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Absorptive in reducta () and Their Evolutionary and Systematic Significance Author(s): David H. Benzing, Thomas J. Givnish and David Bermudes Source: Systematic , Vol. 10, No. 1 (Jan. - Mar., 1985), pp. 81-91 Published by: American Society of Taxonomists Stable URL: http://www.jstor.org/stable/2418437 Accessed: 29-09-2016 15:34 UTC

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This content downloaded from 132.198.9.255 on Thu, 29 Sep 2016 15:34:40 UTC All use subject to http://about.jstor.org/terms Systematic Botany (1985), 10(1): pp. 81-91 ? Copyright 1985 by the American Society of Plant Taxonomists

Absorptive Trichomes in (Bromeliaceae) and Their Evolutionary and Systematic Significance

DAVID H. BENZING

Department of Biology, Oberlin College, Oberlin, Ohio 44074

THOMAS J. GIVNISH

Harvard University, The Biological Laboratories, 16 Divinity Avenue, Cambridge, Massachusetts 02138

DAVID BERMUDES

Department of Biology, Oberlin College, Oberlin, Ohio 44074

ABSTRACT. Brocchinia reducta, a tank-forming member of subfamily (Bromeli- aceae), possesses foliar trichomes capable of absorbing 3H-leucine as do those borne by other mem- bers of the same family (all and some of ). In general, pit- cairnioid trichomes have been considered incapable of participating in nutrient uptake. Other features of anatomy and physiology, such as the presence of the C3 photosynthetic pathway, suggest that either 1) Brocchinia and tillandsioid tank shoots bearing absorptive hairs are a result of convergence or 2) both subfamilies acquired this feature from the same ancestor. All in all, Tillandsioideae and Pitcairnioideae share more vegetative features in common than either does with Bromelioideae and, thus, may be more closely related than was previously suspected. Tank deployment in Bromelioideae seems to have originated independently from a semi-xeric terrestrial habit that incorporated the CAM syndrome. Factors that could have led to the emergence of ab- sorptive trichomes in Bromeliaceae are identified.

Bromeliaceae, an essentially neotropical fam- bromelioids) are absorptive; the foliar append- ily of about 2100 species comprising three ages borne by members of Pitcairnioideae (the subfamilies (Smith and Downs 1974, 1977, 1979) pitcairnioids) are not (Mez 1904; Tietze 1906; has received considerable study over many Aso 1909; Benzing et al. 1976; Sakai and San- years. In addition to systematic problems, sub- ford 1980; Benzing and Pridgeon 1983). In fact, jects of great interest have been vegetative fea- direct assessments of foliar permeability and, tures that enable these to occupy such specifically, the involvement of bromeliad tri- disparate habitats as swamps, , and for- chomes in solute uptake, have been limited to est canopies. Analyses of adaptations have Bromelioideae and Tillandsioideae with the ex- fostered speculation and controversy, much of ception of two species (Benzing and which is centered on ancestral bromeliad hab- Burt 1970; Benzing et al. 1976). Earlier claims itat preferences and interrelationships of (Tietze 1906; Aso 1909) that foliar hairs con- subfamilies. Pitcairnioideae are generally tribute only marginally, if at all, to nutrient ion viewed as containing the most primitive species procurement in Pitcairnioideae were corrobo- in terms of habit, water balance mechanisms, rated. However, definitive judgments on the nutrient uptake, and dependence on soil. Epi- roles of pitcairnioid trichomes in water balance phytism probably developed in Bromelioideae and nutrient absorption must await a more rep- and Tillandsioideae by different routes. resentative survey of the subfamily. Such a Central to speculations on bromeliad evolu- study should certainly include the most likely tion is the foliar . Depending on the bearers of absorptive hairs in Pitcairnioideae: taxon, a foliar indumentum may supplement or taxa of the Brocchinia. fully replace root absorptive function (Benzing Brocchinia is a little-studied assemblage of 18 and Renfrow 1980). Comparative surveys have species endemic to the Guayana Highlands of led to the belief that trichomes over entire northern South America (Smith and Downs shoots of Tillandsioideae (the tillandsioids) and 1974). Some taxa are known from type collec- leaf hbase of tank-forminP Bromelioideae (the tions only; many are quite localized, occurring

