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 aspect of epiphyte ary-layer resistance and radiation reflectance, and biology beyond a few species, most notably Til­ extensive water storage capacity. Locally nar­ landsia recurvata and T. usneoides. Contact with rowed xylem conduits which would ensure that a drying air mass substantially reduced nocturnal mounting water deficits first killed expendable CO2 consumption by these specialized plants organs such as leaves before less replaceable ones possessing crassulacean acid metabolism (CAM) (main stems, particularly their meristems; Zim­ (Lange & Medina, 1979; Martin & Siedow, 1981). merman, 1983) have not yet been reported in Osmotic adjustment offers a means to main­ canopy-dependent vegetation, but they surely tain diffusive conductance while shoots experi­ occur there. ence mild water deficits. In the absence of such An uncommon cell type which improves hy­ capacity, chloroplasts in stressed tissues may dric capacitance occurs widely in xeromorphic outstrip their CO2 supply and productivity di­ orchids (FIGURE 10). Typical locations of spiral­ minishes. Two Malaysian epiphytic ferns (Pyr­ ly-thickened idioblasts are colorless leaf hypo­ rosia adnascens and P. angustata) examined by dermis and chlorenchyma in root and stem cor­ Sinclair (1983b) exhibited somewhat more neg­ tices (pridgeon, 1981). Vascular involvement of ative bulk-leaf water potentials as relative water these lightly lignified, nonsuberized cells is un­ content decreased than could be explained by likely considering the lack of direct connection concentration effects of tissue shrinkage alone. with true water conduction cells. Spirally-thick­ However, data points were too scattered to jus­ ened idioblasts offer two distinct advantages over tify a definitive statement about adjustment. Par­ the more common thin-walled hypodermal cells allel experiments with the epiphytic orchids Den­ of typical succulents: they can shunt their entire drobium tortile and Eria velutina definitely moisture store to nearby labile tissue and con­ indicated no changes in leaf solute potential as tinue to provide mechanical support. Spirally­ desiccation progressed. thickened cells yield their contents at the mo­ Halophytes generate compatible osmotica in ment bulk-leaf water potential becomes low the cytosol in order to balance concentrated vac­ enough to "air seed" the water reservoir through uolar sodium and chloride ions. The most com­ pores that formerly accommodated plasmodes­ mon insulating agents are proline, betaines and mata (Zimmerman, 1983). Thickenings opposite other low-molecular-weight, usually nitrogen­ intercellular spaces (Benzing et al., 1983) prob­ containing, compounds. In glycophytes, presum­ ably prevent massive air intrusions that would ably including the epiphytes, excess osmotica are be difficult or impossible to dissolve when op­ metabolized after rehydration. Hyperfluctuating portunity for refilling returns. moisture supply and oligotrophy may have dic­ tated some interesting choices for the epiphytes. DYNAMIC DEFENSES AGAINST DROUGHT Metabolic lability and cost may have been major determinants. Betaines, for instance, are rela­ Both anatomy and assimilatory pathways of tively inert compared to proline, whose pool size plants are so broadly tolerant that additional reg­ is far less stable. Adjustment is progressively more ulatory mechanisms are necessary to fine tune expensive depending on whether inorganic, non- 28 SELBYANA [Volume 9

FIGURES 10-14. Anatomical features of epiphytic orchids. 10. Spirally-thickened idioblasts from a pleuro­ thallid orchid leaf. SEM. 11. Passage cell in exodermis of Chiloschista luni/era. LM. 12. Autoradiograph of cross section of Epidendrum radicans root. Black objects in ve1anien (VEL) are 3H-Ieucine-labeled microbes. LM. 13. Thick-walled exodermis (EXO) on exposed side of a Campyiocentrum root after velamen has been shed. Abun­ dant cortical chloroplasts present. LM. 14. Cross section of Polyradicion lindenii root showing extensive fungal presence in cortex parenchyma (COR) and passage cell. LM. 1986] BENZING: VASCULAR EPIPHYTISM 29

WET CONFIGURATION

15

DRY CONFIGURATION

17

---15 }J FIGURES 15-17. Diagrammatic anatomical details of epiphytic bromeliads and orchids. 15. Foliar trichome of an atmospheric bromeliad in the wet and dry configurations. 16. Foliar trichome ofPolypodium hirsutissimum. 17. Exodermal passage cell and associated tilosome of Sobralia macrantha. nitrogenous or nitrogenous organic osmotica are Grimmia iaevigata failed to maintain a positive used, especially in dry, infertile habitats (Raven, carbon balance in overly arid sites because its 1985). thalli were relatively dry by day, a condition more The third dynamic defense, dark CO2 fixation, conducive to respiration than to photosynthesis. will be discussed in detail later. Vascular resurrection plants may be at similar risk under such conditions. Other phenomena Water Balance Categories must explain the exclusion of poikilohydrous plants from more humid forests, although the POIKILOHYDRY. Among the few pronoUnced filmy ferns so common there may occasionally poikilohydrous epiphytes is Pofypodium pofy­ experience and tolerate desiccation on an unrec­ podioides, a wide-ranging American fern. Fronds ognized scale. are erect and green during humid periods but HOMOIOHYDRY. Homoiohydrolls epiphytes soon curl and turn brown during drought as rel­ differ from resurrection species on two counts: ative water content drops. Peltate hairs resem­ bling those reported to aid absorption of water their greater capacity to retard water loss and greater sensitivity to desiccation injury. A con­ in mechanically-dependent Brazilian ·Pieopeitis angusta and two polypodiums (Miiller et aI., tinuum of species between extremes is likely. 1981) cover both foliar surfaces, but their role Hygrophytes. These plants exhibit no discern­ here is unclear. Specimens of Poiypodium poiy­ ible xeromorphy. They typically dwell in pluvial podioides, dehydrated to two to five percent of forests or on moist, cool sites in drier habitats, saturation and then placed in liquid water, re­ often just the bases of standing trees and over covered to full photosynthetic capacity and hy­ fallen logs. Like their phorophytes, hygrophilous drature within 12 hours (Stuart, 1969). Numer­ epiphytes are evergreen, but they desiccate so ous bark-dwelling and epiphyllous algae, easily that they are eliminated by even a short bryophytes and lichens are also poikilohydrous; dry season or too much sun. Leaves are thin, why P. poiypodioides has so few vascular coun­ typically small or finely dissected, bounded by a terparts is puzzling. Alpert and Oechel (1985) delicate epidermis, and apparently equipped for found that the lithophilous resurrection moss C3 photosynthesis. Succulent stems and tubers 30 SELBYANA [Volume 9

CORTEX SHRUNKEN CORTEX

STm \ .<.;;;'~.....,.,.dC:::. I I, I, I , AIR GAP BREAKS CONTINUUM I I SUBSTRATUM WET • I SUBSTRATUM DRY ,

EMBOLIZED VELAMEN BREAKS CONTINUUM EXODERMIS MATRIC FORCES REVERSE FLOW

FIGURE 18. Diagrammatic response to dry substrata of a velamentous root vs. a conventional root. Upper sequence represents response of non velamentous root in a drying substratum. Lower series represents reponse of velamentous root under identical stress. Arrows indicate path of water flow. See text for further details.

