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Network Scan Data Selbyana 9: 23-43 THE VEGETATIVE BASIS OF VASCULAR EPIPHYTISM DAVID H. BENZING Department of Biology, Oberlin College, Oberlin, Ohio 44074 ABSTRACT. Vascular epiphytes do not share distinguishing systematic or biological profiles. Taxonomic participation is broad although the group is dominated by higher ferns, members of a few dicot families and monocotyledons, particularly orchids. Except for some general features that promote anchorage in tree crowns and aerial dispersal of diaspores, forms and life processes associated with epiphytism also occur in soil-rooted flora. Among the more pervasive characteristics of canopy-dependent vegetation are drought tolerance and mechanisms promoting access to unusual sources of nutrient ions. Trophic mutualisms are especially common and diverse with ants playing a dominant role. Specific types of epiphytes are described along with associated water ion balance mechanisms. Research topics that seem most likely to reveal significant information on the vegetative basis of epiphytism are identified. Papers on the vegetative and related aspects ers) accounts for most of the approximately of vascular epiphytism appeared only sporadi­ 30,000 species. The second reason for great va­ cally over much of the period following publi­ riety among vascular epiphytes is the heteroge­ cation ofSchimper's remarkably comprehensive neity of their habitats, particularly humid forests and insightful "Die Epiphytische Vegetation where moisture, irradiance and available nu­ Amerikas" in 1888. Mez (1904) demonstrated trients occur in numerous combinations. Agen­ that some bromeliad leaf trichomes are absorp­ cies operating against diversity are climatic rigor tive; Harris (1918) tested the osmotic qualities and the dispersed distribution and imperma­ of epiphyte foliage versus that of hosts; Pessin nence of the epiphytes' substrata. Patchiness is (1925) addressed the autecology of the epiphytic pervasive, ranging from the relatively gross pat. fern Polypodium polypodioides; Oliver (1930) terns created by diversity of trees in individual surveyed New Zealand's canopy-dependent flora; forests to the finer-grained discontinuity of suit­ Went (1940) sought to explain those factors re­ able bark presented by each phorophyte. High sponsible for host selection. In 1952, Richards mortality continues among successfully dis­ treated epiphytes in the now classic "The Trop­ persed progeny; lethal disturbance is frequent as ical Rain Forest" and Curtis reviewed the by then supporting bark fragments exfoliate, colonized respectable bibliography pertaining to canopy­ twigs and branches fall and infested trees even­ dependent flora (169 papers by 154 authors). tually collapse. On average, patch life must be Gessner considered water economy in 1956; Jo­ especially short for the great number ofepiphytes hansson (1974) and Sanford (1969, 1974) iden­ whose generative power is already suppressed in tified climatic correlates of epiphytic orchid dis­ drier forests by drought and mineral insufficien­ tribution in West Africa; Madison published a cy. This complication probably explains why a general treatment in 1977. Most recently, Ben­ few specialized taxa account for so much of the zing considered interactions between epiphytic dependent synusiae in strongly seasonal habitats vegetation and associated biota (Benzing & See­ (FIGURE 1; Benzing, 1978). mann, 1978; Benzing, 1983, 1984) and Pridgeon (1986) synthesized the subject of orchid-root TYPES OF EPIPHYTES structure and function. Publications on epiphyte biology are now appearing at an ever-increasing Categorization of epiphytes has been based on rate. This discussion represents an attempt to many measures, the most popular being the na­ synthesize the literature dealing with the vege­ ture of their dependency on supporting vegeta­ tative aspects of vascular epiphytism. tion, fidelity to forest canopy versus other sub­ strata, exposure preference, and growth habit. DIVERSITY Despite their central importance in ecological classification, mechanisms for acquiring and Epiphytes lack a unifYing profile, in part be­ conserving energy, nutritive ions and water have cause of their diverse origins. If the branch par­ been less effectively employed to identifY types. asites (mistletoes) are included in the count, plants One such distinction is central to much of the that regularly inhabit tree crowns belong to at following discussion: it concerns the nature of least 70 families. However, only about one-quar­ the resource supply. Where moisture and nu­ ter of those taxa (and Orchidaceae above all oth- trient ions are more or less steadily available in 23 24 SELBYANA [Volume 9 MARGIN BETWEEN RESOURCES ACQUIRED AND NEEDED FOR REGENERATION INCREASINGLY NARROW t .