both the desiccation tolerant Syntrichia ruralis (Figure 24) and the desiccation-intolerant Cratoneuron filicinum (Figure 41) maintained their fatty acid phospholipid composition during rapid drying. However, after slow drying, some unsaturated fatty acids decline. After slow drying, S. ruralis exhibits further decline of these fatty acids upon rehydration. Then, after ~105 minutes, they regain their original nondesiccated levels. After rapid desiccation, the decline is smaller and more transient. On the other hand, in C. filicinum most of the phospholipid unsaturated fatty acids decrease during rehydration, and these are never recovered. In contrast to S. ruralis, C. filicinum exhibits very little incorporation of acetate or glycerol during rehydration. Fatty acid concentrations vary widely among the bryophytes (Dembitsky & Rezanka 1995). For example, acetylenic fatty acid concentration in the wetland moss Calliergon cordifolium (Figure 51) was 6.6% but reached 80.2% in the floating thallose liverwort Riccia fluitans. At the very least, these differences suggest that we need to look at the role of fatty acids as protective substances in bryophytes.

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Chapter 2-6: Physiological Adaptations – Water, Light, and Temperature

Figure 52. Ludwigia arcuata, an aquatic tracheophyte that responds to ethylene concentrations to determine leaf shape. Photo by Shaun Winterton, through Creative Commons. Figure 51. Calliergon cordifolium; the genus Calliergon has algal fatty acids. Photo by Jerry Jenkins, Northern Forest Atlas, with permission.

ABA Mediation Noting the ancestral terrestrial life style of bryophytes and their evolutionary history of going back and forth between terrestrial and aquatic environments, Wanke (2011) explored the role of the hormone ABA in submersed-emersed switches. This environmentally responsive hormone has been present throughout the plant kingdom from bryophytes to flowering plants. It can initiate the production of other hormones. Whereas heterophylly (having more than one leaf type on same plant) is common between submersed and emergent leaves of tracheophytes, such heterophylly is rare among bryophytes. In the tracheophyte Callitriche heterophylla, GA (gibberellic acid, a growth hormone) induces cell elongation, causing emergent leaves to resemble submersed leaves (Deschamp & Cooke 1985). On the other hand, GA seems to induce heterophylly through a pathway with the gaseous hormone ethylene, and this antagonizes the synthesis of the hormone ABA. Thus, when aerial shoots of Ludwigia arcuata (Figure 52) were exposed to ethylene, they were induced to form leaves resembling submersed leaf morphology (Kuwabara et al. 2003; Kuwabara & Nagata 2006). Little work has been done with bryophytes and the effects of these three hormones. Yet we know that ACC, the ethylene precursor, has a significant effect on morphology and coloration in Fontinalis squamosa (Figure 1) and F. antipyretica (Figure 12) (Glime & Rohwer 1983). We need to investigate its role in emergent vs submergent morphology.

Added ABA in three bryophytes [mosses Physcomitrella patens (Figure 53) and Atrichum undulatum (Figure 54) and liverwort Marchantia polymorpha (Figure 55)] caused these bryophytes to exhibit a decrease in total chlorophyll and carotenoids (Vujičić et al. 2016). Effects on growth were unclear. It is likely that ABA has effects on desiccation tolerance in aquatic bryophytes, but much more research is needed to understand the role of this hormone in bryophytes.

Figure 53. Physcomitrella patens, a moss that responds to added ABA by a reduction in total chlorophyll. Photo by Hermann Schachner, through Creative Commons.

Chapter 2-6: Physiological Adaptations – Water, Light, and Temperature

Figure 54. Atrichum undulatum, a moss that responds to added ABA by a reduction in total chlorophyll. Photo by David T. Holyoak, with permission.

Figure 55. Marchantia polymorpha with gemmae cups, a liverwort that responds to added ABA by a reduction in total chlorophyll. Photo by Hermann Schachner, through Creative Commons.

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Figure 56. Sphagnum trinitense, an aquatic species, paired with S. recurvum in the experiments by Rice (1995). Photo by Blanka Aguero, with permission.

Figure 57. Sphagnum recurvum, a non-submersed species, paired with S. trinitense in the experiments by Rice (1995). Photo by Malcolm Storey, DiscoverLife.org, with online permission.

Allocation Changes Rice (1995) compared allocation and growth in pairs of aquatic and non-submersed species of Sphagnum (Figure 56-Figure 58). The submerged taxa all had greater relative growth rates and greater allocation to their photosynthetic tissues (Figure 59) when compared to the non-aquatic species (Figure 60). The latter was expressed as higher whole plant chlorophyll content. In this genus, the greater allocation to photosynthetic processes was accomplished by fewer or smaller hyaline cells and a shift in the biochemical partitioning within the photosynthetic cells to favor light-reaction proteins. This latter factor was estimated from chlorophyll to nitrogen ratios. But these adaptations differed by species.

Figure 58. Sphagnum recurvum leaf cells, a non-submersed species, paired with S. trinitense in the experiments by Rice (1995). The less dense chlorophyll content and large hyaline cells are demonstrated in this non-aquatic species. Photo by Malcolm Storey, DiscoverLife.org, with online permission.

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Chapter 2-6: Physiological Adaptations – Water, Light, and Temperature

Most bryophytes seem unable to tolerate high light intensities. Aquatic bryophytes are typically protected from light by water depth, and in woodland streams and small pools, also by canopy cover. At cool temperatures, high light can cause severe reactions in Fontinalis antipyretica (Figure 12), resulting in loss of chlorophyll or production of bright red pigments (Figure 61-Figure 63) (Glime 1984).

Figure 59. Sphagnum cuspidatum, an aquatic species, showing small hyaline cells and dense chloroplasts in the photosynthetic cells. Photo by Hermann Schachner, through Creative Commons.

Figure 61. Fontinalis antipyretica red (especially upper middle) in cold water and high light 15 May 1982 near Rothenfels, Germany. Photo by Janice Glime.

Figure 60. Sphagnum fuscum, a hummock species, with leaf cells that show large hyaline cells that envelope the photosynthetic cells. Photo by Hermann Schachner, through Creative Commons.

Light Proctor (1990) considered most bryophytes to be shade plants, having low chlorophyll a/b ratios¸ and reaching light saturation at relatively low light levels. They behave as C3 plants, despite their ability to dry out to water contents as low as 5-10% of their dry weight. Growth forms can have a profound effect on the ability for light capture. Proctor stated that "bryophyte growth-forms must represent an adaptive balance between water economy and needs for light capture and carbon and mineral nutrient acquisition."

Figure 62. Fontinalis antipyretica red leakage in tropism experiment out of water, a response also seen in high light. Photo by Janice Glime.

Chapter 2-6: Physiological Adaptations – Water, Light, and Temperature

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likely limited by CO2 diffusion into the leaves. The greater area with ventilated photosynthetic tissue (Figure 64), such as that of Polytrichum (Figure 65), may account for the greater productivity of members of that genus.

Figure 63. Fontinalis antipyretica red cells in tropism experiment out of water, a response similar to that in high light. Photo by Janice Glime.

Martin and Churchill (1982) found that both chlorophyll concentrations and a:b ratios were lower in bryophytes than for most tracheophytes. Those mosses collected from habitats with low light levels had higher chlorophyll concentrations and lower chl a:b ratios than those collected from high light levels. These differences suggest that changes in chlorophyll concentrations can adapt bryophytes to low or high light. Thus, we should expect mosses in forest streams to contain more chlorophyll than those in terrestrial habitats. Bryophytes may have relatively low light optima. Using populations from the Keweenaw Peninsula of Michigan, USA, Glime and Acton (1979) found that the Fontinalis duriaei-periphyton association had its maximum productivity at 10ºC, 5400 lux. At 5400 lux it approached light saturation under the experimental conditions, whereas direct sunlight at noon can reach 120,000 lux (Wikipedia 2019). The ability to survive with low growth rates in low light permits bryophytes to live at depths of water that are unavailable to their tracheophyte competitors. For example, Westlake and Dawson (1976) noted that Fontinalis antipyretica (Figure 12) became a significant part of the plant biomass at depths greater than 1 m in the River Frome. Light there is only 30% of incident light. Burr (1941) concluded that Fontinalis (Figure 5, Figure 6, Figure 12, Figure 20) reaches its light compensation at 150 lux at 20ºC and at 40 lux at 5ºC. Nevertheless, some species are tolerant of high light, such as Schistidium agassizii (Figure 21) in Alaskan streams (Bowden et al. 1994) and others (Ormerod et al. 1994). Marschall and Proctor (2004) concluded that, based on 39 species of mosses and 16 of liverworts, bryophytes are generally shade plants. This was supported by total chlorophyll, Chl a:b ratio, PPFD values at 95% saturation mostly 50%). They interpreted this to mean that the photosynthetic tissues of these aquatic autotrophs have a considerable capacity for alternative pathways. But understanding these alternatives has been elusive. Peñuelas et al. (1988) found that aquatic bryophyte shoots had a higher rate of respiratory oxygen uptake (5366 µmol O2 g-1 DW h-1) than did stems of flowering plants,

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Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

but it was lower than those for flowering plant leaves. The cyanide-resistant respiration suggested the existence of an alternative pathway to the usual cytochrome system in all the plants and algae studied. Steemann Nielsen (1947) cautioned that Fontinalis (Figure 2) had quite variable respiratory rates, making long experiments necessary. On the other hand, it has practically no C resource reserves that complicate measurements of photosynthesis in terrestrial tracheophytes. Maberly (1985) examined the roles of photon irradiance, CO2 concentration, and temperature in the aquatic moss Fontinalis antipyretica (Figure 2). Using 7 levels of photon irradiance and 5-6 concentrations of CO2 at the ambient temperature of the collection site, Maberly measured photosynthesis in 4 months during the year. They found no evidence of photoinhibition, and light compensation was low compared to values for this species published elsewhere. The CO2 compensation was typical of that for C3 plants (those plants that initially store carbon from CO2 in a 3-C compound and that are unable to store CO2 in compounds used to complete the photosynthetic cycle later). They found that the slope of photosynthesis vs CO2 concentration increases linearly with temperature in a manner that is consistent with the effects of boundary layer resistance. These measurements clearly demonstrated the interaction of temperature, CO2 concentration, and irradiance on the rate of photosynthesis, emphasizing the need to consider all three factors when determining the upper and lower limits of net photosynthesis. Winter Temperatures Atanasiu (1968) reported on the photosynthesis and respiration of bryophytes in winter. Photosynthesis in some bryophytes occurs under ice (Bowes & Salvucci 1989), a condition wherein light levels are quite low. Measurements indicate that the truly aquatic Fontinalis antipyretica (Figure 2) and F. squamosa (Figure 30) have their greatest vitality in winter, a time when both light levels and temperatures are low, hence reducing respiratory loss (Beaucourt et al. 1999; Beaucourt 2000). Furthermore, photosynthesis does not seem to be affected by internal concentration of nutrients or pigment composition. Beaucourt and coworkers reported that the chlorophyll concentration of Fontinalis antipyretica and F. squamosa in the studied European sites was similar to that found in terrestrial bryophytes and tracheophytes. Growth could occur throughout the year, but varied by season. Greater breadth of the metabolic capacity helps to account for the broader distribution of F. antipyretica when compared to that of F. squamosa. Both species have only moderate nutritional requirements, permitting them to live in oligotrophic (having relatively low concentrations of plant nutrients) waters. They have low chl a: chl b ratios, typical of shade plants, and only limited photoprotective capacity. Nevertheless, their pheophytinization indices indicate a "good degree of vitality." Thus, these shadeadapted plants have rates of photosynthesis and respiration similar to those of shade-adapted tracheophytes. These are accompanied by low apparent quantum yields (measure of how many molecules of a certain substance such as

H2O2, dissolved inorganic carbon, etc. can be produced per photon absorbed by, for example, colored dissolved organic matter), low compensation points (incorporated C = C lost in respiration), and low saturation points (level of light at which more light does not increase photosynthesis). They also develop photoprotective mechanisms at low irradiances and non-photochemical damping. These factors, along with their electron transport rate, indicate that the two aquatic mosses suffer from photoinhibition at relatively low light levels. CO2 Blackman and Smith (1910) were early researchers on the photosynthesis of aquatic plants, including bryophytes. They found that in Fontinalis (Figure 2, Figure 4, Figure 23) the assimilation increased steadily and proportionally as the CO2 concentration increased. Then it stopped abruptly at ~0.023 g CO2 assimilation per hour. They interpreted this as a limit set by the light intensity, creating a CO2 saturation point for that light intensity. Compared to Elodea (Figure 32) in the same study, the Fontinalis was consistently less efficient in its uptake of CO2. They suggested that the lack of an internal atmosphere limited the uptake in the moss. Consistent with the concept of limiting factors, they considered that whatever was in least supply imposes the limit to photosynthesis. The concept is based on Liebig's 1840 Law of the Minimum (Odum 1959), stating that growth is controlled by the scarcest resource, not the total amount of resources available. A variety of factors interact to determine the level of photosynthesis that aquatic plants can achieve. These include use of alternative sources of CO2, alternative sources of carbon besides CO2, carbon-concentrating mechanisms, adaptations to achieve net photosynthesis in low light, and morphological adaptations to increase absorption of inorganic carbon and nutrients (Boston et al. 1989; Bowes & Salvucci 1989; Madsen & Sand-Jensen 1991). Bowes and Salvucci (1989) considered plasticity in the photosynthetic metabolism to be an important adaptation in submersed aquatic macrophytes. They considered dissolved inorganic carbon, light, and temperature to be the main constraints, but pH, oxygen, and mineral nutrients may also contribute to the constraints. Because of low CO2 diffusion rates, aquatic macrophytes typically have low light requirements and low photosynthetic rates. Photosynthesis in some occurs under ice and in some at 35ºC. Their plasticity is most recognizable in their variable CO2 compensation points, in part because of their photorespiration. Nevertheless, alternate ways of obtaining or storing CO2 have not been discovered in bryophytes. CO2 or Bicarbonate Use – or Not James (1928), who included Fontinalis antipyretica (Figure 2) in his studies on CO2 assimilation, noted that measurements of CO2 uptake had assumed that all aquatic plants absorbed CO2 only and could not use bicarbonate, but that this was a false assumption, at least for tracheophytes. Nevertheless, this question continued to puzzle those who studied photosynthesis in aquatic

Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

bryophytes (Ruttner 1947, 1948; Steeman Nielsen 1947; Steeman Nielsen & Kristiansen 1949; Stålfelt 1960a). Stålfelt (1960b) noted that contributors to the publication Handbuch der Pflanzenphysiology. V. Die CO2assimilation had shown the dependence of CO2 assimilation on light, temperature, and carbonic acid, noting the interactions of external and internal factors in CO2 assimilation. Nevertheless, the ability of some aquatic bryophytes to thrive in alkaline streams where free CO2 is scarce, still lacks explanation today. Madsen and Sand-Jensen (1991) also puzzled over the relationship between CO2 concentration and net photosynthesis in aquatic plants, including mosses. They found that it was a more gradual relationship than that predicted by Michaelis-Menten kinetics (equation relating reaction velocity to substrate concentration). This suggested that other factors besides activity of carboxylation enzymes were at play in regulating photosynthesis. When CO2 concentrations in the medium are low, photosynthesis is restricted by the slow diffusion rate into the plant at the carboxylation site. The maximum possible photosynthetic capacity seems to be limited by the enzyme activity or turnover of intermediates in the carbon reduction cycle, including limitations by ATP and reducing agents. But for many of the aquatic macrophytes (~50% of those tested), bicarbonate can be a source of carbon for photosynthesis. A number of researchers have failed to find any use of bicarbonates by aquatic bryophytes (Bain & Proctor 1980). Bain and Proctor used the rise in pH as an indicator of photosynthetic uptake of CO2. They found equilibrium values around pH 8.0-9.0, a limit that indicates the mosses are CO2 limited and unable to use bicarbonate. By comparison, four known bicarbonate-using macrophytes reached equilibrium at pH 10.1 to 10.9. The hornwort Anthoceros husnotii (Figure 65), on the other hand, reached its maximum pH value at 9.5 in 2.0 mM NaHCO3, suggesting a possible uptake mechanism for bicarbonate. Anthoceros, a member of Anthocerotophyta, has pyrenoids (Figure 66), and these have been considered as possible CO2-concentrating organelles (Smith & Griffiths 1996; Raven et al. 2018).

Figure 65. Anthoceros agrestis; maximum photosynthesis of A. husnotii reached a pH of 9.2. Photo by Jean Faubert, with permission.

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Figure 66. Cells of Anthocerotophyta showing doughnutshaped pyrenoids. Photo by Chris Lobban, with permission.

Some aquatic plants, particularly the isoetids, have a carbon-concentrating mechanism that permits the binding of CO2 at night for later use. As noted, we know that among the bryophytes, the Anthocerotophyta (Figure 65) have a CO2-concentrating mechanism in the pyrenoid. However, no such structure is known in the aquatic bryophytes outside this phylum. Is there some other mechanism for trapping CO2 or for converting bicarbonates? Raven et al. (1998) found that most bryophytes tested were typical C3 plants. However, two of the aquatic mosses, Fissidens cf. mahatonensis and Fontinalis antipyretica (Figure 2) behave as if they have a CO2concentrating mechanism. Furthermore, in running water there seems to be little restriction of CO2 fixation due to CO2 diffusion. As noted by Madsen and Sand-Jensen (1991), one option exhibited by tracheophytes is the development of floating or aerial leaves, giving them access to atmospheric CO2. To my knowledge, such a possibility has not been explored in bryophytes. But consider the bryophytes that are partly submersed and partly emergent on rocks. They remain fully hydrated through splash, but have access above the water line to atmospheric CO2. This provides two possibilities. The CO2 could be taken into exposed leaves and transported to other parts of the plant, or the CO2 could be incorporated into intermediate or even final products and then transported to sites where it is needed. Many studies indicate that bryophytes are able to transport substances throughout the plant, so the latter explanation is feasible. Both hypotheses remain to be tested, possibly through tracer studies of labelled atmospheric CO2. Madsen et al. (1993a) demonstrated that net photosynthesis of stream macrophytes declined 34-61% as flow velocity in a stream increased from 1 to 8.6 cm s-1. At the same time dark respiration increased 2.4-fold over that range. These included the moss Fontinalis antipyretica (Figure 2, a species considered unable to use bicarbonates. But how does this relate to CO2 usage? Madsen et al. (1993b) suggested that plant species with a high ability to extract carbon typically, possibly

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Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

through bicarbonate use, had low RUBISCO activity, low chlorophyll concentrations, and low surface to volume ratio. This was particularly true for marine algae. Those species with low ability to extract carbon exhibited an opposite pattern. Madsen and coworkers suggest that it costs less to accomplish carbon assimilation in plants with a CO2- concentrating mechanism. These relationships have not been investigated in bryophytes and should be investigated, especially in the Anthocerotophyta (Figure 65). Having emergent parts permits some semi-aquatic bryophytes to obtain atmospheric CO2 in their growing tips, but this is not an available option for truly aquatic species. Mosses such as Fissidens grandifrons (Figure 67) can live in waterfalls where exposure to atmospheric gasses is more common, but they can also exist and grow in completely submersed conditions in alkaline water where one would not expect to find any free CO2 (Glime & Vitt 1987). So how do these mosses obtain the carbon needed for photosynthesis?

Figure 67. Fissidens grandifrons, a moss that can grow completely submersed in alkaline streams. Photo by Janice Glime.

One possibility is CO2 from sediments and adhering microbes, as reported by Madsen and Sand-Jensen for tracheophytes (1991). In some tracheophytes, the sediments can contribute more than 90% of the total carbon uptake. But many of these tracheophytes have pumping mechanisms that move the CO2 from the sediments, through roots or tubers, to upper parts of the plants. Such a mechanism does not seem possible in bryophytes because of their lack of lacunae (spaces) in the stems where they could carry the CO2 to leaves. Sanford et al. (1974) concluded that CO2 from the bacterial flora was important for the growth of Hygrohypnum ochraceum (Figure 59) in the Sacramento River, California, USA. In their experiments, an increase in dissolved CO2 promoted an increase in elongation. Furthermore, the moss was less abundant in areas of the river that had a lower CO2 level. Nevertheless, in the cold waters of glacial melt streams such as those where Glime and Vitt (1987) found Fissidens grandifrons (Figure 67), we would expect the

transformation of evolved CO2 or loss to the atmosphere to be slowed by the low temperature. With no epidermis or thick waxy cuticle to interfere with CO2 absorption (bryophytes often do have a cuticle – Green & Lange 1995), we could expect the moss to grab the CO2 before all could be lost to the atmosphere or the bicarbonatecarbonate pathway in the water. But again, we have no evidence to support this hypothesis. I would guess that the rapid flow of these glacial streams does not facilitate the accumulation of organic silt. The microbes on the mosses have not been examined. Another possibility that has not been explored is the possibility that the cation exchange sites on moss leaf cells could create an environment in which bicarbonate is converted to CO2 due to lowering of pH at the leaf surface. We know that bryophytes (not just Sphagnum – Figure 54) have cation exchange. That means that the cell walls, including those on the surface, release hydrogen ions, thus creating a microenvironment of lower pH. Or perhaps the carbonic anhydrase in the moss leaf cells (see Steemann Nielsen & Kristiansen 1949; Arancibia & Graham 2003). is able to convert bicarbonates in contact with the moss leaves to CO2 at the leaf surface. Could this be sufficient to effect the change of bicarbonates, and even carbonates to release free CO2 at the moss surface? But the controversy continued. Osmond et al. (1981) found that delta 13C values were consistent with the hypothesis that Fontinalis antipyretica (Figure 2) used almost exclusively free CO2 in photosynthesis. Rather, they considered that the boundary layer diffusion and bicarbonate uptake may determine the assimilation rate. Their data on differences in different flow rates seemed to confirm this. When attempting to test the reliability of radiocarbon dating of aquatic mosses, MacDonald et al. (1987) got a surprise. They found 14C dates in the moss Drepanocladus longifolius (Figure 68) that were considerably older than the plant macrofossils of terrestrial species. The 14C of living D. longifolius in the lake was less than 85% modern. Could the CO2 used by the mosses come from sediment decomposition that releases older 14C?

Figure 68. Drepanocladus longifolius, a species in which extant plants have ancient carbon, suggesting use of CO2 from the sediments. Photo by John Game Flickr Creative Commons.

Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

Burr (1941) concluded that Fontinalis (Figure 2, Figure 4, Figure 23) is more productive in bicarbonate than in CO2, but finding any mechanism to explain such a relationship has been elusive. Allen and Spence (1981) concluded that there was a gradation of bicarbonate users, not a "user" vs "non-user," among aquatic plants. This, in fact, makes some sense for this genus. Farmer et al. (1986) tested 15 species of freshwater macrophytes for activities of RUBISCO and PEP carboxylase in photosynthesis. RUBISCO (enzyme present in plant chloroplasts, involved in fixing atmospheric CO2 during photosynthesis and in oxygenation of resulting compound during photorespiration) was the most active in all species, including the moss Fontinalis antipyretica (Figure 2) and some liverworts, a usage consistent with C3 plants. While we are speculating, we might also consider the possibility of organic sources of carbon such as amino acids. We know that aquatic mosses can take up amino acids (Alghamdi 2003), but this would again require sediments, adhering organisms, or amino acids suspended in the water. And can they serve as a carbon source for photosynthesis in addition to their role as a nitrogen source? Are there other organic acids that can serve as photosynthetic carbon sources? We have tended to underestimate the evolutionary changes in bryophytes (Glime 2011). While tracheophytes were developing all sorts of structural diversification, bryophytes were limited by their lack of lignin and consequent small size. Lacking these options would put more selection pressure on biochemical innovations. This is evidenced by the wide range of biochemical defenses against herbivory. The bryophytes have had even longer than tracheophytes to diversify. Why should we expect them to have evolved fewer adaptations? Rather, with selection pressures acting on a generation with only one set of chromosomes, we should expect more beneficial change to persist while unbeneficial ones can more easily be eliminated. We should pay more attention to their biochemical-physiological adaptations. pH Early studies on aquatic bryophytes indicated that many had a restricted pH range (Iversen 1929). Negoro (1938) reported on bryophyte associations in minerotrophic acidic waters in Japan. The pH can be an important limiting factor for bryophyte colonization (Apinis & Lacis 1936), especially in water. It affects the solubility of CO2 in the water. It can also affect the solubility and availability of other nutrients. Steemann Nielsen (1952) examined several aquatic species, including Fontinalis antipyretica (Figure 2) and F. dalecarlica (Figure 42), regarding their persistence at extreme pH values. Acidity has been sufficiently important that Tremp and Kohler (1993), among others, advocated using water mosses as indicators of acidification to monitor rivers. Tremp et al. (2012) looked at the factors that were important in defining bryophyte communities. Among these, pH is an important determinant of the bryophyte flora. This is reflected in the bicarbonate/ionic strength,

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affecting the availability of CO2. It is manifest in distinctly different bryofloras in hard and soft water. For example, Westlake (1981) considered the presence of Fontinalis (Figure 2, Figure 4, Figure 23) in hard water to be an anomaly. This conclusion was based on the need for this moss to obtain its carbon for photosynthesis as free CO2, with no indication that it can use bicarbonates. Steemann Nielsen (1952) experimented with the effects of lowering the pH on the photosynthesis and coloration of several species of Fontinalis (Figure 2, Figure 4, Figure 23). After populations of Fontinalis dalecarlica (Figure 42) were cultured at pH 3.0-3.1 for 23 hours, photosynthesis was strongly reduced. The leaves, however, still appeared fresh and green. At pH 2.1 the photosynthetic rate decreased further. After 80 minutes the leaves still appeared normal, but after 21 hours the green color was almost totally gone. Fontinalis antipyretica (Figure 2) had even less ability to endure low pH. In fact, this species lost its green color completely after 22 hours at pH 3.0. On the other hand, at pH 3.1 for only 80 minutes, F. antipyretica recovered completely when transferred to less acid water. At pH 4.0 there was only a slight decrease in photosynthesis after one hour. At pH 6.5, there was no decrease after 20 hours. Sorensen (1948) reported a field pH range of 5.5-8.2 for this species. It appears that the main factor separating suitable pH ranges for these two species is the ability to obtain sufficient CO2, but at low pH levels F. antipyretica can suffer severe chlorophyll damage. Much of our understanding of the effects of acid waters on bryophyte communities has come from studies on acid rain effects. Elwood and Mulholland (1989) found that both biomass and productivity of epilithic algae and bryophytes seemed to increase when the stream water pH declined to sustained levels below 5.0, whereas at the same time the fish and macroinvertebrates declined. The benefits of this lower pH might be in the greater availability of free CO2 at those levels. Turner et al. (2001) used phosphatase activities as a measure of pH effects. Enzymes such as these have optimal ranges for temperature and pH and can cease activity when very far out of that range. They found that in the aquatic mosses, phosphomonoesterase (PMEase) activity was at its optimum activity at pH 5.0. For phosphodiesterase (PDEase) the optimum was at pH 5.7. Staining suggested that the PMEase activity occurred in the cell wall of most of the moss species. Not all species exhibited PDEase activities. Tessler et al. (2013) also identified Ca and Mg as important factors in determining bryophyte distribution. These two minerals are indicators of streams with a higher than neutral pH. They also found that bryophyte tissue concentrations of phosphorus were significantly correlated with pH. This was particularly pronounced for Fontinalis cf. dalecarlica (Figure 42) at low pH, with PMEase activity in the range of 4-7 being mostly indifferent to the pH level. The PMEase activity of Scapania undulata (Figure 7) likewise varied inversely with pH level, peaking at intermediate pH, but the activity also varied with the source of the water in the same pH range. Hygrohypnum ochraceum (Figure 59) seemed indifferent to the source of

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Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

the water, having maximum PMEase activity at a pH of 5. Some species [Andreaea rothii (Figure 69), Marsupella emarginata (Figure 70)] had relatively narrow pH optima in a low pH range, typically with peak PMEase activity at the lowest pH conditions tested, while others had narrow ranges at neutral levels [e.g. Hygrohypnum ochraceum, Racomitrium aciculare (Figure 71)]. Species such as Hygrohypnum eugyrium (Figure 72-Figure 73) had a broad pH tolerance range.

Figure 72. Hygrohypnum eugyrium habitat. Hermann Schachner, through Creative Commons.

Photo by

Figure 69. Andreaea rothii, a rock-dwelling species with a narrow low pH range. Photo by Michael Lüth, with permission.

Figure 73. Hygrohypnum eugyrium, a species with a broad pH range. Photo by Hermann Schachner, through Creative Commons. Figure 70. Marsupella emarginata, a species with a narrow low pH range. Photo by Štĕpán Koval, with permission.

Figure 71. Racomitrium aciculare, a species with a narrow pH range around neutral. Photo by Michael Lüth, with permission.

Some bryophytes seem to be more typical in acidic streams. This is true for Scapania undulata (Figure 7) and Nardia compressa (Figure 53) in Wales (pH 5.2-5.8) (Ormerod et al. 1987). Fontinalis (Figure 2, Figure 4, Figure 23), on the other hand, is more typical of streams with a pH of 5.6-6.2. But ability to tolerate a particular pH seems to differ geographically. In the streams of northeastern USA, Fontinalis species are common in acidic streams (pH 4.0-4.5). But in Wales, Fontinalis squamosa (Figure 30) is common, whereas that species does not occur in the northeastern USA. Furthermore, it is likely that physiological races are separated geographically and behave differently. In the travertine streams of the French Alps and Britain, 26 mosses and 8 liverworts were documented in a pH range of 6.9-8.3 (Pentecost & Zhang 2002). The most common species were Eucladium verticillatum (Figure 74) and Palustriella commutata (Figure 75).

Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

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Figure 76. Scorpidium cossonii, a species characteristic of springs and seepages. Photo by Hermann Schachner, through Creative Commons. Figure 74. Eucladium verticillatum, a common species on travertine rock with a pH range of 6.9-8.3. Photo by Michael Lüth, with permission.

Figure 77. Scorpidium revolvens, a species characteristic of springs and seepages. Photo by Hermann Schachner, through Creative Commons. Figure 75. Palustriella commutata, a species that is able to grow in alkaline water. Photo by Michael Lüth, with permission.

Scorpidium scorpioides (Figure 58), S. cossonii (Figure 76), and S. revolvens (Figure 77) often occur in locations of high conservation value in Wales (Graham et al. 2019). These species are typical of springs and seepages and seem to form two distinct groups. Scorpidium cossonii characterizes one and S. revolvens the other, based on pH and electric conductivity. Habitats in Wales have a higher pH than those in Scandinavia. But productivity is not the only factor affected by pH. Hargreaves et al. (1975) found that moss protonemata were more abundant than mature gametophytes in highly acidic streams with a pH value of 3.0 or less. The pH also affects the solubility and uptake of heavy metals. Henricksen et al. (1988) concluded that it was a liverwort that served as a buffer and as a reservoir of aluminum. Massive amounts of aluminum were released at pH < 5. Both mosses and liverworts in the stream carry out ion exchange of base cations and aluminum during acid episodes. These ion exchange sites release base cations during acid episodes, neutralizing the additional H+ in the water. Aluminum was a major contributor to this buffering.

When Davies (2007) exposed shoot tips of Fontinalis antipyretica (Figure 2) to sulfate concentrations for 21 days at various levels of water hardness, the mosses did not respond well. They experienced significant reductions in shoot length, dry weight, and chlorophyll a and b concentrations in soft water. As the hardness as CaCO3 increased, the negative effects of sulfate toxicity decreased. Boundary-layer Resistance Boundary layer resistance can prevent CO2 from crossing into the bryophyte leaf. Jenkins and Proctor (1985) used wind tunnel evaporation measurements to assess the boundary-layer resistance to the photosynthetic They found uptake of CO2 in aquatic bryophytes. resistances of the leafy liverworts Nardia compressa (Figure 53) and Scapania undulata (Figure 7) to range 35 to 5 s mm-1 (siemens = unit used to measure electrical conductance) and 70 to 9 s mm-1, respectively, at water velocities of 0.02-0.2 m s-1. For the streamers of Fontinalis antipyretica (Figure 2), resistance is about 180 15 s mm-1 over the range of water velocity of 0.01 to 0.2 m s-1. They estimated that boundary layer resistance limits photosynthesis at stream velocities below about 0.01 m s−l in Fontinalis and below about 0.1 m s−1 in the mat‐forming species. They considered the mat growth

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Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

form of the liverworts to minimize the boundary-layer resistance at high velocities while minimizing drag. On the other hand, the streamers of Fontinalis permit it to maximize surface area under limiting levels of boundarylayer resistance. While Fontinalis (Figure 2, Figure 4, Figure 23) continued to confound the issue of obtaining CO2 in alkaline water, another Fissidens, F. grandifrons (Figure 67), emerged as doing something different. This species is known to do well in streams with high pH (e.g. Glime & Vitt 1987). Peñuelas (1985) again investigated the ability of these two species to use bicarbonates and CO2 as carbon sources for photosynthesis. He found that in NaHCO3 solutions, Fontinalis was able to increase the pH to a maximum of 9.6, corresponding to a CO2 compensation point of 1.1 mmol m-3 CO2. This increase in pH is too great to be explained by CO2 uptake alone. In fact, although the net photosynthesis decreased at high levels of pH, it did not reach zero until the pH reached 10.10 for Fissidens grandifrons and 11.8-12.0 in Fontinalis antipyretica (Figure 2)! Photosynthesis was even increased at greater bicarbonate concentrations when CO2 was held constant. This led Peñuelas to conclude that these two bryophytes could use bicarbonate. The question still remained – how? Yet, in 1989, Prins and Elzenga (1989) still stated that bryophytes could not use bicarbonates. They suggested three ways by which some aquatic plants might be able to use bicarbonates: 1. carbonic acid symport 2. external acidification of bicarbonate into CO2 3. increase in rate of conversion of bicarbonate into CO2 by carbonic anhydrase. We know that bryophyte leaves (not just Sphagnum – Figure 54) conduct cation exchange (Glime et al. 1982), so this mechanism could be used to accomplish #2. Still, in 1991, Raven considered any CO2-concentrating mechanism in bryophytes to be absent or poorly developed. In 1994, based on an extensive literature survey, Raven et al. further stated that in streamer mosses such as Fontinalis antipyretica (Figure 2), the entry of CO2 is limited only by rates of CO2 diffusion into the moss; they still acknowledged no use of bicarbonate by this moss. So why couldn't they use all three methods simultaneously? Diving Bell One novel idea is that mosses may use their photosynthetic air bubbles (Figure 1) like a diving bell. It is typical to find photosynthesizing aquatic mosses and liverworts covered in tiny air bubbles, a phenomenon known as pearling. If they are able to work like a diving bell, the bubble with a high concentration of photosynthetic O2 would trade its O2 for CO2 that is dissolved in the water, thus creating a gaseous environment containing CO2 at the leaf surface. Such mechanisms are used, in reverse, to keep diving insects and spiders alive under water, sometimes as long as an hour. But the insects carry their "bells" of oxygen-rich air under water, then breathe in O2 and expel CO2. As the O2 concentration diminishes, more diffuses into the diving bell from the water, and the CO2 from their

respiration diffuses from the diving bell into the water. The same mechanism should work for bryophytes, but this mechanism assumes that there is free gaseous CO2 in the water column, not bicarbonate or carbonate. Thus, if it works at all, it presumably works only at lower pH levels where free CO2 exists ... or perhaps at higher pH levels where microbial contributions are available on the surface of the bryophyte. Could microbial respiration at night by periphyton be contained in a diving bell, later to be exchanged for O2 in the daytime? Ecotypes I have already noted the possibility of ecotype differences. For example, Hygroamblystegium fluviatile (Figure 12) and Fontinalis antipyretica (Figure 2) had similar trophic responses to eutrophication in two calcareous lowland streams, and both reached their maximum occurrences in oligotrophic water (Vanderpoorten & Durwael 1999). On the other hand, Hygroamblystegium tenax (Figure 11), H. fluviatile, Fissidens crassipes (Figure 28), and Fontinalis antipyretica had distinctly different response curves in different hydrographic networks, suggesting the presence of physiological races or ecotypes in these species. Such differences could account for the widespread and varied habitats of some species.

Seasons and Phenology Most stream bryophytes occur as perennials and can be found during all seasons of the year (Vieira et al. 2014). They may disappear or diminish during ice breakup or heavy runoff and spates, but otherwise, they must respond to changes in their environment through changes in their physiological behavior. Vieira and coworkers proposed that since bryophytes are able to withstand natural seasonal desiccation and have perennial life-strategies permitting them to be assessed any time of year, they can be suitable tools for the characterization of reference conditions. The environment can signal that it is time to change physiological activity through a number of mechanisms. We have discussed many aspects of nutrients and their variable availability throughout the year. Temperature, light intensity, and photoperiod also offer potential signals to changes in physiological activity. Glime and coworkers (Glime 1982; Glime & Raeymaekers 1987) have measured differences in number of reproductive structures, growth rates, and rhizoid productions of Fontinalis (Figure 2, Figure 4, Figure 23) species in various seasons and modelled these changes based on light and temperature. They found that temperatures ranging from 5 to 15ºC favored branching, but that the optimum temperature differed among species. Branching is greatly reduced in pool conditions compared to that in flowing water. More rhizoids were produced at temperatures above 10ºC, coinciding with periods when water levels were lowest, permitting more opportunity for attachment without fighting heavy flow. Rhizoid production can co-occur with branch production. These life strategies will be further discussed in the next subchapter.

Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

Steinman and Boston (1993) followed the photosynthetic rates and phosphorus uptake of aquatic bryophytes in a woodland stream in Tennessee, USA, for 13 months. The most abundant bryophyte was the leafy liverwort Porella pinnata (Figure 20-Figure 21), with Brachythecium cf. campestre (Figure 78) and Amblystegium (Hygroamblystegium?; Figure 11-Figure 12) following in abundance. The bryophyte abundance peaked in late summer, but was reduced by a severe winter storm. Porella pinnata exhibited significantly greater areaspecific photosynthetic rates than did the other bryophyte species and exceeded the periphyton in P uptake. However the periphyton significantly exceeded the other autotrophs in biomass-specific photosynthesis and P uptake rates.

Figure 78. Brachythecium campestre, a common bryophyte in a woodland stream in Tennessee, USA. Photo by Jerry Jenkins, Northern Forest Atlas, with permission.

Kelly and Whitton (1987) measured shoot growth of Platyhypnidium riparioides (Figure 6) in the Northern Pennines, England. Growth occurred in every month, with the maximum in spring and minimum in winter. Autumn experienced a second, smaller peak. Everitt and Burkholder (1991) observed the seasonal dynamics of the macrophyte communities for a stream flowing over granite in North Carolina, USA. Bryophytes were not dominant, but Fontinalis sp (Figure 2, Figure 4, Figure 23) occurred. In the shaded sites, Fontinalis dominated in the warm seasons, but the red alga Lemanea australis (see Figure 79) dominated during the cool seasons.

Figure 79. Lemanea fluviatilis; L. australis dominates in winter and Fontinalis in the summer in a North Carolina, USA stream. Photo by J. C. Schou, with permission.

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Núñez-Olivera et al. (2001) questioned whether seasonal variations in nutrient contents of aquatic bryophytes were due to internal or external measures. The elements N, P, Na, and Fe showed the most frequent annual cycles. Typically, the lowest concentrations appeared in spring and the highest in autumn. These seasonal cycles depended on the interactions of both internal and environmental factors. Growth in the bryophytes [Fontinalis antipyretica (Figure 2), F. squamosa (Figure 30), Jungermannia exsertifolia subsp. cordifolia (Figure 22), and Apopellia endiviifolia (Figure 25)] caused a dilution of the element concentrations in the bryophyte tissues. Seasonal changes occurred in the environment, causing changes in the element concentrations resulting from runoff, decomposition, changing flow rates, and litter input. Unlike those of heavy metals, the concentrations of elements in the bryophytes did not correlate well with those in the stream water. Beaucourt et al. (2001) concluded that growth in Fontinalis antipyretica (Figure 2) and F. squamosa (Figure 30) was determined by both genetic and environmental factors. They found higher growth in early autumn and spring. We found similar growth patterns in Fontinalis hypnoides (Figure 80) and F. duriaei (Figure 39) (Glime & Acton 1979; Glime 1980, 1982; Fornwall & Glime 1982). Fontinalis antipyretica exhibited a higher growth rate than did F. squamosa, a factor that could contribute to some differences seen in seasonal nutrient uptake (Beaucourt et al. 2001).