are missing. Root systems promptly dry out upon of species: those adapted to avoid prolonged removal from the moist vegetation and debris of drought and those adapted to endure it. Drought their normal substrata. avoiders are not xerophytes at all; they are sea­ sonal mesophytes that restrict vegetative activity Mesopnytes. Plants ofthis group are also most­ to periods when high exchange ratios between ly evergreen and rooted in what are usually moist carbon and water are sustainable. As the habitat media. Shade-tolerant species restricted to lower dries and continued abundant transpiration is no but not the most humid or exposed strata within longer supportable, poorly insulated but produc­ dense rain or cloud forests qualify. Leaves, the tive foliage is shed. Photoperiod and other cli­ major trophic organs here as among the hygroph­ matic changes serve to cue senescence and ab­ ilous forms, are somewhat more resistant to des­ scission. Better-protected perenniating organs iccation. Modest vigor is supported by C3 pho­ lapse into dormancy for intervals about equiv­ tosynthesis, perhaps assisted by some measure alent to a normal dry season, storing carbohy­ of nocturnal CO2 fixation. There is no precise drates and other reserves while generating the demarcation between the drought-tolerant hy­ meristems needed to replace foliage and roots gromorphic and drought-sensitive mesophytic when favorable weather returns. Drought-decid­ epiphytes, nor for this reason is it possible to uous epiphytes occur in the Begoniaceae, Bro­ estimate the size or taxonomic breadth of the meliaceae, Orchidaceae, Polypodiaceae and a group. Many ferns belong here, as do broadleaf scattering of other families. tillandsioid bromeliads without tanks (e.g., Til­ Drought endurers are by far the most numer­ landsia insigne, Guzmania gramini/olia). Also ous and best known of the two drought-adapted included are aroids, gesneriads and others with groups. Conspicuous hallmarks are leathery to only moderate mechanical barriers to water loss. stiff, thick, long-lived foliage and stout, durable roots. Pseudobulbous shoots of a Laeliocattleya Xerophytes. This subset encompasses two types cultivar, for instance, have functioned for up to 1986] BENZING: VASCULAR EPIPHYTISM 31