--- CONTINUOUSLY SUPPLIED --- PULSE SUPPL I ED -- >­ f- U1 UJ INSOLATION :>'" ;; -----.-.---~---.-.-----g-------.-.- I.>.J f­ >­ :r: a.. Cl.­ UJ DARK AND WET DRY AND EXPOSED PREFERRED MICROSITE FIGURE 1. A graphic model illustrating the relationship between the diversity of vascular continuously­ supplied and pulse-supplied epiphytes in native habitats and (1) exposure level and (2) moisture and nutrient availability. rooting media or foliar impoundments, epi­ of Tillandsia, and various orchids that anchor to phytes can be labeled continuously-supplied the most exposed bark surfaces. Several trends (FIGURE 1). Data are few, but debris trapped by in the epiphytic flora follow humidity and fer­ tank bromeliads (Benzing & Renfrow, 1974) and tility along the ecological continuum just de­ that used by early stages ofhemiepiphytic figs on scribed. At one extreme, species native to the palm hosts may be quite nutritive and usually most equable forest differ little in form and prob­ moist (F. Putz & M. Holbrook, pers. comm.). ably physiology from adjacent soil-rooted vege­ Distinguished from continuously-supplied forms tation; not surprisingly, epiphytism among na­ by choice of habitat type, adaptive character and tives of such communities is often facultative. location on the right side of FIGURE 1 are the Epiphytes specialized to counter the strongest pulse-supplied types. Here, moisture and key ions ecoclimatic constraints possess elaborate, some­ are only intermittently available and stress re­ times unique, devices to tap unusual resource duces productivity to a point where fewer ge­ pools, prolong contact with passing canopy fluids notypes can maintain sufficient generative ca­ and maximize resource economy. pacity to cope with habitat patchiness and disturbance as well. Although photon flux may WATER BALANCE be dense, shortages of several macronutrients and adaptations to promote water use efficiency deny The underlying mechanism of the competitive quantum yields achieved by vegetation operating strategy, i.e., robust photosynthesis with the re­ under less oligotrophic and arid conditions. The sulting high relative growth rate, is only possible best known pulse-supplied species are the xe­ on resource-rich sites since the attending require­ romorphic Bromeliaceae, particularly members ments for water, nitrogen and phosphorus are 1986] BENZING: VASCULAR EPIPHYTISM 25 FIGURES 2-5. Epiphyte types. 2. Tillandsia paucij'olia, a pulse-supplied form. 3. Campyiocentrum micrantha, illustrating minimal contact with substratum. 4. Campyiocentrumjascioia, a shootless twig-dwelling orchid. 5. LeafY Catasetum sp. on a rotten branch; bark partially removed to expose humus-embedded roots. 26 SELBYANA [Volume 9 FIGURES 6-9. 6. Protocarnivorous Catopsis berteroniana exhibiting copious epicuticular wax. 7. Hemiepi­ phytic aroid. 8. Strangling Ficus aurea on Sabal palmetto. 9. Ecuadoran Aechmea sp. rooted in an ant nest. 1986] BENZING: VASCULAR EPIPHYTISM 27 high. Resource-deficient sites oblige another kind the transpiration stream in order to maintain of response from native vegetation: as environ­ acceptable water use under changing circum­ mental rigor mounts, stress tolerance becomes stances. Stomata limit water vapor efllux more the major arbiter of success, exceeding vigor and than CO2 influx through turgor-driven changes the capacity to shade out neighbors. Most forest in guard cell aperture which can occur indepen­ canopies resemble the latter situation; they are dently of bulk-leaf water potential. Partial pres­ far from equable. By and large, not competition sure of CO2 in the chloroplasts (Pi) needed to but climatic rigor (aridity in particular) consti­ saturate immediate carboxylation capacity is tutes the more formidable impediment to epi­ somehow translated into altered guard cell turgor phyte survival through its suppressive effect on according to the optimization hypothesis (Far­ carbon gain. quhar & Sharkey, 1982). In essence, guard cell movements minimize transpiration without cur­ STATIC DEFENSES AGAINST DROUGHT tailing potential photosynthetic output, and what physiologists call the "marginal cost of photoas­ Porous surfaces provide little drought protec­ similation" remains relatively favorable despite tion to desiccation-tolerant (poikilohydrous) epi­ fluctuating conditions. phytes. In contrast, homoiohydrous counterparts Under some circumstances which vary with are well insulated against aridity through pos­ species and environmental context, stomatal be­ session of stout-walled epidermal cells covered havior suppresses water loss (and access to CO2) by a thick evaporation retarding cuticle, recessed irrespective of photosynthetic capacity. At pres­ stomata, elaborate indumenta for greater bound­ ent, little is known about this
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