Figure 80. Fontinalis hypnoides, a species with its highest growth in early autumn and spring. Photo by Jean Faubert, with permission.

Martínez-Abaigar et al. (2002a) used Fontinalis antipyretica (Figure 2) and F. squamosa (Figure 30) to track the seasonal variation in N, P, K, Ca, Mg, Fe, and Na in a mountain stream in Spain. The two species had similar elemental concentrations. Fontinalis antipyretica (Figure 2) had a higher nitrogen concentration, perhaps due to greater physiological activity related to its more rapid growth. Concentrations of K, Fe, P, and N increased in every plant segment and increased through summer and autumn, then decreased through winter and spring. The concentrations in the plants seemed to depend on the growth cycle, having only scattered correlations with water conditions.

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Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

We might expect ice to be a problem for aquatic bryophytes. Frahm (2006) observed that aquatic mosses can overwinter in ice. This does not appear to cause any physiological problems for high altitude or high latitude stream bryophytes, but the problems caused by dislodgment of the mosses have been discussed in an earlier subchapter. Kalacheva et al. (2009) assessed the seasonal changes of polyunsaturated acids (PUFA) in Fontinalis antipyretica (Figure 2) from the Yenisei River in Siberia. The relative content of acetylenic acids in fatty acids remained high throughout the year, but achieved its peak in summer. These are highly specific (unique) to the mosses and can serve as biochemical markers in trophic interactions. The relative content of PUFA from the omega3 group was greatest in spring, whereas the omega6 group varied little throughout the year. Pejin et al. (2012) examined fatty acids in the mosses Atrichum undulatum (Figure 81) and Hypnum andoi (Figure 82) in winter. They identified eight fatty acids using the chloroform/methanol extraction, one of which was arachidonic (6.21% of total methanol extractions). They considered A. undulatum to be a good winter source of linoleic acid and alpha-linolenic acid. Kajikawa et al. (2008) reported that the thallose liverwort Marchantia polymorpha (Figure 83) uses linoleic and α-linolenic acid to synthesize arachidonic and eicosapentaenoic acids, respectively.

from 6.6% in the moss Calliergon cordifolium (Figure 8) to 80.2% in the liverwort Riccia fluitans (Figure 9). It is not unusual for bryophytes to produce high amounts of very long-chain polyunsaturated fatty acids such as arachidonic acid and eicosapentaenoic acid (Lu et al. 2019). These are likewise common in marine algae, but are rare in tracheophytes. These fatty acids are typically amplified under conditions of biotic or abiotic stress.

Figure 82. Hypnum andoi, a good winter source of linoleic acid and alpha-linolenic acid. Photo by James K. Lindsey, through Creative Commons.

Figure 83. Marchantia polymorpha, a species that uses linoleic and α-linolenic acid to synthesize arachidonic and eicosapentaenoic acids, respectively. Photo by Michael Lüth, with permission. Figure 81. Atrichum undulatum, a good winter source of linoleic acid and alpha-linolenic acid. Photo by Michael Lüth, with permission.

Fatty acids seem to vary considerably among bryophytes, even when species are closely related. For example, the floating liverwort Riccia fluitans (Figure 9) exhibited a new acetylenic acid (Vierengel et al. 1987), but other tested members of the family Ricciaceae (floating liverwort Ricciocarpos – Figure 57) and other thallose liverworts outside the Ricciaceae had no detectable acetylenic fatty acids (Kohn et al. 1988). However all 12 species of the genus Riccia exhibited acetylenic fatty acids. One study has examined the fatty acid composition of a number of aquatic bryophytes (Dembitsky & Rezanka 1995). The acetylenic fatty acids in triacylglycerols ranged

Huneck et al. (1982) assessed the essential oils in the aquatic leafy liverwort Scapania undulata (Figure 7). The total essential oils ranged only from a low of 0.92 % dry weight in August to a high of 1.39 % in March when sampled from this liverwort in a small stream in a Thuringian Forest in Germany. But the relative constituents varied more widely, with longipinanol reaching its lowest of ~4% of the essential oils in May to a high of ~25% in April. It was always of the lowest concentration, whereas longiborneal was always exhibited the highest concentration except in August when the third oil, longipinene, slightly exceeded it. Ellwood et al. (2007) found a summer/autumn increase in Km and Vmax of bryophytes that corresponded with the seasonal decrease in the phosphate supply in a northern England stream. PMEase and PDEase detection indicated

Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

that this phenomenon was widespread among mosses. The influence of the epiphytes appeared to be negligible. Instead, it is seasonal responses of the enzyme activity to changes in the nutrient supplies and requirements. Given the importance of pigment concentrations in acclimating to light intensities, it is not surprising that these vary with the seasons in aquatic bryophytes (MartínezAbaigar et al. (1994). Using 13 aquatic bryophytes, Martínez-Abaigar and coworkers found chlorophyll contents ranging 2.2-9.2 mg g-1 dry weight and 97-351 mg m-2 shoot area. Phaeopigment ratios differed little with seasons or habitat. However, as noted earlier, a strong decrease occurred in chlorophyll content and chlorophyll a/b ratio in summer, apparently due to desiccation. Those bryophytes that were continuously wet had less dramatic seasonal cycles, and these correlated with changes in light conditions. For forested streams, light intensities vary widely between summer under the canopy and winter when the leaves are gone and the snow and ice are highly reflective. The aquatic leafy liverwort Jungermannia exsertifolia subsp. cordifolia (Figure 22) from a mountain stream in Spain exhibited little difference between years during the three years of study (Núñez-Olivera et al. (2009). However seasonal changes were apparent. New shoots in summer and autumn had a high Fv/Fm ratio and accumulated higher amounts of several hydroxycinnamic acid derivatives than during winter and spring. No DNA damage was evident at any time. Increase of p-coumaroylmalic acid was most responsive to increase in UV-B radiation and was an indirect indicator of ozone loss from the stratosphere. A similar study on Bryum pseudotriquetrum (Figure 84) and Fontinalis antipyretica (Figure 2) yielded similar results (Núñez-Olivera et al. 2010). Like the leafy liverwort Scapania undulata (Figure 7), neither moss species exhibited DNA damage, apparently due to an efficient DNA repair mechanism. Both species exhibited responses to UV-B by increased activity of the xanthophyll cycle and increase in bulk UV absorbance of methanolextractable UV-absorbing compounds, MEUVAC. Changes in chlorophyll fluorescence parameters were less distinctive. Bryum pseudotriquetrum exhibited both MEUVAC and kaempferol 3.7-O-diglycoside responses to radiation levels while Fontinalis antipyretica did not exhibit any correlation with any environmental variables. Furthermore, B. pseudotriquetrum exhibited 3-4X the MEUVAC concentration compared to that of F. antipyretica. Reproductive Signals Reproductive organs are difficult to observe in aquatic species and little research relates to their phenology or signals for their development. I (Glime 1984, 2014b) cultured Fontinalis dalecarlica (Figure 42) from a population at Highlands, North Carolina, USA for 16 weeks to determine phenological signals. Using 4 photoperiods at 8ºC and 1560 lux in artificial streams, I determined that this species behaves as a quantitative shortday (long night) plant. Archegonia were first produced in the regime of 6 hours of light, 18 hours of darkness, but in the longer photoperiods (shorter dark periods), an equal

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number of archegonia were present at the end of the 16 weeks. Longer photoperiods favored growth, branching, and rhizoid production. But at the longest photoperiod (18 hours light, 6 hours dark), both growth and branching were reduced.

Figure 84. Bryum pseudotriquetrum, a species that exhibited both MEUVAC and kaempferol 3.7-O-diglycoside responses to radiation levels. Photo by Michael Lüth, with permission.

One surprise I found was that aerated mosses were able to produce more archegonia than did the submersed mosses (Glime 1984, 2014b). But this in fact could be adaptive for stream mosses. In this stream, male populations usually occupied different rocks from the females. Swimming from one rock to another would seem to be an improbable occurrence for the tiny male sperm in flowing water. Furthermore, could they really put on the brakes and stop at an appropriate female colony? By living above the water, sperm could be splashed by the turbulent water of the riffles and land on a clump of female mosses above the moving water, thus permitting the sperm to swim to the nearest female. Thus, having aerial archegonia seems to be adaptive for fertilization success. See Chapter 2-5 of this volume for a discussion of life strategies in stream bryophytes.

Periphyton Fisher and Likens (1972) noted that the measurement of photosynthesis of the moss component in Bear Brook, New Hampshire, USA, included the productivity of the attached periphyton. This is a problem in measuring productivity of aquatic mosses anywhere. My personal experience indicates that the bryophytes are typically covered with periphyton (Glime & Acton 1979), and attempts to remove them often damage the bryophytes or are ineffective. Furthermore, even if the periphyton are removed, we have modified the system. CO2 from respiring bacteria could compensate for CO2 limitations in the water. Competition for light and nutrients could reduce productivity, as well as competition for CO2. We have already noted that epiphytic algae tend to increase on bryophytes at warmer temperatures. These likewise can block light and compete for CO2, thus reducing the bryophyte productivity. Among these we

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Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

typically find members of the blue-green bacteria (Cyanobacteria). Some of the macrophytes have a high uptake of the toxins from the Cyanobacterium Microcystis (Figure 85) (Pflugmacher 1653). In a study of four macrophytes, the grass Phragmites communis (Figure 86) had the greatest uptake. The moss Vesicularia dubyana (Figure 87) had a much lower uptake. Furthermore, when this species was followed in the succeeding hours, it initially experienced an oxygen decrease, thus a productivity loss. However, after half a day it had recovered and after nine days the oxygen production and consumption had returned to normal levels.

Figure 87. Vesicularia dubyana, a moss with a low uptake of Microcystis toxins. Photo by Tan Sze Wei, AquamossNet.

Figure 85. Microcystis, a blue-green bacterium that produces toxins that can affect aquatic plants. Photo by Yuuki Tsukii, with permission.

Some researchers have assumed that bryophytes were not eaten because of low nutritional quality. However, this is not necessarily true (Liao & Glime 1996). Fontinalis antipyretica (Figure 2) produces the most total phenolics in the summer in the Keweenaw Peninsula of Michigan, USA, when herbivores are the most abundant. The phenolics are the lowest in spring when the growth of the moss is most rapid. Consumption rate on this species was lowest when the phenolic content was at its highest levels. The phenolic contents were also higher in sunny and intermediate habitats than in shady ones. This may be a defensive (stress) response in the higher light intensity where there is more UV radiation and potentially higher temperatures. Acetylenic acids, noted above, are known for their antifungal properties against human pathogens (Xu et al. 2012), so it is likely that they are also effective against potential bryophyte pathogens. Some mosses seem to be able to protect other mosses from herbivory. Fissidens fontanus (Figure 88) in northern Europe seems to be able to survive only when it is mixed with Fontinalis (Figure 2, Figure 4, Figure 23) (Lohammar 1954). Snails are common in the environment, but snails seem to avoid Fontinalis, as demonstrated in aquaria, thus protecting the more edible Fissidens fontanus.

Figure 86. Phragmites communis, a species with high uptake of CO2, especially compared with the aquatic moss Vesicularia dubyana. Photo by Lazaregagnidze, through Creative Commons.

Herbivory and Pathogens Lodge (1991) noted that researchers had put forward the hypothesis that macrophytes offer poor food quality due to low protein content. Nevertheless, macrophytes, including the aquatic bryophytes, are grazed. Lodge points out that often the grazers destroy more tissues than they eat. In any case, bryophytes are often the victims of consumption.

Figure 88. Fissidens fontanus, a species that benefits from growing with Fontinalis as an antiherbivore agent. Photo by Walter Lampa, through Creative Commons.

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In the early stages of biochemical research, Marsili and Morelli (1968) noted the presence of triterpenes in the moss Thamnobryum alopecurum (Figure 89), a streambank moss. Such compounds are typically used as chemical defenses. For example, Toyota et al. (1999) isolated an eudesmane-type sesquiterpenoid from the aquatic leafy liverwort Chiloscyphus polyanthos (Figure 90).

Figure 91. Branta canadensis, a large consumer that avoids Fontinalis, thus protecting the invertebrates living there. Photo by Lystopad, through Creative Commons.

Figure 89. Thamnobryum alopecurum, a streambank moss with triterpenes. Photo by Hermann Schachner, through Creative Commons.

Figure 92. Procambarus spiculifer, a species that avoids eating Fontinalis. Photo by Supertiger, through Creative Commons. Figure 90. Chiloscyphus polyanthos, a leafy liverwort with a eudesmane-type sesquiterpenoid. Photo by Hermann Schachner, through Creative Commons.

Parker et al. (2007) noted that stream mosses could provide refuges for stream macroinvertebrates. In their study, the large consumers Branta canadensis (Canada geese; Figure 91) and Procambarus spiculifer (crayfish; Figure 92) selectively consumed Podostemum ceratophyllum (riverweed; Figure 93) while ignoring the accompanying Fontinalis novae-angliae (Figure 93), despite the greater abundance (89% of biomass) of the moss. On the other hand, the number of macroinvertebrates on the mosses was twice that of the riverweed. In experiments, the researchers found that C18 acetylenic acid, octadeca-9,12-dien-6-ynoic acid, from the moss deterred the feeding by the crayfish. On the other hand, in lab feeding assays the amphipod Crangonyx gracilis (Figure 94) and isopod Asellus aqus (Figure 95) consumed significant amounts of the moss while rejecting the riverweed. These invertebrates were likewise not deterred by the extracted C18 acetylenic acid.

Figure 93. Podostemum ceratophyllum (left) and Fontinalis novae-angliae (right), the latter protecting invertebrates from grazing by geese. Photo by John Parker, with permission.

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Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

Figure 96. Physcomitrella patens with springtails; P. patens has chemical defenses against microbes. Photo by Bob Klips, with permission. Figure 94. Crangonyx sp.. an amphipod that feeds on Fontinalis. Photo from CBG Photography Group, Centre for Biodiversity, through Creative Commons.

There is a much greater discussion of various interactions of stream bryophytes and invertebrates, including insects, in Volume 2, Bryological Interaction.

Summary

Figure 95. Asellus aquaticus, isopods that feed on Fontinalis. Photo by M. J., through Creative Commons.

Living in water makes the bryophytes an excellent habitat for many microbes. By trapping sediments and providing substrate for periphyton, they become an outstanding dinner table for these microbes. But plants can be subject to attack from microbes, so it is predictable that a well-adapted plant in this environment will have mechanisms to prevent it from being attacked by them. Little has been done, beyond the antibacterial activity of Sphagnum (Figure 54), to determine this capability in aquatic bryophytes. However, research on the terrestrial Physcomitrella patens (Figure 96) has revealed several such defense mechanisms (Ponce de León & Montesano 2017). In fact, evidence indicates that these same mechanisms are conserved in flowering plants. These researchers found cell wall defenses that become activated through a MAP kinase cascade. Once pathogens begin their attack, the moss activates production of ROX and induces an HR-like reaction while increasing the levels of some hormones. It is likely that aquatic bryophytes have similar, but probably partially unique, mechanisms.

Although bryophytes require lower nutrient levels than do most tracheophytes, they can still experience limiting conditions. Their ability to accumulate ions makes them suitable bioindicators. Nutrient levels tend to be lowest in spring and highest in autumn. Nitrogen and phosphorus impose the most likely limitations and are typically low in stream habitats. At least some species can use ammonium as an N source, especially at higher pH levels. This seems to be influenced not only by the environment, but also by genetic variation within the species. And even within an individual, the ability to use nitrate vs ammonium can switch dependent on availability. Mosses exhibit little amplification of stored nitrate relative to the water compared to that of some tracheophytes. Evidence suggests that the P:N ratio might increase with P enrichment. Tissue concentration of P increases with time in enriched water, but K seems to be subject to leakage and its levels fluctuate in the tissues. Potassium occurs dissolved in the cells. Calcium is bound to exchange sites in the cell wall. Magnesium is present in both locations. Thus potassium and magnesium are lost when the cells become desiccated and the membranes damaged. The soluble elements N, P, and K occur in the highest concentrations and are most mobile, having their highest concentrations in the apical portions. The least mobile elements (Ca, Mg, Fe) are highest in the basal portions. Species might be able to acclimate to changing water chemistry conditions by altering the uptake efficiency. Heavy metals can cause damage to chlorophyll, loss of cellular organization, disruption of the nucleus, and plasmolysis. At even higher concentrations, deplasmolysis can occur. Locations of cytoplasmic vs cell wall can differ by species of bryophyte. Heavy metals can cause membrane damage and loss of K. Competition by H+ on external exchange sites seems to be responsible for lower metal uptake in acidic water.

Chapter 2-7: Streams: Physiological Adaptations – Nutrients, Photosynthesis, and Others

Many early photosynthetic studies were done on aquatic bryophytes, especially Fontinalis. These included temperature effects on both assimilation and respiration, limiting factors in carbonic acid assimilation, influence of pH, effects of various wavelengths on photosynthesis, discovery of photorespiration, and use of IRGA to measure CO2 metabolism. Bryophytes are typically shade plants, having low chlorophyll a/b ratios. In the water they are usually limited by light, carbon, and nutrients. But their photosynthesis and growth are also affected by pH, boundary layer resistance, loss of red light in deeper water, sedimentation, periphyton, detritus, hydration state, water level fluctuations that cause desiccation, and temperature. Their growth temperature optima are generally 10-20ºC. Although aquatic bryophytes are able to live in alkaline waters where free CO2 concentrations are very low, and they seem to have alternative CO2 pathways, we still don't understand how these work. Lack of internal air spaces prevents the re-use of respired CO2. Aquatic species are often characterized by low apparent quantum yields, low compensation points, and low saturation points. They can suffer from photoinhibition at relatively low light levels. The slope of photosynthesis vs CO2 concentration increases linearly with temperature and may account for photoinhibition at low light levels. For forest species, light levels before freeze-over are higher in winter. In the cold of winter, aquatic bryophyte photosynthesis seems to be unaffected by internal concentration of nutrients or pigment concentration. On the other hand, winter seems to be the period of greatest vitality for those in the water. Photosynthetic plasticity permits the bryophytes to photosynthesize and grow at these low temperatures. CO2 has a low diffusion rate in water, favoring low light requirements and variable CO2 compensation points. At high pH levels, free CO2 quickly converts to other carbon-containing compounds, severely limiting bryophyte photosynthesis. A number of aquatic tracheophytes are able to use bicarbonates in these conditions, but any direct evidence for this pathway in bryophytes has been elusive. One possibility is grabbing CO2 emitted from sediments or bacterial respiration before it gets converted. CO2 from such sources remains longer in cold water. Some periphyton can provide CO2, but they also block light. Typically, boundary layer resistance limits photosynthesis at stream velocities below about 0.01 m s−l in Fontinalis (streamers) and below about 0.1 m s−1 in the mat‐forming species. CO2 could be held in a diving bell, exchanged for photosynthetic O2, but the CO2 must come from somewhere, possibly microbial respiration. Aquatic bryophytes can be active year-round, making them superior organisms for biomonitoring compared to most aquatic tracheophytes. Nevertheless, rhizoid production, branch growth, and biomass gain can occur under different conditions. Higher growth in

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spring seems to benefit from greater nutrient levels, more light, plenty of water, and cool temperatures. On the other hand, nutrient concentrations in the plants seem to correlate with the growth cycle, not the water conditions. Fatty acid types and concentrations vary with season, as do pigment concentrations. Day length can signal the onset of sexual organ development.

Acknowledgments

Many Bryonetters have contributed to these aquatic chapters, permitting me to expand my world view of the taxa.

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Tessler, M., Truhn, K. M., Bliss-Moreau, M., and Wehr, J. D. 2014. Diversity and distribution of stream bryophytes: Does pH matter? Freshwat. Sci. 33: 778-787. Toyota, M., Saito, T., and Asakawa, Y. 1999. The absolute configuration of eudesmane-type sesquiterpenoids found in the Japanese liverwort Chiloscyphus polyanthos. Phytochemistry 51: 913-920. Tremp, H. and Kohler, A. 1993. Wassermoose als Versauerungsindikatoren. Praxiesoriente Bioindikationsvervahren mit Wassermoosen zur Überwachung des Säurezustandes von Pufferswachen Fliessgewässern. [Water mosses as acidification indicators. Practice-oriented bioindication method with water mosses for monitoring the acidity of buffer waters in rivers.]. Landesanstalt für Umweltschutz Baden-Württemberg. Tremp, H., Kampmann, D., and Schulz, R. 2012. Factors shaping submerged bryophyte communities: A conceptual model for small mountain streams in Germany. Limnologica 42: 242-250. Turner, B. L., Baxter, R., Ellwood, N. T. W., and Whitton, B. A. 2001. Characterization of the phosphatase activities of mosses in relation to their environment. Plant Cell Environ. 24: 1165-1176. Ueno, T. and Kanda, H. 2006. Photosynthetic response of the Arctic semi-aquatic moss Calliergon giganteum to water content. Aquat. Bot. 85: 241-243. Vanderpoorten, A. 2000. Hydrochemical determinism and molecular systematics in the genus Amblystegium (Musci). Application to the biomonitoring of surface waters. Bibliothèque des Sciences agronomiques. Vanderpoorten, A. and Durwael, L. 1999. Trophic response curves of aquatic bryophytes in lowland calcareous streams. Bryologist 102: 720-728. Vanderpoorten, A. and Palm, R. 1998. Canonical variables of aquatic bryophyte combinations for predicting water trophic level. Hydrobiologia 386: 85-93. Vanderpoorten, A., Klein, J.-P., Stieperaere, H., and Trémolières, M. 1999. Variations of aquatic bryophyte assemblages in the Rhine Rift related to water quality. 1. The Alsatian Rhine floodplain. J. Bryol. 21: 17-23.

Vázquez, M. D., López, J., and Carballeira, A. 1999. Uptake of heavy metals to the extracellular and intracellular compartments in three species of aquatic bryophyte. Ecotoxicol. Environ. Safety 44: 12-24. Vázquez, M. D., Fernández, J. A., López, J., and Carballeira, A. 2000. Effects of water acidity and metal concentration on accumulation and within-plant distribution of metals in the aquatic bryophyte Fontinalis antipyretica. Water Air Soil Pollut. 120: 1-20. Vieira, C., Aguiar, F. C., and Ferreira, M. T. 2014. The relevance of bryophytes in the macrophyte-based reference conditions in Portuguese rivers. Hydrobiologia 737: 245264. Vieira, C., Aguiar, F. C., Portela, A. P., Monteiro, J., Raven, P. J., Holmes, N. T. H., Cambra, J., Flor-Arnau, N., Chauvin, C., Loriot, S., Dörflinger, G., Germ, M., Kuhar, U., Papastergiadou, E., Manolaki, P., Miniciardi, M. R., Munné, A., Urbanič, G., and Feret, T. 2018. Bryophyte communities of Mediterranean Europe: A first approach to model their potential distribution in highly seasonal rivers. Hydrobiologia 812: 27-43. Vierengel, A., Kohn, G., Vandekerkhove, O., and Hartmann, E. 1987. 9-octadecen-6-ynoic acid from Riccia fluitans. Phytochemistry 26: 2101-2102. Wehner, O. 1928. Untersuchungen über die chemische Beeinflussbarkeit des Assimilationsapparates. [Investigations on the chemical influence of the assimilation apparatus.]. Planta 6: 543-590. Westlake, D. F. 1978. Rapid exchange of oxygen between plant and water. Verh. Internat. Verein. Limnol. 20: 2363-2367. Westlake, D. F. 1981. Temporal changes in aquatic macrophytes and their environment. In: Hoestlandt, H. (ed.). Dynamique de Populations et Qualite de l'Eau. Actes du Symp. de l'Institute d'Ecologie du Bassin de la Somme, Chantilly, 1979. Gauthier-Villars, Paris, pp. 110-138. Xu, T., Tripathi, S. K., Feng, Q., Lorenz, M. C., Wright, M. A., Jacob, M. R., Mask, M. M., Baerson, S. R., Li, X.-C., Clark, A. M., and Agarwal, A. K. 2012. A potent plant-derived antifungal acetylenic acid mediates its activity by interfering with fatty acid homeostasis. Antimicro. Agents Chemother. 56: 2894-2907.

Glime, J. M. and Gradstein, S. R. 2018. Tropics: General Ecology. Chapt. 8-1. In: Glime, J. M. Bryophyte Ecology. Volume 4. Habitat and Role. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Last updated 22 July 2020 and available at .

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CHAPTER 8-1 TROPICS: GENERAL ECOLOGY JANICE M. GLIME AND S. ROBBERT GRADSTEIN

TABLE OF CONTENTS General Ecology ................................................................................................................................................. 8-1-2 Water Relations ........................................................................................................................................... 8-1-5 Light ............................................................................................................................................................ 8-1-8 Life and Growth Forms ............................................................................................................................... 8-1-9 Nutrient Relations ..................................................................................................................................... 8-1-12 Productivity ............................................................................................................................................... 8-1-13 Climate Effects ................................................................................................................................................. 8-1-16 Reproductive Biology and Phenology .............................................................................................................. 8-1-16 Life Cycle Strategies ................................................................................................................................. 8-1-17 Mosses ...................................................................................................................................................... 8-1-18 Antheridia and Archegonia ................................................................................................................ 8-1-20 Monoicous vs Dioicous...................................................................................................................... 8-1-20 Propagules and Regrowth .................................................................................................................. 8-1-21 Propagule Forms ................................................................................................................................ 8-1-22 Fragments .......................................................................................................................................... 8-1-25 Spore Size .......................................................................................................................................... 8-1-26 Diaspore Banks .................................................................................................................................. 8-1-26 Prolonged Protonemal Stage .............................................................................................................. 8-1-28 Liverworts ................................................................................................................................................. 8-1-28 Monoicous vs Dioicous...................................................................................................................... 8-1-28 Neoteny .............................................................................................................................................. 8-1-29 Reduced Numbers of Antheridia and Archegonia ............................................................................. 8-1-30 Short Life Cycles ............................................................................................................................... 8-1-30 Short Spore Longevity ....................................................................................................................... 8-1-31 Prolonged Protonemal Stage .............................................................................................................. 8-1-31 Types of Gemmae .............................................................................................................................. 8-1-32 Diaspore Banks .................................................................................................................................. 8-1-36 Rheophilic Adaptations...................................................................................................................... 8-1-36 Dispersal........................................................................................................................................................... 8-1-37 Sampling .......................................................................................................................................................... 8-1-41 Braun-Blanquet Sampling Method ........................................................................................................... 8-1-42 Drying Specimens ..................................................................................................................................... 8-1-42 Summary .......................................................................................................................................................... 8-1-43 Acknowledgments ............................................................................................................................................ 8-1-43 Literature Cited ................................................................................................................................................ 8-1-43

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CHAPTER 8-1 TROPICS: GENERAL ECOLOGY

Figure 1. World map indicating tropics in pink band, subtropics in orange dotted line. Photo from KVDP, through Creative Commons.

General Ecology Occupying the area between the Tropic of Cancer and the Tropic of Capricorn, the tropics comprise the most complex ecosystems of the world (Figure 1), extending 23º27' north and south of the Equator. The tropical land mass is nearly one-third of the land on the planet (Schuster 1988). Complex ecosystems provide multiple niches (Figure 2), and the tropics undoubtedly provide the highest number of niches anywhere with their multi-storied forests (Figure 3).

Figure 2. Tropical forest and waterfalls at Quebrada Cataguana, Honduras. Photo by Josiah Townsend, with permission.

Bryophytes in the tropics were largely ignored in early botanical studies. Resident botanists, lacking training by bryologists and preceding the development of taxonomic aids, largely ignored the bryophytes (Moreno 1992). Although bryophytes have been recorded from the tropics since the 18th century, tropical bryophyte ecology started to emerge only rather recently because keys to identify tropical bryophytes were long lacking. Early fieldwork in the tropics was done by foreign bryologists, e.g. Goebel (1888), Schiffner (1900), Fleischer (1904-1923) and Giesenhagen (1910) in Asia, and by Spruce (1884-1885) and Spruce and Wallace (1908) in tropical America. Spruce collected extensively in the Amazon regions and the Andes of Ecuador and Peru, and identified the liverworts himself, but gave his moss collections to William Mitten, who subsequently published them in Musci AustroAmericani (Mitten 1869). Early studies on the ecology of tropical bryophytes has been summarized by Pócs (1982) and Richards (1984a). Some of the earliest studies were on epiphyllous (growing on leaves of other plants) bryophytes and will be discussed in the subchapter on epiphylls. In Puerto Rico, Fulford et al. (1970, 1971) described liverwort communities in the elfin (cloud) forest (Figure 4). Griffin et al. (1974; Griffin 1979) reported on altimontane (Figure 5) bryophytes. Steere (1970) took advantage of the haploid condition of bryophytes to report on the effects of ionizing cesium radiation in Puerto Rico.

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Figure 5. Drakensberg, South Africa, altimontane region. Photo by Diriye Amey, through Creative Commons.

Figure 3. Microhabitats in tropical forests. 1: Bases of large trees; 2: upper parts of trunks; 3: macro-epiphyte nests; 4: bark of main branches; 5a: terminal twigs and leaves; 5b: bark of lianas, shrub branches, and thin trunks; 6: Pandanus stems; 7: tree fern stems; 8: palm trunks and basal prop roots; 9: rotting logs and decaying wood; 10: soil surface and termite mounds; 11: roadside banks and cuttings; 12a: rocks and stones; 12b: submerged or emergent rocks in streams. Image modified from Pócs 1982.

Figure 6. Lowland rainforest tree in Colombian Amazon. Photo by Laura Campos, courtesy of Robbert Gradstein.

Figure 4. Elfin cloud forest fog, Luquillo Mountain, Puerto Rico, USA. Photo by Janice Glime.

Once the bryophytes were better known, bryologists began asking ecological questions (e.g. Frahm & Gradstein 1990). Based on the results of elevational transect analyses throughout the tropics, Frahm & Gradstein (1991) recognized five tropical rainforest belts using bryophytes as indicators: lowland rainforests (Figure 6-Figure 7), submontane rainforests (=premontane rainforest; Figure 8), lower montane rainforests (Figure 9), upper montane rainforests (Figure 10), subalpine rainforests (Figure 11).

Figure 7. Canopy in lowland rainforest in Colombian Amazon. Photo by Laura Campos, courtesy of Robbert Gradstein.

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Figure 10. Upper montane forest, Pui-Pui Protection Forest, Peru. Photo by E. Lehr and R. von May, through Creative Commons.

Figure 8. Submontane rainforest, Peruvian Andes. Photo by Robbert Gradstein, with permission.

Figure 11. Subalpine dwarf mossy Polylepis forest in Ecuador. Photo by K. Romoleroux, courtesy of Robbert Gradstein.

Figure 9. Lower montane forest in Colombia, rich in lignified vascular epiphytes. Photo by A. M. Cleef, courtesy of Robbert Gradstein.

To further complicate our ecological understanding, early differences in methodology made ecological comparisons nearly impossible, while poor understanding of the taxonomy gave that area of study priority and limited the kinds of ecological studies that were feasible. The earliest limited ecological studies have included the relationships among climate, mountain topography, vegetation zones (Pócs 1976), ecology, reproductive biology, and dispersal trends (Schuster 1988), biomass (Frahm 1990b), water relations, and CO2 exchange (Zotz et al. 1997).

Richards (1984a) provided a very useful overview of the ecology of tropical forest bryophytes, making it clear that studies at that time were limited and his coverage was superficial. One of the things that quickly becomes obvious is that most of the known ecological information relates to epiphytes (growing on other plants). This is because most of the tropical bryophytes are epiphytes, limited by low light levels and leaf burial on the forest floor. In the Luquillo Mountains of Puerto Rico (Figure 12), three environmental factors cause contrasting communities of leafy liverworts (Bryant et al. 1973). Using area x area (Q-mode) analysis, they demonstrated that high-altitude liverwort communities contrast with those of low altitudes, shaded, moist habitats contrast with open, exposed habitats of all elevations, and disturbed low-elevation habitats contrast with less disturbed habitats of all elevations. Rmode analysis (species x species) produced nearly identical results to those of Q-mode.

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wefts (loosely interwoven, often ascending growth form). Thiers (1988) reported the leafy liverworts Radula (Figure 111), Frullania (Figure 14), and various Lejeuneaceae (Figure 130-Figure 131) to exhibit the mat growth form on their bark substrate; these taxa tend to lack dominance in the main axis. Where they form extensive mats on tree boles, they are able to trap water as it runs down the tree.

Figure 12. Luquillo Mountains, Puerto Rico. Photo by Stan Shebs, through Creative Commons.

For recent species lists of tropical studies, see Gradstein et al. (2001) for tropical America, Churchill et al. (2010) on Bolivia, and many others. For additional older studies and reviews of tropical bryophyte species lists and ecology, see Delgadillo (1976) on Mexico; Lisboa (1976) on the Amazon; Egunyomi (1978) on distribution of pantropical Octoblepharum albidum (Figure 13) in Africa; Pócs (1982) on tropical forests; Gradstein et al. (1983) on Neotropical-African liverwort disjunction; Richards (1984a, b, 1988) on tropical forest ecology; Linares (1986) on the high Andes; Gradstein & Pócs (1989) on tropical rainforest bryophytes; Frahm & Gradstein (1990, 1991) on bryophytes as indicators of tropical rainforests; Frahm & Kürschner (1992) on tropical rainforests in general; Frangi & Lugo (1992) on biomass and nutrients in a Puerto Rico floodplain; Delgadillo (1993) on Neotropical-African disjunction; Miehe & Miehe (1994) on ecology in East Africa; Lösch et al. (1999) on Central African photosynthesis; Merwin & Nadkarni (2002) on tropical ecology, and others.

Figure 13. Octoblepharum albidum, a species that produces most of its juvenile, immature, and mature gametangia during the rainy season in tropical Brazil. Photo by Niels Klazenga, with permission.

Water Relations In general, tropical adaptations reflect moisture conditions, with light and other factors being secondary (Frahm 1990a). Hence, we find that lowland forests are dominated by mats, and montane and cloud forests by

Figure 14. Frullania sp. from the Neotropics, demonstrating mat growth habit. Photo by Michael Lüth, with permission.

Studies on water relations seem to have been more common than other areas of tropical bryophyte ecology. Pócs (1980) studied the water interception and retention by bryophytic cover (biomass) in different types of tropical forest, forming the basis for all other studies on the subject. He found a positive correlation between the amount of "surplus" rainfall (rainfall above 100 mm/month) and the epiphytic biomass in rainforest climates. Rainfall and epiphytes will be discussed in Chapter 8-3 of this volume. When working on disturbance, Norris (1990) suggested four aspects of water relations that required consideration: hydration/dehydration frequency; hydration duration; dehydration duration; degree of water loss. We have since learned that rate of dehydration is important (Greenwood & Stark 2014). As Norris (1990) further surmised, these are all biomass-dependent functions, wherein large colonies typically maintain hydration longer than smaller colonies. Lateral branching of the colony allows lateral movement of capillary water. This spread of the water extends to clones that are in contact with each other. On the other hand, when tufts and cushions are separated, they contribute little to lateral spread of the water over the substrate. Johnson and Kokila (1970) experimented with ten species of tropical mosses to determine their resistance to desiccation. These were exposed to relative humidities ranging 10-76% for four hours. After a recovery period of 24 hours, the researchers found the mosses could be divided into high and low resistance groups. Those species in the high resistance group occur in tropical forests with low humidity. Pócs (1980) found a positive correlation between the amount of "surplus" rainfall (rainfall above 100 mm/month) and the epiphytic bryophyte biomass in rainforest climates. As demonstrated by Larson (1981) mosses with a large surface area to weight ratio are able to absorb water very rapidly.

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Thompson et al. (1994) calculated the bryophyte cover on a single tree of Sloanea woollsii (Figure 15-Figure 16) in a notophyll forest of southeast Queensland, Australia (subtropical), to be 66 sq m. Water collected by the bryophytes in a single rainfall event exceeded that of the maximum daily transpirational loss from the host tree. Hence, bryophytes can contribute significantly to the relative humidity of the forest through evaporation. This is also a typical role in the tropics.

Figure 15. Sloanea woollsii, a species known for a large cover of bryophytes. Photo by Peter Woodard, through public domain.

Figure 16. Sloanea woollsii forest, where many bryophytes grow. Photo by Pete the Poet, through Creative Commons.

Frey et al. (1990) recognized three principles of water conduction and storage by plants. In the wet season, it is necessary to drain off surplus water. In the dry season, storage and use of condensation of water vapor are important. Above 1700 m, structures that encourage condensation from water vapor aid in water capture. They felt that leaves with grooves could permit support as well as a means of draining off excess water, an adaptation that seems to reach its maximum in the cloud forest and subalpine zone. In the lowland forest, water sacs, mats, and smooth bark combine to preserve water during short dry periods. Karger et al. (2012) considered air humidity to be one of the most difficult and time-consuming climatic measurements to obtain. Thus, they tested the use of bryophyte cover as a proxy, a suggestion proposed by van Reenen and Gradstein (1983), van Reenen (1987), and Frahm and Gradstein (1991). Using 26 study sites in tropical forests, these researchers considered the possibility of using bryophyte cover as a surrogate for relative humidity as a climatic measurement. They found only a weak correlation between bryophyte cover and relative humidity across all the sites. However, when the highland (1,800-3,500 m asl) data were separated from that of the lowland (10 m above the ground (Cornelissen & Gradstein 1990).

In the Liquidambar forest (Figure 121) of Mexico, 194 species of mosses were known in 1979 (Delgadillo 1979). Of these, 70% are strictly American. This flora exhibits both a wide altitudinal and latitudinal range in Mexico and represents both tropical and temperate species.

Figure 122. Quercus (oak) tropical montane forest. Photo by Cody Hinchliff, through Creative Commons.

Figure 121. Liquidambar forest canopy, through Creative Commons.

Herrera-Paniagua et al. (2008) reported 212 moss species for the Mexican state of Querétaro. As indicated by endemism, this state has three distinct regions: the conifercloud-temperate forests in the northeast (Sierra Madre Oriental), the more xeric parts in the center and southeast (Mexican Plateau and ecotone areas of the Transmexican Volcanic Belt), and the almost temperate areas in the south (Transmexican Volcanic Belt). The Sierra Madre Oriental province has the highest species richness. The Trans-Mexican Volcanic Belt spans CentralSouthern Mexico from the Pacific Ocean to the Gulf of Mexico between 18°30'N and 21°30'N. Villaseñor et al.

Acebey et al. (2003) found similar high numbers of species in Bolivia (Figure 123). In a submontane rainforest there, they found 80 species on just six trees, 48 liverwort and 32 moss species. But they are quick to point out that finding nearly all the species in the forest requires only a small sample size. They estimate that these six trees had floras that represented 95% of the total bryophyte flora of the forest. Churchill et al. (2010) published a catalog of the bryophytes of Bolivia with discussions of diversity, distribution, and ecology. In Cuba (Figure 124), an island in the Greater Antilles, 383 taxa were reported, mainly from mountain areas (Motito et al. 1992). However, more recent studies seem to be lacking, preventing an evaluation of Cuban species compared to those of other localities.

Chapter 8-2: Tropics: Geographic Diversity Differences

Figure 123. Santa Cruz, Bolivia. Photo by Vincent Raalvia, through Creative Commons.

Figure 124. Montane moist forest on the slopes of Pico Turquino, Santiago de Cuba, Cuba. Photo by Male Gringo, through Creative Commons.

The tropical Andes (Figure 125) has by far the highest bryophyte diversity in the tropical Americas. For a general review on liverwort diversity in the Andes see Gradstein (1995b). Gradstein et al. (1977) compared oil body structures and examined the ecological distributions of selected species of the leafy liverworts in the Andes of Colombia. Churchill and co-workers listed 2,058 moss species names but suggested the actual number was probably closer to 1,500-1,700 because of likely synonyms (Churchill et al. 1995b). The extraordinary biological richness of the Andean region is due to the great climatic and elevational variation of the area as well as historical factors. The authors concluded that an "increase in species diversity from the poles to the equator does not apply to mosses" (Churchill et al. 1995b). The latitudinal gradient has recently been studied by Shaw et al. (2005) for mosses and by Wang et al. (2016) for liverworts. These papers indicate that moss diversity is highest in the Southern Hemisphere and lowest in the Northern Hemisphere, with the tropics having an intermediate level. Liverwort diversity, in contrast, is highest in the tropics.