seven years although three to four seasons is Wong and Hew (1976) demonstrated CAM­ probably average for orchids (Poole & Sheehan, like acid cycling in Pyrrosia longifolia and closely 1982). Occasional taxa are aphyllous stem (Va­ related Drymoglossum pilosel/oides, a rather odd nilla) or root (Polyradicion) succulents. Judged discovery considering the drought performance on performance in culture, drought-enduring of Pyrrosia anguslala and P. adnascens. Resur­ epiphytes mature slowly, like those adapted to rection-like behavior in Sinclair's two filicalean soil. Habitats range from exposed sites at the tops subjects and a photosynthetic pathway thought of trees in everwet communities to various bark to have evolved in land plants to help conserve surfaces in the driest microphyllous forests, sa­ moisture suggests that epiphytic pteridophytes vannas and cactus-scrub communities. possess an interesting array of water balance Features responsible for the exceptional water mechanisms. His findings surely leave no doubt economy of drought-enduring epiphytes are nu­ that different water relations sustain different merous and varied. Xeromorphy is routine, but epiphytes facing the same climatic stress; Pyr­ there are no consistent patterns; there are even rosia and Dendrobium often grow in mixed col­ some surprises. Atmospheric bromeliads exhibit onies and indeed were maintained side by side such delicate leaf boundaries that Tomlinson in his drying runs. A suggestion (Knauft & Ar­ (1969) labeled some species "hydromorphic." He ditti, 1969) that CAM also evolved in epiphytes also provided stomatal counts, other pertinent to tap elevated nocturnal CO2 supplies in dense morphological parameters, and habitat prefer­ forest canopies has not been tested. ences; this data is largely unavailable except for Differences in water use efficiency and related Bromeliaceae. Hyperreflective epicuticular wax­ physiology and ecology of drought-enduring and es and light-scattering trichomes similar to those drought-avoiding epiphytes were illustrated by seen in many desert shrubs are unusual except comparing two neotropical orchids, Calaselum in heliophilic Bromeliaceae and a few orchid and integerrimum and Encyclia tampensis (Benzing fern genera. Leaf shape varies and mesophyll is et al., 1982a). The latter is an evergreen, bark­ usually differentiated into water storage and dwelling form while the former is drought-de­ chlorenchyma tissue. CAM appears to be routine ciduous (FIGURE 5). Much of the Catasetum root in this group, but additional data are needed for system is embedded in rotting wood or organic confirmation. debris and exposed to neither light nor air, a Sinclair's work (1983a, 1983b, 1984) on two habit which designates this species as a humus ferns and three orchids in Malaysia has provided epiphyte. Additional upward-growing, determi­ the most comprehensive workup to date on epi­ nate roots on drier microsites may produce a phyte water relations. All five species co-occur trash-basket impoundment. Encyclia tampensis in humid, essentially aseasonal forests and rarely proved to be a CAM species. Transpiration was encounter dry spells lasting more than two weeks. slow day and night. Catasetum integerrimum ex­ In this respect, they are definitely not among the hibited typical C3 photosynthesis while leafY. most drought-challenged of the evergreen epi­ Daily carbon gain greatly exceeded that achieved phytes. Nevertheless, the orchids showed dis­ by Encyc/ia, but the marginal cost. in moisture tinct CAM-type acid fluctuation. Pyrrosia ad­ was much greater. Dormant Catasetum speci­ nascens was equivocal, and P. anguslala, whether mens, reduced to thick pseudobulbs bearing no well watered or partially desiccated, appeared to foliage or living roots, lost little CO2 or H 20. be a C3 plant. Under induced moisture stress, Assimilation rate clearly demonstrated why this both ferns quickly exhibited decreased leaf con­ species grows faster than Encyclia tampensis and ductance and lower bulk-leaf water potential. The other drought-enduring epiphytes. Accompany­ orchids maintained stomatal mobility far longer ing poor water use efficiency explains why activ­ than Pyrrosia, in part due to a fourfold slower ity is seasonal and deep humus the required sub­ water loss. Some nocturnal conductance was de­ stratum. tected in the orchids through the entire treatment period and relative water content still exceeded Impounding epiphytes. As a rule, leaves pro­ 65 percent after 25 days without watering. Fern vide the structural elements for impoundments; transpiration, much of which appeared to be cu­ roots are occasionally involved. Bromeliaceae ticular, continued a gradual decrease to 13 per­ exhibit the most refined and diverse tank forms; cent by day 30, but presumably little photosyn­ about 1,000 species, roughly half of the family, thesis was possible after three or four days. produce rosulate shoots comprised oftight, over­ Conductance, bulk-leaf water potential and rel­ lapping leaves with inflated bases and .channeled ative water content returned to prestress levels blades (FIGURE 6). Impoundment volume can be following irrigation, rapidly in Pyrrosia, less so substantial; a single large Glomeropitcairnia in the orchids. erectif/ora has been said to contain about 20 liters 32 SELBYANA [Volume 9 of fluid (Pittendrigh, 1948), but the average for Filled tanks must have been partly responsible. all species is on the order of a few hundred milli­ Very likely, stress tolerance would have been liters. Intercepted moisture often moderates need more clearly highlighted had sampling been done for other xeric features one might anticipate from during drier weather and had gas exchange been the environmental context. included among the measurements. Looser leaves characterize other tank species. Little water but considerable litter is intercepted. Moisture Procurement Platycerium and Drynaria feature appressed ster­ ile fronds that form a plant-to-substratum catch­ Epiphytes anchored in all but the wettest for­ ment; roots perfuse this cavity, tapping collec­ ests or in evermoist humus elsewhere possess tions of humus, ant-nest debris and stemflow. either aqueous impoundments or a capacity to Sponge-like reservoirs are provided by root meet all needs during brief contact with canopy masses such as those created by several vela­ fluids. The latter epiphytes are most likely to mentous anthuriums, Catasetum, similar orchid have unusual water balance mechanisms. At­ genera, and certain ferns. The impounding mech­ mospheric bromeliads, orchids and some xero­ anism is not without limitation, however; tank phytic ferns definitely possess unusual absorp­ bromeliads give way to atmospherics as rainfall tive devices. Although different organs and tissues becomes too scarce. Impoundment types in Ec­ are involved, a single basic design is common to uador generally occur where precipitation is at all. In each case, the mechanism is a mini-im­ least 200 cm annually and 8 cm monthly (Gil­ poundment based upon a biphasic system: a su­ martin, 1983). perficial, nonliving, imbibing tissue overlying a Smith et al. (1985) provided the first data on deeper absorptive one containing transfer cells tank epiphyte water relations in a study of 11 which traverse an effective moisture barrier. impounding C3, C3/CAM and CAM bromeliads VELAMENTOUS ROOTS. Epiphytic-orchid roots in a Trinidad rain forest. The plants were assayed are specialized for aerial absorption (FIGURE 12) at four to six hour intervals over two rainy days as are those of some Araceae (e.g., Anthurium). followed by a sunny one. According to pressure The system is especially refined in xeric Orchi­ bomb readings, bulk-leaf water relations were daceae. Typical orchid roots are bounded by a faithful to photosynthetic pathway and second­ conspicuous, multilayered rhizodermis (the ve­ arily to local environment. Xylem tension peaked lamen) of protodermal origin. Dead at maturity, during the day or night respectively for C3 and it forms an absorptive, insulating mantle 1-24 CAM plants, probably mirroring periods of cells thick (Pridgeon, 1986), enclosing a living greatest diffusive conductance. However, values core comprised ofan often chlorophyllous cortex were always low «0.59 megapascals) as were and functional stele. Cell walls within the vela­ those for solute potential. A steep drop in night­ men are elaborately pitted and sculptured, and time solute potential in the CAM species was sometimes differentiated into several anatomi­ favored by acidification at near-record levels for cally distinct zones. Upon contact with fluids, leaf succulents: up to 365 mol H+/m3• The CAM the velamen becomes engorged almost instan­ forms showed reduced tension and slower de­ taneously. Only the pneumathodes remain air­ acidification in stormy compared to clear weath­ filled, repelling moisture by some as yet un­ er, illustrating how quickly carbon and water determined mechanism. Fluids in a saturated relations respond to changing atmospheric con- velamen lie against the outermost cortical layer: ditions. J a uniseriate, suberized hypodermis, largely im­ The photosynthetic pathway followed by G z­ permeable except for its transfer cells (FIGURE mania monostachia, the only C3/CAM inter­ 11) whose protoplasts serve as channels for os­ mediate included in the study, tracked the aridity motic inflow of water and solute uptake. Vela­ of its surroundings. In dense lowland forest in mentous aroid roots are organized along the same deep shade, C3-type fluctuations were recorded. lines, but nothing is known about function. In a drier forest gap not far away, the same species A fair number ofepiphytic and a few terrestrial became a CAM plant. Clearly, some measure of orchids produce tilosomes consisting of numer­ this common, wide-ranging bromeliad's ecolog­ ous lamellate or fibrillar protrusions from the ical amplitude is based on its flexible water re­ velamen just above passage cells (FIGURE 17; lations. Smith et al. failed to demonstrate why Benzing et aI., 1982b; Pridgeon et al., 1983). If CAM and C3 epiphytes are so often vertically the intermeshing branches are nonwettable and segregated in humid forests, as they were here. loosen when infiltrated by moisture, they could Values for bulk-leaf water potential indicated that act as one-way valves, allowing water to pass into none of the species monitored was moisture the cortex while retarding its loss during dry stressed more than another despite the distinct weather. Rugose tilosomes of the Cryptopho­ difference in their photosynthetic syndromes. ranthus type seem less likely to modulate mois- 1986J BENZING: VASCULAR EPIPHYTISM 33 ture exchange ofthis kind, but perhaps their pres­ cell, then through the rest of the stalk, and finally ence impedes passage of potentially pathogenic to the mesophyll below. Later, moisture evap­ microbes and invasive hyphae through what orates, upper central-disc-cell walls collapse, and would otherwise be the most easily breached point shield centers and wings return to their original in the exodermis. positions and plug-like function. In essence, a When engorged velamina eventually embolize heavily trichomed bromeliad leaf is, like the ve­ as drying occurs, they afford protection against lamentous root, bounded by an absorbent, non­ desiccation. Matric forces generated by dry bark living tissue which immobilizes descending can­ may exceed several hundred megapascals, more opy fluids and renders them accessible to a than enough to draw water from the cortex if the basement layer of transfer cells. moisture continuum were not broken. Dry soil The absorptive capacity of trichomes on leaf destroys young, unsuberized roots of several des­ sheaths of tank bromelioids (subfamily Brome­ ert terrestrials that lack a similar mechanism lioideae) has not been investigated adequately. (Jordan & Nobel, 1984). After wet weather re­ Also, claims that foliar hairs of several polypo­ turns, regrowth necessary to restore absorptive diaceous ferns can supplement root function are function is affordable since less than 15 percent based largely on their capacity to take up eosin of total plant biomass was sacrificed. Larger and from flooded leaf surfaces. Foliar hairs of pleu­ more frequent costs are involved for exposed rothallid orchids with similar uptake qualities epiphytes with small shoot/root ratios because failed to rehydrate partially dehydrated leaves they are immediately vulnerable to drought after (Benzing & Pridgeon, 1983). Atmospheric bro­ every rainstorm. Preliminary observations and meliad samples behaved quite differently. Sur­ experiments on orchid roots offer few definitive face wetting dissipated 15-25 percent deficits in answers but pose many interesting questions. a few hours. However, saturated air did not effect Foremost of these is why orchids exhibit such a rehydration, contrary to other experimental find­ variety of root morphologies when the basic an­ ings (DeSanto et aI., 1976). atomical theme is so uniform (Benzing et aI., 1983). PHOTOSYNTHESIS FOLIAR TRICHOMES. Several epiphytic ferns and All epiphytes and mistletoes photosynthesize, Astelia (Liliaceae) possess hairs which may be although some need additional assimilates from absorptive, but those of tillandsioid bromeliads other sources. Certain life stages of several exhibit the most elaborate structure consisting nonparasitic taxa are indisputably dependent on ofa uniseriate stalk subtending a nonliving shield external carbon supplies: gametophytes of of empty cells (FIGURE 16). Radiating from the Lycopodium, Ophioglossum, Psilotum and Tme­ shield center are four equal-sized, thick-walled sipteris, as well as young orchid seedlings, remain cells, one or more symmetrical sets of ring cells achlorophyllous for weeks to many months fol­ and an often elongated and asymmetric wing. lowing germination. Until shoots develop, nu­ Alternately thick and thin zones in outer walls trients are obtained via symbiotic fungi from ad­ of ring cells impart hinge-like qualities for wing jacent organic media. Dependence on host flexure. Stalk cells, particularly the uppermost substrates has allowed considerable reduction of and largest one, contain dense protoplasts green to heterotrophic tissue ratios in dwarf and equipped for absorption (Dolzmann, 1964, 1965). perhaps other mistletoes. The possibility of con­ Light scattering from dry shields is considerable tinuous flow into adult orchids has not been tested (Benzing & Renfrow, 1971). nor is there sufficient evidence to support claims Although other theories have been offered for epiparasitism in canopy-based Orchidaceae (Haberlandt, 1914; Dolzmann, 1964, 1965), (e.g., Ruinen, 1953; Johansson, 1977). water absorption by tillandsioid scales can be described plausibly in terms of osmotic and me­ Photosynthetic Pathways chanical forces alone. Uptake begins when hy­ drophilic shield cells imbibe fluid; as filling pro­ Canopy-dependent flora rarely, if ever, shows ceeds, the upper walls of the four central disc C4 photosynthesis (for possible occurrence in cells rise as adjacent cell cavities expand (FIGURE some orchids, see Avadhani et aI., 1982). Con­ 16). Simultaneously, the wings flex downward ditions congenial to the typical C4 species, i.e., against leaf surfaces. This combined action of specifically, high irradiance and temperature, at elevation of central disc and ring cells and down­ least moderate moisture supply, and fertility, do ward flexure of wings supposedly produces a mi­ not usually coincide in tree crowns. Humid mi­ nute suction, drawing more water under the shield crosites are either shaded by foliage or shrouded and into the central disc cells. Once the latter are by recurrent cloud or fog, thus most appropriate filled, moisture moves osmotically into the dome for C3 activity. Exposed locations offer condi- 34 SELBYANA [Volume 9