81

This content downloaded from 132.198.9.255 on Thu, 29 Sep 2016 15:34:40 UTC All use subject to http://about.jstor.org/terms 82 SYSTEMATIC BOTANY [Volume 10 only on very few . For lack of ornamental #101) is on deposit in the Oberlin College Her- value, brocchinias tend to be missing from hor- barium, as are specimens of nutans (BEN ticultural collections, thus complicating study #102), paucifolia (syn. with T. circin- of their physiology. While relatively confined nata; BEN #103), and T. ionantha (BEN #104); geographically, Brocchinia has evolved a num- these were used to illustrate bromeliad tri- ber of distinct habits and has radiated into a chomes. A second B. reducta voucher (BEN variety of terrestrial habitats and even moist #101) is deposited at the Selby Botanical Gar- forest canopies. No other pitcairnioid produces dens Herbarium (SEL). Other figures were du- tank (fig. 1) and only the occasional Pit- plicated from cited literature. cairnia roots with any frequency in tree crowns. Of all the brocchinias, Brocchinia reducta is RESULTS probably among the most heavily dependent Foliar hairs of Brocchinia reducta differ from on leaves for mineral ion uptake. It usually roots those of other adult bromeliads in at least two in moist, infertile soil and produces tubular ways: all member cells remain alive after mat- shoots partially filled with rainwater and uration and the stalk is multiseriate at its distal remains. The following report describes anal- end (fig. 3). Partially concentric in arrange- yses of B. reducta trichomes: implications of the ment (fig. 4), the trichome of B. reducta lacks findings to relationships among bromeliad the four upper tier disc cells that dominate the subfamilies and to the evolution of epiphytism center of expanded, highly organized, tilland- in Bromeliaceae are discussed. sioid trichome caps (figs. 2, 6, 13, 15, 23). In common with those of the most mesic, shade- MATERIALS AND METHODS tolerant members of Tillandsioideae, B. reducta Brocchinia reducta specimens used in this study trichomes do not extend beyond the epidermal were growing on a damp-sand savanna near concavity in which they are seated (figs. 18, 19, Km 148 along the El Dorado-Santa Elena Road 21, 22). All cells of adaxial and abaxial trichome in Estado Bolivar (5?48'N, 61?25'W) in the Gran shields (caps) and stalks accumulated tritiated Sabana region of southeastern . Sec- leucine (fig. 19). In contrast, trichomes well tions of tissue 4-5 cm square were excised from above the tanks exhibited no uptake and, in leaf bases and blades in the field, rinsed with fact, were partially collapsed by the time col- deionized water and placed in plastic petri lections were made (fig. 20). dishes. A buffered solution (pH 5.7) containing CaCl2 and KH2PO4 (both 10-5 M) and 3H-leu- DISCUSSION cine at 10 ,uCi/ml (specific activity 17.5 mCi/ Profiles of the subfamilies. The morphology of mM) was pipetted onto a confined central area pitcairnioid and fruits varies, ranging on air-dried foliar surfaces. After 0.5 hr, treat- from fairly generalized in such genera as ment solutions were removed with several and to much more specialized in deionized water rinses. Small squares of tissue , Brocchinia, and Pitcairnia. Seeds are na- were then excised from treated areas and im- ked or appendaged. Taxa of Pitcairnioideae ex- mediately killed and fixed in FAA (formalin, ploit a wide continuum of substrata ranging acetic acid, ethanol). Two to three weeks later from relatively equable to decidedly infertile in Oberlin, tissues were dehydrated, embedded and droughty. Pitcairnioids a variety of in Paraplast, sectioned at 8-10 ,um, and mount- trichome forms. Hairs of most species are pel- ed on glass slides. Following removal of the tate and feature uniseriate stalks (figs. 11-12); paraffin and rehydration, slides and tissue were other hairs lack caps (fig. 16; Robinson 1969; coated with NTB-2 Kodak photographic emul- Tomlinson 1969). Root systems are usually well sion, exposed for 8 days, and developed. Scan- developed for absorption and anchorage. Here- ning electron micrographs were prepared us- tofore, no leaves have been found that bear ob- ing critical-point dried, gold-coated specimens vious adaptations for solute or moisture uptake and a Hitachi Model S-405A SEM operating at except for those of Brocchinia. 25 kV accelerating voltage. Specimens stored Many Bromelioideae occupy stressful habi- in FAA were washed and refixed in 2% glutar- tats, a development associated with evolution aldehyde and 1% OSO4 prior to critical-point of unusual habits and trichome specializations. drying. A voucher specimen of B. reducta (BEN Numerous bromelioid genera contain epi-