Figure 125. Andes, Ausangate hillside, Peru. Marturius, through Creative Commons.

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Photo by

In the El Sira Communal Reserve of the Peruvian Andes, Graham et al. (2016) found 171 liverwort species, representing 51 genera and 18 families. This flora flourishes in the high humidity, with sometimes more than 7500 mm in a year. Climate, soils, and microhabitat delineated diverse distributional patterns along the 2000-m elevational range. An example of the high diversity is the San Francisco Biological Reserve in the Andes of southern Ecuador (Figure 126) (Gradstein et al. 2007). The reserve ranges from 1,800 to 3,100 m asl and consists of about 1,000 ha of pristine montane forest and páramo. Almost 570 species of bryophytes (357 liverworts, 206 mosses, 3 hornworts), including more than half the total number of liverwort species known from Ecuador, have been recorded from the reserve and the number is still rising (Schäfer-Verwimp et al. 2013; Gradstein & Benitez 2017). One reason for the high number of species recorded is probably the large number of bryologists who conducted fieldwork in the reserve and studied the collections. As Churchill et al. (2009) remarked: "One could readily predict similar diversity numbers throughout the montane forest of the tropical Andes employing such expertise. This study provides a basis for comparing other localities of similar vegetation and elevational range."

Figure 126. Reserva Biológica San Francisco, southern Ecuador. Photo courtesy of Robbert Gradstein.

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In contrast, lowland habitats are usually less rich in bryophytes and do not provide for the same diversity seen by the rest of the flora and fauna (Churchill et al. 2009). While the number of niches in the multi-layered rainforest is relatively high, much of the tropical lowland is inhospitable to bryophytes, being too dry, too hot, or too dark. Whereas Churchill (1991) suggested that there is no strong latitudinal gradient of species richness from the temperate zone to the tropics, Hallingbäck (1992) further asserted that the temperate regions have a much higher diversity of mosses than is known in the tropics. But "known" may be the operative word. On the one hand, many species have been described as different species multiple times; Ireland (1992) reduced the number of Latin American species of Isopterygium (Figure 127) from 92 to 8, Edwards (1980) accepted only 6 of the 93 species of Calymperes (Figure 128) from West Africa, and Bischler (1984) only 9 of 69 previously described New World Marchantia (Figure 3) species. Many taxa have been viewed as different simply because they were from a new place (O'Shea 2002). On the other hand, we are just beginning to explore the bryophytes high in the canopy through the use of a number of somewhat recent techniques (McClure 1966; Grison 1978; Perry 1978; Whitacre 1981; Parker et al. 1992; Gradstein 1996; Zotz & Vollrath 2003). Cornelissen and Gradstein (1990) report that about 50% of the lowland rainforest bryophyte species of Guyana occur in the crowns and upper bole, typically missed by early bryological studies. Bryologists are beginning to find that the canopy of these primary forests may support many more species than the more-readily studied understory (Cornelissen & ter Steege 1989; Wolf 1993a, b). Bryophytes in the tropics find their dominance in different places from those in the temperate forests.

Figure 128. Calymperes sp. (Calymperaceae), one of the families that dominate in tropical Guyana. Photo by Niels Klazenga, with permission.

In the lowland rainforests of Mabura Hill, Guyana (Figure 129), South America, Cornelissen and Gradstein (1990) found 134 bryophyte species. The dominant bryophyte family is the leafy liverwort family Lejeuneaceae (Figure 6, Figure 15-Figure 16), comprising about 30% of the cryptogamic flora (including bryophytes and lichens). As seems to be typical, the canopy accounted for 50% of the species. The humid mixed forest on loamy soil sports the richest liverwort flora.

Figure 129. Rainforest in Guyana. Photo through Creative Commons.

Figure 127. Isopterygium tenerum; the genus Isopterygium has had many of the same species named by different names in the tropics, creating many synonyms. Photo by John Bradford, with permission.

In Guyana (Figure 129), Calymperaceae (Figure 128), Hookeriaceae (Figure 182), Hypnaceae (Figure 130), Orthotrichaceae (Figure 99), and Sematophyllaceae (Figure 131) dominate the mosses. Lepidoziaceae (Figure 12), Plagiochilaceae (Figure 11), and Frullaniaceae (Figure 2, Figure 7-Figure 8), in addition to the species-rich Lejeuneaceae (Figure 6, Figure 15-Figure 16), are the predominant liverworts (Gradstein 1992). As will be discussed in another subchapter of this chapter, epiphylls (those algae, plants, and fungi living on leaves of other

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plants) are common in the lowland and lower montane rainforests.

Figure 130. Mittenothamnium reptans, in the family Hypnaceae, one of the dominant families from Guyana. Photo by Michael Lüth, with permission.

Montfoort and Ek (1990) have provided us with a detailed study in French Guiana (Figure 132), reporting 154 bryophyte species from only 28 mature trees (22 species) in a lowland rainforest by sampling from tree base to top of the canopy. Of these, 88 were liverworts, with 71 of these in the Lejeuneaceae (Figure 6, Figure 15-Figure 16).

Figure 131. Sematophyllum sp. (Sematophyllaceae), one of the families that dominates in tropical Guyana. Photo by Michael Lüth, with permission.

Figure 132. Cataratas de Kaieteur, Guiana. Photo through Creative Commons.

In Kartabo, Co-operative Republic of Guiana (Figure 132), Graham (1933) also found the most diverse family to be the leafy liverwort family Lejeuneaceae (Figure 6, Figure 15-Figure 16). The most abundant moss here, by far, is Rhaphidorrhynchium subsimplex (see Figure 133), a species that is likewise abundant in Trinidad. Gradstein and Ilkiu-Borges (2009) compiled a guide to the liverworts and hornworts of Central French Guiana, including descriptions of habitats, especially the lowland cloud forest. This guide included 175 species of liverworts and 2 of hornworts, with the Lejeuneaceae again being the most species rich with 117 species. This guide recognized new combinations, providing updated nomenclature.

Figure 133. Rhaphidorrhynchium callidum; R. subsimplex is abundant in Kartabo in the Co-operative Republic of Guiana and in Trinidad. Photo by Juan Larrain, with permission.

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In Moraballi Creek rainforest in the Co-operative Republic of Guyana (Figure 132), few species are very frequent (Richards 1954). Calymperes lonchophyllum (see Figure 134) and Octoblepharum albidum (Figure 135) occur in all synusiae (high canopy epiphytes, shade epiphytes, dead wood) except epiphyllous ones. Like most of the moist rainforests, the stream area is characterized by absence of ground-dwelling bryophytes, abundance of epiphyllous bryophytes, and dominance of the leafy liverwort family Lejeuneaceae (Figure 6, Figure 15-Figure 16).

Figure 134. Calymperes tenerum showing gemmae on leaf tips. Calymperes lonchophyllum is a frequent species, occurring in all synusiae except epiphylls at Moraballi Creek, Guyana. Photo by P. J. de Lange, through Creative Commons.

Figure 135. Octoblepharum albidum, a frequent species occurring in all synusiae except epiphylls at Moraballi Creek, Guyana. Photo by Janice Glime.

The Chocó region (Figure 136) of Colombia has the highest precipitation level in the Neotropical rainforests (Frahm 2012) and one of the wettest rainforests in the

world (Frahm 1994), with an annual rainfall up to 12,000 mm, in some places even up to 15,000 mm. As a result, the bryophyte flora differs from elsewhere and the mosses do not serve as adequate indicators of the vegetational zones. Rather, this location permits us to observe the effects of high humidity on bryophytes.

Figure 136. Everwet lowland rainforest of the Chocó, Pacific coast of Colombia. Photo by Jan-Peter Frahm, with permission.

Frahm (1994, 2012) worked on the moss flora of the Chocó region. Although it has a high level of endemism in flowering plants, birds, and butterflies, the moss flora was too poorly known to assess endemism. Frahm found 125 species of mosses on a transect from sea level to 1600 m elevation, using 10-hectare plots and different altitudes. In contrast, liverwort diversity in the same area was much higher, more than 200 species were reported, including 13 endemic taxa (Gradstein & Reiner-Drehwald 2017). In fact, Frahm (2012) found that mosses comprise only ~10% of the bryophyte cover, whereas elsewhere at the same elevational vegetation zone in the rainforest they comprise 40-50%. Gradstein (pers. comm.) commented that Frahm was able to finish his moss identifications quickly and get them published because there were rather few species only, whereas it took years to complete the many more liverwort identifications. Some of the endemic liverworts of the Chocó region (Figure 136), such as Fulfordianthus pterobryoides (Figure 137), Luteolejeunea herzogii, and Symbiezidium dentatum, all members of Lejeuneaceae (Figure 6, Figure 15-Figure 16), are surprisingly common and widespread in the Chocó despite their absence elsewhere (Frahm 1994).

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The higher liverwort diversity in the Chocó is probably due to the exceedingly high humidity in the area.

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Costa (2003) studied the Amazonian rainforest bryophytes in Acre, Brazil. She revealed 514 species, with two field trips increasing the known bryoflora by 50%. She concluded that the diversity is still poorly known for the Brazilian Amazon. In their study in the Chapada Diamantina region of Brazil, Valente et al. (2013) identified 400 bryophyte taxa, with the forests and campos rupestres (Figure 139; dry, rocky grasslands) accounting for 51% and 40%, respectively. The caatinga (Figure 140; shrub and thorn desert vegetation in interior northeastern Brazil) and cerrado (Figure 141; savanna) accounted for only 5% and 4%, respectively.

Figure 137. The endemic Fulfordianthus pterobryoides on a twig in Chocó, Colombia. Photo by Jan-Peter Frahm, with permission.

When Vital and Visnadi (1994) surveyed the bryophyte flora of the Rio Branco Municipality in Brazil, they found only 76 species of bryophytes; 66 of these were new records for the State of Acre and 2 were new records for Brazil. The only hornwort was Notothylas vitalii (Figure 138). We now know that there are at least 12 species of hornworts in Brazil (Felipe et al. 2016).

Figure 138. Notothylas sp.; N. vitalii was the only hornwort known to Vital and Visnadi from Rio Branco Municipality in Brazil in 1994. Photo by Blanka Aguero, with permission.

Figure 139. Campos Rupestres da Serra da Canastra, Brazil. Photo by Antonio José Maia Guimarães, through Creative Commons.

Figure 140. Caatinga – sertão nordestino, Brazil. Photo by Maria Hsu, through Creative Commons.

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Figure 141. Cerrado, Campo Sujo, Brazil. Photo by Andreza Oliveira Borges, through Creative Commons.

Recent studies mostly support the earlier ones, but changes in nomenclature are reducing the numbers of endemic species. Costa and Peralta (2015) reported 1,524 species of bryophytes in Brazil, including 11 hornwort, 733 liverwort, and 880 moss species. As has been typical, the Lejeuneaceae (Figure 6, Figure 15-Figure 16) are the most abundant (285 species!). Following that record high are Lepidoziaceae (Figure 12) (48), Frullaniaceae (Figure 7Figure 8) (37), Ricciaceae (Figure 52-Figure 53) (36), Plagiochilaceae (Figure 11) (27), Radulaceae (Figure 9Figure 10) and Metzgeriaceae (Figure 13) (26 each), Lophocoleaceae (Figure 142) (18), Aneuraceae (Figure 14) (15), and Calypogeiaceae (Figure 143) (13). Surprisingly, Sphagnaceae (Figure 144) sets the record for mosses with 83 species, followed by Fissidentaceae (Figure 145) (65), Pottiaceae (Figure 146) (63), Dicranaceae (Figure 34, Figure 111) (54), Bryaceae (Figure 147) and Sematophyllaceae (Figure 131, Figure 184) (53 each), Orthotrichaceae (Figure 99) and Pilotrichaceae (Figure 148, Figure 182) (51 each), Calymperaceae (Figure 128, Figure 134) (48), and Hypnaceae (Figure 130) (28). Together, these account for 71% of the known bryophyte species in Brazil.

Figure 142. Lophocolea cf polychaeta (Lophocoleaceae) from the Neotropics; Lophocoleaceae is one of the common liverwort families in Brazil. Photo by Michael Lüth, with permission.

Figure 143. Calypogeia (Calypogeiaceae) from the Neotropics; Calypogeiaceae is one of the common liverwort families in Brazil. Photo by Michael Lüth, with permission.

Figure 144. Sphagnum cuspidatum (Sphagnaceae); Sphagnaceae is the moss common moss family in Brazil. Photo by Michael Lüth, with permission.

Figure 145. Fissidens asplenioides (Fissidentaceae) from the Neotropics; Fissidentaceae is one of the common moss families in Brazil. Photo by Michael Lüth, with permission.

Chapter 8-2: Tropics: Geographic Diversity Differences

Figure 146. Leptodontium stellatifolium (Pottiaceae) from the Neotropics; Pottiaceae is one of the common moss families in Brazil. Photo by Michael Lüth, with permission.

Figure 147. Bryum cellulare (Bryaceae); Bryaceae is one of the common moss families in Brazil. Photo by Li Zhang, with permission.

Figure 148. Crossomitrium patrisiae (Pilotrichaceae) from the Neotropics; Pilotrichaceae is one of the common moss families in Brazil. Photo by Michael Lüth, with permission.

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Other new records include those of Oliveira and Alves (2007) for the State of Ceará, Brazil. Even at this recent date, 35 of the 81 species they identified were new for the state, and one was new for Brazil. In the Parque Ecológico de Gunma, Pará, Brazil, Fagundes et al. (2016) found 103 species, with the liverworts exhibiting the greater diversity (59). Of course the Lejeuneaceae again had the predominant representation of species (42). The rare species predominated with 62 species, whereas generalists were represented with only 47 species. Five new records were uncovered. Oliveira and Bastos (2009) contributed to the knowledge of Anthocerotophyta and Marchantiophyta from Chapada da Ibiapaba, Ceará, Brazil. Of the 10 thallose liverwort species found, this study revealed 3 species of thallose liverworts for the first time in northeastern Brazil. Florschütz-de Waard and Bekker (1987) compared the bryophyte flora in different forest types in West Suriname. They found the highest species richness in the marsh forest and the lowest in the savannah and xeromorphic (having structural adaptations to dry conditions) scrub forests. Based on their microclimatic data, they considered liverworts to have a greater ecological amplitude in these forests than that of mosses, a conclusion different from that in many ecosystems. Although the Neotropics have not been studied to the degree of the temperate systems, most areas have had at least some studies. Spruce (1884-1885), Fulford (1963, 1966, 1968, 1976) and Gradstein (numerous papers, e.g. Liverwort Flora of Brazil by Gradstein & Costa 2003 and Liverwort Flora of French Guiana by Gradstein & IlkiuBorges 2009) studied liverworts. Very little work, however, has been done on the hornworts, a problem that Villarreal (2007) and others are attempting to rectify. A number of additional general Neotropical floristic studies are available, but nomenclature should be reviewed to find more recent revisions: Delgadillo (1976) on bryophyte ecology in Veracruz, Mexico, Mägdefrau (1983 – forests and páramos of Venezuela and Colombia), van Reenen and Gradstein (1983, 1984), Timme (1985 – Peru), Buck & Thiers (1989), Gradstein et al. (1990 – Guianas, especially lowland forest), Richards (1991 – Co-operative Republic of Guiana and West Indies), Sastre de Jesus & Santiago-Valentín [1996 – Puerto Rico, managed forests of Cupressus (Figure 25) and Acacia (Figure 26)], Churchill (1996 – Andes), Gradstein (1998 – páramos), Benavides et al. (2006) in the Colombian Amazon, Gradstein et al. (2016) on bryophytes of Sierra Nevada de Santa Marta, Colombia among others. More recently, Delgadillo-Moya et al. 2017) have studied mosses in the cloud forests of Veracruz, Mexico. They suggested that the terminology of Humid Mountain Forest provided the broadest conceptual and geographical term. Nevertheless, using the most restrictive definition of the cloud forest, they found 323 species and varieties through literature searches, field, and herbarium records. A few have ventured into ecological studies such as the vegetative variability of liverworts as demonstrated by Bazzania (Figure 149) (Bernecker 1990) or the differences among physiognomies in species richness and distribution (Valente et al. 2013). Others have sought to make broader statements regarding the ecology and biogeography

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(Gradstein & Pócs 1989). More recent studies, particularly on epiphytes, epiphylls, altitude, and rock outcrops, will be covered in more detail in subsequent subchapters of this chapter. These studies point to the need for more studies in order to gain a clear understanding of tropical bryophyte ecology.

Table 2. Percent of endemism in tracheophytes and bryophytes in tropical countries. From Frahm 2003.

Galapagos Islands Cuba Kilimanjaro Usambara Mtns. Réunion Mauritius

Tracheophytes

Bryophytes

50% 50%

10% 12% 6% 3% 9% 6%

Figure 149. Bazzania sp., a genus with vegetative variability from the Neotropics. Photo by Michael Lüth, with permission.

Endemism Endemism (condition of species being unique to defined geographic location) has in the past been considered high in the tropics. In 1994 Delgadillo reported 48% endemism for mosses in the Neotropics. He suggested that endemism for mosses is higher in Bolivia, Costa Rica, and Ecuador than in other Neotropical areas. But he also considered that low numbers in some areas may be due to insufficient study. In others, low numbers result from strong connections with adjacent land masses having suitable habitat. I would also caution that high numbers may be the result of synonymy. Frahm (2003) concluded that the rate of endemism is much higher in the tropics than outside the tropics but it is always much lower than that of tracheophytes (Table 2). Furthermore, we must consider these earlier numbers of endemics with skepticism. Throughout the tropics, many researchers worked independently of each other. They encountered bryophytes that were new to them and gave them new names. But researchers in other locations encountered these same bryophytes and gave them different names. There were no comprehensive keys to species from the tropics, and it was difficult to know that a species had already been named by someone else in a different location. Schuster (1982) explained the high degree of endemism in the liverwort flora of Gondwanaland (Figure 150) as a result of the break up and dispersal of Gondwanaland. The resulting isolation permitted speciation that led to endemism. This was further enhanced by extinctions in the Antarctic, leaving behind an isolated flora in New Zealand. Schuster attributes the current degree of endemism seen in the Antipodes (Australia and New Zealand) to the climate changes and breakup of Gondwanaland.

Figure 150. Gondwana Box Log Falls; Gondwanaland has a high degree of liverwort endemism. Photo by Malcolm Jacobson, through Creative Commons.

In Australia (Figure 105), endemism in the Wet Tropics is among the highest in the country (Stevenson et al. 2012). That area likewise had the highest number of species. Areas having high numbers of species were not necessarily the areas with endemism. Schuster (1982) contended that only two areas had high levels of endemic genera: Australasia and South America. India (Figure 151) has few endemic groups, most likely reflecting wide-spread extinction of cool-adapted taxa. By contrast, Schuster listed 39 genera and 11 subgenera of leafy liverworts that were endemic to tropical America. All but two of these endemic genera are in the families Acrobolbaceae (Figure 152), Cephaloziellaceae (Figure 151, Figure 155-Figure 156), Gymnomitriaceae (Figure 153), Jungermanniaceae (Figure 154), and Plagiochilaceae (Figure 11), or the very specialized Lejeuneaceae (Figure 6, Figure 15-Figure 16). (Note that family classification may be different now.) The endemic

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species, furthermore, are usually highly specialized. One common feature of the liverwort genera Pteropsiella and Protocephalozia in the Lepidoziaceae (Figure 12) and Phycolepidozia (Figure 151, Figure 155-Figure 156) in the Cephaloziellaceae is that they develop either a thalloid or confervoid (loosely interwoven) gametophyte (Figure 156).

Figure 151. Phycolepidozia indica growing on rock in a forest fragment at Mt. Tandiandamol at 1600 m in the Western Ghats, India. Photo by Uwe Schwarz, courtesy of Robbert Gradstein.

Figure 152. Acrobolbus ciliatus, in the Acrobolbaceae, a family with several endemic species in the Neotropics. Photo by Blanka Aguero, with permission.

Figure 153. Gymnomitrion concinnatum, in the Gymnomitriaceae, a family with several endemic species in the Neotropics. Photo by Herman Schachner, through Creative Commons.

Figure 154. Jungermannia rubra with perianth, in the family Jungermanniaceae, a family with a number of Neotropical endemic species. Photo by Ken-ichi Ueda, through Creative Commons.

Figure 155. Phycolepidozia indica habitat in forest fragments on Mt Tandiandamol, Western Ghats, at 1600 m. Photo by Uwe Schwarz, courtesy of Robbert Gradstein.

Figure 156. Phycolepidozia indica, a species that can develop either a thalloid or confervoid (loosely interwoven) gametophyte. Photo by Uwe Schwarz, courtesy of Robbert Gradstein.

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In Australia (Figure 105), at least four endemic species of the moss Macromitrium (Figure 99) occur in higher elevation rainforests dominated by Nothofagus moorei (Figure 157; not tropical) (Ramsay et al. 1987). Of these, the tropical rainforests have three endemic Macromitrium species: M. erythrocomum (Figure 99), M. dielsii, and M. funiforme (Andi Cairns, pers. comm. 7 October 2019).

Figure 159. Sphagnum palustre with capsules in Sweden. Photo by Oskar Gran, through Creative Commons.

Africa In sub-Saharan Africa (Figure 160), O'Shea (1997b) reported 77% of the 3,000 taxa to be endemic. However, he warned that this figure may be misleading because the bryophyte flora of Africa was (and still is) so poorly known (and many may turn out to be synonyms).

Figure 157. Nothofagus moorei forest. Photo by David, through Creative Commons.

Karlin et al. (2012) used Sphagnum palustre (Figure 158) in Hawaii to explore the viability of a species from a single propagule. They concluded that this species currently has significant genetic diversity in Hawaii and that vegetative propagation does not preclude evolutionary success. This species is not known to produce sporophytes in Hawaii, although it does in other parts of the world (Figure 159).

Figure 158. Sphagnum palustre, a species with significant genetic diversity in Hawaii. Photo by Bernd Haynold, through Creative Commons.

Figure 160. Sub-Saharan Ruwenzori moss. Photo by Albert Backer, through Creative Commons.

Pócs (1998) found a high species diversity (~700 species known in 1998) along the Eastern Arc Mountains of Africa (Kenya and Tanzania; Figure 161), with only 32 (4.5%) endemic species, a low number even when compared to that of tracheophytes in the area.

Figure 161. Usambara Mountains, Eastern Arc Mountains, Tanzania. Photo by Joachim Huber, through Creative Commons.

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Asia In 2003, O'Shea reported 11% bryophyte endemism in Sri Lanka. The bryophyte flora of Sri Lanka is relatively rich, with 561 taxa. In fact, Gunawardene et al. (2007) considered the Western Ghats and Sri Lanka to be biodiversity hotspots. In the Azores (Figure 162), of the 89 epiphyllous bryophyte species, 14 were considered endemic to the Azores or to Macaronesia (Sjögren 1997). These are somewhat frequent members of the endemic epiphyllous (Figure 163) association, the Cololejeuneo-Colurion: Cololejeuneetum azoricae (see Figure 44, Figure 163, Figure 164).

Figure 164. Colura leratii in Fiji. Photo courtesy of Tamás Pócs.

Figure 162. Island of Ponta Delgada, Azores. Photo by Laragheast, through public domain.

The Asian endemics of the Ptychanthoideae (Figure 38) in the Lejeuneaceae (Figure 6, Figure 15-Figure 16) tend to be restricted to subtropical and temperate regions, with the majority also known from Eocene fossils (Gradstein 1991). They are largely relicts (something that has survived from earlier period). The Lejeuneoideae (Figure 165-Figure 166) are mainly in the tropical rainforests of the Malesian archipelago, are frequently highly specialized, and have no fossil records.

Figure 163. Cololejeunea diaphana and Lejeunea floridana, common epiphylls. Photo by Scott Zona, through Creative Commons.

Figure 165. Lejeunea flava (Lejeuneoideae) growing as an epiphyte. The Lejeuneoideae are common in tropical rainforests of the Malesian archipelago. Photo by Linda Phillips, through Creative Commons.

Figure 166. Lejeunea flava (Lejeuneoideae), growing as an epiphyll. Photo by Yang Jia-dong, through Creative Commons.

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In 1987 Piippo et al. reported 48% endemism among the liverworts of New Guinea; 23% of the moss species seemed to be endemic. Most of these occur between 1500 and 3500 m elevation. The researchers found a high degree of endemism in the Frieda River Area and concluded that this is due to the high levels of metals in the area. The leafy liverworts Bazzania (Figure 149), Frullania (Figure 2, Figure 7-Figure 8), Plagiochila (Figure 11), and Radula (Figure 9-Figure 10) have a high degree of species endemism. The highest percentages of endemics among liverworts were in the Plagiochilaceae (Figure 11) (78%) and Schistochilaceae (Figure 167) (74%). Among the mosses, the number of species is much smaller, so the percentages may not be meaningful. The most notable may be the Bryaceae (Figure 168) with 35 species, 12 of which were considered endemic. The researchers cautioned that many of the families had not been studied well, so these numbers for both mosses and liverworts should be considered preliminary. All of these numbers will need revision after eliminating synonymy.

Figure 167. Schistochila sp., in the family Schistochilaceae, a family with many endemics in New Guinea. Photo by Li Zhang, with permission.

Figure 168. Bryum billardieri; Bryum is a genus with 12 endemic species in New Guinea. Photo by Jan-Peter Frahm, with permission.

Piippo (1994a) reported 38.2% endemism in Western Melanesia among the 440 species there. The highest reported endemism occurs in Frullaniaceae (Figure 2,

Figure 7-Figure 8) and Plagiochilaceae (Figure 11). Although this is a slightly more recent study, synonyms again create a problem in determining endemism. Piippo (1994b) also studied the liverwort family Lejeuneaceae (Figure 6, Figure 15-Figure 16) of Western Melanesia and reported that only 20.5% of these species were endemic. She attributed this to the large number of epiphyllous species in the family, a group that is widespread throughout the tropics. Australia Ramsay et al. (1987) considered about 50-60 of the mosses to be endemic to the Wet Tropics bioregion in northeast Queensland (Ramsay & Cairns 2004). This number is most likely no longer accurate due to new discoveries and synonymy of old ones. One might expect a high number here; the next closest known population is 5400 km away (Figure 169) from the Australian populations (Meagher & Cairns 2016).

Figure 169. Australian tropical distance map. Meagher & Cairns 2016.

From

In his report to the IUCN on areas and bryophytes to be protected, Streimann (2000) noted that "a reasonable number of endemics and restricted species are generally found in higher, more moist ranges in north Queensland." This area includes several high peaks with high levels of rainfall and cloud cover. Such endemics as Calyptrochaeta brassii (see Figure 78) (Streimann 2001) and Dicranoloma braunii (Figure 170) occur on Mt. Finnigan. On the Bellenden-Ker Range, Clastobryum dimorphum, once considered an endemic to the Wet Tropics, has been reduced to a variety of the more widespread Clastobryum cuculligerum (see Figure 79), now as var. dimorphum (Cairns et al. 2019). Mniodendron comatulum (Figure 171; treated as Hypnodendron comatulum in TROPICOS) is another endemic to the Australian tropics. Because of many nomenclatural changes and synonymies, the number of endemics is most likely different from that suggested by Ramsay et al. (1987), and it is likely that more endemics will be discovered in the future in this relatively underexplored part of Australia.

Chapter 8-2: Tropics: Geographic Diversity Differences

Figure 170. Dicranoloma billarderii, a species common in southern Australia; D. braunii is known only from Mt Finnigan in the Wet Tropics of Australia, but is widespread in continental SE Asia, Malesia and Oceania (Klazenga 2012). Photo by Niels Klazenga, with permission.

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considered the area to be unique in harboring life-forms and structural diversity of mosses that have been lost in other tropical areas of Mexico. As suggested by earlier studies, when DelgadilloMoya et al. reported on moss endemism in the entire Mexican flora, they were only able to verify 77 endemic species out of the nearly 1000 species. They identified three main areas of endemism in Mexico: lowland areas in various states, the mountain area along 19020ºN lat., and the highlands in Oaxaca and Chiapas. Their data suggest that the highest numbers of endemic species occur in the Trans-Mexican Volcanic Belt, Sierra Madre Oriental, Chihuahuan Desert, and Sierra Madre del Sur. Although many areas have not been explored, they do not anticipate many additions to the endemic list. It is likely that more species will reveal a wider distribution as other areas of the Neotropics are explored. Fortunately, there are now good Neotropical bryologists who are increasing our knowledge of that bryoflora. Costa et al. (2015) examined the species richness and floristic composition on an elevation gradient in the Itatiaia National Park in Brazil. They reported 519 taxa, representing 10 elevations, using literature, herbarium samples, and data banks. These represented 34% of the total Brazilian bryoflora. In southeastern Brazil, the endemic Bromeliophila natans (Figure 172) is difficult to distinguish from Lejeunea (Figure 173) (Gradstein 1997). It was so-named because it lives in the basins of bromeliads (Figure 174) (Heinrichs et al. 2014). The Neotropical moss Philophyllum tenuifolium (Leucomiaceae; Figure 175) is also restricted to this unusual habitat.

Figure 171. Mniodendron (syn.=Hypnodendron) comatulum, endemic to the Australian Wet Tropics. Photo by Clive Shirley, Hidden Forest , with permission.

Neotropics Holz and Gradstein (2005) found more endemics in the oak (Quercus) forests of Central America than in the páramo. They considered that the high percentages of endemic bryophytes in oak forests in Central America reflected the importance of climatic changes associated with Pleistocene glaciations. In an older publication, Delgadillo (1998) likewise reported a high endemic element, with ca. 47% endemics. At that time, he reported 2,900 species of mosses, a number that decreases when systematic studies uncover synonymy. He considered isolation as the major contributor to endemism. Delgadillo et al. (2003) compared endemism in the mosses, grasses, and Asteraceae. Of the 2,373 endemic taxa known among these groups, 86 are mosses; 2030 are Asteraceae. In an earlier study, Delgadillo and Cárdenas (2002) reported no endemic taxa from the Monies Azules Biosphere Reserve, where they identified 136 species and varieties, plus 8 more from published records. In the Chiapas, Mexico, Delgadillo and Cárdenas (2002) found that endemic taxa are "virtually absent." Nevertheless, they

Figure 172. Bromeliophila natans, an endemic species that lives in bromeliad basins. Drawing from Heinrichs et al. 2014, slightly modified, through Robbert Gradstein.

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It is interesting that Spruceanthus theobromae (Figure 176) is endemic to the Cacao (source of cocoa) plantations (Figure 177) of western Ecuador (Gradstein 1999). Kautz and Gradstein (2001) concluded that because of its host specificity on Cacao and its exclusive occurrence in plantations, it should be removed from the World Red List of Bryophytes and its status changed to that of a near threatened species. Its survival depends on the low management intensity of plantations such as those in western Ecuador.

Figure 173. Lejeunea floridana and Cololejeunea cardiocarpa on leaves. Photo by Scott Zona, with permission.

Figure 176. Spruceanthus theobromae, a species endemic to Cacao plantations in western Ecuador. Photo by Robbert Gradstein, with permission. Figure 174. Bromeliads in the trees, showing basins where bryophytes can grow. Photo by Gail Hampshire, through Creative Commons.

Figure 177. Cacao plantation in Cameroon. Barada-nikto, through Creative Commons.

Figure 175. Philophyllum tenuifolium herbarium specimen. Photo from Natural History Museum, London, through Creative Commons.

Photo by

Due to the efforts of a number of bryologists, the flora of Brazil is reasonably well known. Endemism in the Atlantic rainforest of Brazil reaches 242 endemic species out of the 1,337 species present (Costa & Peralta 2015). The dense ombrophilous (tolerant of wet conditions) forest here has 73% of these species represented, 62% of which are endemic. The southeastern region, with 1,228 species in total, has 219 endemic species. But the Atlantic rainforest in southeastern Brazil has most of the endangered species. Further monographic, worldwide or continent-wide studies may reduce the number of endemic species, but numbers are starting to approach reality.

Chapter 8-2: Tropics: Geographic Diversity Differences

Pócs (2019) recently reported a large number of liverworts new to Peru, two of which are endemic: Colura ochyrana (Figure 178) and Drepanolejeunea halinae (Figure 179), both restricted to the Andes.

Figure 178. Colura ochyrana, a new endemic species from the Peruvian Andes. Photo modified from Pócs (2019), with permission.

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for a long enough period of time that a new species evolved. On the other hand, if the population originated from lower elevations, it might have become a new species through the founder principle (loss of genetic variation that occurs when new population is established by very small number of individuals from larger population), followed by natural selection for characters that suited their mountain habitat. To try to answer this question, Merckx et al. (2015) examined the species on Mount Kinabalu, a 4,095 m high mountain in Sabah, East Malaysia. They found that most of the unique species of the mountain are younger than the mountain (6 million years). This mountain exhibits a mix of pre-adapted immigrant lineages and descendants from local lowland ancestors, suggesting that the species did not arrive by long distance. Nevertheless, substantial shifts from lower to higher vegetation zones in these lowland groups were rare. The presence of sibling pairs of Frullania (Figure 2, Figure 7-Figure 8) with each member of the pair at a different elevation range of the same mountain (Figure 180) would tend to support the latter (Glime et al. 1990). Is there any reason to think that both processes could not occur? Is one of them the dominant cause?

Figure 180. Levins and Freeman-Tukey niche width and elevational range of sibling pairs of Frullania on Mount Albert Edward, Papua New Guinea. Redrawn from Glime et al. 1990. Figure 179. Drepanolejeunea halinae, a new endemic species from the Peruvian Andes. Photo modified from Pócs (2019), with permission.

Visnadi (2015) likewise reported on the Atlantic Forest of southeastern Brail, at Mata Atlântica. This research revealed 199 species newly known for the area, bringing the total for the area to 220 species. This added two new records for Brazil and revealed locations of 13 Brazilian endemic species. Causes of Endemism Merckx et al. (2015) surmise that tropical mountains are diversity hot spots, but also exhibit a high degree of endemism. They point out that researchers have debated whether these mountain endemics originate more from local lowland taxa or from long-range dispersal from cool localities elsewhere. The latter could be similar to the separation of many frog species on different mountain tops, as discussed in the interaction chapter on amphibians in volume 2. This would presume that the species arrived, but was separated from interbreeding with the original species

Patiño et al. (2014) attempted to explain the emergence of endemism by questioning why some genera diversify and others do not. Speciation on islands through gradual change from a founder population has been termed anagenetic speciation. They challenge this approach, saying that this process does not lead to "rapid and extensive speciation within lineages." Using surveys of the endemic bryophyte, fern, and seed plant floras of nine oceanic archipelagos, they showed that anagenesis (species formation without branching of evolutionary line of descent) was highest in bryophytes (73%), as measured by the proportion of genera with a single endemic species. Ferns had 65% and seed plants 55%. They concluded that "the dominance of anagenesis in island bryophytes and pteridophytes [ferns] is a result of a mixture of intrinsic factors, notably their strong preference for (sub)tropical forest environments, and extrinsic factors, including the long‐term macro‐ecological stability of these habitats and the associated strong phylogenetic niche conservatism of their floras."

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Dangers to Endemics Silva et al. (2014) raised concerns about conserving key species of bryophytes. They created potential distribution models for ten species that had been classified as bio-indicators of environmental quality and/or were endemic to the Atlantic Forest or to Brazil. Distributions of nine of the species could be explained by the Mean Diurnal Temperature Range. They raised concern that these species were not known in all the potentially suitable areas and that only 27% of the potentially suitable areas overlapped with Conservation Units. While these species were not specifically endemic, this approach could be used for determining the need for areas to protect endemic species. Like Silva and coworkers (2014), Raxworthy et al. (2008) found that temperature was important in shifting altitudinal distributions of plants and animals, with increasing temperature likely to surpass a warming threshold for some species. Of three endemic species in the tropical montane of Madagascar, two could not be relocated after 10 years. In addition, out of nine species analyzed, seven species had shifted their distributions to higher elevational means. In the 10 years of study, the mean lower elevation limit had shifted upward 29-114 m.

Calymperaceae (Figure 128, Figure 134) and Sematophyllaceae (Figure 131, Figure 184), in particular, as well as Fissidentaceae (Figure 17, Figure 37), Leucobryaceae (including Octoblepharum; Figure 112), Pilotrichaceae (Figure 182), and Pterobryaceae (Figure 183) (Pócs 1982). The Calymperaceae are distributed primarily in the humid lowland tropical and subtropical forests (Reese 1993). These primarily epiphytic taxa are usually dioicous but produce numerous gemmae at their leaf tips, facilitating short-distance dispersal (Gradstein & Pócs 1989). Whereas Calymperes (Figure 128) is restricted to the lowlands, another tropical member of Calymperaceae, Syrrhopodon (Figure 185), extends up to more than 2,000 m elevation. Both are primarily corticolous (growing on bark), but occur also on logs in the first stages of decomposition. In the Sematophyllaceae, Taxithelium planum (Figure 184) is abundant enough to be termed a weed in the lowland tropical forests of the Americas (Buck 1985; Churchill & Salazar Allen 2001).

Tropical Rainforests Whitmore (1998) provided an introduction to the tropical rainforest. These forests are evergreen, and the precipitation occurs more or less equally throughout the year, exceeding ca. 2000 mm per year. Under the umbrella of rainforests (Figure 181), Frahm and Gradstein (1991) recognized elevational rainforest types (see Chapter 8-1). The elevations of the different types of rain forest are lower on islands than on the continent. In areas with prolonged dry periods (>3 months), these forests are replaced with deciduous forests, seasonal forests, and savannahs. These types of forests will be discussed more specifically in the subchapters on Altitude. Figure 182. Cyclodictyon sp., representing Pilotrichaceae, a family that increases in representation as one goes toward the tropics. Photo by Michael Lüth, with permission.

Figure 181. Hawaiian tropical rainforest. Photoeverywhere, through Creative Commons.

Photo from

Early researchers in the tropics considered the tropics to be an "inexhaustible" source of new bryophyte species (Pócs 1982). Richards (1954) bemoaned the scantiness of studies on the species and their ecology in tropical rainforests. As one moves from the temperate zone into the tropics, there will be an increase in members of the moss families

Figure 183. Pireella pohlii, representing Pterobryaceae, a family that increases in numbers as one goes toward the tropics. Photo by Michael Lüth, with permission.

Chapter 8-2: Tropics: Geographic Diversity Differences

Figure 184. Taxithelium planum, a common moss species in lowland Neotropical forests. Photo by Michael Lüth, with permission.

Figure 185. Syrrhopodon gaudichaudi from the Neotropics, where the genus is known up to 2000 m asl. Photo by Michael Lüth, with permission.

Ramsay et al. (1987) stressed the importance of learning the role of bryophytes in the rainforest ecosystem in order to encourage more study of rainforest bryophytes. Jordan et al. (1980) could only hypothesize on the role of epiphytes in scavenging nutrients and moderating the flux of nutrients in the throughfall. Since then, Nadkarni and her students have greatly increased our knowledge of the role of bryophytes in nutrient relationships in the tropics (see Nutrient Relations in Chapter 8-1 of this volume). Elevation and waterways are major contributors in determining the flora. Dixon (1935) described that below the Borneo ridgetop, cushions of the moss family Dicranaceae (Figure 34, Figure 111) are relatively common on both the ground and on logs, but liverworts remain more abundant. Near the stream, the large, pendent moss Spiridens reinwardtii (Figure 83) might be found on tall tree ferns. Dixon also reported abundant Macromitrium ochraceum (Figure 99) under the thin cover of Dacrydium (Figure 186; Podocarpaceae) and Leptospermum (Figure 187; Myrtaceae).

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Figure 186. Dacrydium cupressinum; the genus Dacrydium provides cover for Macromitrium ochraceum near streams in Borneo. Photo by James Shook, through Creative Commons.

Figure 187. Leptospermum trinervium, in the genus that provides cover for Macromitrium ochraceum near streams in Borneo. Photo by John Tann, through Creative Commons.