tions well suited to CAM; this pathway may be, constraints. Epiphytic members of Ericaceae, in fact, better represented in the epiphytes than Melastomataceae, and other predominantly in any other ecological type, even desert inhab­ woody families are probably exclusively C3 itants. plants, but confirmation is lacking. Winter et al. Crassulacean acid metabolism offers greater (1983) judged Agapetes, Ficus, Fagraea, Procris latitude than either C3 or C4 photosynthesis for and Schefflera, all of which have active vascular coping with fluctuating moisture supplies. Much cambia, to be incapable of CAM. So far, only the of what is known about CAM in epiphytes be­ woody stranglers of Clusia have been shown to yond its occurrence is based on a few taxa, mostly fix CO2 by night (Ting et aI., 1985b). More ex­ orchids and bromeliads. The reports of Martin tensive analyses will be necessary to establish the and co-workers on Tillandsia usneoides (Martin importance of CAM and CAM-like behavior in et aI., 1981; Martin & Siedow, 1981; Martin & predominantly herbaceous groups such as Ges­ Peters, 1984) are especially enlightening because neriaceae and Piperaceae. Despite considerable laboratory and field results were coordinated. succulence and an epiphytic habit, at least some Peperomia camptotricha from everwet forest in ofthese are C3 plants (e.g., Boea ofGesneriaceae southern Mexico displayed the widest array of and three Australian peperomias; Winter et al., photosynthetic patterns (Sipes & Ting, 1985). 1983; Ting, unpubI.). Young foliage CAM-cycled, while older organs Photosynthetic roots occur in most epiphytic took up about as much or more CO2 by night as orchids and some aroids. Chloroplasts reside in by day. As moisture stress was applied, first CAM illuminated cortical, and sometimes stelar, and then CAM-idling developed in young and parenchyma (Benzing et aI., 1983). Most orchid old leaves. Photoperiod was another determi­ roots are oval to round, but those of leafless nant of photosynthetic pathway. Effects oftem­ (shootless) Campylocentrum pachyrrhizum and perature, humidity and season are best known several Phalaenopsis are almost planar. Taenio­ for Tillandsia usneoides; nocturnal acidification phyllum rhizophyllum roots are, as the name im­ in this species proved to be very sensitive to plies, even more leaflike. Root mantle develop­ numerous ecoclimatic factors (Martin et aI., ment and other structural features which might 1981). logically reflect trophic capacity do in fact seem Evidence for the pervasiveness ofCAM in epi­ to be related to photosynthetic vigor. Shootless phytes is mostly based on stable carbon isotope species and epiphytes with noticeably reduced data. Winter et ai. (1983) surveyed about a third leaf surface never possess velamina exceeding of Australia's vascular epiphyte flora (127 of380 two to three layers. Light harvest is probably species representing 17 families). Sixty-six tested improved for Campylocentrum pachyrrhizum species were CAM types (from Asclepiadaceae, after the delicate rhizodermis is sloughed off the six; Orchidaceae, 55; Polypodiaceae, three; and exposed side (FIGURE 13). Interspecies function Rubiaceae, two). The remainder, including 11 of differs enough to require separate analyses to es­ 19 dicotyledons, were C3 species. Unfortunately, tablish how orchidaceous and other green roots isotope data do not resolve those questions which affect whole-plant carbon balance. Roots of concern capacity to CAM-idle or to coordinate shootless orchids and related semileafless species C3/CAM switching with environmental signals like Kingidium taeniale are indeed primary (facultative taxa). A peculiar pattern of deuteri­ trophic organs. None, however, fixed CO2 as vig­ um : hydrogen discrimination accompanies orously as did leaves (Benzing & Ott, 1981; CAM-cycling for as yet undetermined reasons Avadhani et al., 1982). Net dark fixation was (Sternberg et aI., 1984), but this technology has revealed in several shootless genera (Benzing & not been used to examine many epiphytes (Ting Ott, 1981; Benzing et al., 1983; Cockburn et aI., et aI., 1985a). Medina and Troughton (1974), 1985; Winter et aI., 1985). Titratable acid fluc­ Medina et aI. (1977), and Griffiths and Smith tuated considerably less in roots of several leafy (1983) gathered substantial isotope data for Bro­ species (e.g., Epidendrum radicans). Similar ma­ meliaceae, thereby providing the most compre­ terials examined by others (Avadhani et al., 1982; hensive coverage of a single heavily epiphytic Goh et al., 1983) showed no net photosynthesis, family. Bromelioideae, a subfamily containing but they still have trophic significance. Exposed many tank epiphytes, exhibits CAM almost ex­ root tissue often comprises half or more of the clusively. Tillandsioideae proved to be mixed: leafy orchid body, especially during juvenile softleaf tank forms are C3 types, while the at­ stages. mospheric forms fix substantial amounts of CO2 via PEP carboxylase. Shade Adaptation Crassulacean acid metabolism in epiphytes and terrestrials alike is associated with particular Shade-tolerant plants, including some epi­ habits which may reflect the same biomechanical phytes, exhibit several mechanisms which en- 1986] BENZING: VASCULAR EPIPHYTISM 35 hance photon capture in their dimly lit habitats. a single week. Total bulk atmospheric deposition The bromeliads Aechmea fulgens, Nidularium was mostly soluble and amounted to about 25 bruchellii and several species of Vriesea and Til­ percent of the total phosphorus flux through the landsia, some Anthurium and certain gesneriads ecosystem. A useful compilation of nitrogen in­ possess abaxial mirrors that recycle red light (the puts has been obtained for a deciduous forest in proportionally more abundant form in shade Tennessee (Lindberg et al., 1986); additions suf­ light) back into overlying chlorenchyma (Lee et ficient to satisfy five to ten percent of the aggre­ aI., 1979). Bromeliads with bicolored foliage usu­ gate nitrogen requirement for community growth ally feature horizontal leaf attitudes and little were identified. Depending on certain character­ self-shading (Benzing & Friedman, 1981 b). istics, individual plants could be benefited to an Closely-related forms higher in the forest profile even greater degree. For instance, a hypothetical are often concolorous and multilayered; their leaf resident epiphyte able to scavenge nitrate from blades are more upright. Those multilayered dry vapor and particulates could draw on a more rosettes that do occur deeper in the forest canopy plentiful nitrogen supply than an ammonium have relatively thin, transparent foliage. Essen­ specialist largely restricted to wet deposition. Ni­ tially monolayered Nidularium bruchellii displays trate, the dominant incoming form of nitrogen a faint bluish-green iridescence reminiscent of (about 75 percent), was more abundant in dry the thin film optical interference responsible for vapor and particulates compared to ammonium greater relative absorption of red light by shade­ which was most concentrated in precipitation. A adapted Selaginella willdenovii (Lee & Lowry, constellation of nonnutritive metals in soil-like 1975). Another response to low photon flux cen­ proportions (e.g., aluminum, barium, gallium, tered on stomatal modification is described be­ iron, yttrium) found on shoots of Tillandsia us­ low. Shade acclimatization has been examined neoides throughout the southeastern United States in Tillandsia usneoides (Martin et al., 1986); be­ implies that considerable particulate loads were yond increased chlorophyll content, shade-grown trapped by this species' trichome shields (Shack­ differed little from sun-grown samples. Winter lette & Connor, 1973; Connor & Shacklette, et al. (1986) demonstrated that several CAM or­ 1984). Nutritional consequences of this finding chids, a fern, and a vining Hoya fix CO2 the same were not determined. way in bright sun and deep shade. Moreover, Interaction between atmospheric and terres­ quantum yields fori photosynthetic oxygen evo­ trial phenomena further assure that nutrient flux lution indicated that there is no intrinsic reason through a forest canopy is nonuniform in time why CAM should be disadvantageous in shaded and space. A few storms can have dispropor­ canopy habitats. tionate influence. Kellman et al. (1982) discov­ ered that more than half of the annual wet-de­ NUTRITION posited calcium, potassium and phosphorus in a relatively dry Honduran forest arrived within one Plant nutrients enter forest canopies from the to ten rainy days. Finer sampling would have atmosphere and soil. Soil-borne ions brought up­ revealed considerable variation even during in­ ward by tree transpiration are captured according dividual events; solute concentration drops to the epiphyte's capacity to tap leachates, lit­ quickly after precipitation has washed dust from terfall and certain animal products such as ant the atmosphere. Nutritional unevenness is fur­ excrement. Likewise, delivery from the atmo­ ther magnified within the canopy: initial flushes sphere involves multiple vehicles of potentially become charged with ions accumulated on plant varying utility to particular epiphyte forms. Dry surfaces since the last storm by dry deposition vapor and particulates deliver nitrogen as am­ and migration from within. However, enrich­ monium and nitrate. Rainfall carries small but ment at one level may be accompanied by dim­ nutritionally significant quantities of all the es­ inution at another, thus depriving plants farther sential elements (Benzing & Renfrow, 1980). downstream. Jordan and Golley (1980) recorded There are no comprehensive data on air-borne considerable nutrient scavenging in a wet Ven­ deposition of key elements for a tropical ecosys­ ezuelan forest, but the responsible organisms were tem, but substantial "filterable" phosphorus as­ not identified. sociated with unidentified carriers was found set­ The mineral nutrition of epiphytes, especially tling in a consistent seasonal pattern over a pulse-supplied types, is both advantaged and Colorado coniferous forest (Lewis et aI., 1985). constrained through arboreal existence. On the Sedimentation of what was presumed to be bio­ positive side, uptake of ions that tend to be im­ logically derived (but not from pollen) phos­ mobilized by soil (e.g., phosphate) is unimpeded phorus peaked in early summer as a single short by the same physical/chemical processes in tree pulse. At this time as much as 33 percent of the crowns. Moreover, epiphytes are not subjected annual input (up to 15 mg/m2) accumulated in to the high, potentially toxic reactivity of 36 SELBYANA [Volume 9