This content downloaded from 132.198.9.255 on Thu, 29 Sep 2016 15:34:40 UTC All use subject to http://about.jstor.org/terms 1985] BENZING ET AL.: BROCCHINIA 83

5 cm\

1-~~~~~~~~~~~~~~~~~DM CELL

CENTRAL DISC CELLS

WING ~ ~ ~ ~ NE

2S~~~~~~===~~~~~~~ ~~~~jT H ~OF INE

A 30 ,UM

FIGS. 1-8. Aspects of bromeliad anatomy. Stalk regions of trichomes are stippled. 1. Habit of Brocchinia reducta (BEN #101). 2. Top view of B. reducta trichome cap. 3. Cross section of B. reducta trichome stalk. 4. Radial organization of B. reducta trichome cap. 5. Xeric Tillandsia trichome cap: hydrated configuration. 6. Top view of central region of xeric Tillandsia trichome stalk. 7. Xeric Tillandsia trichome cap: dehydrated configuration. 8. Cross section of xeric Tillandsia trichome stalk.

phytes, most of which are tank formers. Their moisture and organic matter (Benzing et al. expanded, tightly overlapping leaf bases, lined 1976; Sakai and Sanford 1980). All Bromelioi- with peltate epidermal hairs that are absorptive deae possess essentially epigynous flowers and in the species examined so far, entrap abundant fleshy or leathery, indehiscent fruits.

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9 'lS0 1v0 65

11 ~~~~~100

60 3 5

12 13 5

14

50 4

15 16 17

FIGS. 9-17. Trichome structure of bromeliads and Statice pruinosa. Bars are in Am. 9. Cap of fosterianum (from Tomlinson 1969). 10. Cap of serrulata (from Robinson 1969). 11. Cap of Fosterella pendiluflora (from Tomlinson 1969). 12. Cap of argentea (from Robinson 1969). 13. Cap of Ca- topsis nutans (BEN #102). 14. Trichome of Statice pruinosa (from Liphschitz and Waisel 1982; magnification not given). 15. Cap of (BEN #103). 16. Trichome of Navia wardackii (from Robinson 1969). 17. Stalk of .