Several additional studies are helpful in understanding the rainforest bryophyte communities. Giesenhagen (1910) described moss species of the rainforest. Pócs (1987) reported the changes in the biomass and productivity of bryophytes in east African rainforests. Gradstein and Pócs (1989) discussed tropical rainforest ecosystems and biogeography. Equihua and Gradstein (1995) compared the bryophyte communities of a rainforest with those of an old field. A more recent comprehensive study is that of Gradstein and Sporn (2010) on land use gradients. Pantropical Distributions Although liverworts seem to reach particularly high diversity in the tropics, moss richness estimates, based on 86 taxonomic checklists, do not support the hypothesis of a richer moss flora in the tropics compared to that of other latitudes (Shaw et al. 2005). Nevertheless, the latitudinal gradient for just North, Central, and South America was significant. Molecular data suggest that the Southern Hemisphere exhibits a higher diversity than does the Northern Hemisphere. The tropics are intermediate. Furthermore, virtually all the moss lineages are represented in all three latitudinal zones. Hence, it should be no

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surprise that mosses have travelled long distances and that many tropical mosses, particularly above the species level, are pantropical. This reasoning fits the Baas-Becking Hypothesis that everything is everywhere, a principle that seems to apply well to organism with small, resistant propagules such as spores (see Volume 2, Chapter 2-6; Pisa et al. 2013). By examining tropical bryophyte communities in both Old World and New World tropics, Kürschner and Parolly (1999) could compare the differences. They concluded that although communities may be similar among the Americas, Africa, and Asia, there is not a pantropical (in tropics of both Eastern and Western Hemispheres) bryophyte flora. Could this be a result of too many bryologists giving different names to the same species in different places? In any case, there are clear similarities among the bryophyte communities of the three continents and a pantropical class of epiphyte communities can be recognized. Earlier, similarities and differences among the bryofloras of the tropical Americas, Africa, and Asia have been described by Theodor Herzog (1926) in his classical treatise Geographie der Moose. Recent studies such as that of Dauphin L. and Grayum (2005) support the relatively large number of pantropical species, with 16% of their 55 collected species of bryophytes from the dry lowland forests and moist montane forests of the Santa Elena Peninsula and Islas Murciélago, Guanacaste Province, Costa Rica, being pantropical. While most of the species are not pantropical, many families and genera are, and certain general community characters are present. For example, Germano and Pôrto (2006) examined bryophytes in Pernambuco, Brazil (Figure 188), and found that the community distribution patterns and growth forms were similar to those of other humid tropical forests, but in Pernambuco the richness was somewhat less. In their study, the most diverse bryophyte flora was that of corticolous (living on bark) bryophytes (33% of species). Epixylic (growing on wood, i.e., trunks without bark, mostly logs) bryophytes were next (23%). With this high diversity, it is somewhat surprising that communities share 75% of the species. Liverwort diversity is higher than that of mosses, with a ratio of 23:1 among the epiphyllous (living on leaves) and 2:1 among corticolous species. However, terricolous (living on ground) species exhibited a 1:3 ratio of liverworts to mosses. The researchers also found that epixylic species were not specific for degree of decomposition, nor did richness vary with degree of decomposition.

Figure 188. National Park of Catimbau, Pernambuco, Brazil. Photo by Guilherme Jófili, through Creative Commons.

The mangroves, in contrast to the high diversity in other parts of the Wet Tropics, have very little diversity, with only Calymperes (Figure 64-Figure 65) species present on the mangrove trees (Ramsay & Cairns 2004). The terrestrial Taxithelium leptosigmatum (Figure 66Figure 67) forms extensive mats on mud and exposed mangrove roots, especially if there is a high input of fresh water. Substrate Specificity Usable substrates in the understory of mature lowland forests are somewhat limited. The forest floor is typically covered with leaf litter that buries bryophytes. Rock surfaces may be available, especially vertical surfaces, if there is sufficient light. The forest itself provides trunk, branches, and leaf surfaces as substrates. At higher elevations, the soil and rock surfaces provide suitable surfaces. Soil in disturbed areas and other areas with sufficient light provides an available substrate. Bien (1982) examined substrate specificity of the leafy liverworts in a rainforest in Costa Rica. A later subchapter will be devoted to the leaf as a substrate for epiphyllous liverworts. In a study in the Ecological Reserve of Gurjaú, Pernambuco, Brazil, Germano and Pôrto (2005) found few species that have substrate specificity. Rather, they typically occurred on two or three types of substrates. Some, however, were exclusively corticolous (barkdwelling): Archilejeunea fuscescens (see Figure 189), Cheilolejeunea rigidula (see Figure 190), Lejeunea monimiae (Figure 191), some species of Frullania (Figure 2, Figure 7-Figure 8), and additional members of the Lejeuneaceae (Figure 6, Figure 15-Figure 16, Figure 191Figure 192). Few epiphyllous species were restricted to leaves, including several species of Cololejeunea (Figure 163) and Leptolejeunea elliptica (Figure 192). Only Neckeropsis disticha (Figure 193) was restricted to rocks (rupicolous). On the ground the typical bryophytes were Fissidentaceae (Figure 17, Figure 37), thallose liverworts, and the hornwort Notothylas vitalii (see Figure 194).

Figure 189. Archilejeunea olivacea; Archilejeunea fuscescens is a species that grows exclusively on bark at Pernambuco, Brazil. Photo by John Braggins, through Creative Commons.

Chapter 8-2: Tropics: Geographic Diversity Differences

Figure 190. Cheilolejeunea imbricata; Cheilolejeunea rigidula is a species that grows very commonly on bark at Pernambuco, Brazil. Photo by Yang Jia-dong, through Creative Commons.

Figure 191. Lejeunea monimiae, a species that is strictly corticolous in the Pernambuco study site in Brazil. Photo by Elena Reiner-Drehwald, with permission.

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Figure 193. Neckeropsis undulata, a family (Neckeraceae) that indicates very shady, wet habitats in the tropics. Photo by Michael Lüth, with permission.

Figure 194. Notothylas javanica; N. vitalii is a similar common hornwort on the ground in the Ecological Reserve of Gurjaú, Brazil. Photo by Li Zhang, with permission.

Forest Floor

Figure 192. Leptolejeunea elliptica, a species restricted to leaves at the Pernambuco study site in Brazil. Photo by Yang Jiadong through Creative Commons.

The forest floor of the lowland rainforest is nearly devoid of bryophytes, suffering from the same leaf burial found in temperate deciduous forests (Richards 1954), but also suffering from the multi-layered canopy that blocks a large percentage of the sunlight. But decaying logs, stumps, and branches here can host a number of taxa. It is here, in the low light and high humidity, that one finds Leucobryum (Figure 195) and mosses in the Hookeriaceae (Figure 182), Hypnaceae (Figure 130), and Sematophyllaceae (Figure 131, Figure 184) (Gradstein & Pócs 1989). Liverworts of the Lepidoziaceae and Lophocoleaceae (Figure 196), rather than the seemingly ever-present Lejeuneaceae (Figure 6, Figure 15-Figure 16, Figure 191-Figure 192), thrive here. Generally, only on road cuts, termite mounds, and other disturbed soil can one find bryophytes, including many Fissidens (Figure 17, Figure 37) species.

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Figure 197. Trichomanes petersii and bryophytes. Rockhouses have collections of plants similar to these. Photo by Robbin Moran, with permission through Dale Vitt. Figure 195. Leucobryum juniperoideum; Leucobryum occurs on stumps, logs, and branches in the tropics. Photo by Hermann Schachner, through Creative Commons.

Figure 196. Leptoscyphus sp., a tropical representative of the Lophocoleaceae, where the family is common on logs. Photo by Paul Davison, with permission.

Rockhouses Outside the tropics, rockhouses can mimic the conditions prevailing in some tropical habitats. These rockhouse cliffs, occurring as geologic formations in the eastern United States, are sufficiently deep holes among the rocks to buffer both temperature and moisture extremes. Added to this are very low light conditions, thus in several ways mimicking conditions deep under the tropical rainforest canopy. These caves house a group of endemic species whose closest relatives are tropical, as well as disjunct species with a primarily tropical range (Farrar 1998). Although the ferns are the most conspicuous of these plants, the bryophytes are the most numerous (Figure 197). Farrar suggests that their vegetative reproduction and adaptation to net photosynthetic gain in very low light makes their existence in these unusual habitats possible. Evidence of morphology, physiology, genetics, and geology suggest that they have persisted in these relict habitats since the pre-Pleistocene when the eastern U.S. experienced tropical and subtropical climates.

Summary Although some bryophytes are pantropical or have disjunct distributions on both sides of the Atlantic, their specialized habitats often restrict their distributions. This is indicated by a higher beta diversity among than within tropical regions. Nonetheless, the greatest number of bryophyte species occurs in the tropics. But many publications represent synonyms and many areas remain to be explored. Furthermore, it appears that increase in species diversity from the poles to the equator does not apply to mosses. Tropical liverwort families are dominated by Lejeuneaceae, Frullaniaceae, Radulaceae, Plagiochilaceae, and Lepidoziaceae, with lesser numbers in Metzgeriaceae and Aneuraceae. The moss Fissidens has ~90 species in Africa. In tropical Asia and Australia, common mosses include the large species in Dawsoniaceae, Pterobryaceae, Ptychomniaceae, and Hypnodendraceae. The liverwort family Lejeuneaceae is particularly speciesrich in Asian tropics. In the Australian Wet Tropics, moss species richness correlates strongly with patch area, mean annual rainfall, and tracheophyte species richness. The greatest species richness occurs in the rainforests of high mountain peaks and on the Atherton Tableland of the Wet Tropics bioregion. The tropical mangroves have little diversity, with only Calymperes species as epiphytes. Road cuts and downed forests permit the growth of such large mosses as those in Polytrichaceae. Several liverwort families are very species rich. In the Neotropics, typical moss families are Pilotrichaceae, Phyllogoniaceae, Lembophyllaceae, Dicranaceae, Octoblepharaceae, and Phyllodrepaniaceae. Dominant liverwort families include Monocleaceae and Lejeuneaceae, with the subfamily Ptychantheae mainly in Asia and subfamily Brachiolejeuneae mainly in the Neotropics. An inordinate number of endemic species has been reported from the tropics, but this number has been

Chapter 8-2: Tropics: Geographic Diversity Differences

steadily decreasing as synonyms are determined. Furthermore, the rate of bryophytic endemism is much lower than that of tracheophytes. O'Shea reported that 77% of the sub-Saharan bryophyte flora was endemic, but warned that this large number probably represented many synonyms. Some of the liverwort families in Asia reach such high numbers, but mostly the endemism reported there is notably lower. Records in the Neotropics are similar to those of Asia. Tropical mountains are often diversity hot spots, and distance from similar habitats can lead to endemism, but these also are a source of many synonyms. Nevertheless, differences in selection pressures with elevation can cause speciation. But endemic species, by their very nature of having a restricted distribution, increase their probability of extinction. Only 27% of the areas deemed suitable for them occur in protected areas. Much exploration is still needed in areas of little or no collecting, hinting at more new species and endemic species on the horizon. The Australian Wet Tropics are still underexplored. There is a greater chance for discovery of new endemic species there because of the distance from other tropical areas of the world. The tropical rainforest provides a wide range of niches due to its multiple levels of vegetation heights. To the usual substrata of rocks, logs, trunks, and branches, the tree and shrub leaves add a highly diverse assemblage of liverworts. The soil, however, typically has too many leaves and not enough light penetration for bryophytes to survive. As one goes from the temperate zone to the tropics, the moss families Calymperaceae, Sematophyllaceae, Fissidentaceae, Leucobryaceae/Octoblepharaceae, Pilotrichaceae, and Pterobryaceae increase in representation. Liverworts are typically more species-rich than mosses. In the eastern United States, rockhouses created on mountainsides and slopes provide a tempered environment where a number of tropical species are able to survive.

Acknowledgments My appreciation goes to Noris Salazar Allen for her efforts to make a very early version of this chapter reliable. Her helpful discussions kept me going on this part of the world I know so little about. S. Robbert Gradstein has been very helpful in discussions, obtaining images and references, and in providing a critical review of the chapter. Without his input this chapter would be far less complete. Tatiany Oliveira da Silva provided a critical reading for clarity, provided additional references, and shared her knowledge of the Amazon. Andi Cairns was a huge help in providing me with literature and images for the Australian tropics. Claudio Delgadillo-Moya provided me with more current references to update the treatment of Mexican tropics.

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Ramsay, H. P. 1987. Studies on the reproductive biology of some mosses from the Australian Wet Tropics. Proc. Ecol. Soc. Austral. 15: 273-279. Ramsay, H. P. and Cairns, A. 2004. Habitat, distribution and the phytogeographical affinities of mosses in the Wet Tropics bioregion, north-east Queensland, Australia. Cunninghamia 8: 371-408. Ramsay, H. P., Streimann, H., and Harden, G. 1987. Observations on the bryoflora of Australian rain forests. Symp. Biol. Hung. 35: 605-620. Ramsay, H., Cairns, A., and Meagher, D. 2017. Macromitrium erythrocomum (Bryophyta: Orthotrichaceae), a new species from tropical Queensland, Australia. Telopea 20: 261-268. Raxworthy, C. J., Pearson, R. G., Rabibisoa, N., Rakotondrazafy, A. M., Ramanamanjato, J. B., Raselimanana, A. P., Wu, S., Nussbaum, R. A., and Stone, D. A. 2008. Extinction vulnerability of tropical montane endemism from warming and upslope displacement: A preliminary appraisal for the highest massif in Madagascar. Global Change Biol. 14: 1703-1720. Redfearn, P. L. 1990. Tropical component of the moss flora of China. Trop. Bryol. 2: 201-222. Reenen, G. B. A. van and Gradstein, S. R. 1983. Studies on Colombian cryptogams. XX. A transect analysis of the bryophyte vegetation along an altitudinal gradient on the Sierra Nevada de Santa Marta, Colombia. Acta Bot. Neerl. 32: 163-175. Reenen, G. B. A. van and Gradstein, S. R. 1984. Analisis de la vegetacion de briofitas en el transecto Buritca – La Cumbre (Sierra Nevada de Santa Marta, Colombia). [Analysis of the bryophyte vegetation in the Buritca – La Cumbre transect (Sierra Nevada de Santa Marta, Colombia).]. Studies on Tropical Andean Ecosystems 2: 189-202. Reese, W. D. 1993. Calymperaceae. Flora Neotropica Monograph 58: 1-101. New York Botanical Garden, USA. Reese, W. D. and Stone, I. G. 1995. The Calymperaceae of Australia. J. Hattori Bot. Lab. 78: 1-40. Reinwardt, C. G. C., Blume, C. L., and Nees von Esenbeck, C. G. 1824. Hepaticae Javanicae, editae coniunctis studiis et opera. Nova Acta Physico-Medica Academiae Caesareae Leopoldino-Carolinae Naturae Curiosorum 12: 181-238. Renner, M. A. M. 2011. New records, range extensions and descriptions for some unfamiliar Australian Lejeuneaceae (Jungermanniopsida). Telopea 13: 563-576. Renner, M. A. M. 2014. Radula subg. Radula in Australasia and the Pacific (Jungermanniopsida). Telopea 17: 107-167. Renner, M. A. M. 2018. A revision of Australian Plagiochila (Lophocoleinae: Jungermanniosida). Telopea 21: 187-380. Renner, M. A. M. and Wilson, T. 2018. Two new species of Acromastigum (Lepidoziaceae: Jungermanniopsida) from Queensland, Australia. Telopea 21: 45-55. Renner, M. A. M., Devos, N., Brown, E. A., Konrat, M. J. von. 2014. A revision of Australian species of Radula subg. Odontoradula. Austral. Syst. Bot. 26: 408-447. Richards, P. W. 1954. Notes on the bryophyte communities of lowland tropical rain forest, with special reference to Moraballi Creek, British Guiana. Vegetatio 6: 319-328. Richards, P. W. 1991. A bryologist in British Guiana and the West Indies. J. Bryol. 16: 437-441. Ros, R. M., Cano, M. J., and Guerra, J. 1999. Bryophyte checklist of northern Africa. J. Bryol. 21: 207-244. Rowe, K. C., Achmadi, A. S., and Esselstyn, J. A. 2016. A new genus and species of omnivorous rodent (Muridae: Murinae) from Sulawesi, nested within a clade of endemic carnivores. J. Mammal. 97: 978-991.

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Wang, J., Vanderpoorten, A., Hagborg, A., Goffinet, B., Laenen, B., and Patiño, J. 2016. Evidence for a latitudinal diversity gradient in liverworts and hornworts. J. Biogeogr. 44: 487488. Webb, L. J. 1968. Environmental relationships of the structural types of Australian rain forest vegetation. Ecology 49: 296311. Whitacre, D. 1981. Additional techniques and safety hints for climbing tall trees, and some equipment and information sources. Biotropica 13: 286-291. Whitmore, T. C. 1998. An Introduction to Tropical Rain Forest. 2nd edn. Oxford University Press, 282 pp. Wigginton, M. J. 2001a. British Bryological Society expedition to Mulanje Mountain, Malawi. 15. Lejeuneaceae, and the occurrence and frequency of foliicolous taxa. Trop. Bryol. 20: 83-96. Wigginton, M. J. 2001b. A small collection of bryophytes from Ethiopia. Trop. Bryol. 20: 27-29.

Wolf, J. H. D. 1993a. Epiphyte communities of tropical montane rain forest in the northern Andes. I. Lower montane communities. Phytocoenologia 22: 1-52. Wolf, J. H. D. 1993b. Diversity patterns and biomass of epiphytic bryophytes and lichens along an altitudinal gradient in the northern Andes. Ann. Missouri Bot. Gard. 80: 928-960. Wołowski, K., Godzik, B., and Wöjcicki, J. J. (eds.). 2014. Festschrift for Tamás Pócs on the occasion of his 80th. birthday. Parts 1 and 2. Polish Bot. J. 58, parts 1, 2. Yano, O. 1981. A checklist of Brazilian mosses. J. Hattori Bot. Lab. 50: 279-456. Yano, O. 2011. Catálogo de musgos Brasileiros: Literatura original, basiônimo, localidade-tipo e distribuição geográfica. [Catalog of Brazilian mosses: Original literature, basiônimo, locality-type and geographical distribution.]. São Paulo, Instituto de Botânica. Zotz, G. and Vollrath, B. 2003. The epiphyte vegetation of the palm Socratea exorrhiza – Correlations with tree size, tree age and bryophyte cover. J. Trop. Ecol. 19: 81-90.

Glime, J. M. 2018. Tropics: Epiphyte Ecology, part 1. Chapt. 8-3. In: Glime, J. M. Bryophyte Ecology. Volume 4. Habitat and Role. Ebooksponsored by Michigan Technological University and the International Association of Bryologists. Last updated 22 July 2020 and available at .

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CHAPTER 8-3 TROPICS: EPIPHYTE ECOLOGY, PART 1 TABLE OF CONTENTS Water Relations ................................................................................................................................................... 8-3-4 Water Content .............................................................................................................................................. 8-3-4 Growth Forms and Life Forms ..................................................................................................................... 8-3-5 Osmotic Potential ....................................................................................................................................... 8-3-10 Desiccation Recovery ................................................................................................................................ 8-3-12 Rainfall Interception .................................................................................................................................. 8-3-12 Fog Interception ......................................................................................................................................... 8-3-14 Microclimate ..................................................................................................................................................... 8-3-15 Nutrient Dynamics ............................................................................................................................................ 8-3-18 Rainfall vs Throughfall .............................................................................................................................. 8-3-19 Nitrogen Dynamics .................................................................................................................................... 8-3-20 Pulse Release ............................................................................................................................................. 8-3-21 Keystone Resource..................................................................................................................................... 8-3-22 Canopy Roots ............................................................................................................................................. 8-3-23 Productivity and Biomass.................................................................................................................................. 8-3-12 Epiphyte Litterfall ............................................................................................................................................. 8-3-31 Summary ........................................................................................................................................................... 8-3-32 Acknowledgments ............................................................................................................................................. 8-3-33 Literature Cited ................................................................................................................................................. 8-3-33

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Chapter 8-3: Tropics: Epiphyte Ecology, part 1

CHAPTER 8-3 TROPICS: EPIPHYTE ECOLOGY, PART 1

Figure 1. Celaque cloud forest in tropical Honduras. Photo by Josiah Townsend, with permission.

Barkman (1958) has contributed the definitive work on cryptogamic epiphytes (bryophytes, lichens) in 628 pages. It provides an account of the ecology and adaptations as they were known at the time and is the "bible" on cryptogamic epiphyte ecology. The work is restricted to temperate regions and does not treat tropical epiphytic bryophytes, which were very little known at the time. Nevertheless, much of the ecological information provided in this book is also valid for the tropics. I was surprised to learn that approximately 10% of the tracheophytes are epiphytes (Prosperi & Michaloud 2001). It was not a surprise to learn that these are almost exclusively tropical, where they represent up to 25% of the tracheophytes. Overall, bryophytes comprised 40% of the epiphytic biomass in a neotropical cloud forest in Costa Rica (Nadkarni 1984) compared to 6% in the leeward cloud forest (Ingram & Nadkarni 1993). In both forests, bryophytes were most abundant among the smallest branches. The gnarled, windblown trees and the frequent mist in the elfin forest provide extremely favorable conditions for bryophytic growth (see Lawton & Dryer 1980).

The epiphytic habitat (Figure 1) is the most diverse one for tropical rainforest bryophytes, with 14 of the 15 main bryophyte families being predominantly epiphytic (Figure 1) (Gradstein & Pócs 1989). This is where the greatest bryophytic biomass of the rainforests occurs (Hofstede et al. 1993). Not surprisingly, the dry weight of epiphytes in the tropics is generally less than that shown in a New Zealand study (Hofstede et al. 2001), where lower temperatures and shorter dry periods are more favorable for bryophytes. In a New Zealand lowland, a single tree supported 61 tracheophyte species compared to 94 nontracheophytes (lichens included). Pócs (1980) found a positive correlation between the amount of "surplus" rainfall (rainfall above 100 mm/month) and the epiphytic biomass in rainforest climates. Among the early studies on bryophytic epiphytes, one must note the Japanese studies (Horikawa 1932, 1939, 1948, 1950; Kamimura 1939; Horikawa & Nakanishi 1954; Hattori & Noguchi 1954; Hattori & Kanno 1956; Hattori et al. 1956; Hattori 1966; Hattori & Iwatsuki 1970; Iwatsuki 1960, 1961, 1962, 1963a, b; Iwatsuki & Hattori 1955, 1956a, b, c, d, e, f, 1957, 1959a, b, 1965a, 1965b, 1966,

Chapter 8-3: Tropics: Epiphyte Ecology, part 1

1968, 1970, 1987; Mizutani 1966). Hosokawa (1950, 1951, 1953, 1954) and coworkers (Hosokawa & Kubota 1957; Hosokawa & Odani 1957; Hosokawa & Omura 1959; Hosokawa et al. 1954, 1957, 1964) pioneered in describing epiphytic communities. Another important early study from Asia is the work by Tixier (1966) on epiphytic communities in Vietnam. Went (1940) discussed the sociology of tracheophytic epiphytes of Java. Gradstein et al. (2007) compared the species richness on various substrates in southern Ecuador. This study demonstrated the preponderance of epiphytes there (Figure 2).

Figure 2. Substrate types of liverworts and hornworts at Reserva Biológica San Francisco, southern Ecuador. Number above each bar is number of species on that substrate type; e = epiphytic (bark); s = soil (incl. humus); r = rock; el = epiphyllous (living leaves); d = decaying wood. From Gradstein et al. 2007.

Frahm (1990a, 1994) found that in Borneo lowland and montane rainforests, even bark texture (smooth, fissured, flaky, or striped) made a difference in the epiphytic communities that developed. All bryophytes were considered to be acidophilic, with epiphytic bryophytes having no significant correlation with pH. On the other hand, rich concentrations of Na, K, and Mg seemed to be important in the substrate. Akiyama et al. (2001) contributed to the knowledge of the Borneo bryophyte flora through two expeditions to the Kinabalu National Park in Malaysia. They reported 203 moss species and 31 liverwort species, with 25 species added to the checklist for the park and 17 new to Borneo. Kürschner and Parolly (1998a) examined pantropical (tropical regions of both Eastern & Western Hemispheres) features that determined distribution of the epiphytic bryophytes. They found that distribution is correlated with structural parameters of the tree stands and with temperature zone intervals. Using only supraspecific taxa (i.e., above the species level) they concluded that communities at low altitudes and those at high altitudes, respectively, resemble each other more pantropically than do lowland and montane communities on the same continent. Kürschner and coworkers were instrumental in elucidating epiphytic bryophyte communities in Africa (Kürschner 1995a, b). Kürschner and Parolly (1999) sought to derive a consistent system for classifying the tropical epiphytes on a pantropical basis. Instead of using species, they used higher classification levels. For the lowland and submontane tropics they recognized the CoenoPtychanthetalia (Figure 3), whereas in the montane zones they recognized the Coeno-Bazzanio-Herbertetalia

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(Figure 4-Figure 5). Using this thinking, they found that the low-altitudinal and high-altitudinal communities are more silimar to each other pantropically than the communities of lowland and montane vegetation units occurring on the same continent.

Figure 3. Ptychanthus striatus; the Pychanthalia synusia is typical in the lowland and submontane tropics, with pantropic distribution. Photo by Li Zhang, with permission.

Figure 4. Bazzania sp. from the Neotropics, a genus characteristic of the Coeno-Bazzanio-Herbertetalia in the montane zone. Photo by Michael Luth, with permission.

Figure 5. Herbertus aduncus, in a genus characteristic of the Coeno-Bazzanio-Herbertetalia in the montane zone. Photo by Barry Stewart, with permission.

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Chapter 8-3: Tropics: Epiphyte Ecology, part 1

Much remains to be found among the tropical bryophytes. Lee and Pócs (2018) have recently added to our knowledge of the distribution of the large genus Lejeunea (Figure 6), describing the new species Lejeunea konratii from Fiji.

Figure 6. Lejeunea flava; L. konratii was a new species in Java in 2018. Photo by Jia-dong Yang, through Creative Commons.

Some epiphytic bryophytes are facultative, growing on other types of substrate. Ando (1969) reported that the epiphytic bryophytes on Buxus microphylla var. insularis (=B. sinica var. insularis; Figure 7) also grew on limestone ridges in Taishaku.

Figure 7. Buxus microphylla. Epiphytic mosses of this species also grow on limestone ridges. Photo by Sage Ross, through Creative Commons.

Frahm and Kürschner (1989) investigated factors related to bryophyte success on trees. Rhoades (1995) provided an extensive review on the nontracheophyte epiphytes of the canopy, including distribution, abundance, and ecological roles, but this paper mainly focuses on temperate forests.

Water Relations The distribution of epiphytic bryophytes in the tropics seems to be all about water. The bryophytes in the crowns of the trees generally are more desiccation-resistant than are those at the tree base (Hosokawa & Kubota 1957; Hosokawa et al. 1964). Water is always a primary limiting factor for epiphytes, and in the tropics the daily change from wet to dry can be particularly problematic (Johnson & Kokila 1970). For some species in the saturated rainforests, as little as 4 hours of exposure to a relative humidity of 63% or less can result in damage. Thus, such sensitive species often live on the wettest sides of the trees. Within a range of 10-76% humidity for four hours, two groups of mosses emerged. One group had low resistance, but the other had a high resistance to desiccation. This latter group of species grew in microhabitats of the forest with low humidity. Löbs et al. (2019) opined that our understanding of the role of the extensive epiphytic bryophyte cover was largely unknown, noting their potential importance in biosphereatmosphere exchange, climate processes, and nutrient cycling. Their water content could have important impact on local, regional, and even global biogeochemical processes. The researchers measured a vertical gradient from the Amazon Tall Tower Observatory in the Amazonian rainforest and determined that only minor variations occurred in the monthly average ambient light intensity above the canopy, but that different patterns emerged at different heights. At 1.5 m, the values were extremely low, exceeding 5 µmol m-2 photosynthetic photon flux density only 8% of the time. These values differed little throughout the year. The temperatures likewise showed only minor variation throughout the year, with larger values and more height dependence during the dry season. Water levels, on the other hand showed more variability. At higher levels they were affected by the frequency of wetting and drying; at low levels near the forest floor they retained water over a longer time period. They concluded that water content is the deciding factor for overall physiological activity, with light intensity determining whether net photosynthesis or dark respiration occurs. Temperature was of only minor importance. Light was limiting on the forest floor; in the canopy the bryophytes had to withstand a larger variation in microclimatic conditions. Water Content Klinge (1963) reported on the epiphyte humus from El Salvador. Their role in forest water and nutrient dynamics, however, seemed to attract little attention. Water content of bryophytic epiphytes in an old-growth forest in Costa Rican cloud forest reached maximum values of 418% of dry weight, with a minimum of 36% (Köhler et al. 2007). The epiphytic bryophytes experienced more dynamic wetting and drying cycles than did the canopy humus. The maximum water loss from bryophytes through evaporation was 251% (dry weight), whereas it was only 117% from the canopy humus, following three days of sunny weather with no intervening precipitation. Pócs (1989) estimated that high altitude epiphytic bryophytes in Tanzania can absorb up to 30,000 L ha-1 of water during one rainstorm. When high humidity and high

Chapter 8-3: Tropics: Epiphyte Ecology, part 1

temperatures occur at the same time, as they often do, they cause respiratory losses that cannot be balanced by photosynthesis in these C3 plants, thus limiting their productivity, especially in the lowland forests (Richards 1984, Frahm 1990b). Karger et al. (2012) measured the relationship of bryophyte cover to air humidity at two elevation ranges in the tropics. When the highland site (1800-3500 m asl) was considered separately from the lowland site (95 taxa) are of xerotropical origin. Many are unique relicts of a formerly more widely distributed flora and are concentrated primarily in the escarpment mountains of the Arabian Peninsula and Socotra Island. Magdum et al. (2017) colleted nine species of corticolous mosses in Panhalgad in the Western Ghats, India, in different seasons, providing the first record of the mosses from the Kolhapur District. These mosses were Pogonatum microstomum, Campylopus flexuosus (Figure 35), Leucobryum bowringii (Figure 36), Fissidens bryoides (Figure 37), Fissidens macrosporoides, Loiseaubryum nutans, Anomobryum auratum (Figure 38), Bryum capillare (Figure 39), and Bryum uliginosum (Figure 40).

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Chapter 8-5: Tropics: Epiphyte Geographic Diversity

Figure 35. Campylopus flexuosus, an epiphyte in Panhalgad of the Western Ghats. Photo by Štĕpán Koval, with permission.

Figure 38. Anomobryum auratum in India, an epiphyte in Panhalgad of the Western Ghats. Photo by Michael Lüth, with permission.

Figure 39. Bryum capillare, an epiphyte in Panhalgad of the Western Ghats. Photo by Michael Lüth, with permission.

Figure 36. Leucobryum bowringii, an epiphyte in Panhalgad of the Western Ghats. Photo through Creative Commons.

Figure 37. Fissidens bryoides, an epiphyte in Panhalgad of the Western Ghats. Photo by Janice Glime.

Figure 40. Bryum uliginosum, an epiphyte in Panhalgad of the Western Ghats. Photo by Štĕpán Koval, with permission.

Chapter 8-5: Tropics: Epiphyte Geographic Diversity

Kürschner (2003) conducted a phytosociological analysis in southwestern Arabia in the Asir Mountains. The characteristic species are drought-tolerant Afromontane mosses, with Orthotrichum diaphanum (Figure 41) and Syntrichia laevipila (Figure 42) being most prominent. Life forms and life strategies correlate with the environment. The Orthotricho-Fabronietum socotranae (see Figure 43) is a drought-tolerant association that is both xerophytic and tolerant of high light. This formation is dominated by cushion, short-turf, and mat-forming perennial stayers that have regular sporophyte production. The Leptodonto (Figure 44)-Leucodontetum schweinfurthii (see Figure 45) association is typical of subhumid areas with sciophytic (shade-loving) vegetation. Its bryophytes are liverworts in addition to the mosses that are predominantly tails or fan-forming pleurocarpous perennial shuttle species. The mosses typically have large spores, adapting them for short-range dispersal that is either passive (with moderately low reproduction) or generative reproduction. This sciophytic group has a much higher diversity of life forms and life strategies than the xerophytic group.

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Figure 43. Fabronia sp.; Fabronia socotrana is a prominent epiphytic species in the Asir Mountains in southwestern Arabia. Photo by Michael Lüth, with permission.

Figure 44. Leptodon smithii; the Leptodon community is typical of the sub-humid area in the Asir Mountains in southwestern Arabia. Photo courtesy of Jeff Duckett and Silvia Pressel. Figure 41. Orthotrichum diaphanum, a species of dry locations in the Asir Mountains of southwestern Arabia. Photo by Michael Lüth, with permission.

Figure 45. Leucodon treleasii; the LeptodontoLeucodontetum schweinfurthii community is typical of the subhumid area of the Asir Mountains in southwestern Arabia. Photo by Jan-Peter Frahm, with permission.

Figure 42. Syntrichia laevipila with capsules, a prominent species in the Asir Mountains in southwestern Arabia. Photo by Michael Lüth, with permission.

Additional references that may be useful regarding tropical epiphyte diversity in the Asian region include Frahm (1990 – Malaysia), Tixier (1966 – Indonesia), Osada & Amakawa (1956 – Tsushima Islands, Japan).

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African Region Exploration of tropical African bryophytes is relatively new. Augier (1974) listed corticolous (growing on bark) bryophytes in the submontane forest of western Cameroon (Figure 46). Akande et al. (1982) examined corticolous bryophytes in Ibadan, Nigeria. On the 8 phorophytes on two sites they examined, they identified 20 bryophyte species. Entodontopsis nitens (Figure 47) is common and present on both sites. They considered Frullania dilatata (Figure 48-Figure 49) and Entodontopsis tenuinervis to be accidental species. They found the pH of the bryophytes to be similar to that of their bark substrate. In 28 comparisons, 11 bryophyte species combinations have a similarity of 50% or more. Entodontopsis nitens and Pelekium gratum (Figure 50) have a high degree of association, as do E. nitens and Mastigolejeunea florea (see Figure 51), Entodontopsis nitens and Erythrodontium barteri, Entodontopsis nitens and Calymperes palisotii (Figure 52-Figure 53), and Erythrodontium barteri and M. florea. Light is important in determining the height of the bryophytes on the trees. There seems to be no indication of preference for tree species, but the number of trees sampled was limited.

Figure 47. Entodontopsis nitens, a common epiphytic species in Ibadan, Nigeria. Photo from Wilding et al. 2016, with permission.

Figure 48. Frullania dilatata on smooth bark, a species considered to be accidental in this habitat in Ibadan, Nigeria. Photo by Bernd Haynold, through Creative Commons.

Figure 46. Menchum Falls, NW Province, Cameroon. Photo by Nick Annejohn and family, through public domain.

Figure 49. Frullania dilatata lobules. Photo by Hermann Schachner, through Creative Commons.

Chapter 8-5: Tropics: Epiphyte Geographic Diversity

Figure 50. Pelekium cf. gratum, a species that shares a 50% similarity index with Entodontopsis nitens. Photo by Shyamma L., through Creative Commons.

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Figure 53. Calymperes palisotii, a species that shares a 50% similarity index with Entodontopsis nitens. Photo by Scott Zona, through Creative Commons.

Odu (1985) found a greater species richness of epiphytic bryophytes in lowland and freshwater forests than in the mangrove forests of the Niger Delta in Nigeria (Figure 54). He suggested that atmospheric humidity and air impurities may be influencing the bryophytes found. Calymperes (Figure 52-Figure 53, Figure 55) and Octoblepharum (Figure 56) occur all over the Niger Delta, whereas others are restricted to the lowland freshwater forests. Those in the mangrove forests require adaptations that permit their tolerance of salt water. Further discussion of the mangrove forest is in the Tropics subchapter Hydric and Xeric Habitats.

Figure 51. Mastigolejeunea repleta; M. florea shares a 50% similarity index with Entodontopsis nitens. Photo by Y. M. Wei, courtesy of Robbert Gradstein.

Figure 54. Mangrove roots in the Niger Delta, Nigeria. Photo through Creative Commons.

Figure 52. Calymperes palisotii on bark. Photo by Scott Zona, through Creative Commons.

Figure 55. Calymperes tenerum, a common species in the mangrove forests of Thailand. Photo from the Auckland Museum, through Creative Commons.

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Chapter 8-5: Tropics: Epiphyte Geographic Diversity

Figure 56. Octoblepharum albidum, a common species in the mangrove forests of Thailand. Photo by M. C. Nair, K. P. Rajesh, and P. V. Madhusoodanan, through Creative Commons.

Akinsoji (1991) reported 26 tracheophytic epiphytes from a tropical rainforest in southwestern Nigeria. As noted elsewhere regarding bryophytes, bark texture makes a difference. Akinsoji found that rough bark is able to collect soil, nutrients, and moisture for epiphytic growth, all features that could benefit bryophytes as well. Trees with smooth bark lacked debris and dust accumulation or moisture retention and had only one or two epiphytes. More recently, Ezukanma et al. (2019a, in review) examined corticolous bryophytes in agroforests of southwestern Nigeria. Only 14 bryophytes were identified. Seven leafy liverwort species were present, but in only two families – Lejeuneaceae (Figure 14, Figure 51) and Radulaceae (Figure 24). Similarly, seven moss species were found, but they were distributed in five families – Calymperaceae (Figure 52-Figure 53), Entodontaceae (Figure 57), Fissidentaceae (Figure 16), Hypnaceae (Figure 58), and Leucomiaceae (Figure 59) with one species each, and Plagiotheciaceae (Figure 60) with two species. Cashew forests (Figure 61) had eight species, kola (Figure 62) had seven, and cocoa (Figure 63) had six. Only the liverworts Thysananthus nigrus (see Figure 64) and Mastigolejeunea auriculata (Figure 65) were found in all three forest types. Entodontopsis nitens (Figure 47) was the most frequent species, occurring in the kola forest and having a frequency of 27.6%. Next in frequency were Mastigolejeunea auriculata (23.65%) and Entodontopsis nitens (18.92%) in the cocoa agroforest.

Figure 58. Chryso-hypnum diminutivum (Hypnaceae) from the Neotropics; this family is frequent on trees in the agroforests of Nigeria. Photo by Michael Lüth, with permission.

Figure 57. Entodon sp. (Entodontaceae); this family is frequent on trees in the agroforests of Nigeria. Photo by Cindy Hough, through Creative Commons.

Figure 60. Plagiothecium undulatum (Plagiotheciaceae), a family that occurs on trees in agroforests in Nigeria. Photo from Proyecto Musgo, through Creative Commons.

Figure 59. Leucomium strumosum (Leucomiaceae), a family that occurs on trees in agroforests in Nigeria. Photo by Claudio Delgadillo Moya, with permission.

Chapter 8-5: Tropics: Epiphyte Geographic Diversity

Figure 61. Cashew trees in Brazil. Photo by Ben Tavener, through Creative Commons.

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Figure 64. Thysananthus repletus (= Mastigolejeunea repleta) from China; Thysananthus nigrus is present in all three forest types in southwestern Nigeria. Photo by Y. M. Wei, courtesy of Robbert Gradstein.

Figure 62. Kola (Cola nitida) plantation in Malaysia. Photo by Michael Hermann, through Creative Commons.

Figure 65. Mastigolejeunea auriculata, a liverwort found in all three of these types of agroforests in Nigeria. Photo by Paul Davison, with permission.

Figure 63. Cacao plantation in Cameroon. Barada-Nikto, through Creative Commons.

Photo by

Ezukanma et al. (2019b, in press) also assessed the epiphytic bryophytes in the urban agroforests of Ibadan, Nigeria. They studied the corticolous bryophytes up to 2m on the phorophytes of 30 trees in Citrus (Figure 66) and Mangifera (Figure 67) plantations. Here they identified 19 species, 13 leafy liverworts and 6 mosses. Five species

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were in both forest types. The mango forests had higher bryophyte diversity and more even distribution of species. The researchers suggested that this might relate to the frequent pruning of the crowns in the mango agroforest. The moss Calymperes palisotii (Figure 52-Figure 53) was the most abundant species, especially in the Citrus plantations. Corticolous species were generally absent at the base of the phorophyte, occurring with a mean height of 1.39 m (range of 1.17-1.60) on Mangifera and 1.11 m (range of 0.48-1.8) on Citrus. The moss Rhacopilopsis trinitensis (Figure 68) had the highest mean height, extending up to 1.8 m. Ceratolejeunea beninensis (see Figure 80-Figure 81) was second in abundance, likewise in the Citrus forest. As in the cashew, kola, and cacao forests, Mastigolejeunea auriculata (Figure 65; in the Mangifera forests) and Entodontopsis nitens (in the Citrus forests; Figure 47) were species with high frequencies. There were 13 liverwort species, 12 in Lejeuneaceae (Figure 14, Figure 51) and 1 in Jubulaceae (Figure 69). The six moss species were in four families, with 3 in Stereophyllaceae (Figure 47) and 1 each in Calymperaceae (Figure 52Figure 55, Figure 82), Hypnaceae (Figure 58), and Leucomiaceae (Figure 59). Twelve species occurred in both forest types. Figure 68. Rhacopilopsis trinitensis, the species that reaches the greatest heights on Mangifer and Citrus phorophytes. Photo by Juan David Parra, through Creative Commons.