aluminum present in many tropical soils, and rhizospheres, while others might increase the flowing canopy fluids repeatedly replenish nu­ root's capacity to capture passing solutes. For trient-depleted rhizospheres. But there may be unknown reasons, nitrogenase activity was es­ attending complications: fluid turnover reduces pecially pronounced in the phyllosphere of cer­ capacity to modify adjacent media (often the tain epiphytic orchids in India (Sengupta et al., greatest source of supply) in the same ways soil­ 1981). Perhaps epiphyte leaves, rather than of­ rooted species solubilize nutrients (secretion of fering any special chemical advantage, simply protons, chelators). In addition, exposure to air live long enough to encourage denser bacterial precludes maintenance of finely-divided root colonization. systems, resulting in low contact and lessened Epiphytes engage in several ant/plant associ­ opportunity to extract ions from what is essen­ ations, two of which grant nutritional advantage tially a two- rather than three-dimensional (pen­ (Madison, 1979; Huxley, 1980; Longino, un­ etrable) substratum. pubL). Arboreal cartons create rooting media (FIGURE 9) for neotropical "nest-garden" plants Trophic Strategies representing diverse families (e.g., Araceae, Bro­ meliaceae, Gesneriaceae, Orchidaceae, Pipera­ MUTUALISM. Microbial mutualists are in­ ceae). Obligate members ofthis small specialized volved in improving the nutrition ofmost plants. flora produce myrmecochores which encourage Roots of a number of adult orchids have been dispersal to suitable substrata. Physiological bas­ found to contain hyphal coils and pelotons sim­ es for nest preference have not been examined. ilar to those routinely associated with myco­ Quite intriguing is the near-total restriction of trophic seedling stages. In South Florida, heavy ant-fed myrmecophytes to the forest canopy involvements were noted in shootless Harrisella (Thompson, 1981). One or more epiphytes of at porrecta, Polyradicion lindenii and Campylocen­ least six families (Asclepiadaceae, Bromeliaceae, trum pachyrrhizum growing on Fraxinus caro­ Nepenthaceae, Orchidaceae, Piperaceae, Poly­ liniana(Benzing & Friedman, 1981a). Three leafy podiaceae) contain ant colonies in shoots (Hux­ encyclias and epidendrums growing mostly on ley, 1980). No elaborate trophic rewards beyond Taxodium distichum in the same forests were those designed for pollinators and certain seed infected more sporadically. An assessment of dispersers are usually offered, unlike the situa­ Malaysian materials persuaded Hadley and Wil­ tion with terrestrial ant plants where defense is liamson (1972) that neither mature terrestrial nor the plant's primary benefit. At present, demon­ epiphytic forms remained significantly fungus­ strations of nutrient flux between ant and plant dependent beyond early juvenile stages. How­ are cursory (Benzing, 1970a; Huxley, 1978; ever, evidence that orchid fungi can also enhance Rickson, 1979). There are no available data on absorption of phosphorus in heterotrophic seed­ nutrient budgets or peculiarities of uptake. lings (Smith, 1966, 1967) and adult terrestrial Tank epiphytism incorporates mutualism, in Goodyera repens (Hadley, 1984) indicates that this case with an extensive microflora, diverse benefit need not end with the development of invertebrates and some vertebrates. The system green tissue. is humus-based in the sense that plants act as The presence of vesicular-arbuscular mycor­ passive filter feeders on falling plant debris. The rhizas would seem unlikely in forest canopies cost ofdegradative enzymes borne by animal and given the large size and poor dispersibility of the some pitfall plant carnivores is obviated by the massive fungal spores involved. Holbrook and tank bromeliad's moist microcosm wherein veg­ Putz (unpubL) noted arbuscules in soil but not etable material can be processed by an abun­ in palm trunk roots of two Venezuelan strangler dance of detritivores and saprophytes. Essential figs. Familiar ectotrophic systems should not be ions thus liberated into tank fluids enter the plant expected either, since families best known for through leaf bases. Tank nutrition is complex this type of mutualism are scarcely, ifever, rep­ and varied and more fully discussed elsewhere resented in canopy-dependent floras. Some ter­ (Benzing, 1986). restrial species in the Ericaceae, like orchids, as­ sociate with septate fungi capable of releasing CARNIVORY. Carnivorous epiphytes belong to nitrogen and perhaps other essential ions from two, possibly three, families: Lentibulariaceae complex organic substrata on older bark in hu­ (Utricu/aria), Nepenthaceae, and perhaps Bro­ mid tropical forests (St. John et aI., 1985). meliaceae. The epiphytic bladderworts differ lit­ Algae and bacteria inhabiting velamina could tle from terrestrial forms and, in fact, grow under benefit epiphytic aroids and orchids (FIGURE 12) much the same conditions; all are hygromorphic much as free-living mutualistic soil microbes en­ and root in continuously moist humus, bryo­ hance terrestrial plant nutrition. Some prokary­ phyte mats or bromeliad tanks. Moss-covered otes may reduce dinitrogen, as do those in soil rocks and fallen logs accommodate similar 1986] BENZING: VASCULAR EPIPHYTISM 37