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.0

'10~~~~~~~~~~~'I

2 ,/f'5 r 2 /

~~~ 25 ~~ 10.

4 0 ~ ~ ~ ~ ~ .

FIGS. 18-23. Trichome structure of bromeliads. Bars are in Am. 18. Adaxial leaf base trichome of Brocchinia reducta: untreated control. 19. Adaxial leaf base trichome of B. reducta after treatment with 3H-leucine. 20. Collapsed adaxial B. reducta trichome. 21. Intact adaxial leaf base trichomes of B. reducta. 22. Adaxial leaf base trichome of B. reducta showing loose cuticular filaments. 23. Abaxial trichome of atmospheric (BEN #104) showing soft hinges in uplift mode.

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Tillandsioids usually root on bark or rock such as those noted when dry shields of at- rather than in soil. A majority produce tanks. mospheric tillandsioids abruptly fill with water. Peltate absorptive trichomes may densely cov- Brocchinia reducta, tank bromelioids, and mesic er the entire shoot, particularly in the case of tillandsioids provide proof that uptake func- the xeric, nonimpounding, largely rootless "at- tion in bromeliad trichomes need not be ac- mospherics"-those species most specialized for companied by expanded, elaborately sculp- moisture and mineral absorption in canopy tured, mobile, concentric shields. Shield habitats (Benzing and Renfrow 1980; figs. 5-8, mobility associated with the most advanced til- 15, 23). While bearing less advanced flowers landsioid trichomes is probably indispensable and fruits, tillandsioids feature wind-borne only if moisture and salts must be drawn ex- seeds with elaborate comas. clusively from fluids whose contact with leaf , a genus of just two tank til- surfaces is brief. landsioid species native to Venezuela and the Theories on the ecological history of Bromeli- southernmost Lesser Antilles, is of special in- aceae. Central to theories of bromeliad evo- terest to this discussion since its propagules, lution is the modification of leaves to promote like those of Brocchinia, possess hairs at both independence from soil. Pitcairnioideae has re- ends. Moreover, Glomeropitcairnia ovaries are ceived little note because most pitcairnioid taxa half-inferior while those of Brocchinia are half- are exclusively terrestrial. Pittendrigh (1948) to fully inferior. Flowers of other Tillandsioi- proposed that Bromelioideae entered the epi- deae are fully hypogynous. Additionally, tri- phytic biotope by way of a soil-based ancestor chome stalks of Glomeropitcairnia, as well as those resembling humilis Jacq., a semi-suc- of certain brocchinias, contain more super- culent species native to impoverished, season- posed cells than do those of most other pitcair- ally dry soil. This bromelioid exhibits rudi- nioids and all other tillandsioids. Stalk cell mentary impoundments in which small number can be as low as three-e.g., atmo- amounts of debris and moisture are exploited spheric Tillandsia (fig. 8; Tomlinson 1969). Re- by upward-growing roots and foliar trichomes. ductions in the number of stalk cells have been More advanced subfamily taxa owe their suc- thought to signal evolutionary advancement in cess in tree crowns to better-developed, rosu- Bromeliaceae (Harms 1930; Tomlinson 1969). late, tank shoots (e.g., , ). Pit- Trichome shield specialization. Shields of tri- tendrigh (1948) also posited a xeric, soil-rooted chomes borne by atmospherics (figs. 5-7, 15, prototype for Tillandsioideae on the grounds 23) are positioned closely enough to create a that primitive epiphytic tillandsioids were sim- confluent, light-scattering indumentum that ilar to modern atmospherics in lacking tanks; promotes water economy and provides protec- later, more mesomorphic forms emerged. Thin, tion from intense insolation in exposed, arid impounding leaves appeared, bearing fewer, habitats (Benzing et al. 1978). Movements pro- less complex (and functionally less important) moted by soft hinges, wall thickenings, and leaf blade trichomes. Pittendrigh's scheme runs subjacent sculpturings in the central shield re- counter to another proposed earlier. Schimper gion (figs. 5-7) maximize stalk cell contact with (1888) postulated a mesic, pre-epiphytic, stock passing canopy fluids. When shields are dry, that dwelt in the forest understory before gain- the central disc collapses and wings flex up- ing access to lower branches; xeric, heliophilic ward, enhancing both water retention and light came later (fig. 24). scattering (figs. 5-7; Mez 1904; Benzing et al. Pittendrigh's belief that mesmorphic, im- 1978; Benzing 1980, pp. 68-73; Benzing and pounding forms such as lingulata (L.) Pridgeon 1983). Shields of mesic tillandsioids Mez and simplex (Vell.) Beer remain ba- bearing narrower, less mobile margins (fig. 13) sically heliophilic (a fundamental tenet of his still participate in moisture and nutrient ion theory) was challenged by findings that such accumulation (Mez 1904; Benzing et al. 1976). species employ C3 carbon fixation and are ef- Some bromelioids and other pitcairnioids in ficient harvesters of weak light (Benzing and addition to Brocchinia also bear foliar hairs that Renfrow 1971a, b; Benzing and Friedman 1981; show crude radial alignments of upper cells Griffiths and Smith 1983). Values for 613C (Me- (figs. 2, 9-12; Benzing 1980). Flooding of asso- dina et al. 1977), nocturnal CO2 uptake and acid ciated leaf surfaces produces no shape changes rhythms (Coutinho 1965; McWilliams 1970;