Figure 66. Citrus (orange) plantation. Braxmeier, through Creative Commons.

Photo by Hans Figure 69. Jubula hutchinsiae (Jubulaceae), a family that occurs on Citrus trees in Nigeria. Photo by Jonathan Sleath, with permission.

Figure 67. Mangifera (mango) picking, Réunion Island. Photo by B. Navez, through Creative Commons.

Biedinger and Fischer (1996) compared the diversity of epiphytic tracheophytes, bryophytes, and lichens in the montane rainforests and dry forests of Rwanda and Zaïre They identified 167 species of tracheophytes, 45 of mosses, 82 of liverworts, 78 corticolous lichens, and 57 epiphyllous lichens. While the numbers may be replaced with more recent studies, the proportions are likely to be more accurate. In South Africa, Dilg and Frahm (1997) explored the epiphytic flora in southern Drakensberg. They found only 38 species, 12 of which were liverworts and 26 were mosses. The Podocarpus (Figure 70) forest provides a habitat with high humidity and fire protection; it has the highest number of bryophyte species.

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Andes of Colombia increases with altitude. Wolf (2003) found that the greatest liverwort diversity occurs in the transition zone where two distinct floras are in contact. Sillett et al. (1995) examined the bryophyte communities of six Ficus tuerckheimii (Figure 72) trees in a Costa Rican lower montane wet forest. They found 109 species on the three intact forest trees and only 76 on the three isolated trees. Of these, 52 species occurred only on the intact forest trees; 18 were only on the isolated trees. Species richness, cover, and frequency of pendants, tall turfs, tails, and fans were significantly higher on the trees in the intact forest. Isolated trees had higher rates of evaporation from the inner crowns, more macrolichen cover, and higher levels of sunlight compared to the intact forest trees. Ordination analysis revealed a desiccation gradient ranging from the sheltered intact forest trees to the exposed isolated trees.

Figure 70. Podocarpus cunninghamii trunk with epiphytic bryophytes. Photo by Rudolph89, through Creative Commons.

In addition to these studies, Frahm (1994) reported on ecology of epiphytic bryophytes on Mt. Kahuzi in Zaire. Additional references that may be useful regarding epiphytic diversity in the African tropics include Kürschner (1984 – Saudi Arabia; 1990a – moss societies on Mt. Kinabalu, North Borneo; 1995 – Eastern Congo), Pócs & Szabo (1993 – Mt Elgon, Kenya), Gill & Onyibe (1986 – phytosociology of epiphytes on oil palm in Benin City, Nigeria), Ezukanma (2012 – agroecological corticolous species in southwestern Nigeria). A number of references by Ah-Peng and coworkers will be addressed in other appropriate subchapters of this chapter. Neotropics The Neotropics are rich in bryophyte species. In a sixhectare upper montane Quercus forest (Figure 71) in Costa Rica, Holz et al. (2002) found 206 species, comprised of 100 moss species, 105 liverwort species, and 1 hornwort. They found three main groups of microhabitats in the forest: forest floor, including the tree base; the phyllosphere (space surrounding the leaf); other epiphytic habitats. Life forms differ with the humidity and light levels, as discussed in earlier subchapters. Van Reenen (1987) noted that the epiphytic cover of bryophytes in the

Figure 71. Quercus copeyensis; in Costa Rica; the Quercus forest is home to more than 200 bryophyte species. Photo through Creative Commons.

Delia et al. (2015) reported 34 epiphytic moss species from El Zancudo, Honduras. They concluded that the montane rainforest that borders Honduras and El Salvador is bryologically diverse, but is largely unexplored.

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Figure 73. Guyana waterfall and forest near Paramakatoi. Photo by Kevin Gabbert, through public domain.

Large trees support more species than small ones, with a typical logistic curve of increasing numbers of species related to both plot size and tree DBH (diameter at breast height) (Figure 74) (Gradstein et al. 1996).

Figure 72. Ficus tuerckheimii, Costa Rica. Photo by Dick Culbert, with online permission.

Richards (1954) considered the Moraballi Creek in Cooperative Republic of Guyana to have four main bryophyte synusiae (structural units of major ecological community characterized by relative uniformity of life form or height): high epiphytes, shade epiphytes, epiphylls, dead wood communities. Although these communities are very distinct in both structure and composition, several species, such as Calymperes lonchophyllum (see Figure 52-Figure 55) and Octoblepharum albidum (Figure 56), occur in all but the epiphyllous synusiae. The epiphyllous species are highly specialized, as will be discussed in a later subchapter. Korpelainen and Salazar Allen (1999) demonstrated genetic variation in three species of Octoblepharum, perhaps explaining their ability to occur in multiple community types. Richards (1954) found that Moraballi Creek synusiae differ in their growth (and life) forms of the species, creating differences in community structure. This results in differences between the very dry habitat of the high epiphyte synusiae and the more moderated shade epiphyte synusiae. The latter is characterized by freely projecting or dangling shoots and large thin-walled cells. The Moraballi Creek rainforest bryophyte synusiae differ markedly from those of temperate forests by the absence of ground-dwelling bryophyte synusiae, the presence of epiphyllous bryophytes, and the preponderance of liverworts, especially Lejeuneaceae (Figure 14, Figure 51). In a semi-deciduous tropical forest of southern Guyana (Figure 73), Sipman (1997) found 100 species of lichens, with 8 out of 14 trees lacking lichens on leaves completely, whereas 3 had 34-46 taxa! Instead, the foliicolous lichens are most likely to grow close to the ground. In contrast to the 34-46 species of lichens on a single tree, they were able to find only 18 bryophyte taxa on canopy leaves.

Figure 74. Relationship between number of epiphyte species and plot size and tree DBH in Mexico. Species-area curves are solid symbols, cumulative number of species vs cumulative diameter of all trees sampled are open symbols. Squares represent humid montane cloud forest; circles represent humid lowland forest. Modified from Gradstein et al. 1996.

Gradstein et al. (1990) investigated the epiphytic bryophytes in the dry evergreen forest and mixed forest of the Guianas (Figure 73) using mountaineering techniques. They discovered that the lowland rainforest is not as poor in species as had been thought, once the bryophytes of the canopy are included in the exploration. More than 50% of the local species may occur in the canopy. The mixed forest has the most species. A single tree can support up to 67 species, with 50 species being an average number. The 28 trees sampled supported 154 species of bryophytes. Only a few trees are needed to find most of the species of the local area. Most of the species in this area are rather common, with 80% being widespread in the Neotropics. In the Colombian Amazon (Figure 75), Campos et al. (2015) established 384 plots on 64 trees in four localities.

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These exhibited 160 species of epiphytic bryophytes, with a preponderance of liverworts (116 species; 44 species of mosses). These included collections from the base to the outer canopy, including 16 trees at each locality. The highest representation of families (Figure 76) included the leafy liverworts Lejeuneaceae (Figure 14, Figure 51) (55%) and Lepidoziaceae (Figure 2) (8%), and the mosses Calymperaceae (Figure 52-Figure 55) (10%), Octoblepharaceae (Figure 56) (6%), and Sematophyllaceae (Figure 10) (5%). The most common genera were members of Lejeuneaceae – Cheilolejeunea (Figure 77) (11%), Pycnolejeunea (Figure 78) (8%), Archilejeunea (Figure 79) (8%), and Ceratolejeunea (Figure 80-Figure 81) (8%) – and the moss Syrrhopodon (Calymperaceae; Figure 82) (7%).

Figure 77. Cheilolejeunea frangrantissima, in one of the most common genera of Lejeuneaceae in the Colombian Amazon. Photo by Scott Zona, with permission.

Figure 75. Lowland rainforest in Colombian Amazon. Photo by Laura Campos, courtesy of Robbert Gradstein. Figure 78. Pycnolejeunea pilifera, member of a common leafy liverwort genus in the mangrove forests of Thailand. Photo by MNHN – Paris, Muséum National d'Histoire Naturelle, MB, through Creative Commons.

Figure 76. Species richness per family in 4 locations of Colombian Amazon. Modified from Campos et al. 2015.

Figure 79. Archilejeunea japonica, in one of the most common genera of Lejeuneaceae in the Colombian Amazon. Photo from Digital Museum, Hiroshima University, with permission.

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Figure 80. Ceratolejeunea cubensis, in one of the most common genera of Lejeuneaceae in the Colombian Amazon. Photo by Scott Zona, with permission.

Figure 81. Ceratolejeunea cubensis, showing lobules at leaf insertions. Photo by Scott Zona, with permission.

Figure 82. Syrrhopodon gaudichaudii, in one of the most common genera in the Colombian Amazon. Photo from Michael Lüth, with permission

Wolf et al. (2003) found that the richness per surface area decreases significantly with branch diameter (Figure

83) in the upper montane rainforest of the Cordillera in Colombia. Diversity is highest when the standing crop is at intermediate levels and is negatively correlated with the area of the largest species. On the other hand, evenness (similarity of frequencies of different units making up population or sample) is less on older branches. The inner canopy species have the smallest niche widths. When only branch segments are sampled, the vegetation is highly variable, whereas that on whole trees is more uniform. The species follow a species area curve that approaches a flat line after sampling only four trees. The liverworts have the greatest richness in the contact transition zone between two distinct floras. Wolf and coworkers suggested that the arrival time of aggressive competitors such as those that form large patches may be "crucial." Many accidental species maintain a high richness and suggest that dispersal of propagules is important in creating richness.

Figure 83. Branch or trunk diameter in the canopy of the upper montane rainforest and Simpson's index of diversity. Open circles indicate a group of seven samples that do not adhere to increasing dominance with diameter. Modified from Wolf et al. 2003.

In flooded (Figure 84) and "tierra firme" (upland habitat where elevation does not allow water, even during high water season, to inundate forest; Figure 85) forests of the Colombian Amazon, Benavides et al. (2004) found 109 bryophyte species on 14 0.2-ha plots. Mosses and liverworts had opposite responses to moisture, with many more liverworts than moss species in the tierra firme, but total richness (mosses + liverworts) differed little between the flooded and non-flooded habitats (Figure 86). The use of the habitat differed between the two forest types, with differences in humidity being the major factor in determining bryophyte communities. Nevertheless, soil was a little-used substrate for both groups in both habitats (Figure 86). Epiphyll species assemblages (e.g. Figure 87) were not strongly affected by floodplain vs tierra firme. Life forms differed between the two habitat types, with more fan and mat bryophyte species in the floodplains, and more epiphytic liverworts (hence, almost no wefts) in the tierra firme forest (Figure 88).

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Figure 87. Epiphylls on leaf. Photo by Jessica M. Budke, with permission. Figure 84. Várzea forest with açaí palms, the flooded forest of the Amazon. Photo by Frank Krämer through Creative Commons.

Figure 85. Amazon rainforest, Brazil. Photo by Phil P. Harris, through Creative Commons. Figure 88. Distribution of bryophyte life forms in tierra firme and floodplain in the Aracuara region of Colombia. Modified from Benavides et al. 2004.

Figure 86. Distribution of bryophyte substrates in tierra firme and floodplain in the Aracuara region of Colombia. Modified from Benavides et al. 2004.

Oliveira and ter Steege (2013) determined that epiphytic bryophytes in the tierra firme forests of the Amazon Basin exhibited a typical species abundance distribution (Figure 89). Kelly et al. (2004) described the epiphytic communities of a montane rainforest in the Venezuelan Andes (Figure 90). They surveyed 20 trees, all in a site of only 1.5 ha at 2600 m asl. The non-tracheophyte epiphytes were recorded in 95 sample plots and yielded 22 moss and 66 liverwort species, as well as 46 species of macrolichens. Few of the bryophytes in these communities are endemic (native distribution restricted to a certain country or area), although they are mostly restricted to the Neotropics. The dominant bryophyte on the lower trunks is Syrrhopodon gaudichaudii (Figure 91), along with the fern Elaphoglossum hoffmannii (Figure 92). The intermediate levels are dominated by the leafy liverwort Omphalanthus filiformis (Lejeuneaceae; Figure 93) and the orchid Maxillaria miniata (see Figure 94). The upper crowns are dominated by the lichens Usnea (Figure 95) and Parmotrema (Figure 96). Diversity of non-tracheophytes is

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greatest in the upper crowns; tracheophyte diversity is greatest at the intermediate levels. As noted in a number of other studies cited herein, similarity is low among plots of the same community, but between-tree and between-stand similarities are relatively high.

Figure 89. Species abundance distribution based on the complete dataset. Axis x is species ranked by number of records. Modified from Mota de Oliveira and ter Steege 2013.

Figure 92. Elaphoglossum hoffmannii, a fern that typically accompanies Syrrhopodon gaudichaudii on lower trunks in montane rainforests in the Venezuelan Andes. Photo by Robbin Moran, with permission.

Figure 90. Montane rainforest in Venezuelan Andes. Photo by Jorge Paparoni, through Creative Commons.

Figure 93. Omphalanthus filiformis, a dominant leafy liverwort at intermediate levels of tree trunks in a montane rainforest in the Venezuelan Andes. Photo by Michael Lüth, with permission.

Figure 91. Syrrhopodon gaudichaudii, the dominant bryophyte on the lower trunks in a montane rainforest in the Venezuelan Andes. Photo by Michael Lüth, with permission.

Figure 94. Maxillaria molitor; Maxillaria miniata is the dominant flowering plant species, along with the leafy liverwort Omphalanthus filiformis, at intermediate levels in the montane rainforest of the Venezuelan Andes. Photo from Megadiverso, through Creative Commons.

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In 2017, Gradstein and Benitez added 15 liverwort species to the known flora of Ecuador. They furthermore described two species new to science. One might not think of looking in a savannah for epiphytes because of the high exposure to sunlight and low moisture. Nevertheless, bryophytic epiphytes do grow there in an Amazonian savanna in Brazil (Figure 97). Gottsberger and Morawetz (1993) found that lichens dominate on the young trees, typically becoming less abundant as the tree ages. Bryophytes are most abundant on older trees and seem to suppress the lichen growth.

Figure 95. Usnea from Cumbre Vieja, Canary Islands. Members of this genus dominate the crowns of the montane rainforest in the Venezuelan Andes. Photo by Fährtenleser, through Creative Commons.

Figure 97. Amazonian savannah (Cerrado) in Brazil. Photo by Paulo Q Maio, through Creative Commons.

Additional references that may be useful regarding tropical diversity in the Neotropical epiphytes include Chung (1996 – Panama), Wolf (1993 – Colombia); JovetAst (1949 – groupings of epiphytic mosses in the French West Indies); Frahm (1987a, b – composition of moss vegetation in Peruvian rainforests); Frahm (1987a, c – composition of moss vegetation in Peruvian rainforests).

Figure 96. Parmotrema perlatum. Members of this lichen genus dominate the crowns of the montane rainforest in the Venezuelan Andes. Photo by Alan J. Silverside, with permission.

By comparison, Costa (1999) studied the epiphytic bryophyte diversity of both primary and secondary lowland rainforests in southeastern Brazil, a subtropical region. Unlike many earlier studies, hers included the forest canopy. She found 75 bryophyte species, 39 mosses and 36 liverworts. The highest species richness is exhibited by the mature secondary hillside rainforest, with 43 species. The highly degraded hillside rainforest has the lowest diversity, with only 6 species, and the hillside secondary rainforest with only 5 species. As in so many other studies, the leafy liverwort family Lejeuneaceae (Figure 14, Figure 51) is the "most important" with 23 species (30 %) and the moss family Sematophyllaceae (Figure 10) with 7 species (10%). Demonstrating the importance of the canopy species in understanding species diversity, Costa found that 45% of the bryophyte species occurred exclusively in the canopy. The most common life form is the mat, describing 45% of the species. Forest destruction is more detrimental to shade species than to sun species. Even after 20-45 years, many bryophytes had not returned, but after 80 years the communities were similar to those of primary forest.

Summary Full understanding of the bryogeography of epiphytes is still hampered by our need for comprehensive systematic studies that identify synonyms and demonstrated genetic relatedness. In Australian tropical rainforests, epiphyte succession is usually rapid, with seven genera occurring in all the major rainforest types (including non-tropical ones): Macromitrium, Racopilum, Hymenodon, Pyrrhobryum, Rhizogonium, Sematophyllum, and Thuidium (Pelekium?). In general, the mosses in Pterobryaceae and Neckeraceae occur as epiphytes throughout the tropics, along with Sematophyllum and Taxithelium. The liverworts Frullania and Lejeuneaceae dominate the branches. The tribe Ptychantheae is predominant among Asian Lejeuneaceae, whereas the tribe Brachiolejeuneae predominates in the Neotropics. In Indonesia, the characteristic low-elevation tree-base moss families are Calymperaceae, Fissidentaceae, Hypopterygiaceae, Leucobryaceae, Meteoriaceae, Neckeraceae, Pterobryaceae, and Thuidiaceae, and the leafy liverwort families Lejeuneaceae, Lophocoleaceae, Porellaceae, and Radulaceae. By

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contrast the higher elevations have mostly leafy liverworts in Herbertaceae, Lepidoziaceae, Mastigophoraceae, Scapaniaceae, Schistochilaceae, and Trichocoleaceae. In Africa, Calymperes and Octoblepharum species occur all over the Niger Delta, whereas in agroforests Ezukanma et al. (2019 in review) found only Lejeuneaceae and Radulaceae among the liverworts, but found five families of mosses. African studies are limited and promise many more species on future expeditions. Bryophyte diversity in the Neotropics is particularly rich and increases with altitude. Intact forests typically have pendants, tall turfs, tails, and fans. Calymperes lonchophyllum and Octoblepharum albidum are common in all communities except as epiphylls. Larger trees support more species than do small ones by providing more niches. For the Neotropics in general, the Lejeuneaceae are again the most species-rich family; the most highly represented moss families are Calymperaceae, Octoblepharaceae, and Sematophyllaceae. Fewer endemics occur here compared to those of the flowering plants, and as more systematic studies occur, the number is diminishing.

Acknowledgments My appreciation goes to Noris Salazar Allen for her efforts to make this chapter reliable and up-to-date. Her helpful discussions kept me going on this part of the world I know so little about. Andi Cairns helped me to resolve some of the apparent conflicts in the Australian literature and bring information up to date.

Literature Cited Akande, A. O., Olarinmoye, S., and Egunyomi, A. 1982. Phytosociological studies on some corticolous bryophytes in Ibadan, Nigeria. Cryptog. Bryol. Lichénol. 3: 235-248. Akinsoji, A. 1991. Studies on the epiphytic flora of a tropical rain forest in southwestern Nigeria. II. The bark microflora. Vegetatio 92: 181-185. Ariyanti, N. S., Bos, M. M., Kartawinata, K., Tjitrosoedirdjo, S. S., Guhardja, E., and Gradstein, S. R. 2008. Bryophytes on tree trunks in natural forests, selectively logged forests and cacao agroforests in Central Sulawesi, Indonesia. Biol. Conserv. 141: 2516-2527. Augier, J. 1974. Bryophytes corticoles a l'etage submontagnard dans l'ouest Camerounais. [Corticolous bryophytes at the submontane stage in western Cameroon]. Ann. Fac. Sci. Univ. Fed. Cameroun 17: 97-93. Benavides, J. C., Idarraga, A., and Alvarez, E. 2004. Bryophyte diversity patterns in flooded and tierra firme forests in the Araracuara Region, Colombian Amazonia. Trop. Bryol. 25: 117-126. Biedinger, N. and Fischer, E. 1996. Epiphytic vegetation and ecology in central African forests (Rwanda, Zaire). Ecotropica 2: 121-142. Campos, L. V., Steege, H. ter, and Uribe, J. 2015. The epiphytic bryophyte flora of the Colombian Amazon. [Los briófitos epífitos de la región Amazónica de Colombia.]. Caldasia 37: 47-59.

Cairns, A., Meagher, D., and Ramsay, H. 2019. A revised checklist of the moss flora of the Australian Wet Tropics. Telopea 22: 1-30. Chung, C. C. 1996. Musgos epifitos de un sendero de interpretación, Parque Nacional Altos de Campaña, Panama. Un report preliminar. [Epiphytic mosses of an interpretation trail, Altos de Campana National Park, Panama. A preliminary report.]. Briolatina 39: 5-7. Churchill, S. P. and Salazar Allen, N. 2001. Mosses. In Gradstein, S. R., Churchill, S. P., and Salazar Allen, N. Guide to the Bryophytes of Tropical America. Mem. N. Y. Bot. Gard. 86: 240-571. Costa, D. P. 1999. Epiphytic bryophyte diversity in primary and secondary lowland rainforests in southeastern Brazil. Bryologist 102: 320-326. Delia, R., Búcaro, R., Touw, A., and Stech, M. 2015. Epiphytic mosses from the understory of a forest in El Zancudo ("Los Bolsones"), La Paz, Honduras. Bryo. Div. Evol. 36: 45-50. Dilg, C. and Frahm, J.-P. 1997. Untersuchungen zur Flora der epiphytischen Moose der südlichen Drakensberge (Südafrika). Investigations on the flora of the epiphytic mosses of the southern Drakensberg (South Africa).]. Trop. Bryol. 13: 35-45. Ezukanma, I. O. 2012. Survey of corticolous bryophytes in selected agroecological sites in Ibadan, Southwestern Nigeria. M.Sc. Thesis. Dept. of Botany. University of Ibadan. xix+95pp Ezukanma, I. O., Tessler, M., Salaam, A. M., Chukwuka, K. S., and Ogunniran, A. J. 2019a. Diversity of corticolous bryophytes of selected lowland agroforests in Southwest, Nigeria. (in review). Ezukanma, I. O., Tessler, M., Salaam, A. M., Chukwuka, K. S., and Ogunniran, A. J. 2019b. Epiphytic bryophytes of urban agroforests in Ibadan, Southwest, Nigeria. J. Bryol. (in press). Frahm, J.-P. 1987a. Ökologische Studien an der epiphytische Moosvegetation in Regenwäldern NE-Perus. [Ecological studies on the epiphytic moss vegetation in rainforests of NO-Peru.] In: Ergebnisse der BRYOTROP Expedition nach Peru 1982. Beih. Nova Hedw. 88: 143-158. Frahm, J.-P. 1987b. Struktur und Zusammensetzung der epiphytischen Moosvegetation in Regenwäldern NO-Perus. [Structure and composition of epiphytic moss vegetation in rainforests of NO-Peru.]. Nova Hedw. Beih. 88: 115-141. Frahm, J-P. 1990. The ecology of epiphytic bryophytes on Mt. Kinabalu, Sabah (Malaysia). Nova Hedw. 51: 121-132. Frahm, J.-P. 1994. The ecology of epiphytic bryophytes on Mt. Kahuzi (Zaire). Trop. Bryol. 9: 137-152. Gill, L. S. and Onyibe, H. I. 1986. Phytosociological studies of epiphytic flora of oil palm (Elais guineensis) in Benin City, Nigeria. Feddes Rep. 97: 691-695. Gottsberger, G. and Morawetz, W. 1993. Development and distribution of the epiphytic flora in an Amazonian savanna in Brazil. Flora 188(1): 145-151. Gradstein, S. R. 1991. Diversity and distribution of Asian Lejeuneaceae subfamily Ptychanthoideae. Trop. Bryol. 4: 116. Gradstein, S. R. 1992. The vanishing tropical rain forest as an environment for bryophytes and lichens. In: Bates, J. W. and Farmer, A. M. (eds.). Bryophytes and Lichens in a Changing Environment. Clarendon Press, Oxford, pp. 234258. Gradstein, S. R. and A. Benitez, A. 2017. Liverworts new to Ecuador with description of Plagiochila priceana sp. nov.

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and Syzygiella burghardtii sp. nov. Cryptog. Bryol. 38: 335348. Gradstein, R. and Culmsee, H. 2010. Bryophyte diversity on tree trunks in montane forests of Central Sulawesi, Indonesia. Trop. Bryol. 31: 95-105. Gradstein, S. R., Montfoort, D., and Cornelissen, J. H. C. 1990. Species richness and phytogeography of the bryophyte flora of the Guianas, with special reference to the lowland forest. Trop. Bryol. 2: 117- 126. Holz, I., Gradstein, S. R., Heinrichs, J., and Kappelle, M. 2002. Bryophyte diversity, microhabitat differentiation, and distribution of life forms in Costa Rican upper montane Quercus forest. Bryologist 105: 334-348. Jovet-Ast, S. 1949. Les groupements des muscinées épiphytes aux Antilles françaises. [The groupings of epiphytic mosses in the French West Indies.]. Rev. Bryol. Lichénol. 18: 682686. Kelly, D. L., O'Donovan, G., Feehan, J., Murphy, S., Drangeid, S. O., and Marcano-Berti, L. 2004. The epiphyte communities of a montane rain forest in the Andes of Venezuela: Patterns in the distribution of the flora. J. Trop. Ecol. 20: 643-666. Korpelainen, H. and Salazar Allen, N. 1999. Genetic variation in three species of epiphytic Octoblepharum (Leucobryaceae). Nova Hedw. 68: 281-290. Kürschner, H. 1984. Epiphytic communities of the Asir Mountains (SW Saudi Arabia). Studies in Arabian bryophytes 2. Nova Hedw. 39: 177-200. Kürschner, H. 1990a. Die epiphytischen Moosgesellschaften am Mt. Kinabalu (NordBorneo, Sabah, Malaysia). [The epiphytic moss communities at Mt. Kinabalu (North Borneo, Sabah, Malaysia).]. Nova Hedw. 51: 1-76. Kürschner, H. 2003. Epiphytic bryophyte communities of southwestern Arabia - phytosociology, ecology and life strategies. Nova Hedw. 77: 55-71. Kürschner, H. 2008. Biogeography of South-West Asian bryophytes - with special emphasis on the tropical element. Turk. J. Bot. 32: 433-446. Magdum, S. M., Lavate, R. A., Patil, S. M., and Dongare, M. M. 2017. Biosci. Discov. 8: 796-801. Odu, E. A. 1985. Preliminary studies on the bryophyte flora of the mangrove and fresh water swamp forests in the Niger Delta. In: Wilcox, B. H. D. and Powell, C. P. (eds.). Proceedings of the Workshop on the Mangrove Ecosystem of the Niger Delta, Port Harcourt (Nigeria), 19-23 May 1980, pp. 68-87. Oliveira, S. M. and Steege, H. ter. 2013. Floristic overview of the epiphytic bryophytes of terra firme forests across the Amazon basin. Acta Bot. Brasil. 27: 347-363. Osada,T. and Amakawa, T. 1956. An observation on the ecological distribution of pendulous bryophytes in the Tsushima Islands. J. Hattori Bot. Lab. 17: 52-54. Pócs, T. 1982. Tropical forest bryophytes. In: Smith, A. J. E. (ed.). Bryophyte Ecology. Chapman & Hall, London, pp. 59-104. Pócs, T. 1984. Synopsis of the African Lepidoziaceae K. Müll. Proceedings of the Third Meeting of the Bryologists from Central and East Europe, Praha, 14-18 June 1982, Universita Karlova Praha, pp. 107-119. Pócs, T. and Szabo, A. 1993. The epiphytic vegetation the endemic giant groundsel (Senecio barbatipes) of Mt. Elgon, Kenya. Opera Bot. 121: 189-194.

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Ramsay, H. P. and Cairns, A. 2004. Habitat, distribution and the phytogeographical affinities of mosses in the Wet Tropics bioregion, north-east Queensland, Australia. Cunninghamia 8: 371-408. Ramsay, H. P., Streimann, H., and Harden, G. 1987. Observations on the bryoflora of Australian rain forests. Symp. Biol. Hung. 35: 605-620. Ramsay, H. P., Vitt, D. H., and Lewinsky-Haapasaari, J. 2012. Australian Mosses Online. 47. Orthotrichaceae. . Ramsay, H., Cairns, A., and Meagher, D. 2017. Macromitrium erythrocomum (Bryophyta: Orthotrichaceae), a new species from tropical Queensland, Australia. Telopea 20: 261-268. Reenen, G. B. A. van. 1987. Altitudinal bryophyte zonation in the Andes of Colombia: A preliminary report. In: Pocs, T., Simon, T., Tuba, Z., and Podani, J. (eds.). Proc. IAB Conf. Bryoecology, Symp. Biol. Hung. 35B: 631-637. Richards, P. W. 1954. Notes on the bryophyte communities of lowland tropical rain forest, with special reference to Moraballi Creek, British Guiana. Vegetatio 6: 319-328. Sillett, S. C., Gradstein, S. R., and Griffin, D. III. 1995. Bryophyte diversity of Ficus tree crowns from cloud forest and pasture in Costa Rica. Bryologist 98: 251-260. Sipman, H. J. M. 1997. Observations on the foliicolous lichen and bryophyte flora in the canopy of a semi-deciduous tropical forest. Abstr. Bot. 21: 153-161. Sjögren, E. 1997. Epiphyllous bryophytes in the Azores Islands. ARQUIPÉLAGO. Ciências Biol. Marinhas. [Life Marine Sci.] 15: 1-49. Vitt, D. H. and Ramsay, H. P. 1985a. The Macromitrium complex in Australasia (Orthotrichaceae: Bryopsida). Part 1. Taxonomy and phylogenetic relationships. J. Hattori Bot. Lab. 59: 325-451. Vitt, D. H., Koponen, T., and Norris, D. H. 1995. Bryophyte flora of the Huon Peninsula, Papua New Guinea. LV. Desmotheca, Groutiella, Macrocoma and Macromitrium (Orthotrichaceae, Musci). Acta Bot. Fenn. 154: 1-94. Wilding, N., Hedderson, T., Ah-Peng, C., and Malombe, T. 2016. Bryophytes of Kenya’s coastal forests: A guide to the common species. Indian Ocean Commission, Biodiversity Project, 58 pp. Wolf, J. H. D. 1993. Ecology of epiphytes and epiphytes communities in montane rain forests, Colombia. Ph.D. dissertation, University of Amsterdam, The Netherlands. Wolf, J. H. D. 2003. Diversidad y ecología de comunidades epifíticas en la Cordillera Central, Colombia. [Diversity and ecology of epiphytic communities in the Cordillera Central, Colombia.]. Studies on tropical Andean Ecosystems. Kramer, Vaduz, Alemania, 502 pp. Wolf, J. H., Hammen, T. van der, and Santos, A. G. dos. 2003. Diversidad y ecología de comunidades epifíticas en la Cordillera Central, Colombia. La Cordillera Central Colombiana. [Diversity and ecology of epiphytic communities in the Cordillera Central, Colombia. The Colombian Central Mountain Range.]. Transecto Parque Los Nevados. Estudios de Ecosistemas Tropandinos 5: 453-502. .

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Glime, J. M. and Pócs, T. 2018. Tropics: Epiphylls. Chapt. 8-6. In: Glime, J. M. Bryophyte Ecology. Volume 4. Habitat and Role. Ebooksponsored by Michigan Technological University and the International Association of Bryologists. Last updated 23 July 2020 and available at .

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TABLE OF CONTENTS Epiphyllous Communities ................................................................................................................................... 8-6-2 Fossil Records ..................................................................................................................................................... 8-6-9 Biomass Contributions ........................................................................................................................................ 8-6-9 Microclimate ....................................................................................................................................................... 8-6-9 Colonization ...................................................................................................................................................... 8-6-13 Succession ......................................................................................................................................................... 8-6-13 Host Preference ................................................................................................................................................. 8-6-16 Growth Structure ............................................................................................................................................... 8-6-18 Bryophyte Adaptations...................................................................................................................................... 8-6-18 Morphology................................................................................................................................................ 8-6-19 Water Relations .......................................................................................................................................... 8-6-20 Life Cycles ................................................................................................................................................. 8-6-23 Neoteny ............................................................................................................................................... 8-6-24 Life Strategy Types .................................................................................................................................... 8-6-25 Host Adaptations ............................................................................................................................................... 8-6-25 Drip Tips .................................................................................................................................................... 8-6-25 Leaf Size and Shape ................................................................................................................................... 8-6-26 Leaf Age .................................................................................................................................................... 8-6-26 Leaf Longevity ........................................................................................................................................... 8-6-27 Leaf Chemistry........................................................................................................................................... 8-6-27 Interactions ........................................................................................................................................................ 8-6-28 Nutrient Exchanges .................................................................................................................................... 8-6-28 Host Leaf Leachates............................................................................................................................ 8-6-28 Bryophyte Leachates........................................................................................................................... 8-6-28 Seed Beds............................................................................................................................................ 8-6-29 Nitrogen Fixation ....................................................................................................................................... 8-6-29 Herbivore Protection .................................................................................................................................. 8-6-30 Micro-organisms ........................................................................................................................................ 8-6-32 Negative Impacts on Leaves ...................................................................................................................... 8-6-33 Light Interference....................................................................................................................................... 8-6-33 Species Richness ............................................................................................................................................... 8-6-34 Asia ............................................................................................................................................................ 8-6-34 South Pacific Islands .................................................................................................................................. 8-6-39 Africa ......................................................................................................................................................... 8-6-39 Neotropics .................................................................................................................................................. 8-6-40 Central America .................................................................................................................................. 8-6-40 South America .................................................................................................................................... 8-6-41 Bromeliad Basins .............................................................................................................................................. 8-6-43 Fragmented Habitats ......................................................................................................................................... 8-6-45 Sampling Epiphylls ........................................................................................................................................... 8-6-46 Summary ........................................................................................................................................................... 8-6-47 Acknowledgments ............................................................................................................................................. 8-6-47 Literature Cited ................................................................................................................................................. 8-6-47

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Chapter 8-6: Tropics: Epiphylls

CHAPTER 8-6 TROPICS: EPIPHYLLS JANICE M. GLIME AND TAMÁS PÓCS

Figure 1. Epiphyllous Lejeunea floridana and Cololejeunea cardiocarpa. Photo by Scott Zona, with permission.

Epiphyllous Communities A unique community occurs in the tropics, especially in the wet rainforests, the epiphyllous community (Figure 1), i.e. those bryophytes, lichens, algae, fungi, and bacteria that live on the leaves of higher plants. Among these, bryophytes contribute most of the biomass (Bentley 1987). A discussion of tropical epiphytes would not be complete without considering these bryophytes that spend their lives on leaves. Some of the earliest bryophyte studies in the tropics were on epiphyllous species, typically on trees and shrubs. These included studies by Goebel (1888, 1889), Massart (1898), Busse (1905), Pessin (1922), Richards (1932), Allorge et al. (1938), and Allorge & Allorge (1939). Later, Winkler (1967, 1970) reported on epiphyllous communities of both upland and lowland rainforests of tropical Americas. Foliicolous bryophytes occur predominantly on the upper surface of leaves (epiphyllous), but some do occur on the lower surface (hypophyllous) (Santesson 1952). This leaf habitat is termed the phyllosphere (Ruinen 1961). These communities are mostly restricted to the rainforests of the humid tropics and subtropics, but some have been

reported, albeit not well-developed, in wet temperate regions as well: Japan (Schiffner 1929), the Appalachian Mountains, USA (Schuster 1959; Ellis 1971), British Columbia (Vitt et al. 1973), the Caucasus (Pócs 1982b; Vězda 1983), Macaronesia (Sjögren 1975, 1978) and the Pyrenees (Vězda & Vivant 1972). In equatorial regions, these foliicolous communities occur from sea level to about 3000 m asl, where they become limited by lack of forest substrate. Pócs (1976a, 1982a) concluded that the upper limit is determined by the frequency of night frosts and the degree of oceanity. Optimal conditions, on the other hand, occur in the lower montane rainforest belt. In East Africa this occurs at ~1500-2000 m. Luo (1990) noted the need for very moist air in the habitats of epiphyllous liverworts. This defines the primary distribution of epiphyllous liverworts in the tropical or subtropical regions of IndoMalay, Central and South America, central Africa, and the Asian-Pacific regions of South Korea and southern Japan south to Australia. Among the early studies, Jaag (1943) investigated epiphytes and epiphylls on ferns (Figure 2-Figure 3), examining these as they related to the leaf renewal rate and leaf life.

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usually occur only near streams and in swampy areas. Exceptionally, they can occur also in dry woodlands if they are affected by mist/cloud formation regularly (Pócs.1976b). The long-lived, somewhat leathery leaves of tropical forest trees make it predominantly possible for bryophytes to become established there, particularly in the more humid sites. But they can also occur on bamboo (Doei 1990) and palm leaves as well (Schuster & Anderson 1955), even on fern and other herbaceous plant leaves and exceptionally on succulents. In western Nigeria, for example, as many as 1200 shoots/colonies can occur on one 58x35 mm leaf of Citrus sinensis (Figure 4) (Olarinmoye 1975c).

Figure 2. Blechnum loxense tree fern at treeline in the Ecuadorian Andes at 3500 m asl, with Jan Peter Frahm. Members of this genus often have epiphylls. Photo courtesy of Robbert Gradstein.

Figure 4. Citrus sinensis, a species that can house as many as 1200 epiphytic shoots on a 6 x 3 cm leaf section. Photo by Antandrus, through Creative Commons.

Filmy fern leaves usually have a special epiphyllous community formed by tiny Cololejeunea (Figure 5-Figure 6) and hookerioid moss species (Pócs 1978).

Figure 3. Lejeunea cf. epiphylla on Blechnum wattsii. Photo by Tom Thekathyil, with permission.

Richards (1952) has written one of the definitive treatises on tropical plant ecology. In it, he describes the epiphyllous community as common in tropical, montane, and subtropical rainforests, particularly in wet forests. The epiphylls occur mostly on the upper surfaces of evergreen leaves. In tropical forests that are seasonally dry, they

Figure 5. Cololejeunea minutissima, in a genus that is among the epiphylls in the world. Photo by Michael Lüth, with permission.

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Figure 6. Cololejeunea magnilobula, in a genus that is among the epiphylls in the world. Photo by Yang Jia-dong, through Creative Commons.

In the 1990's Pócs (1996, 1997) reported 1,000 epiphyllous species of liverworts worldwide. Although this includes epiphyllous species that are not exclusively tropical, most are in the tropics (Figure 7). Among these, Asia had the highest reported number of any continent at 504 species, with 224 in the Malesian archipelago alone. These worldwide epiphylls are divided among the Lejeuneaceae genera Cololejeunea (389 species; Figure 5-Figure 6), Ceratolejeunea (114 spp.; Figure 8), Drepanolejeunea (98 spp.; Figure 9), Colura (76 spp.; Figure 10), Diplasiolejeunea (68 spp.; Figure 11), Prionolejeunea (59 spp.; Figure 12), Aphanolejeunea (54 spp.; Figure 13; this genus is now included in Cololejeunea), Leptolejeunea (48 spp.; Figure 14), and Microlejeunea (34 spp.; Figure 15), the Radulaceae genus Radula (13 spp.; Figure 16), and another 12 genera with fewer than 10 species each. This distribution of genera and numbers of species is likely to have changed since that time as synonyms have been identified and genera have been split or unified and new species have been described. For example, TROPICOS lists only 29 currently accepted species names in Diplasiolejeunea, listed above as having 68 in the tropics, but the World Checklist of liverworts and Hornworts (Söderström et al. 2016) lists more than 90! These epiphyllous genera are susceptible to losses whenever the forest is disturbed.

Figure 7. Epiphyll floristic regions of the world. Modified from Pócs 1996.

Figure 8. Ceratolejeunea cubensis, in a genus that is among the epiphylls in the world. Photo by Scott Zona, with permission.

Figure 9. Drepanolejeunea hamatifolia, in a genus that is among the epiphylls in the world. Photo by Barry Stewart, with permission.

Figure 10. Colura calyptrifolia, a species that is among the epiphylls in the world. Photo by David T. Holyoak, with permission.