species. Regardless of the medium, traps pre­ cannot escape due to the lubricating effects of sumably capture small aquatic animals. Canopy­ copious wax particles on leaves. Subsequently, dependent Nepenthes are mostly hemiepiphytic the prey drowns and decomposes, releasing nu­ vines that again differ little in habit and nutri­ trient ions that enter the shoot via absorptive tional adaptation from soil-based relatives. The trichomes. Catopsis berteroniana recruited more case for carnivory in Bromeliaceae is more prey than did several other tank bromeliads when equivocal. tested in southern Florida (Fish, 1976; Frank & Certain impoundment bromeliads have been O'Meara, 1984), but more definitive experi­ labeled carnivores, but these claims are not en­ ments are needed to assess the proposed role of tirely persuasive. In his classical work on neo­ ultraviolet reflectance. In addition, quantifica­ tropical ant plants, Wheeler (1921) said of Til­ tion of nutrients in plants and tanks, and rates landsia with hollow bulbous bases that ants of interception, are essential in order to deter­ "make fatal incursions into water-containing mine whether prey represents significant nutri­ chambers." His trapping sequence could not be tional input. If the shoot is unusually attractive corroborated, however, using either Tillandsia to terrestrial insects and enough of them can be butzii or T. caput-medusae collected in Costa recruited to counter unusually oligotrophic con­ Rica and Mexico (Benzing, 1970a). Dissected ro­ ditions in tree crowns, then designation as a low­ settes proved to have dry axils teeming with brood grade carnivore would be justified. and adult ants, and all attempts to fill intact ro­ settes with water by immersing or spraying failed. Atmospheric Nutrition Nest debris contained considerable soluble ni­ trogen. Radiocalcium administered to axils of Neither humus nor appreciable animal prod­ several intact shoots was taken up, presumably ucts are available to pulse-supplied species. Mist/ by leafbase trichomes, and translocated through­ tangle epiphytes of the Orchidaceae barely con­ out treated specimens. tact host surfaces (FIGURES 3, 4); roots of at­ Picado (1913) sought evidence to prove that mospheric bromeliads securely grip the substra­ epiphytic Bromeliaceae include carnivorous tum but are essentially nonabsorptive (FIGURE species. Indeed, amino acids placed in foliar im­ 2). Some other root systems (e.g:, Codonanthe, poundments of certain tank-producing tillands­ Hoya) seem too reduced to provide much service ioids in Costa Rica were seemingly absorbed by beyond that of holdfast. As noted previously, the adjacent leaf surfaces. He also reported hydro­ shoot epidermis and root mantle have some­ lytic enzymes in mucilage released by injured times evolved to accommodate a widely inter­ specimens. No specialized secretory glands were mittent resource supply. described, nor could Picado prove that the ob­ Orchid root anatomy which proves so effica­ served proteins were of botanical rather than mi­ cious for water balance may have another impact crobial origin. Species of Aechmea, Billbergia and on mineral nutrition. It is not clear at this point Neoregelia with no compelling carnivorous traits how different thicknesses and arrangements of are also capable of absorbing amino acids from rhizodermal cells affect bulk exchange between tank fluids (Benzing, 1970b). Capacity to utilize imbibed canopy fluids and those still flowing simple nitrogenous byproducts of impounded along root surfaces. Very likely, transfer cells vegetable material is consistent with the humus­ seated up to 24 cell widths and several milli­ based nutrition characteristic of most tank bro­ meters beneath the root surface lack full access meliads (Benzing, 1986). to ions in passing fluids. On the other hand, stag­ Catopsis berteroniana (FIGURE 6) of subfamily nation within the engorged velamen could be Tillandsioideae is reputedly carnivorous (Fish, advantageous in view of the high nutrient con­ 1976). Its rosette is upright, more chlorotic than tent of initial flushes of rainfall and canopy leach­ most, and covered with a loose, whitish, cuticu­ ates. lar powder. Leaf bases are coated more heavily Greater insight into root specialization for than are blades. Exposed sites at the tops of tree mineral nutrition will require additional inves­ crowns are preferred, and tanks contain rela­ tigation ofthe exodermis, particularly its transfer tively more animal remains and less plant ma­ junctions, under conditions that approximate terial than do most other impounding brome­ those in nature. Like transfer cells in general, liads. Occasional specimens growing in partial exodermal passage cells of Sobralia macrantha shade intercept considerable falling plant debris, (FIGURE 17) contain dense protoplasts equipped how~ver. Prey acquisition by this species is sup­ with many mitochondria and membranes (Ben­ posedly encouraged by cuticular ultraviolet re­ zing et aI., 1982b). Chemical qualities of the ve­ flectance that attracts flying insects as they orient lamen are probably also important. Velamina toward sky light while negotiating canopy ob­ stripped from Vanilla planifolia exhibit unusual structions. Animals tumble into tank fluids and buffering qualities (Bottger et aI., 1980) that may 38 SELBYANA [Volume 9

help roots immobilize passing cations. Radio­ functional tradeoff"s provides some insight into isotopes have been used to demonstrate ion and why reduction may have occurred. In both lin­ water uptake and translocation by aerial roots of eages all three basic vegetative functions are many orchids (e.g., Haas, 1975). Absorption ki­ combined in a single organ system, thus provid­ netics have never been measured. Dycus and ing equal opportunity for similar benefit. Knudson (1957) obtained rather puzzling results Shootlessness and rootlessness can enhance fit­ which suggested that such roots are impenetrable ness in two ways: (1) energy and material are to ions except where velamina have been dis­ diverted away from production of functionally torted by growth against bark or some other solid specialized vegetative tissue, and (2) ontogeny is object. simplified enough to abbreviate the life cycle. In Bromeliad trichomes also participate in nu­ the first instance more resources become avail­ trient absorption. Direct evidence of their in­ able for reproductive tissue; in the latter, a short­ volvement in nutrition was obtained by auto­ ened juvenile phase fosters heightened fecundity radiography with tritiated amino acids (Benzing according to a simple mathematical function et aI., 1976). Corroboration was obtained using (Steams, 1976). Of course, neither development radiolabeled calcium, phosphorus and sulfur would be so critical were epiphytic habitats equa­ (Benzing & Pridgeon, 1983). Trichomes of nine ble, but they are not. The pulse-supplied forms pleurothallid orchids failed to absorb these ele­ are especially constrained; stress curtails their ments. Longer-term studies demonstrated that productivity, yet high mortality obliges substan­ atmospheric Tillandsia paucifolia can luxury­ tial fecundity. Together, these two impediments consume phosphorus (but not nitrogen or potas­ favor resource allocations conducive to repro­ sium) and also has remarkably high affinity for ductive rather than competitive activity. amino acids and numerous metals (apart from Occurrence of multipurpose organs and cor­ potassium and calcium; Benzing & Renfrow, responding diminution of others among special­ 1980) and for amino acids (Benzing, unpubl.). ized epiphytes is not unexpected. Compared to Trichomes located on the leaf sheath surfaces of soil-based vegetation, many epiphytes occupy a tank bromeliads, although apparently slower to relatively uniform environment. Polarization of absorb (Benzing et aI., 1976), may still playa their bodies, originally a requisite for plant life prominent role in nutrition since contact with on land where both aerial (drying) and subter­ an ion source is more or less continuous. Struc­ ranean (dark) environments were accommodat­ turally similar organs lining the tanks of New ed, is less essential. The pulse-supplied form in Zealand Astelia (Oliver, 1930) remain unstudied. particular inhabits a single medium, albeit not Trichomes borne by several polypodiaceous ferns the aquatic one that harbored progenitors ofland take up eosin, but more definitive experiments flora. It is not surprising that a long-standing are required to confirm trophic function. functional and structural differentiation between shoot and root systems has become blurred in VEGETATIVE REDUCTION some very specialized epiphytes. Whatever their identity, the advantages of extreme vegetative An especially intriguing question concerns the reduction in epiphytic Bromeliaceae and Orchi­ unusual habits of epiphytes beyond those de­ daceae must be considerable because substantial signed to promote impoundment and nidifica­ complications accompany both conditions. By tion. The most curious examples come from Bro­ basic design (e.g., lack of stomata), the root is a meliaceae and Orchidaceae. While pronounced poor second to a leaf as an organ for conservative vegetative reduction is involved in both in­ water use during photosynthesis. The bromeliad stances, different organ systems are affected. In option comes at a high price also; trichomes of Tillandsia and closely related Vriesea a near­ the sort covering the atmospheric bromeliad in­ complete suppression of root development has terfere with life in shady habitats and totally pre­ occurred. Every intermediate condition possible clude existence in overly humid ones (Benzing between profuse and very sparse rooting exists & Renfrow, 1971; Benzing et aI., 1978). in less specialized relatives. The Sarcanthinae (Orchidaceae) exhibit a progression of compa­ CONCLUSIONS rable degree but opposite direction: abbreviated bodies produce no shoot beyond the short stem Of the vegetative mechanisms serving epi­ needed to support undiminished root production phytes, those concerned with maintenance ofhy­ and an occasional axillary scape. Congeneric drature show the narrowest tolerance. Each time leafy and shootless forms (e.g., Campylocentrum; an epiphyte's moisture source dries out for any FIGURES 3, 4) provide evidence of how fast veg­ length of time, disastrous consequences may re­ etative form has changed in some clades. Con­ sult if there is a delayed or inappropriate reac­ sideration of environmental constraints and tion. Adaptation to drought in forest canopies, 1986] BENZING: VASCULAR EPIPHYTISM 39

as elsewhere, requires coordinated structure, continuous moisture supply and their CO2 source physiology and phenology, and deployment of is usually very humid. Nevertheless, the ubiquity mechanisms incorporating all three variables is of dilute cell sap suggests that many epiphytes, especially limited for pulse-supplied epiphytes. like Sinclair's subjects, may be especially well Moisture supply is never reliable enough for these equipped to anticipate the uncommon but po­ species to support the demand of highly produc­ tentially lethal drought. High stomatal sensitiv­ tive foliage. Nor does the classic resurrection pat­ ity serves other vegetation facing the same prob­ tern appear to be viable. Survival is possible only lem. Gas exchange is curtailed at high water through high capacitance, often augmented by potentials in six evergreen trees in a New Zealand mini-impoundment, and economical water use. cloud forest (Jane & Green, 1985). Root growth, This third phenomenon offers especially fertile which in these species is inhibited by almost con­ ground for further inquiry into the basis of xe­ tinuously saturated soil, obliges preparedness to rophytic epiphytism. minimize transpiration soon after the infrequent Sinclair's (1983a, 1983b, 1984) work reveals drought begins to eliminate the shallow moisture a glimpse of what may be a widespread type of source. physiological response to intermittent moisture According to the optimization hypothesis, supply among epiphyte flora. Both the ferns and plants do not expend moisture needlessly and orchids he examined possessed dilute cell sap. tend to hold marginal costs of carbon gain rel­ Turgor was consequently low even at full hydra­ atively constant through coupling diffusive con­ tion and the bulk-leaf water potential at which ductance with photosynthetic capacity as deter­ stomata apparently closed was also unusually mined by endogenous and environmental factors. high. Clearcut orchid data were not obtained, but Where growing conditions are extreme, stomatal at effectively zero foliar conductance, relative accommodations can be quite specialized, as in water content had only decreased to about 85 Paphiopedilum. a paleotropical genus of pre­ percent for the orchids and 94 percent for the dominantly forest-dwelling and often epiphytic ferns, far less water loss than normally accom­ C3 slipper orchids. Achlorophyllous guard cells panies stomatal closure in much xerophytic ter­ known only in these plants long puzzled phys­ restrial vegetation. Mistletoes hold the record for iologists since photophosphorylation normally low solute potential and insensitive stomata provides energy for the substantial potassium flux among canopy-dependent forms, but here very and malic acid synthesis required for typical sto­ negative water potential is needed to divert matal movement. Paphiopedilum apparently enough of the host's transpiration stream to ob­ grows so consistently in deeply shaded, oligotro­ tain sufficient nutritive solutes, particularly ni­ phic habitats that foliar conductance need never trogen. Ehlringer et al. (1985) demonstrated that be very high to utilize photosynthetic capacity high conductance maintained by these plants, fully. Sufficient energy (and ultimately guard cell even while hosts were drought stressed, was a turgor) for maximal aperture is available from necessary part of the parasite's mineral nutrition. mitochondria and perhaps the little known blue­ Harris's earlier survey (1918) of Jamaica and light-driven electron transport system. South Florida epiphytes and Spanner's (1939) Additional cases may exist where extreme en­ data on Myrmecodia and Hydnophytum antici­ vironment has fostered unconventional control pated Sinclair's discoveries. In addition, Harris of diffusive conductance in canopy-based flora. found that solutes were fully two to three times Pulse-supplied epiphytes from the most stressful more concentrated in adjacent phorophyte than exposures grow slower than most plants, includ­ in epiphyte foliage. Understory herbs also ex­ ing Paphiopedilum, perhaps because the con­ ceeded counterparts rooted in the canopy above. straints on their productivity are greater. Atyp­ His data are particularly noteworthy because they ical epidermal features such as those of some concern structurally diverse epiphytes belonging atmospheric bromeliads (Tomlinson, 1969) are to four families and hence convincing evidence all the more interesting given the epiphyte's slow that solute potential is generally high in canopy­ maturation even when well watered and fertil­ dependent species. ized in culture. Claims that Tillandsia usneoides Epiphytes need not maintain concentrated os­ lacks mobile guard cells, and tinier T. bryoides motica; unlike trees, they are not required to has no stomata at all, have proven incorrect support tall water columns or overcome asso­ (Martin & Peters, 1984). Findings from T. us­ ciated flow resistance. In addition, conservation neoides should not discourage further inquiry, measures like CAM and xeromorphy reduce peak however, because this is one of the most vigorous demand for many species. More mesophytic of the atmospheric species. Precedents exist for forms are spared severe desiccation under nor­ land plants lacking normal (perhaps all) me­ mal circumstances simply because supporting chanical control of gas exchange. Shootless or­ humus or impoundments provide a relatively chids gain carbon by astomatous roots alone. 40 SELBYANA [Volume 9