Chapter 8-6: Tropics: Epiphylls

Figure 11. Diplasiolejeunea cavifolia, a pantropical epiphyllous liverwort species that is among the epiphylls in the world. Photo by Hermann Schachner, through Creative Commons.

Figure 12. Prionolejeunea saccatiloba with perianth and androecium, in a genus that is among the epiphylls in the world. Photo by Michaela Sonnleitner, with permission.

Figure 13. Cololejeunea sintenisii, in a genus that is among the epiphylls in the world; Cololejeunea sicifolia dominates communities in dry microsites of Central America, but is rare in wet microsites. Photo by Pedro Cardosa, Biodiversidad, with permission.

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Figure 14. Leptolejeunea elliptica, in a genus that is among the epiphylls in the world. Photo by Yang Jia-dang, through Creative Commons.

Figure 15. Microlejeunea ulicina, in a genus that is among the epiphylls in the world. Photo by Malcolm Storey, , with online permission.

Figure 16. Radula complanata, in a genus that is among the epiphylls in the world. Photo by Malcolm Storey, , with online permission.

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In 1997 Lücking estimated the number of epiphyllous bryophyte species to be only about 535 worldwide. He found 83 species of epiphyllous bryophytes in a Costa Rican tropical rainforest. A single leaf of the palm Welfia georgii (Figure 17; see also Figure 18) had 24 species. Nearly all the epiphylls were liverworts, with 78 species in the family Lejeuneaceae (Figure 6-Figure 15). The others were Radula (Radulaceae; Figure 16), Metzgeria (Metzgeriaceae; Figure 19, Figure 127), and Frullania (Frullaniaceae; Figure 20). Crossomitrium patrisiae (Figure 21) was the only epiphyllous moss species. Only 17% of the bryophytes are widely distributed on more than one continent in the tropics; the others in this study are Neotropical, with 11% known only from Costa Rica.

Figure 19. Metzgeria furcata. Members of this genus are epiphyllous on the palm Welfia georgii (Figure 17). Photo by Malcolm Storey, , with online permission.

Figure 17. Everwet lowland rainforest of the Chocó with dominance of Welfia georgii. Photo by Jan-Peter Frahm, with permission.

Figure 20. Frullania pycnantha; some members of this genus are epiphyllous on the palm Welfia georgii (Figure 17). Photo by John Braggins, with permission.

Figure 18. The palm Welfia regia with epiphytes on its leaf bases. Welfia georgii (Figure 17) can have 24 bryophytic epiphylls on a single leaf. Photo by David J. Stang, through Creative Commons.

Figure 21. Crossomitrium patrisiae, a species that is epiphyllous on the palm Welfia georgii (Figure 17). Photo by Jan-Peter Frahm, with permission.

Chapter 8-6: Tropics: Epiphylls

Epiphylls can include rare and endangered species, not to mention many species yet to be discovered. For example, Reiner-Drehwald and Drehwald (2002) discovered the extremely rare and critically endangered epiphyllous Lejeunea drehwaldii (Figure 22) in northern Peru. It exhibits some of the more common adaptations of epiphyllous species: leaf lobes that are bordered by hyaline cells, strongly inflated lobules, and cylindrical perianths, characters that are common to its family, Lejeuneaceae (Figure 6-Figure 15).

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leafy liverworts have been found on Rhododendron maximum (Figure 25), Leucothoe editorum (Figure 26) (both in Ericaceae) (Schuster 1959), and Magnolia grandiflora (Figure 27) (Guerke 1973). The moss Taxithelium planum (Figure 28) occurs on Sabal palmetto (Serenoa repens; Figure 29) (Schuster & Anderson 1955). On Buxus colchicus leaves at the foot of the Caucasus Mountains five liverwort species occur that are growing otherwise on different substrates (Pócs 1982b). All these host species have leathery, persistent leaves. Even in the boreal coniferous zone a few epiphyllous lichens occur on needle-like gymnosperm leaves.

Figure 22. Lejeunea drehwaldii on leaf. Photo by Elena Reiner-Drehwald and Uwe Drehwald, with permission.

Identification problems have made ecological studies difficult. On the one hand, many species have multiple names in various places throughout the tropics. Others have never been described and some important epiphyllous genera do not yet have an up-to-date revision. And some species that have been described represent multiple cryptic species that cannot be distinguished morphologically, as demonstrated in the epiphyllous genus Diplasiolejeunea (Lejeuneaceae; Figure 11, Figure 23) (Dong et al. 2012).

Figure 24. Thuja occidentalis, in a northern genus that gets epiphylls. Photo by Raul654, Longwood Gardens, through Creative Commons.

Figure 25. Rhododendron maximum, an evergreen species outside the tropics that get epiphylls. Photo by S. B. Johnny, through Creative Commons.

Figure 23. Diplasiolejeunea plicatiloba, in a genus with cryptic species. Photo by David Tng, , with permission.

Because of the need for a stable substrate that lasts several years and maintains sufficient humidity, these associations are almost entirely restricted to tropical and subtropical regions with few notable exceptions, such as those living on the leaves of Thuja (Figure 24) species (Vitt et al. 1973). One of the northernmost records of nonThuja epiphylls in North America is in Louisiana, where

Figure 26. Leucothoe editorum is known to have epiphylls in non-tropical regions. Photo by David Stang, through Creative Commons.

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The success of many epiphylls may reflect the fact that the tiny leafy liverworts have leaves in two rows that look as if they were ironed to the substrate (Figure 22). Such a flattened conformation provides the least exposure to the drying atmosphere (Figure 30).

Figure 27. Magnolia grandiflora, an evergreen species that gets epiphylls outside the tropics. Photo by Andrew Butko, through Creative Commons.

Figure 30. Lejeuneaceae epiphylls showing their flattened habit. Photo by Janice Glime.

Some epiphylls are facultative (capable of functioning under various environmental conditions). Geissler (1997) considered five populations (4 species) of the leafy liverwort Marchesinia subgenus Marchesiniopsis (Figure 31) to be "accidentally foliicolous" (accidentally growing on leaves), i.e., facultative. She considered their rainforest habitat to correspond with optimal conditions in equatorial primary forest in Latin America and Africa.

Figure 28. Taxithelium planum in the Neotropics, a moss that occurs on Sabal palmetto (Serenoa repens). Photo by Michael Lüth, with permission.

Figure 31. Marchesinia subg. Marchesiniopsis; M. brachiata from St. Helena, a species growing here on bark, but that can be an accidental epiphyll. Photo By M. Wigginton, courtesy of Robbert Gradstein.

Figure 29. Serenoa repens (Saw Palmetto); leaves of this species can have growths of the moss Taxithelium planum. Photo by Homer Edward Price, through Creative Commons.

Alvarenga and Pôrto (2007) found that species richness and abundance of epiphytic bryophytes increased with altitude in lowland and submontane areas of Pernambuco, Brazil. However, fragmentation can negate that effect. Fragment size and isolation are important factors, with isolation having a negative effect for epiphylls in particular. Furthermore, species with smaller niches were more affected than those with large niches. Sipman (1997) studied the lichens and bryophytes in the crowns of semi-deciduous trees in southern Guyana.

Chapter 8-6: Tropics: Epiphylls

Whereas the lichens grew preferentially close to the ground, the bryophytes could be found in the crowns. He found 18 taxa of bryophytes associated with canopy leaves. These seemed to follow a distribution pattern similar to that of the lichens. Other studies that describe this fascinating group of communities include those of Kiew (1982) on leaf color, epiphyll cover, and damage on Iguanura wallichiana (Figure 32) in Malaya. Lücking (1995a, b) described the diversity, ecology, and interactions of epiphylls in a tropical rainforest in Costa Rica; Lücking and Lücking (1998) examined adaptations and convergences of organisms living in the phyllosphere (space surrounding the leaf, where epiphylls are found). Baudoin (1985) analyzed the distribution patterns of epiphyllous bryophytes on the Soufrière of Guadeloupe. Pócs (1978) reported on the distribution of epiphyllous communities in East Africa, and Reynolds (1972) reported on stratification of tropical epiphylls. Farkas and Pócs (1997) reported on systematics, distribution, ecology, and uses. Winkler (1967, 1970) reported on the epiphyllous bryophytes in cloud forests of El Salvador and Colombia. Olarinmoye (1977) examined the relationship of the epiphylls to the host tree. Gradstein and Lücking (1997) summarized a symposium on epiphyllous bryophytes. The symposium emphasized floristics and ecology, including diversity analyses and the role of these bryophytes in the tropical rainforest.

Figure 32. Iguanura wallichiana var. major, a species that appears to be harmed by epiphylls. Photo by David J. Stang, through Creative Commons.

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developed foliicolous communities to be 0.139 g 100 cm-2 of host leaf area, or 0.216 g g-1 of host leaf dry mass. This figure can be extrapolated to 69.5 kg foliicolous biomass ha-1 forest (assuming that leaves occupied by foliicolous communities cover at least half the ground area at these localities). The interceptive capacity of this foliicolous biomass is 2.357 g 100 cm-2 host leaf area, or 1175 L ha-1 according to experiments by Pócs (unpublished). These figures include the entire community of algae, bacteria, lichens, fungi, and bryophytes. They are valid only where conditions are optimal, such as condensation zones (van Reenen & Gradstein 1983). Under less favorable conditions, foliicolous communities are restricted to certain moist habits such as streamside and near waterfalls, to certain forest layers such as leaves of the lower shrubs, or are lacking entirely. By comparison, Carroll (1979) found the biomass of foliicolous communities in oceanic temperate regions to be ~50 kg ha-1, of which 30 kg is composed of fungi and 20 kg of algal cells.

Microclimate Epiphyllous species require shade and high humidity, thus confining them mostly to the understory and lower parts of the canopy (Gradstein 1992). On the other hand, in lowland cloud forests they can also occur in higher parts of the canopy (Gradstein et al. 2010). An average of 3-13 species of bryophytes can occur on a single leaf. Light and available moisture appear to play the most important roles in the distribution of epiphyllous bryophytes within the tropical evergreen forests. In Costa Rica, Reynolds (1972) found that bryophytic epiphylls existed up to about 10 m under a 24-m canopy, where they disappeared, but lichens persisted nearly to the top of the canopy. Reynolds attributed this limited bryophyte distribution to availability of continuous moisture. In the subtropical evergreen forests of southeast China (Figure 33) the light intensity in the open can be 632 times as great as that in some forested areas supporting epiphyllous liverworts (Wu et al. 1987). For these liverworts to thrive through the winter, they require about two hours of direct light and ten hours of diffuse light. In general, it seems that shade and moisture promote growth while high light and drought hinder it. Heavy rains hinder colonization (Busse 1905), most likely contributing to the greater biomass found on lower branches than on upper ones.

Fossil Records The oldest evidence of bryophytes is a fossil record from the Middle Carboniferous period, 330 million years ago. But fossil records of bryophytic epiphylls have been lacking (Barclay et al. 2013). Barclay et al. (2013) described an epiphyllous moss, Bryiidites utahensis, from a single fossil leaf specimen from the middle Cretaceous, at least 95 million years ago. The moss presence was only 450 µm long, represented by a spore and protonema. This fossil suggests that central North America had a tropical maritime climate at that time.

Biomass Contributions Pócs (unpublished) has found the foliicolous biomass in tropical montane rainforest (mossy forest) with well-

Figure 33. China – Emei Shan lush misty forest in the Sichuan Basin, China. Photo by McKay Savage, through Creative Commons.

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Chapter 8-6: Tropics: Epiphylls

Wu et al. (1987) found that temperature and humidity, in addition to light, are the main factors influencing communities of epiphyllous liverworts in subtropical evergreen forests of southeast China. They observed that these liverworts did not occur in very shady or dark forests. They studied the light intensities in a subtropical evergreen forest beside streams where the dominant epiphyllous liverworts were Cololejeunea ocelloides (Figure 34), Leptolejeunea elliptica (Figure 14) (both Lejeuneaceae), Radula acuminata (Figure 35; Radulaceae), and Frullania moniliata (Figure 36; Frullaniaceae). They sampled at 0.5 m intervals in the range of 0.5-2 m. There was no discernible difference in species composition in the heights sampled, but 10 m from the streams the epiphyllous liverworts were rare. Figure 36. Frullania moniliata, a dominant epiphyll beside streams in subtropical evergreen forests in China. Photo by Yang Jia-dong, through Creative Commons.

Figure 34. Cololejeunea ocelloides, a dominant epiphyll beside streams in subtropical evergreen forests in China. Photo by Yang Jia-dong, through Creative Commons.

Figure 35. Radula acuminata, a common epiphyllous species in broad-leaved forests of Guangdong, China. Photo by Yang Jia-dang, through Creative Commons.

Jiang et al. (2014) noted that epiphyllous liverworts usually grow in areas that are constantly moist with evergreen forest trees in the tropical and subtropical regions. They also considered them to be species that are very sensitive to both pollution and climate change. They also found that humidity, temperature, and light are important limiting factors for these epiphylls. The researchers used the Area Under the receiver operating characteristic Curve (AUC) and True Skill Statistic (TSS) and the Wilcoxon paired test in comparing model performances. These tests indicated that climatic and remotely sensed vegetation variables were the best predictors of bryophyte composition on a macrohabitat scale. The researchers concluded that epiphyllous liverworts could be useful indicators of forest degradation at broad spatial scales. Reyes (1981) has shown that epiphylls are very good indicators of air pollution. In Cuba, in a large area around the Nicaro nickel metallurgical works, epiphylls do not occur even among favorable macro-climatic conditions. Pócs (1989) has found that epiphylls disappear when the forest canopy is partly loosened by invasive tree species, due to the decreasing air moisture. Marino and Salazar Allen (1991) compared the tropical epiphyllous communities (all liverworts) on two shrub species on Barro Colorado Island, Panama. They used five randomly selected shrubs in each site (dry light, dry shade, wet light, wet shade) for each of Hybanthus prunifolius (Figure 37) and Psychotria horizontalis (Figure 38). To determine cover, they used leaf transects (midrib and 2 parallel to midrib) to determine the epiphyll cover. The small gaps with greater light clearly had more cover than did the shaded sites. Interestingly, the dry ridges had significantly more cover than did the wet creek area. There was little difference in epiphytic communities (15 species overall) between the two shrub species in the same environmental conditions. The dry site epiphylls were dominated by Cololejeunea sicifolia (see Figure 120); in the wet sites, Leptolejeunea elliptica (Figure 14) dominated. They suggested that C. sicifolia was rare in the wet site due to competition from L. elliptica. On the other hand, L. elliptica was limited by insufficient moisture on the dry sites.

Chapter 8-6: Tropics: Epiphylls

Figure 37. Hybanthus prunifolius, a species that supports epiphyllous bryophytes on Barro Colorado Island, Panama. Photo by Barry Hammel, through Creative Commons.

Figure 38. Psychotria horizontalis, a species that supports epiphyllous bryophytes on Barro Colorado Island, Panama. Photo by Daniel H. Janzen, through Creative Commons.

Freiberg (1999) looked at microclimate as it affects the Cyanobacteria (Figure 39) on leaves in a premontane rainforest of Costa Rica. He found seven species of Cyanobacteria, with the two most frequent being Scytonema javanicum and Scytonema hofmannii (Figure 39). He found that air humidity is more important than light in determining their relative abundance, a factor that also determined abundance of the epiphyllous bryophytes. On moist sites, these two Cyanobacteria species and the bryophytes appeared nearly simultaneously on leaves that were 6-9 months old. However, on drier sites, the Cyanobacteria did not appear until 6-9 months after the bryophytes became established. When Spathacanthus hoffmannii (Figure 40) leaves were 2-5 years old, the average leaf cover of bryophytes was 20-30%, that of Scytonema javanicum 2-3%, and that of Scytonema hofmannii 0.1-0.2%. When bryophytes were present, the Scytonema hofmannii was more frequent, whereas Scytonema javanicum did not seem to be influenced by bryophyte presence.

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Figure 39. Scytonema hofmannii (Cyanobacteria); Scytonema javanicum and S. hofmannii grow as epiphylls on Barro Colorado Island, Panama. Photo from Utex, through Creative Commons.

Figure 40. Spathacanthus hoffmannii, a host for epiphyllous bryophytes and Cyanobacteria. Photo by Armando Astrados, with online permission.

Kraichak (2014) found that the beta diversity (ratio between regional and local species diversity) of epiphyllous bryophyte communities on Moorea, French Polynesia (Figure 129), fluctuated with the microclimate. The beta diversity among these epiphylls on different host types tended to increase as the daily range of vapor pressure deficit increased at that site. Kraichak suggested that the high fluctuations in these microclimatic conditions might augment the habitat quality differences among the host types, causing greater dissimilarities among these epiphyllous communities. However, Kraichak detected no change in niche breadth. In western Nigeria, Olarinmoye (1974) followed the growth of four epiphyllous liverworts [Radula flaccida (Figure 41), Caudalejeunea hanningtonii (see Figure 42), Leptolejeunea astroidea (see Figure 14), and Cololejeunea obtusifolia (Figure 43)] for ~18 months. Growth of larger species always exhibited faster growth. The wet and dry seasons caused a growth periodicity, but there was no dormancy. However, growth was reduced considerably during the dry season.

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Chapter 8-6: Tropics: Epiphylls

Figure 41. Radula flaccida habit with gemmae, a common epiphyllous liverwort in tropical Africa, with a parasitic bryophilous Ascomycetes on its left-most leaf. Photo by Michaela Sonnleitner, with permission.

Sonnleitner et al. (2009; Sonnleitner 2008) explored microclimatic effects by sampling epiphyllous bryophytes on two leaves per tree of 57 individual trees in a tropical lowland rainforest in Costa Rica. They sampled from three adjacent sites that had different microclimates and found that pronounced daily humidity fluctuations placed considerable restraints on the epiphyll distribution and colonization. Phorophyte species, air temperature, and light availability were only weakly correlated with epiphyll cover and diversity. Nevertheless, all of these factors influenced the species composition of the epiphyll communities. The ability of the forest to buffer the microclimate seems to be important to the success of these epiphylls. Lücking (1995a) provides additional information on microhabitat preferences of epiphylls in a tropical rainforest in Costa Rica. Monoculture affects epiphyll establishment and success differently from the natural forests. Arnold and Fonseca (2011) examined the effects of monoculture that replaced the Araucaria forest (Figure 44) in southern Brazil. The natural Araucaria forest (Figure 44) has a larger percentage of leaves with epiphylls than does the Eucalyptus plantation (Figure 45), a fact the researchers attribute to the shadier and moister microclimate of the natural forest. Nevertheless, monocultures help to maintain epiphylls in areas that might otherwise be devoid of forest.

Figure 42. Caudalejeunea lehmanniana; Caudalejeunea hanningtonii is an epiphyllous species with no dormancy, but with seasonal growth in Nigeria. Photo by Scott Zona, with permission. Figure 44. Araucaria forest, an epiphyll host that is being replaced by monoculture plantations such as Eucalyptus in southern Brazil. Photo by Jason Hollinger, through Creative Commons.

Figure 43. Cololejeunea obtusifolia, an epiphyllous species with no dormancy, but with seasonal growth in Nigeria. Photo by Tamás Pócs, with permission.

Figure 45. Eucalyptus plantation in Nilgiris, India. Such plantations have fewer epiphyll species than native Araucaria forest in southern Brazil. Photo by Shyamal, through Creative Commons.

Chapter 8-6: Tropics: Epiphylls

Monge-Nájera (1989) found that both absolute and relative cover by epiphylls are higher in forest clearings than in the understory at Monte Verde, Costa Rica. They suggested this was due to the high atmospheric humidity in the area and the presence of heliophilic (sun-loving) bryophyte species.

Colonization Kursar et al. (1988) determined rates of leaf colonization by epiphylls in Panama. Coley and Kursar (1996) found that epiphylls have both positive and negative effects on the host leaves. Conversely, the host leaf can affect the rate of epiphyll colonization. For epiphylls, establishment on the host leaves is the most difficult step, requiring adherence of a spore or gemma and protonema through rainstorms that would attempt to wash them off. Young leaves are usually first colonized by lichens, then by liverworts, and perhaps mosses (Richardson 1981). Mosses seldom become established on the leaves, but more often grow onto them from neighboring twigs. Colonization can be rapid and dynamic, as demonstrated for a leaf from El Salvador that was colonized by 7 species in the period from May to December (Figure 46) (Winkler 1967). Winkler found that young leaves were colonized by liverworts within three months in the montane rainforest of San Salvador. Nevertheless, these could die during subsequent dry weather.

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significantly from the growth rate of non-foliicolous species (cf. Hawksworth & Chater 1979). According to Winkler (1967) and Olarinmoye (1975c), colonization and growth rate of foliicolous liverworts coincide with climatic periods and are greatest during rainy seasons when atmospheric humidity is high. The host leaves are colonized first by eufoliicolous (true leaf-dwelling) taxa possessing an adhesive apparatus (Aphanolejeunea – Figure 13, Cololejeunea – Figure 5-Figure 6, Drepanolejeunea – Figure 9, Leptolejeunea – Figure 14, and others) and by hemiepiphyllous taxa. Many of the early colonizers are soon overgrown by others that lack special devices to adhere to the leaf surface (Pócs 1978).

Figure 46. Progression of epiphyllous species on a leaf in El Salvador from May to December. A. May 1962. B. August 1962, with 3 colonies. C. October 1962, with 2 additional colonies and 2 lost. D. December 1962, with 2 new colonies and 2 colonies lost. From Winkler 1967.

Succession There is a succession in leaf colonization. There are pioneer species (like members of the genus Leptolejeunea – Figure 14), which can appear even on short-lived (e.g. banana – Figure 47) leaves, and those which occur only in a well-established epiphyllous community on perennial leaves. Richards (1932) made the first observations of succession in foliicolous communities, using leaf pairs of different ages in the Guyana rainforest. Harrington (1967) in West Africa and Winkler (1967) in Central America made careful studies on colonization and growth of foliicolous communities by observations on host leaves in sample plots for periods of over 200 days. All authors concluded that foliicolous growth in bryophytes and lichens does not exceed 3-7 mm annually, hence does not differ

Figure 47. Musa sp. (banana), substrate for some Leptolejeunea species. Photo by Jean-Pol Grandmont, through Creative Commons.

Daniels (1998) conducted an extensive study on establishment and succession of epiphyllous bryophytes on the understory palm Geonoma seleri (see Figure 48) in Costa Rica. Using 914 pinnae from 100 individual palms, he inferred chronology based on the position of the frond on the palm. He also selected 50 pinnae and examined them repeatedly from frond emergence to abscission. Daniels concluded that there is no succession in the classical sense. Rather, the composition of species is highly variable. However, as expected, the cover values of individual species does change significantly over time. But no stable climax community emerges. Furthermore, the bryophyte assemblage development is not influenced by the season of emergence of the frond. It is somewhat

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Chapter 8-6: Tropics: Epiphylls

surprising that canopy closure and height of palm tree have no significant effect on total cover of epiphyllous bryophytes.

Figure 50. Iguanura wallichiana var. major, a species that is not colonized by epiphylls in the first 6 months, but bryophytes can cover half the leaf surface by 30 months. Photo by David J. Stang, through Creative Commons.

Figure 48. Geonoma seleri, a host of epiphyllous bryophytes in Costa Rica. Photo from INaturalist, through Creative Commons.

Kiew (1986) studied epiphyll colonization in a Malayan rainforest. Leaves on the shrub Thottea dependens (see Figure 49) live up to 70 months and become completely covered with epiphylls. The longestliving leaves were those of the palm Iguanura wallichiana (Figure 50). These leaves had no epiphyll colonists in the first 6 months. Bryophytes didn't colonize until approximately 2 years, but they then covered half the leaf surface in another 6 months.

Figure 49. Thottea sivarajanii; Thottea dependens leaves live up to 70 months and can become completely covered with epiphylls. Photo by Vinayaraj, through Creative Commons.

Olarinmoye (1975c) reports no orderly successional colonization or phenological rhythm in order of species establishment in his western Nigerian study. Rather, colonization depends on nearness of propagules, number produced, and their ability to become established. Subsequent succession, however, does at some locations seem dependent on competition and seasonal changes. Lichens are common cohabitants with the bryophytes, and liverworts seem always able to overgrow the crustose lichens, but the foliose lichens are able to overgrow even the large, fast-growing Radula flaccida (Figure 41). On the other hand, the large Caudalejeunea hanningtonii (see Figure 42) seems to be able to overgrow all types of lichens and algae, at least at Alkenne and Gambari, Nigeria. But even some of the algae can overgrow the small, slowgrowing liverworts. The large, tufted or shelf-forming Trentepohlia (Figure 51-Figure 52) is one such alga, whereas the Cyanobacteria (Figure 39) tend to live in association with the liverworts without overtaking them. Despite all this competition, the ultimate winner seems to be Radula flaccida, which eventually occupies the entire leaf surface. That is, until the dry season in Erin-Odo, when only Leptolejeunea astroidea (see Figure 14) remains, mixed with scattered shoots of Cololejeunea nigerica. And at Ojo Rocks, where Caudalejeunea hanningtonii predominates in the wet season, it likewise disappears in the dry season, being replaced by thick felts of Leptolejeunea astroidea. It appears quite clear that the large Radula flaccida and Caudalejeunea hanningtonii are unable to prosper during the dry season. Richards (1996) stated that epiphyllous species do not also occur on bark, but in fact, there are a number of examples where both substrates are occupied. He cites only one example for this, the genus Floribundaria (Figure 55), that establishes on twigs, then expands onto the leaves. He suggests that such species are not able to establish directly on a leaf.

Chapter 8-6: Tropics: Epiphylls

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little among their sites in Panama, liverwort cover increased with rainfall. In their experimental plots, liverwort cover increased from 1.7% in the controls to 20.5% in irrigated plots, whereas lichen cover decreased in response to the same watering regime. Surprisingly, liverworts at one site grew more quickly in high light compared to shade, and Coley and coworkers suggested that the liverworts were competitively superior to the lichens, resulting in the negative association between them. Contrasting sharply with the conclusion that bryophytic epiphytes require long-lived leaves, the short-lived leaves of Alseis (Figure 53) had 27% cover whereas the long-lived ones of Ouratea (Figure 54) had only 2% one year after removal of epiphytes. Within one year, the liverworts had colonized 45% of the leaves that had a lifetime of only one year, whereas they had colonized only 5% of the leaves of those with longer lives. This is, however, consistent with the known presence of chemical defenses of long-lived leaves against herbivores and pathogens. These defenses could affect the liverworts directly or by preventing growth of Cyanobacteria (Figure 39) or fungi that might benefit them.

Figure 51. Trentepohlia aurea on cypress in California, USA; some Trentepohlia species can overgrow epiphyllous liverworts. Photo by Jason Hollinger, through Creative Commons.

Figure 53. Alseis costaricensis, in a genus with short-lived leaves that can have extensive cover of epiphylls, in Guanacaste dry forest. Photo by Daniel H. Janzen, through Creative Commons.

Figure 52. Trentepohlia abietina with akinetes, in an alga genus with some members that can overgrow epiphyllous liverworts. Photo by A. J. Silversides, with permission.

Coley and Kursar (1996) examined the causes and consequences of epiphyll colonization in tropical forests. Coley et al. (1993) found that while lichen cover changed

Figure 54. Ouratea brevicalyx, in a genus with long-lived leaves that develop poor epiphyll cover, in Venezuela. Photo by Vojtěch Zavadil, through Creative Commons.

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Chapter 8-6: Tropics: Epiphylls

Figure 56. Distichophyllum; Distichophyllum mniifolium occurs primarily on filmy fern leaves. Photo by Phil Bendle, through Creative Commons.

Figure 55. Floribundaria floribunda (Meteoriaceae), a species that colonizes leaves only after becoming established on twigs. Photo through Creative Commons.

Figure 57. Cololejeunea mocambiquensis, a species that is epiphyllous on filmy fern leaves. Photo modified from Tomas Pocs, with permission.

Host Preference There seems to be little preference by the foliicolous communities for a particular host species. Rather, their occurrence seems to depend primarily on microclimatic conditions and availability of suitable leaf surfaces (Santesson 1952; Tavares 1953; Richards 1984b). Nevertheless, some species do seem to have preferences. Members of the Hookeriaceae (e.g. Distichophyllidium africanum, Distichophyllum mniifolium – see Figure 56), and certain liverworts (e.g. Cololejeunea mocambiquensis – Figure 57, C. tanneri, Lejeunea gradsteiniana – Figure 58, L. lyratiflora) occur primarily on filmy fern leaves, whereas others (Diplasiolejeunea cavifolia – Figure 11, Cheilolejeunea xanthocarpa – Figure 59) prefer hard, smooth, leathery leaf surfaces (Pócs 1978, 1985). Overall, the epiphylls have a relationship with size, age, and texture of phorophyte leaves.

Figure 58. Lejeunea gradsteiniana with perianths and antheridia, a species that is epiphyllous on filmy fern leaves. Photo by Tamas Pocs, with permission.

Chapter 8-6: Tropics: Epiphylls

Figure 59. Cheilolejeunia xanthocarpa, a species that prefers hard, smooth, leathery leaf surfaces. Photo source unknown.

Winkler (1967) considered leaf hair density and quality of phorophyte leaves to be important. He pointed out that a stellate hair cover may inhibit foliicolous growth. Foliicolous species also seem to avoid waxy, waterrepelling leaf surfaces (Richards 1932), but may be abundant on other surfaces, e.g. on leaves of planted citrus trees (Figure 4) in rainforest clearings. Pócs (pers. comm. May 2019) suggested that it was the sugary, sticky exudates of the citrus leaves that discouraged the epiphylls. A long life for the host leaf is also important, although some leaves with only a 3-4-month life span are occasionally colonized. In Cuba, Pócs observed a large vegetation of Leptolejeunea sp. (Figure 14) on smooth banana leaves (Figure 47). In habitats that were relatively dry, but affected by mist, foliicolous species occurred only on evergreen leaves such as the succulent Agave (Figure 60), Aloe (Figure 61), Sansevieria (Figure 62), Bromeliaceae (Figure 143), and Cactaceae (Figure 63) leaves or phyllocladia (branches that look like leaves).

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Figure 61. Aloe vera; Aloe species provide a substrate for epiphylls in dry communities. Photo by Biology Big Brother, through Creative Commons.

Figure 62. Sansevieria trifasciata; Sansevieria species provide a substrate for epiphylls in dry communities. Photo by Mokkie, through Creative Commons.

Figure 63. Macrocoma tenue on cactus. Photo courtesy of Tatiany Oliveira da Silva.

Figure 60. Agave americana, a substrate for epiphylls in dry communities. Photo by Marc Ryckaert, through Creative Commons.

It appears that substrate preference diminishes further with increasing air humidity. In an everwet rainforest, foliicolous species occur on many kinds of host leaves. Several species tend to occur on other substrates as well (elective foliicolous species). On the other hand, terricolous (soil-dwelling), rupicolous (rock-dwelling), or

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Chapter 8-6: Tropics: Epiphylls

corticolous (bark-dwelling) species may occur on leaf surfaces in this kind of wet forest (accidental foliicolous species such as certain species of Bazzania – Figure 64).

To these, Pócs (1982b) added the bryophyte category of hemiepiphyllous – those species that start their lives on branches, but subsequently grow from the twig to the leaf blade via the petiole, subsequently forming a community there.

Bryophyte Adaptations

Figure 64. Bazzania peruviana; some species of Bazzania become accidental epiphylls. Photo by Felipe Osorio-Zúñiga, with permission.

Growth Structure Fitting (1910) considered three groups to classify foliicolous lichens on leaves: 1. species penetrating the leaf tissue 2. species growing subcuticularly on the epidermis 3. species growing supracuticularly Fünstück (1926) considered that most foliicolous lichens penetrate into the mesophyll, others (Santesson 1952; Brodo 1973; Margot 1977) disagreed with this concept. Nevertheless, even some liverworts do this and can take nutrients from the leaf tissue (Berrie & Eze 1975). One can also distinguish between the obligately foliicolous species (those unable to grow elsewhere) and the facultative foliicolous species (those able to also grow on other plant parts and even on rocks). Sérusiaux (1977) divided this even further: 1. strictly foliicolous: never occurring on substrata other than leaves locally eufoliicolous: restricted to the phyllosphere in a definite geographical area, while occurring on other substrata elsewhere 2. pseudofoliicolous taxa: not restricted to living leaves and occurring also on other substrata elective pseudofoliicolous: showing highest vitality and abundance on living leaves indifferent pseudofoliicolous: occurring both on living and other substrata and not showing any preference accidental foliicolous species: normally corticolous, saxicolous, or terricolous, and occurring on leaves only accidentally (e.g. the leafy liverwort Bazzania – Figure 64; mosses in the Meteoriaceae (Figure 55).

Epiphytic life forms in general are considered late results of evolution. Among phanerogams, almost all epiphytic groups are at the tips of phylogenetic tree branches (Emberger, cited by Tixier 1980) and this seems also to be true for bryophytes (Vitt 1984). Hence, we should expect that special adaptations exist. In the tropical rainforest, epiphytism among bryophytes is probably the result of coevolution since the Cretaceous (Gradstein & Pócs 1989). Most of the foliicolous bryophytes are in the leafy liverwort family Lejeuneaceae, a family that is diversified most strongly in the rainforest, especially the subfamilies Lejeuneoideae and Cololejeuneoideae. The Lejeuneaceae has several morphological adaptations, as noted below, but its most significant evolutionary trend in the phyllosphere is its shortened life cycle. Several taxa may reach reproductive maturity in an early stage of development (neoteny). Gradstein (1997b) pointed out that many epiphyllous species are facultative – also able to grow on bark or other substrates. He described the typical epiphyllous species (those growing exclusively or almost exclusively on leaves) as shade epiphytes of the understory. These are small, pale-colored, appressed (Figure 65), with rhizoids in bundles that form large adhesive discs. They sometimes are neotenous (condition in which juvenile characters remain in adults). Gemmae (Figure 66), used in shortdistance dispersal, are common.

Figure 65. Epiphylls on leaf, demonstrating their small size, pale color, and appression to leaf. Photo by Jessica M. Budke, with permission.

Chapter 8-6: Tropics: Epiphylls

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Figure 66. Radula australis with gemmae on leaves. Photo by Paul Davison, with permission. Figure 68. Rhizoids at base of underleaf on leafy liverwort. Photo courtesy of Andi Cairns.

Morphology There must be some advantage in being a small, flattened, leafy liverwort when inhabiting a leaf surface, as nearly all the epiphyllous bryophytes fall in this category, mostly in the family Lejeuneaceae (Figure 6-Figure 15). Many of these adaptations have been described for liverworts (Massart 1898; Evans 1904, 1935; Schiffner 1929; Renner 1933; Jovet-Ast 1949; Winkler1967, 1970; Bischler 1968). Some thallose liverworts, e.g. species of Metzgeria (Figure 67), are anchored to the leaf surface by rhizoids that arise randomly from the ventral thallus surface (Figure 67). In most of the foliicolous liverworts, these anchoring rhizoids develop at a definite place (Figure 68), such as the main axis, on the lobule in Radula, or at the base of underleaves in Lejeuneaceae (Figure 68, Figure 69).

Figure 67. Metzgeria conjugata ventral view showing rhizoid clusters. Photo by N. J. Stapper, with permission.

Figure 69. Microlejeunea ulicina showing rhizoids near leaf bases. Note the rotifer peering out from the middle leaf. Photo by Blanka Shaw.

In the Lejeuneaceae the rhizoids are usually fused together to form an adhesive disc that enhances the attachment to the leaf surface. The attachment of rhizoids is strengthened by a glutinous mucus secreted by the rhizoid disc. Winkler (1967) tested this attachment experimentally and found that adhesion is stronger on smooth leaf surfaces than on rough ones. Perhaps Chiloscyphus koponenii (see Figure 70) in the Geocalycaceae can provide some clues as to the important structures contributing to success in this habitat. This leafy epiphyllous liverwort from Papua New Guinea possesses many characteristics similar to those of some genera of epiphyllous Lejeuneaceae, including its tiny size, ability to fragment and grow from fragments, two-lobed and often toothed leaves, thin-walled cells, small trigones (cell wall swellings), very shallow but wide underleaves with two lobes, two teeth, and numerous rhizoids (Piippo 1998), which many times fuse into a firm rhizoid plate. It is likely that the small size, the saccate lobules, and close adherence to the leaf surface (often with aid of a hyaline margin) are especially adaptive to maintaining moisture.

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Eze and Berrie (1977) found that under the extreme drying conditions of sodium chloride solution or silica gel, liverwort leaf cells did not plasmolyze, but instead the cell walls folded inward and became contorted. The oil bodies (Figure 72) lost their shape, and after rehydration they all coalesced into one, indicating that the membrane of the oil body had been destroyed. The oil body content of these liverworts is high, comprising 17% of the dry cell, whereas liverworts from more moist habitats (Plagiochila praemorsa and P. integerrima; see Figure 73) exhibit oil body contents of about 5%. Although the role of the oil bodies is still largely speculative, their large volume helps to reduce the loss of cell volume as the cell dries, thus somewhat preserving the cell shape. The oil body itself is unaffected by water loss. It could also be a potential source of energy upon rehydration. Figure 70. Chiloscyphus pallescens branch (left) and leaf cells with small trigones (right). Photo by Paul Davison, with permission.

Bernecker-Lücking and Morales (1999) considered the flattened stem and reduced lobule of Cololejeunea sigmoidea (Figure 71) to be adaptations to being a closely appressed epiphyll. But Olarinmoye (1975c) considered that for western Nigerian epiphylls the small size and closely appressed shoots were a disadvantage in competition with other species not so appressed. Instead, he considered Radula flaccida (Figure 41) and Caudalejeunea hanningtonii (see Figure 42) to be at a competitive advantage due to their larger size and faster growth, while he considered the small, appressed form to have a possible advantage in competing with erect species of smaller size. Fragmentation is useful for short-distance dispersal and spreading, and Olarinmoye considered the production of "copious propagules" of more than one type to provide a competitive advantage over those with only one type. For example, Radula flaccida produces numerous gemmae, but it can also produce as many as 10,000 spores in a single capsule, with 90% viability in the first few hours, dropping to about 40% after three weeks out of the capsule. And these capsules are produced only occasionally. Numerous rhizoids would aid in maintaining the position on a waxy leaf surface during a torrential onslaught, and some leafy liverworts have rhizoids or other parts with adhesive secretions that aid in maintaining attachment (Winkler 1967; Berrie & Eze 1975).

Figure 72. Plagiochila asplenioides showing leaf cells with oil bodies (bright, oblong structures in cells). Photo by Malcolm Storey, , with online permission.

Figure 73. Plagiochila asplenioides; Plagiochila praemorsa and P. integerrima have only about 5% content of oil bodies. Photo by Malcolm Storey, DiscoverLife.org, with online permission.

Water Relations Figure 71. Cololejeunea sigmoidea growing as an epiphyll. Photo by Yang Jia-dong, through Creative Commons.

Bryophytes in general act like sponges to absorb water. Epiphylls are no exception. The bryophytes are also able to

Chapter 8-6: Tropics: Epiphylls

hold water for a greater period of time than the leaf surface. This moist environment permits colonization by nitrogenfixing Cyanobacteria (see Figure 39). Pócs (pers. comm. May 2019) concluded that the most effective method to ensure continuous water saturation seems to be subcuticular growth, a method used by about 6% of the foliicolous lichen species. Among liverworts, this method seems to be lacking. Instead, for many success seems to be a leaf lobule that retains water, as found in Radulaceae (Figure 74), Jubulaceae (Figure 75), and Lejeuneaceae (Figure 76). This lobule, in many cases among epiphylls, develops into a watersack, with the most sophisticated ones in Colura (Figure 77; Lejeuneaceae). This genus has a special closure apparatus. Other epiphyllous liverworts have hyaline leaf margins (e.g. species of Cololejeunea – Figure 78 and Diplasiolejeunea – Figure 11). These hyaline margins consist of dead cells, which may absorb water, adhere quite close to the substrate, and retain water below the leaf surface. They apparently form a capillary system that promotes the distribution of available water (e.g. a raindrop) along the liverwort shoot.

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Figure 76. Cheilolejeunea evansii branch showing leaf lobules. Photo by Paul Davison, with permission.

Figure 77. Colura leaf showing well-developed lobule. Photo courtesy of Jan-Peter Frahm.