Crassulacean acid metabolism cannot improve Epiphyte biology must move on to incorporate water economy here, and were it not for the close a broader view ofplant integrative quality. While stoichiometry achieved during daytime deacidi­ aspects of vegetative function and related exter­ fication and refixation (Cockburn et aI., 1985), nal constraints were treated separately in this much regenerated CO2 would be lost. discussion, no plant's capacity to live as an epi­ Further inquiry into epiphyte photosynthesis phyte can be described solely in terms of re­ is also needed to address other basic questions sponses to drought, infertile substrata or shade. concerning plant survival in tree crowns. Among Plants adjust internal resource allocations and stomatous species, ability to shift fixation path­ the time and mode ofprocurement so that growth way may provide as yet poorly understood flex­ is governed by availability of all required re­ ibility in the face of rapid, frequent or unpre­ sources (Bloom et aI., 1985). The greatest chal­ dictable changes in moisture supply. Epiphytic lenge facing workers who wish to characterize vegetation seems to show widespread CAM-cy­ botanical adaptation lies in identification of those cling that may exist primarily to poise the plant coordinated combinations of life history, phe­ for CAM-idling under stress (Ting, 1985). A more nology, and structure/function that foster plant thorough characterization of astomatous CAM exploitation of specific habitats. No less a charge would help elucidate the full significance of applies to persons interested in understanding shootlessness in Orchidaceae. There is another the basis of epiphytism. challenge: discovery of the trophic implications of such unusual anatomical features as the tbree­ LITERATURE CITED tiered foliar anatomy of certain Peperomia and succulent gesneriads-a colorless adaxial hypo­ ALPERT, P. AND W. C. OECHEL. 1985. Carbon balance dermis and deeply chlorophyllous upper meso­ limits the microdistribution ofGrimmia laevigata, phyll over a less pigmented lower layer. These a desiccation-tolerant plant. Ecology 66: 660--669. arrangements might enhance efficient water use AVADHANI, P. N., C. J. GoH, A. N. RAo, AND J. AR­ during photosynthesis by concentrating CO2 , DITT!. 1982. Carbonfixationinorchids.pp.173- Efforts should be made to resolve epiphytic 193 in J. ARnITTI, ed., Orchid biology-reviews vegetation into better-defined nutritional types. and perspectives, Vol. 2. Cornell Univ. Press, Ith­ aca. Recognition of pulse-supplied and continuously­ BENZING, D. H. 1970a. An investigation oftwo bro­ supplied forms and among the latter group, of meliad myrmecophytes: Tillandsia butzii Mez, T. ant garden, carnivorous, humus-based, and im­ caput-medusae E. Morren and their ants. Bull. poundment groups, is only a beginning; classi­ Torrey Bot. Club 97: 109-115. fication emphasizing more fundamental mech­ --. 1970b. Foliar permeability and the absorp­ anisms is both desirable and possible. It is already tion of minerals and organic nitrogen by certain clear that slow growth and capacity for luxury tank bromeliads. Bot. Gaz. 131: 23-31. consumption of certain ions (Benzing & Ren­ --. 1978. The life history profile of Tillandsia frow, 1980) can mitigate effects of scarce, inter­ circinnata (Bromeliaceae) and the rarity of ex­ treme epiphytism among the angiosperms. Sel­ mittent supply for Tillandsia paucifolia; inves­ byana 2: 325-337. tigation is needed to determine the breadth and --. 1983. Vascular epiphytes: a survey with spe­ underlying processes of this precedent. Another cial reference to their interactions with other or­ aspect ofepiphyte nutrition that could be studied ganisms. Pp. 11-24 in S. L. SUTTON, T. C. profitably is the chemical nature ofcanopy-based WHITMORE, AND A. C. CHADWICK, eds., Tropical substrates and properties of the plants that use rain forest: ecology and management. British Eco­ them. Continuously-supplied species, particu­ logical Society, Oxford. larly those dependent on humus and animal --. 1984. Epiphytic vegetation: a profile and sug­ products, probably include taxa specialized for gestions for future inquiries. pp. 155-172 in E. MEDINA, H. A. MOONEY, AND C. VAZQUEZ- YANES, uptake ofammonium; or possibly organic solutes eds., Physiological ecology of plants of the wet that are abundant in the sources. As for the pulse­ tropics. Proc. international symposium, Mexico. supplied types, recognition that atmospheric in­ Dr. W. Junk Publishers, Boston. puts to forest ecosystems can be substantial, var­ --. 1986. Foliar specialization for animal-as­ ied in form and nutritive quality, and unevenly sisted nutrition in Bromeliaceae. In Insects and accessible to particular epiphytes suggests the the plant surface. Oxford Univ. Press, London (in possibility of broad trophic diversity even here. press). In fact, the colloquial name "air plant" may be --, A. BENT, D. Moscow, G. PETERSON, AND A. more descriptive than was previously thought. RENFROW. 1982a. Functional correlates of de­ ciduousness in Catasetum integerrimum (Orchi­ Finally, mycorrhizal relationships might prove daceae). Se1byana 7: 1-9. to be as important for certain epiphytes as they --, --; AND W. E. FRIEDMAN. 1982b. Roots are for most terrestrial flora. ofSobralia macrantha (Orchidaceae): structure and 1986] BENZING: VASCULAR EPIPHYTISM 41

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