Figure 74. Radula from the Neotropics, showing lobule at arrow. Photo by Michael Lüth, with permission.

Figure 78. Cololejeunea grossepapillosa leaf showing hyaline marginal cells. Photo by Yang Jia-dong, through Creative Commons.

Figure 75. Jubula japonica leaves and lobules. Photo by Yang Jia-dong, though Creative Commons.

Dietz et al. (2007) examined surface wetness in an oldgrowth tropical montane forest in central Sulawesi, Indonesia. The canopy remained wet 25-30% of the time in the May-August study. The lower canopy surface

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wetness is continuous for up to 22 hours per day or more. During dry periods, wetness is contributed by dewfall in the second half of the night, affecting primarily the uppermost canopy. This causes radiative heat loss and under-cooling of the leaves. The researchers suggest that epiphyll colonization might take advantage of this surface water. Epiphylls may also steal water from the host leaves as drying commences. Barkman (1958) reported osmotic potentials as low as -90 bars in epiphytes, and Berrie and Eze (1975) have shown transfer of both water and phosphate from host to epiphyll. In the leafy liverwort Radula flaccida (Figure 41) in Nigeria, the osmotic potential can reach -30 to -35 bars while the potential in leaf cells of two species of their hosts are only down to -10 to -12 bars (Eze & Berrie 1977). This osmotic differential could facilitate transfer of host leaf water to the epiphyll. Larson (1981) compared the morphologies of various lichens and bryophytes to determine their water relations. Water uptake to saturation required only three minutes in Polytrichum juniperinum (Figure 79-Figure 80) to more than 300 minutes in the lichen Stereocaulon saxatile (Figure 82). The large surface area to weight ratio was the major contributor to rapid uptake in P. juniperinum and other species with a high ratio. It is likely that the lamellae on leaves (Figure 81-Figure 80) of P. juniperinum contribute to this rapid uptake, but this species also has internal conduction to contribute to water movement. Nevertheless, this suggests that species with small capillary spaces have an advantage in both uptake and holding of water.

Figure 81. Polytrichum juniperinum leaf showing tops of lamellae. Photo courtesy of John Hribljan.

Figure 82. Stereocaulon saxatile, a lichen with a very slow water absorption rate. Photo by Ed Uebel, through Creative Commons.

The host may reap some advantage from the association of drying epiphylls. In some cases, the thick growth of bryophytes and other epiphylls may aid in evaporative cooling as they release the water retained during a rainstorm (Olarinmoye 1976). And this water may also be absorbed by some tracheophyte leaves, thus contributing to their health. Figure 79. Polytrichum juniperinum, a species with very rapid water uptake. Photo by Bob Klips, with permission.

Figure 80. Polytrichum juniperinum leaf lamellae in cross section, providing extensive capillary space. Photo courtesy of John Hribljan.

Nutrient Budget The foliicolous species seem to have a low nutrient budget and are very effective at using nutrients. They depend on rainwater for most of their nutrients, including leachates from canopy throughfall. Some epiphyllous liverworts, however, are able to take up nutrients from the mesophyll tissue of the host leaves (Berrie & Eze 1975), using rhizoids that penetrate the cuticle. Water-soluble salts could pass from the host leaf tissue into the epiphylls in this way. Thus, we could consider the epiphyllous liverworts to be semiparasitic. On the other hand, the Cyanobacteria (Figure 39) that inhabit many of these liverworts can carry out nitrogen fixation. Harrelson (1969) and Edmisten (1970a) demonstrated that N fixation in leaves having foliicolous bryophytes was higher than that of leaves with no epiphylls. The interaction of the

Chapter 8-6: Tropics: Epiphylls

epiphylls and nitrogen fixation is discussed further below under Interactions. Life Cycles Reproductive strategies are usually important in habitat limitation, and this appears to be true for epiphyllous liverworts as well (Zartman et al. 2015). Unfortunately for most vegetation studies, the life cycle is slow and makes it difficult to predict long-term survival. Epiphyllous species, on the other hand, must complete their life cycles in a relatively short period of time because their leaf substrate is short-lived. In fact, they have some of the shortest generation times known for terrestrial plants. The most common type of life strategy among foliicolous bryophytes appears to be that of the perennial shuttle (During 1979). A shortened life span is characteristic, permitting them to complete the cycle before the leaf falls and the habitat becomes unfavorable. This makes us wonder if any species has taken advantage of this programmed change in the microhabitat, perhaps producing capsules or gemmae only after the leaf substrate falls to the ground. Zartman and coworkers (2015) investigated the relationship of the leafy liverwort Radula flaccida (Figure 41) in a central Amazonian rainforest to the seasonal precipitation. By marking 154 colonies, the researchers followed colony growth, extinction, recolonization, and rates of sexual and asexual expression. They found that the dry season increased mortality due to both increased leaf fall and R. flaccida colony mortality. Asexual reproduction decreased significantly in the dry months, but sporophyte density seemed unrelated to rainy season or dry season. Sporophyte density did, however, relate to a threshold colony size. Kraichak (2012) considered asexual propagules to be adaptive among tropical leafy liverworts in the Lejeuneaceae (Figure 6-Figure 15). He tested several potentially adaptive traits and only asexual reproduction seemed to be evolved in the presence of epiphylly. Other traits associated with epiphylly appeared to result from shared evolutionary history, not adaptive evolution. Epiphyllous mosses are much rarer than epiphyllous leafy liverworts. The epiphyllous moss Crossomitrium patrisiae (Figure 21) is dioicous (having male and female organs on separate plants), presenting a particularly challenging reproductive mode for this habitat. Alvarenga et al. (2013) set out to determine what permitted its success as an epiphyll. To do this, they examined 797 ramets (ramet – individual in a clone) for total length, presence, number of gametoecia (sexual reproductive structures and surrounding bracts), and number of fertilized perichaetia (modified leaves enclosing female reproductive structures and later the seta). They found high rates of sexual expression (76%). They unexpectedly found a highly male-biased population (0.43 females to 1 male) at the ramet level, n=604. Despite the isolation, with only 36.7% of the shrubs and 12.8% of the colonies having cooccurring sexes, the species nevertheless has one of the highest rates of fertilization known for any dioicous bryophyte. Nearly 90% of the mixed colonies produced sporophytes, with 40% of the female-only ramets producing sporophytes. Individual female ramets exhibited

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74% sporophyte production. The researchers suggested that the species invests in the success of the sporophyte rather in the number of perichaetia in a species that demonstrates low levels of abortion. To further elucidate this unusual reproductive strategy, Alvarenga et al. (2016) experimented with threshold colony sizes and alternative reproductive strategies. They followed growth, reproduction, and fate of 2101 colonies of C. patrisiae for two years and found that asexual expression, but not sexual onset, was limited by a threshold colony size. Age and threshold size did not correlate. Colonies with brood bodies survived nearly twice as long as did sterile or solely sporophytic colonies. Nevertheless, reproductive strategy had no effect on colony growth rate. He and Zhu (2011) compared the spore output of 26 selected species, representing 11 genera in the Lejeuneaceae. The mean spore output for these species ranges from 257 in Cololejeunea magnilobula (Figure 83) to 5038 in Ptychanthus striatus (Figure 84). The Lejeuneaceae has a much lower but more stable spore output than other leafy liverwort families. However, among eight species of Ptychanthoideae, Acrolejeunea pusilla (Figure 85) is the only species with a mean spore output of less than 1000 spores per capsule.

Figure 83. Cololejeunea magnilobula, a species that produced a mean of only 257 spores in a Chinese population. Photo by Yang Jia-dong, through Creative Commons.

Figure 84. Ptychanthus striatus, a species that produced a mean of 5,038 spores in a Chinese population. Photo by Yang Jia-dong, through Creative Commons.

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Figure 85. Acrolejeunea pusilla, the only species in Ptychanthoideae with a mean spore output of less than 1000 spores per capsule. Photo by Li Zhang, with permission.

Lücking and Lücking (1998) looked for adaptations and convergences in the phyllosphere, using mosses, lichens, and insects. Sierra et al. (2018) looked at the mechanisms of species assembly in epiphyllous bryophytes. These small organisms have the advantage of a short period of assembly that must be completed during the life of the host leaf. Sierra and coworkers studied the frequency and distribution of 55 species of epiphyllous bryophytes inhabiting 5 leaf-age classes on the understory shrub Piper grande (Figure 88) in a Panama premontane tropical forest. They found that dispersal was an important contributor to the assembly pattern, particularly for early arrivals. These early arrivals also had greater probabilities of sexual and specialized asexual reproduction. They concluded that interspecific variation in dispersal capacity, combined with various indirect effects, are the prerequisites for the high alpha diversity (average species diversity in habitat or specific area) of these epiphyllous communities.

The moss Ephemeropsis trentepohlioides (Figure 86) has globose gemmae and spores that can germinate in the capsule, and protonemata can extend out of the capsule (Bartlett & Iwatsuki 1985). Like E. tijbodensis, this species can cover an entire leaf by expansion of its persistent protonemata (Figure 87). The bunches of erect filaments increase its surface area for adsorbing water. Nevertheless, this species has seldom been reported from leaves – it usually grows on twigs.

Figure 88. Piper colubrinum; P. grande is an understory tree that hosts 55 species of epiphylls in the Panamanian premontane forest. Photo by Vinayaraj, through Creative Commons. Figure 86. Ephemeropsis trentepohlioides with capsules, a species with spores that can germinate in the capsule. Photo by David Tng , with permission.

Figure 87. Ephemeropsis trentepohlioides mature growth form of protonema that can cover a leaf. Photo by Bill and Nancy Malcolm, with permission.

Neoteny Pócs (1980) observed that young gemmalings of Lejeuneaceae with 2-3 pairs of leaves produced gametangia. Gemmae also apparently are important in the life cycle of foliicolous liverworts (Schiffner 1929) and gemmae production together with sexual reproduction may significantly accelerate their propagation (see also Schuster in Richards 1984b, p. 1270). In some foliicolous taxa sexual organs are produced "directly" on an expanded, persistent protonema which is thallose in Metzgeriopsis pusilla (see Figure 127) and Radula yanoella (Figure 89) (Schuster 1980) and filamentous in the moss genus Ephemeropsis (Figure 86-Figure 87) (Fleischer 1929; Tixier 1974). The vegetative leafy gametophore in these plants has almost completely become suppressed as the result of neotenic evolution. The neotenic life-cycle of foliicolous taxa may be seen as an adaptation to the relatively short life span of the "evergreen" host leaves and represents a striking example of an evolutionary strategy to survive the hazards of life in the tropical rainforest.

Chapter 8-6: Tropics: Epiphylls

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Syrrhopodon on leaf surface) or occupying over-mature center of round colonies (window contact of Kiss 1982) Accidental (non-adapted) settlers that cannot reach maturity after germination (non-epiphyllous bryophytes like Bazzania or Leucoloma)

Host Adaptations While epiphylls are not parasitic (Olarinmoye 1976), they can reduce photosynthesis and in some cases may encourage the growth of fungi by maintaining a higher humidity on the leaf surface. They can also block stomatal openings, hampering gas exchange. Hence, we might expect some trees to have evolved adaptations that discourage the growth of epiphylls.

Figure 89. Radula yanoella, a leafy liverwort with a thallose protonema. Photo by Michaela Sonnleitner, with permission.

Life Strategy Types Colonizers (primary Adhesive apparatus or colonists of Winkler 1967) hemiepiphyllous growth, abundant gemmae and spores temporary

Small size, short life cycle (e.g. Aphanolejeunea)

resistant

Appressed or subcuticular growth, or ciliae, setae, perpendicular structures, or size preventing overgrowth (Cololejeunea with hyaline margin, Colura)

Drip Tips Some leaves have special adaptations that permit them to slough off the cuticle on a regular basis, getting rid of the epiphytes at the same time (Attenborough 1995). Some tropical biologists have attributed the success of some leaves in preventing epiphyte colonization to the presence of a drip tip (Figure 90) that increases the flow of water from the leaf, thus making the habitat less hospitable for colonization (Briscoe 1994). For example, O'Brien (1994) asked if drip tips can affect the population dynamics of fungal pathogens and epiphyllous organisms such as bryophytes. Junger (1891) found fewer epiphylls on leaves with drip tips and believed that the tip was an adaptation to avoid interference with assimilation that could handicap the plant. He contended that taxa with rounded or cordate bases and rounded apices lacked any special adaptation for getting rid of water and appeared to support larger populations of epiphyllous plants (Junger, in Howard 1969).

Occupants (secondary colonists) overrunner and overgrower (see Kiss 1982)

Fast growth rate, loose, creeping habit or robust size (Radula flaccida, Diplasiolejeunea, Cheilolejeunea spp.)

squeezer (line contact Physical or chemical pressure of Kiss 1982) against another species (latter by Frullania) Explerents (sensu Ramensky 1938, tertiary colonists) space economizer

replacer

Utilizing space between other species, e.g. by hypophyllous growth, pendulous from leaf margin, e.g. Meteoriaceae) Settling in the debris of dead, decomposing plants (e.g.

Figure 90. Drip tips on sacred fig leaves. Photo by Challiyil Eswaramangalath Vipin, through Creative Commons.

However, recent experiments have shown that the tip does not increase the drying speed and thus the adaptive value in warding off epiphyllous taxa is doubtful. MongeNájera and Blanco (1995) noted that leaf substrates vary in both biochemistry and morphology. Using plastic ribbon

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Chapter 8-6: Tropics: Epiphylls

tape as artificial leaves the researchers found that the epiphyll cover differed little after nine months of exposure on five shapes and two sizes. Furthermore drip tips did not affect the epiphyll cover. But cover was four times higher in a clearing than in a shaded understory. Panditharathna et al. (2008) noted that drip tip (Figure 90) lengths were greatest in seedlings and least in canopy trees, an observation that would seem to negate likely benefits for epiphylls or for preventing their establishment on leaves. Lücking and Bernecker-Lücking (2005) found no significant difference in the development of lichen colonies on leaves with drip trips and those without. On the other hand, leaves lacking drip tips accumulated more debris in the apex and concomitantly few lichens in this region. It might be the same for bryophytes. The drip tips cause a difference in accumulated drop size and residence time on the leaf. On those leaves with drip tips, the water forms smaller drops that run off more frequently. Ivey and DeSilva (2001) experimented with drip tips (Figure 90) in Costa Rica (Figure 91) from 23 November to 2 December during the rainy season to see if having a drip tip reduces colonization. With a sample of 28 saplings and three leaves per tree for each treatment, they were unable to show any effect on the bryophytic epiphylls. However, fungi had greater cover on the leaves that were missing their drip tips. They found instead that the bryophytes tended to be on the drier parts of the leaves, away from bases, midveins, and tips. Fungi, on the other hand, tended to be in those very regions. Nonetheless, 9 days is much too short to expect much effect on colonization rate by bryophytes. Their experiment did demonstrate that the drip tip had little effect on helping the leaf to shed debris, but those with drip tips intact had significantly less water retention (about half) compared to those with the tip cut off. Ivey and DeSilva suggested that prevention of fungi might be the important adaptation and that epiphylls may not be a significant factor in reducing photosynthesis by the host leaves because of their slow growth. By the time they have achieved significant cover, the leaf is ready to senesce. But Ellenberg (1985) has argued that the tip is an environmental response to high humidity, not an adaptation to it, whereas Edmisten (1970b) has argued that it might reduce nutrient leaching. The latter might even be of some benefit to bryophytes if it means that more nutrients remain on the leaf and might help explain their greater abundance near the drier margins.

Figure 91. Montane oak forest in Costa Rica. Photo by Jorge Antonio Leoni de León, through Creative Commons.

Ellenberg (1985) discussed the drip tips found on many tropical leaves. They occur mostly in humid areas of warmer zones. The prevailing hypothesis was that these tips would facilitate drainage of water from the leaves, thus preventing growth of epiphyllic algae, lichens, and bryophytes. But this hypothesis was not supported by field observations or by experiments with leaves and leaf models. These tips typically develop before the leaf expansion and rarely develop after the leaf has expanded fully. Those tips that develop before the leaf expands expose the tips to the environment outside the buds. Their role, if any, in preventing epiphyll colonization remained a matter of conjecture. Leaf Size and Shape Monge-Nájera and Blanco (1995), also working in Costa Rica (Figure 91), likewise found that leaf shape had little or no influence on epiphyll cover. What did matter in their study was light. The epiphyllous cover in a clearing was four times that found in the dark understory of the tropical forest, regardless of leaf size or shape. However, in an earlier Costa Rican study, while finding a similar relationship between clearings and epiphyllous cover, Monge-Nájera (1989) found that epiphyllous cover increases more rapidly than the size of the leaves. This is somewhat offset by an increasing rate of herbivory on the epiphylls as the tree leaves increase in size. Epiphyllic cover is generally higher on larger leaves, as demonstrated by epiphyllous liverworts in Monteverde, Costa Rica (Figure 91) (Monge-Nájera 1989). Perhaps this is because the growth of the epiphylls increases more rapidly than does the leaf area. Once again, degree of epiphylly does not correlate with leaf shape. Surprisingly, both absolute and relative epiphyllic cover are higher in the forest clearing than in the understory. Monge-Nájera attributed this to the greater light in a region with overall high atmospheric humidity. The ratio of bryophytes to lichens in these communities depends on environmental conditions. Drier, more open habitats seem to favor lichens and are usually poor in bryophytes. The number of foliicolous species in one locality varies between 20-50 for lichens and 30-90 for bryophytes. A single leaf will average 5-25 lichen species and 3-13 bryophyte species, with a maximum of 45 and 20, respectively (Jovet-Ast 1949; Santesson 1952; Tixier 1966; Pócs 1978). The number of species increases with leaf area, to a maximum at 5-8 cm2 and remains more or less constant above that (Sjögren 1975; Pócs unpublished). Leaflets of compound leaves should in this respect be treated as separate leaves because the composition of the foliicolous communities often varies among the leaflets of one leaf. Leaf Age The number of species and individuals is also determined by the age of the host leaves. Richards (1932) observed a decrease of species number and increase in number of individuals with leaf age. However, Olarinmoye (1975c) and Pócs (1978) observed an increase in number of both species and individuals. On Marattia (Figure 92) fern leaflets Pócs observed an increase of the average plantlet number from 588 to 1754 per 100 cm2 within 1-2 years. One explanation for the observed differences in number of

Chapter 8-6: Tropics: Epiphylls

species is that as the colonies increase in size, competition may eliminate some of the species.

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Voglgruber (2011) reported that up to 80% of a leaf may be covered by epiphylls, where they can have a significant effect of reducing photosynthesis of the host leaf. Voglgruber studied the relationship in the humid tropical rainforest of Piedras Blancas National Park, Costa Rica. The rates of colonization were host specific. The fastest colonization was on Costus laevis (Figure 93) leaves; the slowest were on Asplundia pittieri (Figure 94) leaves, among the six species studied. Voglgruber tested the cuticles and identified long-chained alkanes, alkanols, sterols, and unidentifiable compounds. The species and leaf ages differed in wax composition. The data support the hypothesis that epicuticular wax chemistry has an effect on the growth of the epiphylls.

Figure 92. Marattia fraxinea; the genus Marattia serves as a substrate for epiphylls. Photo by Vassia Atanassova, through Creative Commons.

Leaf Longevity Coley et al. (1993) questioned whether long-lived leaves may attain a higher epiphyll cover as suggested by Richards (1954), Pócs (1982a), and Bentley (1987). This hypothesis had never been tested before. Coley and coworkers found that rather than having higher cover, these long-lived leaves actually have both lower colonization rates and lower accumulated cover throughout the life of the leaf. They suggest that characters that protect the leaves from herbivory and environmental events might also protect them from epiphylls. But they also suggest that there may also have been selection for leaf characters that specifically protect them from epiphyll colonization. They suggest that the rapid colonization on short-lived leaves would cause detrimental effects when persistent over long periods of long-lived leaves. One of the limiting factors that prevents bryophytes from making leaves their home is that the leaf is short lived and the bryophyte is slow growing. This generally limits colonization to those leaves that endure for more than one year and that live in regions where the atmospheric moisture or frequency of rain is ample for growth on a substrate that doesn't hold water. Leaf Chemistry On the other side of the story is the co-adaptation of the host leaf. Coley et al. (1993) found that longer-lived leaves actually had greatly reduced rates of epiphyll accumulation, suggesting that these leaves have some sort of defense against the epiphylls. Liverworts colonized 45% of the leaves with one-year lifetimes, but only 5% of longer-lived leaves. If this is indeed an adaptation against epiphylls rather than just an adaptation against pathogens (longer-lived leaves are known to have good defenses against pathogens), then it implies that epiphylls present a problem for their host leaves. On the other hand, liverworts may actually protect the host leaves from herbivory – see below, and may encourage the development of nitrogen-fixing Cyanobacteria (Figure 39).

Figure 93. Costus laevis, a species whose leaves are colonized quickly by epiphylls. Photo by Dick Culbert, through Creative Commons.

Figure 94. Asplundia pittieri with epiphylls, one of the species with the slowest epiphyll colonization rates. Photo from Earth.com, with permission.

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Interactions We might well ask if there is any advantage to the liverwort, or disadvantage to the host, resulting from this close association. Bentley (1987) reported that leafy liverworts, especially Lejeuneaceae (Figure 6-Figure 15), form dense coverage on leaves in the rainforest. Suitable leaves can be completely covered in only two years (Coley et al. 1993). Cornelissen and ter Steege (1986) suggest that the ecological and evolutionary effects of epiphylls on their host leaves may be significant. Working in a rainforest of Guiana, they examined the liverworts and lichens that formed the dominant epiphylls and demonstrated both positive and negative effects by the epiphylls. They also found that host leaf characteristics can influence the colonization rates of epiphylls. Nutrient Exchanges Host Leaf Leachates The role of leachates from the host leaf in the success of the epiphylls should not be ignored. Olarinmoye (1981, 1982) found that leachates and extracts of various tracheophyte leaves greatly increase extension growth of gemmaling shoots, leaf size, and rhizoid production of the leafy liverwort Radula flaccida (Figure 41), although they have no effect on the initiation of gemma growth. Rhizoid branching differs, depending on availability of the leachate, with long, straight and little-branched rhizoids when grown in leachates, but short, much-branched, and crooked rhizoids in some extracts. Extracts from Averrhoa carambola (Figure 95) killed all the cultures within four weeks. But are the liverworts ever exposed to the cell contents? We need tracer studies to determine if these extractable substances ever contact the liverworts. The leachates are available to them and have an important role in promoting the successful establishment and growth of these epiphylls, particularly in tropical areas with abundant annual rainfall. Often they provide nearly all of the nutrient supply.

Pócs (pers. comm.) observed that leaves of planted orange trees at Amani Station (Tanzania) with mass occurrence of aphids were covered by a sticky, sugarcontaining exudate that promoted copious colonization by epiphylls, mostly Leptolejeunea (Figure 14) sp. and also some specimens of Diplasiolejeunea cornuta. Bryophyte Leachates Montagnini et al. (1984) gathered indirect evidence that minerals are transferred from epiphylls to host leaves. They found that the concentrations of Cd, Pb, Ni, and Cr were higher in leaves that had epiphylls than in leaves that lacked them. The tropical Amazonian bryophytes usually have lower concentrations of heavy metals than in those from temperate zones, suggesting that long-range transport of these air pollutants is limited. It seems logical that if heavy metals in leaves increase as the result of epiphyll colonization, other nutrients might increase as well. Epiphylls live and die on the leaves where they live. Hietz et al. (2002) found a correlation in leaf delta 15N with that of epiphylls, suggesting that there was at least some exchange of nitrogen between the epiphylls and the host leaves (or that leaves with epiphylls might have more Cyanobacteria). Jordan et al. (1980) examined the role of bryophytes in scavenging nutrients from rainfall and subsequent nutrients in the throughfall in Venezuela. They hypothesized that nutrients were intercepted by epiphylls in the canopy, conserving nutrients in the forest. They supported this by demonstrating that nutrient flux of calcium, sulfur, and phosphorus in rainfall was greater than that in the throughfall. Ruinen (1965) reported that epiphylls on coffee leaves (Figure 96) can increase the coffee leaf nitrogen content by up to 60% in about one week due to the ability of the epiphylls to retain the nitrogen. These bryophyte (mostly liverwort) assemblages most likely help to maintain the necessary humidity and nutrient retention for the included micro-organisms to survive.

Figure 96. Coffee plantations with dwarf trees in the distance, in Colombia. Photo courtesy of Robbert Gradstein.

Figure 95. Averrhoa carambola leaves and fruits. Extracts from these leaves kill cultures of the leafy liverwort epiphyll Radula flaccida. Photo by Dinesh Valke, through Creative Commons.

Witkamp (1970) used paired leaf discs to compare retention of added elements by epiphylls from a tropical rainforest at El Verde, in El Yunque, Puerto Rico (Figure 97). He found that the epiphylls increased 137cesium by 6.7-20 times that of the cleaned leaf discs. For phosphorus it was 4.7-18.3, for manganese 1.7-4.7, and for strontium

Chapter 8-6: Tropics: Epiphylls

1.9-2.9. These numbers indicate the significant role that epiphylls can play in mineral nutrient retention.

Figure 97. El Yunque forest, Puerto Rico. Photo by Matt Shiffle, through Creative Commons.

Volcanic activity can be a major contributor to bryophyte nutrients. Baudoin (1985) reported that epiphyllous bryophytes can be used satisfactorily as indicators of volcanic air pollution and nutrient contributions. Similarly, Witkamp (1970) used epiphyllous bryophytes in studies of irradiation at El Verde, Puerto Rico (Figure 97) by measuring mineral retention. According to Pócs (1990) near the Great African Rift Valley with active soda volcanoes, leafy epiphylls do not occur at all, even in wet rainforests, due to the alkalinecontaining dust accumulated in the soil, air, and on the bryophyte substrates including leaf surfaces, and their components accumulate even in the epiphytic mosses. Seed Beds In some cases, old leaves have such a dense covering of bryophytes (Figure 98) that seeds of epiphytic flowering plants germinate there (Richards 1932) or spores of ferns – a disadvantage to the host plant, no doubt, but possibly an advantage to that tracheophyte.

Figure 98. Dense covering of bryophytic epiphylls on a palm in Guyana. Photo copyright Patrick Blanc, with implied online permission.

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Nitrogen Fixation Zhou et al. (2009) noted that epiphylls obtain their nutrients independently. However, there are indications that substances can be exchanged between epiphylls and host plants. They report that nitrogen fixation within the epiphyll community provides 10-25% of the nitrogen for the understory forest in tropical ecosystems. Nitrogen fixation is the process of converting atmospheric nitrogen into a form that is usable by plants, typically to NH4+. The most important contribution of epiphylls to leaves is most likely through the nitrogen-fixing organisms they harbor. Nitrogen-fixing Cyanobacteria (Figure 39), particularly Scytonema (Figure 39) (Basilier 1979), are often associated with the epiphyllae, and this added nitrogen could be of benefit to the host leaf as well. Bentley (1987) suggested that epiphyllous bryophytes, especially liverworts in the Lejeuneaceae (Figure 6-Figure 15), enhance moisture levels, permitting nitrogen-fixing bacteria to subsist. Bentley and Carpenter (1980) found that epiphyllous liverworts improve the microenvironment for Cyanobacteria and other nitrogen-fixing bacteria by increasing the leaf moisture. Using radioactive tracers, Bentley and Carpenter (1984) were able to show a direct transfer of fixed N from the epiphyllous micro-organisms to the host leaf on the palm Welfia georgii (Figure 17) and estimated that such transfer could account for 10-25% of the host leaf N content. Most of the N fixation appeared to occur among filamentous Cyanobacteria associated with leafy liverworts, as well as within a thick layer of coccoid Cyanobacteria immediately above the leaf cuticle (Carpenter 1992). Nitrogenase activity, indicating nitrogen fixation, in the W. georgii association produces about 270 mg N per ha daily. Furthermore, this association may benefit the forest as water dripping from these leaves is enriched in nitrogen compared to rainwater (Richards 1984a). Bentley and Carpenter (1980) examined the effects of desiccation on nitrogen fixation rates among epiphylls. Fixation on leaves that had been dried for 12 hours was only 0.66 ng N per 10 cm2 h-1, whereas that on continuously hydrated leaves was 18.69 ng N per 10 cm2 h-1. Intermediate rates occurred after 2 and 4 hours of rehydration. The bryophytic epiphytes helped to maintain moisture on the leaf surface, prolonging the duration of fixation. In general, Cyanobacteria (Figure 39) are the typical contributors of nitrogen fixation on leaves. Bentley (1987) considered glucose and mineral nutrients leached from host leaves, light intensity, and desiccation to be the major influences on the co-occurrence of the Cyanobacteria and epiphyllous bryophytes. Bentley found that a significant portion of the fixed nitrogen is transferred to the host leaf and may contribute 10-25% of the total nitrogen in the leaf. The bryophytes most likely contribute to the fixation rates by maintaining moisture longer than leaves with no epiphylls. Although desiccation has a dramatic effect on fixation, recovery is quite rapid, reaching the levels of moist controls within 4 hours. Berrie and Eze (1975) contend that the bryophytes are also able to draw water from the host leaves, contributing further to maintaining moisture for the fixation. Low light reduces the rate of fixation. The water flowing on a leaf actually has less

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nitrogen than rainfall collected in the open, suggesting very efficient uptake mechanisms on the leaf surface. High N fixation rates are associated with dense cover of epiphyllous bryophytes, especially for leafy liverworts in the Lejeuneaceae (Figure 6-Figure 15). Bentley suggested that the bryophytes enhance the moisture levels on the leaf, encouraging microbial growth. One can observe that a few hours after rain, when the naked leaf surface is already dry, under the cover of epiphylls a still good amount of moisture is preserved. Roskoski (1980) measured nitrogen fixation by epiphylls on coffee (Coffea arabica; Figure 99). The C2H2 reduction (a measure of N fixation) was similar at all sites in Vera Cruz, Mexico, despite differences in shade, averaging 3.21 nmoles C2H2 reduced per leaf with epiphylls per day. This suggests that the shading/light intensity within the range encountered was unimportant in the fixation rate. Furthermore, he found no correlation between percent epiphyll cover and magnitude of nitrogenfixing activity. Roskoski concluded that the nitrogen fixation associated with epiphylls is not an important N source for that coffee ecosystem.

Figure 99. Coffea arabica, a species that commonly hosts bryophytic epiphytes, with fruit, in Hawaii. Photo by Forest and Kim Star, with permission.

For the epiphyllous liverworts living on leaves of the undergrowth, as opposed to higher levels of the canopy, these Cyanobacteria (Figure 39) may even be a necessity. Canopy leaves and epiphytes remove so much of the nutrients before the rainfall reaches the lower branches that liverworts like Radula flaccida (Figure 41) are likely to be nutrient limited (Olarinmoye 1975a). In support of this suggestion, Olarinmoye found that the standard bryophyte media used by other researchers (Diller et al. 1955; Basile 1965; Bennecke in Schuster 1966) caused aberrant plants, and he was forced to reduce the concentration to 10-20% of the standard. The greatest percent of buds producing leafy shoots occurred in the 10% solution; growth was highest in the 10 and 20% media as well. Even in distilled water the gemmalings exhibited appreciable growth extension, although they were not as healthy as in the diluted nutrient media. Wanek and Pörtl (2005) acknowledged the role of freeliving nitrogen-fixing organisms and throughfall to provide nutrients to epiphyllous bryophytes, but added that the

bryophytes also obtained nutrients from leachates of the host leaf. On the other hand, bryophytic epiphylls lose quantities of nutrients after drying events, and these can be absorbed by host leaves. However, when the researchers measured the nitrogen leachates from the epiphylls of four species in a lowland tropical wet forest in Costa Rica, they contributed less than 2.5% of the lost leaf N after 14 days. Nevertheless, 180 days of observations demonstrated that the nitrogen in the phyllosphere was highly dynamic, with the bryophytes at times being sinks and other times being sources. Freiberg (1994, 1998, 1999) measured nitrogen fixation on leaves in a premontane rainforest in Costa Rica. He found maximum rates on 26 ng N cm-2 leaf area h-1 and determined that two species of Scytonema (Sc. javanicum, Sc. hofmannii – Figure 39; Cyanobacteria) contributed most of that. The rates of fixation correlated with the leaf area covered by Scytonema. This fixation was dependent on rainfall and ceased completely in 2-3 days with no precipitation. Liquid water was necessary – fog and mist were not helpful. Light and temperature both influenced the rate. In a follow-up study, Freiberg (1999) identified seven species of epiphyllous Cyanobacteria in a primary premontane rainforest in Costa Rica. Harrelson (1969) further discussed the epiphyllae of tropical leaves and their relationship to nitrogen fixation, noting that nitrogen fixation was greater in leaves with epiphylls. Goosen and Lamb (1986) measured nitrogen fixation associated with leaves in one tropical and two subtropical rainforests. Herbivore Protection Coley et al. (1993) found that Cololejeunea (Figure 13), Leptolejeunea (Figure 14), and Lejeunea (Figure 3) (all Lejeuneaceae) were common epiphylls. They hypothesized that the liverworts might protect their host leaves from herbivores. Liverworts are known for their rich terpenoids, and experiments show that leaf cutter ants (Figure 100) prefer leaves with no epiphylls. On the other hand, the epiphylls hold moisture that may increase pathogenic infection. The epiphylls also block light, reducing photosynthesis, possibly making the leaves a less desirable food source.

Figure 100. Atta cephalotes carrying a cut piece of a leaf. Photo by Jim Webber, through Creative Commons.

Epiphylls have a little more direct relationship with the leafcutter ants (Atta cephalotes; Figure 100), albeit a

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negative one. These ants are known for their attacks on leaves. When Wetterer (2003) removed the epiphylls from the base and two side branches of a grapefruit (Citrus paradisi; Figure 101), the ants chose to cut leaves from the cleaned branches nine out of ten times. This behavior suggests that the epiphylls provide protect the host leaves from the leafcutter ants.

Figure 103. Leaf cutter ant consumption on old and young leaves of Citrus paradisi with epiphylls undisturbed and epiphylls removed. Error bars represent one standard error. Modified from Mueller & Wolf-Mueller 1991.

Figure 101. Citrus paradisi, a species on which epiphylls seem to provide protection from leafcutter ants that would eat the leaves. Photo by Amada44, through Creative Commons.

For some leaves, the antiherbivore role may be significant. For example, in Costa Rica, leafcutter ants (Atta cephalotes; Figure 100) preferentially clipped leaves of Citrus paradisi (Figure 101) and Cyclanthus bipartitus (Figure 102) from which epiphylls had been removed (Figure 103-Figure 104) (Mueller & Wolf-Mueller 1991). This benefit may be derived from the greater processing effort required of the ants when epiphylls cover the leaves or from decreased palatability due to secondary compounds found in epiphyllous lichens and bryophytes. In particular, liverworts are rich in terpenoids that are toxic to both the leafcutter ants and the fungus they cultivate (Hubbell et al. 1983; Howard et al. 1988; Coley et al. 1993). Citrus leaves with epiphylls are less preferred by leaf cutter ants, most likely due to these terpenoids (Coley et al. 1993).

Figure 102. Cyclanthus bipartitus, having leaves that are eaten by leafcutter ants. Photo by David J. Stang, through Creative Commons.

Figure 104. Leaf cutter ant damage on leaves of two species of tropical plants; leaves have epiphylls retained and epiphylls removed. Error bars represent one standard error. Modified from Mueller & Wolf-Mueller 1991.

In a southern Ecuadorian montane rainforest, Bodner et al. (2015) found many caterpillars (Lepidoptera) that were not feeding on leaves as might be expected. Instead, they feed on lichens, dead leaves, and epiphylls, including bryophytes. Bodner et al. (2011) conducted feeding trials with caterpillars in the Montane Forest Zone in Southern Ecuador. They found that more than 22% of the caterpillars did not eat the leaves, but rather ate dead leaves and epiphylls. In some cases, up to 80% were epiphyll consumers. Similarly, Callaghan (1992) found that the butterfly Pentila picena cydaria (Figure 105) laid its eggs singly on live trees that were covered with lichens and mosses in a Nigerian cola forest. The initially white eggs soon became dark brown (within a day). The caterpillars subsequently fed on the epiphylls.

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Chapter 8-6: Tropics: Epiphylls

Figure 105. Pentila picena cydaria, a species whose caterpillars feed on epiphylls. Photo by Grose-Smith and Kirby, through public domain.

Yet another butterfly, Sarota gyas (Figure 106), uses the epiphylls (DeVries 1988). The larvae of this species rest on the upper surfaces of leaves and feed on the epiphylls, where they blend in. The epiphylls are primarily Cyanobacteria (Figure 39) and leafy liverworts in the Lejeuneaceae (Figure 6-Figure 15). Others (Lycaenidae: Lipteninae) in the Nigerian cola forest feed on epiphyllic lichens and fungi as larvae (Callaghan 1992).

Figure 106. Sarota gyas in Ecuador, a species whose larvae feed on the epiphylls. Photo by Harold Greeney, through Creative Commons.

Micro-organisms The same lobules that hold water for the leaves of many epiphyllous liverworts also serve as the habitat for some species of protozoa (Barthlott et al. 2000). In the liverworts Pleurozia (Figure 107) and Colura (Figure 108), the openings of these sacs can be closed by a movable lid. This caused some researchers to hypothesize that sacs could trap small animals, a theory that they supported by finding ciliate protozoa in them. These protozoa feed on bacteria on the surface of the plants, but there seems to be no evidence that there is any mechanism to attract the protozoa to the liverwort. Hence, there is thus far no evidence that the protozoa provide any useful function for the liverwort leaves.

Figure 107. Pleurozia purpurea showing lobules with several of the protozoan Blepharisma living in them. Photo courtesy of Hess.

Figure 108. Colura saccophylla SEM showing lobules. Photo by John Braggins, with permission.

Epiphyllous bryophytes can provide a suitable habitat for a number of kinds of micro-organisms, and the role of these micro-organisms in affecting the health of the host is largely unknown. Leafy liverworts in Ecuador, Costa Rica, and Puerto Rico support the growth of at least eleven species of slime molds (Myxomycetes), especially in lowland rainforests with high annual rainfall (Schnittler 2001). Among these, Arcyria cinerea (Figure 109), Didymium iridis (Figure 110), and D. squamulosum (Figure 111) have the most common (frequency of 5966%). While these produce visible sporocarps in culture, it is likely that they exist in their amoeboid stage among the epiphylls, in which case they may contribute to controlling bacteria.

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community has experienced few studies, and more information is needed to asses how it affects the epiphyllous bryophytes and vice versa. Negative Impacts on Leaves

Figure 109. Arcyria cinerea, a species that often occurs on leafy liverworts in the Central American tropics. Photo by Malcolm Storey, through Creative Commons.

Most of the impacts of epiphylls on their host leaves seem to be positive. However, epiphyll rhizoids may actually penetrate the epidermal cells of the host, presumably serving as a means of anchorage (Berrie & Eze 1975). This can result in the death of some leaf epidermal cells, permitting more rhizoids to enter. It appears that this penetration contributes to water loss, as leaves with extensive epiphyllous colonies and those stripped of their epiphyllae both have a high evaporative loss compared to uninhabited leaves of the same age. Further detriment to the leaf may occur if the sites of penetration serve as entry points for leaf pathogens. So far, this has not been demonstrated, except for senescent leaves. (But could it be that the penetration has contributed to the senescence?) Light Interference

Figure 110. Didymium iridis, a species that often occurs on leafy liverworts in the Central American tropics. Photo by Sava Kristic, through Creative Commons.

Figure 111. Didymium squamulosum, a species that often occurs on leafy liverworts in the Central American tropics. Photo by BioImages, the Virtual Field Guide, through Creative Commons.

A number of ascomycetous fungi parasitize epiphyllous liverworts. According to Döbbeler (1997) and Döbbeler and Hertel (2013) more than 400 known fruitbody-forming species of Ascomycetes (Figure 41) occur obligately on the gametophytes of mosses and hepatics. A good portion of them is specialized to epiphyllous liverwort hosts. Küttner (2005) used 4x4 cm leaf squares to investigate parameters that controlled epiphyllous micro-organisms in a tropical humid lowland rainforest in Costa Rica. The size of these microbial communities was influenced by both species and leaf age of the host leaf. On the other hand, site had little or no effect on the composition or size of the epiphyllous microbial community. This microbial

In some areas, the bryophytes become so abundant that they can seriously interfere with photosynthesis by intercepting the light (Attenborough 1995). In other cases, light interference is scant; Eze and Berrie (1977) found that even under the heaviest colonization of Radula flaccida (Figure 41), only 2% of the light was intercepted by that liverwort. They found no difference in the chlorophyll content of colonized and uncolonized parts of the host leaf. Furthermore, they found no loss of photosynthetic product from the host to the epiphyll, or from epiphyll to host. Coley et al. (1993) found that epiphyllous liverworts in several locations in Panama transmitted 44% of the light through liverworts in a single layer and that transmission did not differ between saturated and blotted dry liverworts. Conflicting reports on the effects of epiphylls on Cacao trees have been discussed above. Roskoski (1981) found that the number of leaves with epiphylls is lowest on Coffea arabica (Figure 99) in a shadeless site. The percent cover of epiphylls is inversely related to the number of young coffee leaves, making them highest in February and lowest in May. Height strata have no significant effects on number of leaves with epiphylls. Epiphylls do affect the host leaves by reducing the photosynthetic area of the trees, with shading ranging 0.5-19.7%. Nevertheless, the epiphylls do not seem to cause any detrimental effects on the coffee productivity. Zhou et al. (2014) compared the effects of lichens vs liverworts on host leaf traits in the tropical montane rainforest, Hainan Island, China. They studied effects of epiphyllous lichens, liverworts, and uncolonized leaves on leaf characters of Photinia prunifolia (Figure 112). Colonization by lichens significantly decreases leaf water content, chlorophyll a and a + b content, whereas liverworts have no effect on these. Furthermore, lichens have more effect on net photosynthesis than do liverworts. Lichens caused an increase in leaf light compensation point by 21% and a decrease of the light saturation point by 54%, whereas liverworts exhibited contrary effects. This study suggests that the type of epiphyll is important in assessing potential decreases in productivity of the host plant.

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species reported, 14 of which were endemic to the Azores or to Macaronesia. Nan and Zhu (2007) reported a much smaller number of species (19 epiphyllous liverworts) in the Maoershan Nature Reserve, Guangxi, China. Boecker et al. (1993) reported on epiphylls of the Canary Islands. Table 1. Number of epiphyllous liverwort species known in genera having pantropical distribution, based on Pócs 1978. These constitute 60% of the ~1000 foliicolous liverwort species described at the time. Revisions have eliminated some of these species.

Neotropics Figure 112. Photinia prunifolia, a species of the moist tropical forest. Photo by Caroline Léna Becker, through Creative Commons.

Composition Communities

and

Distribution

of

Based on studies through the 20th century, Pócs (unpublished) considered indications that some genera or species are typical for certain geographic or vegetational units or altitudinal belts. In Africa, for example, Radula flaccida (Figure 41), Cololejeunea auriculata, C. jonesii, and all species of Leptolejeunea (Figure 14) seem to be typical of lowland rainforest, whereas Radula stenocalyx, Cololejeunea jamesii, C. malanjae, C. tanzaniae, C. zenkeri, and all species of Drepanolejeunea (Figure 9) seem to be restricted to submontane and montane forest habitats. Ericaceous heaths have endemic species of Colura (C. berghenii, C. hedbergiana, C. ornithocephala, and C. saroltae) that are apparently restricted to ericaceous leaves and twigs. Within the montane rainforest habitat Tixier (1966) was able to distinguish the lower and upper strata by their characteristic foliicolous communities. Winkler (1970) found a significant correlation between certain groups of species within the same geographic area. Host preference allows two different foliicolous communities to occur at close distances, e.g. on evergreen shrubs and on filmy ferns within the same forest habitat (Pócs 1978).

Species Richness As already noted, the most common of the epiphyllous species are in the leafy liverwort family Lejeuneaceae (Figure 6-Figure 15), a dominant member of the epiphyllous bryophyte flora in lowland rainforests (Piippo 1994). Many of these species are endemic, for example 20.5% in Western Melanesia [Papua New Guinea, Papua (West Irian), and the Solomon Islands]. The family Lejeuneaceae (Figure 6-Figure 15) is repeatedly considered the most diverse and abundant family among the epiphylls. However, the species and even the tribes differ by continent and between the Old World and Neotropics. Many of the epiphyllous species extend outside the tropics into the Macaronesian Azores, Madeira, and the Canary Islands. Even in these subtropical locations, several of the species belong to typical tropical families of Lejeuneaceae and Radulaceae (Figure 16) (Sjögren 1997). These islands had 89 epiphyllous

Aphanolejeunea Colojeunea Colura Diplasiolejeunea Drepanolejeunea Leptolejeunea Microlejeunea Radula sec epiphyllae

24 40 14 19 34 11 12

Africa incl islands 9 72 18 28 18 5 6

Asia, Oceania, Australia 8 41 41 8 37 24 11

6

5

8

The epiphyll richness varies with altitude differently in the different parts of continents or islands. In continental East Africa the highest epiphyllous diversity occurs at 1500-1800 m near the coast and at 1800-2500 m inside the continent (Pócs 1978, 1994), while in more oceanic conditions, like in the Indian Ocean islands (Mascarenes, Seychelles) we can observe the highest epiphyllous diversity already from 600 m above the sea level. Asia In India, the epiphyllous species of liverworts are restricted to the Eastern Himalayas, South India, and Andaman and Nicobar Islands (Lal 2003). By 2003, only a small number of epiphyllous species were known; 39 species in 14 genera were all that had been identified. These were in only three families: Lejeuneaceae s.l. (Figure 6-Figure 15), Radulaceae (Figure 16), and Metzgeriaceae (Figure 19). But Dey and Singh (2012) soon reported 89 taxa of epiphyllous liverworts from the Eastern Himalayas, of which 66 species belong to Lejeuneaceae. Gao and Be (1988) identified 12 species of epiphyllous liverworts from Daiwa Shan, Jiulong, China. Despite the small number of species, these represented 10 genera and 5 families, occurring at 650 m asl. As has been common when exploring these small organisms, these researchers found that five of the genera and six of the species were new to China. Ji and Wu (1996) reported only 10 species in 1 family and 4 genera from Jinggangshan Nature Reservation, Jiangxi Province. Nevertheless, one species was new for China. When Li and Wu (1992) assessed epiphyllous liverworts from Heishiding Natural Reserve, Guangdong Province, China, they reported only 13 species in two families and 7 genera. The most common species among these were Leptolejeunea elliptica (Figure 14) and Radula acuminata (Figure 35). Leptolejeunea hainanensis and Cololejeunea floccosa (Figure 113) occur in the broadleaved forests in ravines at 350-600 m asl.

Chapter 8-6: Tropics: Epiphylls

Figure 113. Cololejeunea floccosa, an epiphyllous liverwort species that occurs in the broad-leafed forests in ravines at 350600 m asl in Guangdong Province, China. Photo by Yang Jiadong, through Creative Commons.

Liu et al. (1988) found slightly more species (17 species) when investigating the epiphyllous liverworts from southern parts of Anhui Province, East China. Nevertheless, these occurred in only 10 genera and 4 families. Not surprisingly, 11 of these species were new for the province. Only one was new for China. The researchers were unable to show any obligate relationship between the epiphyllous liverworts and the host species. They did determine that leaves that were thin, soft, and/or rough were less suitable for these liverworts than those that were thick, rigid, and smooth. They surmised that the distribution of these liverworts is currently much narrower than it was in the distant past. Zhu et al. (1994) found a greater species richness at the Fengyangshan Nature Reserve, Zhejiang Province, China. They identified 33 species of epiphyllous liverworts. These researchers found two species new to China. Among the more diverse assemblages of epiphyllous bryophytes in China, the Wuyanling of Zhejiang Province supports 18 species, in 3 families and 13 genera (Zhang & Hu 1991). Rhaphidolejeunea foliicola (Figure 114) and Leptolejeunea elliptica (Figure 14) are the dominant epiphyllous liverworts in the region. Most of the epiphyllous species occur on leaves of Ilex latifolia (Figure 115), Symplocos sumuntia (see Figure 116), Trachelospermum jasminoides (Figure 117), and Rhododendron ovatum (Figure 118).

Figure 114. Raphidolejeunea foliicola, a dominant epiphyll of the Wuyanling of Zhejiang Province, China. Photo from , permission unknown.

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Figure 115. Ilex latifolia, a host for epiphyllous bryophytes in China. Photo by Kristine Paulus, through Creative Commons.

Figure 116. Symplocos cochinchinensis with a variety of epiphylls, including leafy liverworts; Symplocos sumuntia is a host for epiphyllous bryophytes in China. Photo by Vinayaraj, through Creative Commons.

Figure 117. Trachelospermum jasminoides, a host for epiphyllous bryophytes in China. Photo by Ανώνυμος Βικιπαιδιστής, through Creative Commons.

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Zhu et al. (1992) found 27 epiphyllous liverworts in Babaoshan, Guangdong, China. Even this larger number is only distributed in 6 families. The dominant epiphyllous species are Radula acuminata (Figure 35), Leptolejeunea elliptica (Figure 14), and Cololejeunea spinosa (Figure 120).

Figure 120. Cololejeunea spinosa epiphyllous on a fern. Photo by Ying Jia-dong, through Creative Commons.

But et al. (2000) examined the epiphyllous liverworts on rosette leaves of Ardisia (Figure 121) species in China. This species in China, including Hong Kong, hosts only 12 species of epiphyllous liverworts, but these include 9 genera. There is no apparent species-specific relationship to the hosts. Figure 118. Rhododendron ovatum, a host for epiphyllous bryophytes in China. Photo from Horticultural Society of London, through public domain.

Ji et al. (2001) found 14 epiphyllous species in the Matoushan Nature reserve of Jiangxi Province, China. These occur at 450-950 m asl in evergreen broad-leaved forests. They are distributed in 5 families and 10 genera. Leptolejeunea elliptica (Figure 14) and Lejeunea flava (Figure 119) are the most common of these species.

Figure 121. Ardisia crenata. In China members of this species host only 12 species of epiphyllous liverworts. Photo by Kenpei, through Creative Commons.

Figure 119. Lejeunea flava, a common facultative epiphyllous species in the evergreen broad-leaved forest of Jiangxi Province, China. Photo by Scott Zona, with permission.

But and Gao (1991) identified 28 species of epiphyllous liverworts from 25 sites in the Kowloon Peninsula, Hong Kong. These are mostly located at 30-200 m asl. Summarizing the epiphyllous liverworts known in China up to the year 1990, Luo reported 102 species, in 11 families and 32 genera (Luo 1990). Of these, the largest family is the Lejeuneaceae (Figure 6-Figure 15) with 21 genera and 85 species. Cololejeunea (Figure 6, Figure 13, Figure 113) is the largest genus, which has altogether 48 epiphyllous species in China according to Zhu and So (2001).

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Some of the Chinese epiphyllous liverworts are facultative, occurring on soil rocks, and tree trunks. These include Calypogeia (Figure 122), Cephaloziella (Figure 123), Frullania (Figure 20), Lepidozia (Figure 124), Metzgeria (Figure 19, Figure 127), Plagiochila (Figure 73), Porella (Figure 125), and Radula (Figure 16, Figure 35). In China, the epiphyllous species extend to 31º N. Most of the Chinese species occur in the South Yangtzi River areas at 200-2,800 m asl, where warm, moist air currents come from the Pacific and Indian Oceans, there is considerable geographical relief, and several large rivers add to the moisture.

Figure 125. Porella perrottetiana; the genus Porella is a facultative epiphyll in China. Photo by Yang Jia-dong, through Creative Commons.

Figure 122. Calypogeia tosana; the genus Calypogeia is a facultative epiphyll in China. Photo by Yang Jia-dong, through Creative Commons.

Figure 123. Cephaloziella integerrima; the genus Cephaloziella is a facultative epiphyll in China. Photo by David T. Holyoak, with permission.

Figure 124. Lepidozia reptans; the genus Lepidozia is a facultative epiphyll in China. Photo by Yang Jia-dong, through Creative Commons.

More recently, Zhu and So (2001) studied the epiphyllous liverworts of China, recording 168 species. Of these, 14 are endemic. They recognize obligate, common facultative, and occasional epiphylls. In China, the epiphylls prefer tropical and subtropical forests with evergreen, thick, hard, smooth leaves. These epiphylls are most common in Yunnan, Hainan, and Taiwan, where they are highly frequent in the cloud-zone forests at 800-1500 m asl. Jiang et al. (2014) identified six core distribution areas for the epiphyllous liverworts of China, concluding that it was the macrohabitat factors that most affected their distribution. The genera of Chinese epiphylls tend to be pantropical in their distribution. In subtropical evergreen forests of southeast China, Wu et al. (1987) found four leafy liverworts to be dominant, each in a genus that is common throughout the tropics [Leptolejeunea (Figure 14), Radula (Figure 16), Cololejeunea (Figure 6), and Frullania (Figure 20)]. The genus Cololejeunea (Figure 6, Figure 13, Figure 113) preferentially lives on leaf surfaces or other aerial parts of tracheophytes in wet forests (Yu et al. 2014). Among 70 species of Cololejeunea in their study, Yu and coworkers found that there were only weak correlations between morphological variations and species diversity. These differences were not linked to epiphytism, although some characters did show positive or negative relationships. Cololejeunea is described by its small gametophyte size and the occurrence of adaptive features such as compressed, thin stems, lack of underleaves, inflated lobules, and asexual propagules (Gradstein 1997b; Gradstein et al. 2006; Kraichak 2012). It is able to live on substrates that are extremely ephemeral, smooth, have limited access to nutrients and water, and may have exposure to light (Yu et al. 2014). Diplasiolejeunea (Figure 11, Figure 23, Figure 126) is an epiphyllous genus with a pantropical distribution (Dong et al. 2012). It ranges from lowlands to more than 4,000 m asl. In contrast to Cololejeunea (Figure 6), these species prefer to live on leathery, harder leaves. Their morphological diversity hides their genetic diversity, with four morphologically semi-cryptic species. Based on

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molecular data, the genus exhibits a deep split into a Palaeotropical (relating to phytogeographical kingdom comprising Africa, tropical Asia, New Guinea, and many Pacific islands, excluding Australia and New Zealand; Old World tropics) clade and a Neotropical (North, South, and Central American tropics) clade. Nevertheless, D. cavifolia (Figure 11) and D. rudolphiana (Figure 126) remain valid pantropical species, providing evidence for transcontinental dispersal from the Neotropics to the Palaeotropics. The molecular data support the subgenus Physolejeunea (Figure 23) as Palaeotropical and the subgenera Austrolejeuneopsis (Figure 126) and Diplasiolejeunea (Figure 11) as Neotropical. The subgenus Physolejeunea is primarily epiphytic, whereas Austrolejeuneopsis and Diplasiolejeunea are primarily epiphyllous. But these disjunct subgenera also separate on ocelli, which are present in Diplasiolejeunea and absent in Physolejeunea and Austrolejeuneopsis.

Figure 127. Metzgeriopsis growing on a palm leaf on Bukit Larut, Malaysia, 1100-1200 m, with bryologist Kien Tai Yong left. Photo courtesy of Robbert Gradstein. Figure 126. Diplasiolejeunia rudolphiana (subgenus Austrolejeunepsis) from the Neotropics. Photo by Michael Lüth, with permission.

A number of other Chinese studies on epiphylls have been published: Chen & Wu 1964; Wu & Lou 1978; Wu et al. 1983; Wu & Guo 1986; Dengke & Wu 1988; Li & Wu 1988; Li 1990, 1997; Ji & Liu 1998; Ji et al. 1998a, b, 1999, 2001; Peng et al. 2002. Asia and the Pacific are home to the epiphyllous liverwort Metzgeriopsis (Figure 127). One unusual epiphyllous moss species, Ephemeropsis tjibodensis (Figure 128), forms horizontal protonemata on monocots, whereas it grows on lawyer vines and broad-leaved trees in Malaya and Queensland, Australia (Goebel 1888; Győrffy 1916; Richardson 1981). These protonemata have photosynthetic side branches that grow upwards and end in long bristles. The basal protonemata have holdfasts that attach the moss to the leaf surface. The leafy gametophore and capsule, on the other hand, are both quite small (Bower 1935). Meijer (1972) found only one location in West Sumatra where the moss had capsules, and suggested that we need to include studies on all the epiphyllous liverworts associated with this moss to get clues as to the longdistance recent dispersal versus the ancient distribution of this unusual moss.

Figure 128. Ephemeropsis tjibodensis protonematal mat on a palm leaf in Fiji. Photo by Tamás Pócs, with permission.

In southern Thailand, the most recent study reports that epiphylls number 54 liverwort species and 1 moss species (Pócs & Podani 2015). Additional studies on epiphylls include those of Japanese researchers Horikawa (1932, 1939, 1948), Kamimura (1939), Tixier (1966), and Mizutani (1966, 1975).

Chapter 8-6: Tropics: Epiphylls

South Pacific Islands Kraichak (2013) studied the epiphyllous bryophytes on the island of Moorea, French Polynesia (Figure 129). As leaves age and epiphyll succession occurs, there are significant changes in abundance, species richness, and composition. These successional changes in epiphylls on Inocarpus fagifer (Figure 130) do not follow any single trajectory, causing older leaves to have divergent communities.

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Piippo (1994) found that 20.5% of the western Melanesian and Malaysian Lejeuneaceae (Figure 6-Figure 15) were endemic, but this is actually somewhat lower than the figure for liverworts in general (38.2%). She attributed the smaller number of endemic Lejeuneaceae to the many epiphyllous taxa. The epiphyllous taxa tend to be particularly widespread in the lowland rainforests. Eggers and Pócs (2010) added 13 new epiphyllous liverwort species new to the flora of Samoa (Figure 131) in the South Pacific islands. Söderström et al. (2011) reported more than 70 epiphyllous liverwort and hornwort species from Fiji Islands. Our understanding of dispersal patterns and mechanisms, as well as the ecology, will remain poor until we have a better understanding of the distribution of the species in these poorly studied areas.

Figure 129. Polynesia – Moorea Island. Photo by Anne Caillaud, through Creative Commons.

Figure 131. American Samoa forest. Photo from US Department of Agriculture, through public domain.

Africa

Figure 130. Inocarpus edulis, an epiphyll host. Photo by Tau'olunga, through Creative Commons.

In Africa, epiphyllous bryophytes have not been studied in many areas. Busse (1905) was among the first to become intrigued with identifying these bryophytes in Africa He wrote eight pages on the occurrence of these epiphylls in the rainforest of Cameroon. Pócs has been one of the early explorers of the African epiphylls (e.g. Pócs 1975). In 1978 Pócs reported 185 species of epiphyllous bryophytes for the entire continent of Africa. In a country where many areas have not been explored, this number is likely to be a very low estimate. Pócs and Tóthmérész (1997) found an average of 8-9 species per leaf in epiphyllous communities in East Africa (Figure 132) and the nearby Indian Ocean islands. Degraded habitats are more likely to have only 3-4 species. The number of species within habitats varies from 14 to 25. Nevertheless, this total number does not correlate with habitat degradation due to increased beta diversity (ratio between regional and local species diversity).

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Figure 132. Uganda – Murchison Falls, Nile River, in East Africa. Photo by Rod Waddington, through Creative Commons.

On Bioko Island in Equatorial Guinea, Müller and Pócs (2007) found 57 species of epiphyllous bryophytes, of which 55 were liverworts and 2 were mosses. One of these, Cololejeunea papilliloba (Figure 133) was new to Africa. Only 24 of the liverworts were previously known to the island.

Figure 134. Nyika miombo, Malawi, showing diminishing forests in the background. Photo by Dr. Thomas Wagner, through Creative Commons.

Host leaf size, age, and texture play important roles in the distribution of East African (Figure 132) epiphylls (Pócs 1978). Pessin (1922) found that some types of leaves are preferred and others avoided. Host specificity may play a role based on longevity of the leaf, water-holding capacity, overgrowth by mold, and other factors. Wetability is important – essential – but it is the glabrous (smooth) and leathery leaves that are usually colonized. This most likely is because these are the persistent leaves, and that longevity is necessary for the bryophytes to become established. But in many rainforests, it seems that host specificity is of little importance. Olarinmoye (1971, 1975a) found similar growth of Radula flaccida (Figure 41) on leaves of eight different taxa in a laboratory experiment. And in western Nigeria (Olarinmoye 1975b), he found no specificity among the bryophytes for any particular tree species. Neotropics Central America

Figure 133. Cololejeunea papilliloba, a species unknown in Africa until 2007. Photo by Barbara Thiers, NY Botanical Garden, through Creative Commons.

As in most of the tropics, in Malawi (Figure 134) the Lejeuneaceae (Figure 6-Figure 15) are abundant, with 64 taxa found during a single collecting trip of the BBS (Wigginton 2001) of which 45 were epiphylls. As has been common in tropical collecting trips, 51 species of the 64 taxa were new to the Malawi bryoflora.

Like Olarinmoye (1975b) in Africa, Marino and Salazar Allen (1991) likewise found that it is light and microsite, not shrub species, that determines the epiphyllous communities on Hybanthus (Figure 37) and Psychotria (Figure 38) in the Neotropics. In this case, the epiphylls grow poorly in the shade but as expected are very sensitive to quite small differences in moisture. For example, Cololejeunea sicifolia (see Figure 13) dominates communities in dry microsites but is rare in wet microsites, whereas Leptolejeunea elliptica (Figure 14) dominates in wet microsites and is relatively rare in dry microsites. When the two shrubs grow together in the same microsites, their epiphyllous communities are similar. Equihua and Pócs (1999) reported 26 liverwort and 1 moss species growing as epiphylls in the Lacandon Forest in Chiapas, Mexico. Nine were new for the country, all members of the Lejeuneaceae (Figure 6-Figure 15). It is interesting that the epiphylls worldwide are nearly all liverworts, especially in the family Lejeuneaceae (Figure 6-Figure 15), suggesting that this family has some special adaptations for this habitat. For example, in El Salvador Winkler (1967) found 66 species of liverworts, but only 12 species of mosses on leaves, a number that is actually quite high. In the rainforest on Bioko Island of

Chapter 8-6: Tropics: Epiphylls

Guinea, Müller and Pócs (2007) found 57 species of epiphyllous bryophytes, of which only two were mosses and the remainder were liverworts. Dauphin (1999) reported 98 liverwort, 54 moss, and 1 hornwort species among epiphytes from Cocos Island, Costa Rica (Figure 135). In this study, more than 60% of the species have a Neotropical or Pantropical distribution. Less than 5% are endemic. The Lejeuneaceae (Figure 6Figure 15; many as epiphylls) and Lepidoziaceae (Figure 136) comprised most of the taxa. Few thallose liverworts or moss taxa were found. Dauphin attributed the greater bryophyte species count in the Galapagos Archipelago to greater habitat variety, particularly wet and dry habitats. But most of the bryophytes in this Cocos Island study area are corticolous (46%), with only 25% epiphyllous.

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the liverwort family Lejeuneaceae (Figure 6-Figure 15). Other epiphyllous liverworts include Metzgeria (Figure 19, Figure 127) and Radula (Figure 16). Of the few species of mosses, most are in the genus Crossomitrium (Figure 21). In this study, the diversity, distribution, and density were related to microclimate, especially humidity, but they also related to differences in the vegetation. South America In a superhumid tropical lowland forest of Chocó, Colombia, epiphyllous bryophytes have had little study, leading to an assumption of rarity that might not be justified (Benavides & Sastre de Jesús 2011). Among these poorly known or rare species are Cololejeunea gracilis (Figure 137), Leptolejeunea tridentata (see Figure 14), and Otolejeunea schnellii. The researchers found that the diversity and composition of epiphyll species differs little between the palm and non-palm leaves. Disturbance affects epiphyll cover, species richness, and diversity of rare species negatively. The rare species do not agree well with the global or national red lists, again reinforcing the need for more studies.

Figure 135. Cocos Island beach and forest, Costa Rica. Photo by J. Rawls, through Creative Commons.

Figure 137. Cololejeunea gracilis var. linearifolia on leaf. Photo courtesy of Tamás Pócs.

Figure 136. Lepidozia cupressina (Lepidoziaceae) from the Neotropics where this family is occasionally one of the epiphylls. Photo by Michael Lüth, with permission.

By contrast, Bernecker-Lücking (2000) reported 56 mosses and 106 liverworts growing on Cocos Island, Costa Rica. Of these, 45 were epiphyllous. Like the study of Lücking (1997) and Dauphin (1999), these had primarily Neotropical affinities. One surprising result of their study was the discovery of epiphylls growing on the undersides of leaves in the mountainous area, perhaps due to the high light intensity there. Most of the epiphyllous species are in

In the Colombian Amazonia, Benavides et al. (2004) found a total of 109 bryophyte species in a non-flooded and a floodplain forest. The life forms differed little in the two forest types, but the species of mosses and liverworts were different. On the other hand, the floodplain had more fan and mat species, whereas the non-floodplain had more epiphytic liverworts. The epiphyll species seemed to differ little between the habitats. Benavides and coworkers suggested that the epiphyll habitat is stressful enough that the habitat differences have little effect. One of the common genera of leafy liverworts among the epiphylls is Frullania (Figure 20), although none of its species is typically epiphyllous. Von Konrat and Braggins (1999) reported eleven epiphyllous species in New Zealand, New Caledonia, and Colombia, with 29 more that had been listed previously as epiphylls in other regions of the world. Epiphyllous species of Frullania range from sea level to 2,500 m and can be considered facultative or accidental on the leaf substrate. The genus also occurs on rocks and bark. The largest number of epiphyllous Frullania species occurs in the floristic regions of New Zealand, New Caledonia, Macaronesia, and Madagascar (Braggins & von Konrat 1999).

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Pócs (2002) explored the Neotropical species of Cololejeunea (Figure 6) from Ecuador and Brazil and found two new species: Cololejeunea ecuadoriensis and C. schusteri. In fact, it is unusual to find a tropical study that does not include new species. In 2018, Pócs found the epiphyllous liverwort Reinerantha foliicola (Lejeuneaceae; Figure 138) in Venezuela, in a genus previously described from Ecuador by Gradstein et al. (2018) as a new genus.

Figure 139. Mitthyridium micro-undulatum; some members of Mitthyridium prefer leaf petioles. Photo by Jan-Peter Frahm, with permission.

Figure 138. Reinerantha foliicola, an epiphyllous lefy liverwort from Ecuador and Venezuela. Photo modified from Gradstein et al. 2018, with permission.

Figure 140. Calymperes nicaraguense; its family, the Calymperaceae, is common among epiphytes in the Neotropics; some species prefer midribs. Photo by Michael Lüth, with permission.

Campelo and Pôrto (2007) provided a checklist including both epiphyllous and epiphytic bryophytes of Frei Caneca RPPN, Jaqueira, Pernambuco State, Northeastern Brazil. This was a remnant Atlantic forest at 750 m alt. They found 21 families, with the liverworts in Lejeuneaceae (Figure 6-Figure 15; 31 species) and the mosses in Calymperaceae (Figure 139-Figure 142; 7 species) predominating in species number. Most of the species (67%) are Neotropical, but 15% are pantropical. Orbán (1997) has shown that different genera of Calymperaceae prefer to colonize different parts of the leaves, like Mitthyridium (Figure 139) mostly the petiole, Calymperes (Figure 140), Leucophanes (Figure 141), and some Syrrhopodon (Figure 142) the midrib, while other Syrrhopodon species grow on the margin. Zartman and Ilkiu-Borges (2007) have provided a key, descriptions, and illustrations for the epiphyllous bryophytes of Central Amazonia. To facilitate bryological work in both English and Spanish, the keys and descriptions are provided in both languages.

Figure 141. Leucophanes sp., a genus that prefers the midribs of leaves. Photo by Niels Klazenga, with permission.

Chapter 8-6: Tropics: Epiphylls

Figure 142. Syrrhopodon cf. platycerii; some members of this genus may prefer the leaf midrib or the margin. Photo by Niels Klazenga, with permission.

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Figure 144. Bromeliophila natans, a species that occurs in bromeliad basins. Drawing from Heinrichs et al. 2014; courtesy of Robbert Gradstein.

Bromeliad Basins Some bryophytes live on bromeliad leaves (Figure 143) and in the basins of water provided by them. Bromeliophila helenae and B. natans (Figure 144) grow exclusively in the leaf axils of bromeliads (Gradstein 1997a; Gradstein et al. 2001; Benavides & Callejas 2004; Heinrichs et al. 2014). Bromeliophila natans, which like its sister species is barely distinguishable from Lejeunea (Figure 3), is apparently endemic to southeastern Brazil (Gradstein 1997a). It occurs, often submerged, in terrestrial bromeliads such as Vriesea glutinosa (Figure 145), Aechmea nudicaulis (Figure 146), and Quesnelia arvensis (Figure 147), mostly on open sites in the coastal rainforest. Bromeliophila helenae, a montane species, is known from the Guayana Highland of Venezuela and on the island of Dominica in the central Lesser Antilles. It grows in the basins of both terrestrial and epiphytic bromeliads such as the terrestrial Brocchinia hechtioides (see Figure 148-Figure 149).

Figure 143. Epiphyllous liverwort on bromeliad leaf. Photo by Jessica M. Budke, with permission.

Figure 145. Vriesea glutinosa, one of the bromeliads with basins in which Bromeliophila natans sometimes occurs. Photo by BotBin, through Creative Commons.

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Figure 148. Brocchinia tatei on the north ridge of Mt Roraima, Guyana, at 2000 m asl; the liverwort Bromeliophila helenae grows in the basins of Brocchinia hechtioides. Photo courtesy of Robbert Gradstein.

Figure 146. Aechmea nudicaulis, Brazil, one of the bromeliads with basins in which Bromeliophila natans sometimes occurs. Photo by Marcia Stefani, through Creative Commons.

Figure 147. Quesnelia arvensis, one of the bromeliads with basins in which Bromeliophila natans sometimes occurs. Photo by John Thagard, through Creative Commons.

Figure 149. Insectivorous plant Utricularia humboldtii growing in leaf axils of the bromeliad Brocchinia tatei at Mt. Roraima north ridge at 2000 m. Photo courtesy of Robbert Gradstein.

Chapter 8-6: Tropics: Epiphylls

In Puerto Rico, 13 out of 65 bromeliads sampled near the radiation center in 1965 had bryophytes in their basins (Maguire 1970). Mosses in these aerial basins are rare, with the only known species being Philophyllum tenuifolium in the Leucomiaceae, occurring submerged or emergent in Vriesia (Figure 145) and Nidularium (Figure 150) of Guatemala, SE Brazil, and Peru (Gradstein et al. 2001). The basin of water created in the middle of the youngest leaves is available to keep the bromeliad hydrated and thus provides an aquatic habitat for bryophytes.

Figure 150. Nidularium procerum. Nidularium is one of the bromeliads with basins in which the moss Philophyllum tenuifolium sometimes occurs. Photo by Bocabroms, through Creative Commons.

Fragmented Habitats Deforestation is creating forest fragments in many areas of the tropics. Oliveira et al. (2011) reported that they could detect no edge effect on epiphytic bryophytes in a fragmented landscape of an Atlantic forest in northeast Brazil. Furthermore, canopy openness was not correlated with bryophyte richness. Here we explore if this absence of edge effect holds as well for the epiphyllous bryophytes in the Neotropics. Zartman (2003) discussed the effects of this habitat fragmentation on epiphyllous bryophyte communities in central Amazonia. He found that regionally common taxa were often reduced in epiphyll diversity in small forest fragments. On the other hand, rare taxa were often more abundant in fragments than in continuous forest habitat. Larger fragments (100 ha) exhibited higher species richness, abundance, and among-site variation than did the smaller fragments (1 & 10 ha). Like Daniels (1998), Zartman and Nascimento (2006) took advantage of the accelerated life cycles, high rates of local extinction, and naturally patchy substrates of epiphyllous bryophytes to look at the effects of habitat fragmentation. They examined both local abundance and regional distribution of 67 epiphyllous bryophyte species in Amazonia. The landscape was experimentally fragmented and demonstrated that changes in local abundance caused by habitat fragmentation can be explained by fragment size rather than nearness to the forest edge. The simultaneous inter-specific decline in epiphyll local abundance and regional distribution in small (1-10 ha) forest fragments support metapopulation predictions of the importance of immigration in ameliorating risk of patch extinction (i.e.

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the rescue effect). They concluded that their results provide indirect evidence that dispersal limitation, not compromised habitat quality due to edge effects, can account for species loss from small tropical forest fragments. They further concluded that preservations of rainforest areas of at least 100 ha are necessary for the long-term persistence of these epiphyllous communities. Alvarenga and Pôrto (2007) explored eight Atlantic forest fragments in Pernambuco, Brazil, ranging in size from 7 to 500 ha to determine the effects on epiphytes and epiphylls. Habitat fragmentation existed in the lowland and submontane forests (Alvarenga & Pôrto 2007). Despite the increase in richness, diversity, and abundance with altitude, clear evidence exists that fragment size and isolation are more important as determinants of these community parameters. Isolation is the most important factor, emphasizing the importance of dispersal. Furthermore, the greatest proportion of shade species occurs in larger fragments with lower degrees of isolation. Fragments also increase the number of species with larger niches (generalists) while decreasing the number with smaller niches that were likely to specialize on shady or sunny areas. In the Eastern Arc Mountains of Kenya, Malombe et al. (2016a) investigated fragmentation and its effect on the sensitive epiphylls. Using a disturbance gradient up to 200 m from the forest edge in three moist forest fragments, they collected at least four leaves from each host species. They found 96 epiphyllous bryophyte species. No correlation was evident between the environmental variables (relative humidity, temperature) and the forest edge gradient. Nevertheless, epiphyll diversity differs with site-specific characteristics. Forest edge distance does not have a significant influence on richness or distribution of the epiphyllous bryophyte species. Instead, these parameters depend on microhabitat variables such as tree species composition, sunlight exposure, and spatial and dimensional canopy structure. Malombe et al. (2016b) also examined fragmentation effects on the composition, abundance, and species richness of epiphyllous bryophytes in fragments of tropical cloud forests in the Eastern Arc Mountains of Kenya. Again using a disturbance gradient extending 200 m out from the forest edge, they collected four leaves from each phorophyte at three sites, totalling 1,387 leaves from 489 phorophytes. This revealed 95 species of bryophytic epiphylls. Once again, richness did not change with distance from the forest edge. And as in their moist forest fragment study, richness depended on the tree species composition and microhabitat, including exposure to sunlight and canopy structure. Hylander et al. (2013) studied fragmentation effects in the moist Afromontane forests of Ethiopia. This study differed from most in that the forest margins were still in heavy use by local farmers, creating a mosaic landscape. Going into the forest instead of away from it, they found strong edge effects on canopy cover and number of stumps. Heavy usage by humans was indicated by paths, beehives in trees, and timber harvesting, and perennial crops such as coffee and spices. The number of epiphyllous bryophytes increased from 20 m to 75 m inward from the edge. They concluded that the edge effects on epiphyllous bryophytes do not get worse over time.

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Chapter 8-6: Tropics: Epiphylls

Silva and Pôrto (2010) similarly studied the species richness and diversity of both epiphytic and epiphyllous bryophytes on an edge to interior gradient in a large remnant of the Atlantic forest in Northeast Brazil. The researchers estimated light differences using hemispherical photographs. They found no significant difference in species richness or diversity based on distance from forest edge up to 1084 m inside. Altitude, however, causes an increase in bryophyte diversity, especially for epiphylls and shade-tolerant bryophytes. Canopy cover is somewhat less important than altitude. Differences within the forests are more important than distance from the edge. Alvarenga et al. (2009) also studied bryophytic epiphylls in fragmented forests of northeastern Brazil, from forest edge to 100 m within the fragment. They found decreasing abundance both locally and regionally resulting from habitat loss. They concluded that this is related to both sexual and asexual expression. Frequently-fertile species are more frequent in forest fragments than infertile species. Nevertheless, the landscape and habitat quality are more important in epiphyll richness and presence than distance from forest edge. As in the above studies, habitat modification is less important than forest characteristics, but they nevertheless play a role. They concluded that fragmentation results in negative and long-term effects in fragmented landscapes. Connectivity between patches is important in successful conservation. Zartman et al. (2012) experimented with recolonization rates by stripping bryophytes from their branches. When both local and neighboring phorophytes within 400 m2 plots were experimentally denuded, the extinction events increased, along with a reduction in colonization. When no denuding occurred, losses of the epiphylls were subject to rescue effects from neighboring leaves. The researchers suggest that negative densitydependent growth in within-leaf populations indicates resource limitation or intraspecific competition. Zartman and Shaw (2006) considered the demographic mechanisms causing species loss in the tropics to be greatly underexplored. To contribute to the understanding of the impact of fragmentation, they chose the epiphyllic leafy liverworts Radula flaccida (Figure 41) and Cololejeunea surinamensis (see Figure 71). They transplanted these two species to study sites with areas ranging 1, 10, 100, up to 110,000 ha. All the transplants exhibited significantly positive local growth with a nearly constant per-generation extinction probability of 15%. In reserves of 100 ha or greater, the colonization rate nearly doubled (to 48%) compared to small reserves (27%). They considered this an indication that epiphyll loss in small fragments was due to reduced colonization. Pócs (1996) emphasized that conservation of epiphytes "can only be achieved through the rigorous protection of the forests."

Sampling Epiphylls Collection of the epiphyllous bryophytes requires the same techniques as for bryophytes on branches at the same level in the forest, including use of ropes, bow and arrow, or climbing. Ecological methods, however, may be somewhat different. In a study of epiphylls in Colombia, Benavides and Sastre de Jesús (2011) used 10 x 10 cm quadrats in 30

plots, totalling 240 samples. They recommend the Floristic Habitat Sampling, a method that focuses on mesohabitats as the sampling unit. Unfortunately, that does not provide the randomness required for statistical comparisons. They therefore recommend a combination of a systematic grid of 1-several km2 with Floristic Habitat Sampling within the plots. Vanderpoorten et al. (2010) emphasized that many bryophytes are annual or identifiable during only part of the year. They claimed that completely random plot sampling or systematic sampling are both likely to miss species and variation within the sampling area unless the sampling effort is very high (number of plots, large number of sampling dates). The IUCN uses the Area of Occupancy for recording rare species. This is defined as the area calculated by summing all 2x2 km grid squares that actually have the taxon. But Vanderpoorten and coworkers recommend reducing the mesh size because the Area of Occupancy values decline sharply with a reduction in scale. This occurs because the bryophyte species have a more linear and fragmented distribution. Collection is necessary to identify or verify most bryophytes and to permit DNA analysis now or later. For epiphyllous bryophytes, it is necessary to collect entire leaves that host them and to put them in new papers in a plant press so that the host leaf remains flat. They should be lightly pressed until they are dry. Bryophytes living on leaves are typically collected by collecting host leaves. These are preserved by pressing and drying. Pócs and coworkers (Pócs 1978; Pócs & Podani 2015) found that 30 (50 preferred) randomly collected leaves from a hectare are usually representative of most species occurring there. Each leaf can be considered as a separate stand which can be studied and compared by the methods generally used in phytosociology. These should be examined microscopically. Pócs (1978, 1982b) counted the number of foliicolous plantlets on each leaf and related that number to leaf area. Frequency is used to represent the presence of a certain species on different leaves among the samples collected. To determine cover values, one can use a celluloidin film solution spread over the leaf (Tamás Pócs, unpublished). Once this has hardened, it can be removed, together with the foliicolous community, and examined under a microscope at low magnification using a square grid ocular micrometer. This can provide the data to determine cover values. Carroll (1979) developed another method when surveying the epiphyllous organisms on Douglas fir needles (Pseudotsuga menziesii). He used photographs of random sections of needles and extrapolated these to total needle area. This method is especially useful where collecting is not allowed or sampling would be too destructive. Benavides and Sastre de Jesús (2009) similarly used digitized images for estimating bryophyte cover. They compared accuracy, efficiency, and objectivity among three methods: Braun-Blanquet cover classes, grid percentage, and digital image processing. Two observers used clay tiles that had been planted with Neckeropsis disticha (Figure 151) and estimated cover by the three methods. Accuracy was determined by comparing cover values with the dry weights. Efficiency was a measure of time and data

Chapter 8-6: Tropics: Epiphylls

variability. Objectivity was compared between observers. The digital method was the most efficient in time in the field (p