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XERIC TILLANDSIOIDS

t

r ME S IC TI LL ANDSOID

~~INCREASING / @ EXPOSUREA i _B FIG. 24. A schema depicting three theories of tillandsioid evolution, each based on an ancestor adapted to dissimilar degrees of exposure and humidity. Schimper (1888): Common ancestor A via stippled arrows to mesic, thence to xeric, tillandsioids (perhaps via heterochrony; Tomlinson 1969; Benzing and Burt 1970). Medina (1974): Common ancestor B via broken arrows to both mesic and xeric tillandsioids. Pittendrigh (1948): Common ancestor C via solid arrows to xeric, thence to mesic, tillandsioids.

Medina 1974; Medina and Troughton 1974; mixed photosynthetic strategies (Kluge and Griffiths and Smith 1983), and leaf anatomy Ting 1978). (Ortlieb and Winkler 1977) further indicate that Pittendrigh's theory of a xeric ancestral home thin-leaved, sparsely trichomed tillandsioids for Tillandsioideae seemed to draw support operate in the C3 mode, and that more xeric, from the fact that the most primitive floral less shade-tolerant relatives with succulent anatomy is found in Tillandsia, the genus con- shoots fix much of their CO2 via CAM. The C3 taining the most xeric, heliophilic tillands- pathway is considered basic in taxa exhibiting ioids. Even if we grant that vegetative and re-

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productive systems evolved synchronously, this adults of related atmospherics. Medina theo- proposal should be subjected to intense scru- rized that these anatomical peculiarities of tank tiny. Within Tillandsia, both floral anatomy and juveniles could be explained just as well by re- degree of xerophytism vary. According to Smith capitulation of ancient xeric traits. A demon- (1934), subgenus Allardtia of Tillandsia possess- stration that seedlings of many modern tank- es the least specialized flowers in the genus. forming tillandsioids are indeed more similar However, many of its species utilize C3 pho- to atmospheric relatives than to their own later tosynthesis, and have tanks and mesomorphic growth stages in certain aspects of epidermis foliage with sparse trichome development. and habit would help resolve this question. Only two of eight taxa tested exhibited CAM Seedling physiology also should be examined (Medina 1974). Recent findings confuse the to determine whether a period of complemen- search for the primitive tillandsioid habit still tary CAM activity accompanies what appears further. The basic floral structure of subgenus to be transient xeromorphy. The neotenic ar- Allardtia also occurs among some very special- gument as applied to tillandsioid evolution is ized atmospheric populations in other subgen- most appealing if based on the premise that era of Tillandsia and may be polyphyletic (Gard- selective pressures impinging on tank seed- ner 1982). Gilmartin (1983) has concluded from lings and atmospherics are much alike, and a cladistic analysis of the entire Tillandsia/ Vrie- shared juvenile characters are adaptive for the sea complex that xerophytism arose more than same reasons in both cases. If Medina's bioge- once in Tillandsioideae. She also proposed that netic alternative is right, these traits, when these genera are basically mesic and noted that present in seedlings of tank species, would primitive members of Tillandsia subg. Phytar- either complement processes other than water rhiza are tank-forming, inhabitants and carbon balance or be vestigial-i.e., non- that can tolerate low light intensities. functional. Medina (1974) adopted a third position vis- Medina's (1974) belief that juveniles and a-vis tillandsioid evolution, largely on the basis adults of soft-leaved impounding taxa are not of photosynthetic behavior throughout the likely to differ in moisture requirement be- group and the habitat preferences of many cause they share the same mesic habitats pre- South American Pitcairnioideae. He proposed sumes that both are equally resistant to desic- that xeric and mesic lines very likely radiated cation and acquire and use water in the same into canopy habitats after diverging from a he- fashion. This is not necessarily so. Small-size liophilic C3 stock that was adapted to open sites seedlings tend to have less favorable surface- on wet soils of the sort many pitcairnioids in- to-volume ratios than have adults, thus less ca- habit today (fig. 24). He also pointed out that pacity for moisture retention. Moreover, tank exposure preferences of extant tillandsioids may tillandsioid seedlings remain tankless for sev- not reflect those of precursors. We agree, but eral years (pers. obs.); without access to im- continue to believe, as implied earlier (Benzing pounded fluids, they experience stronger and Renfrow 1971a), that analysis of the pho- drought selection than do more mature speci- tosynthetic apparatus and leaf anatomy of xe- mens. Even very brief rainless episodes must ric, heavily trichome-invested tillandsioids may challenge small plants anchored on shallow, reveal relictual qualities reflecting earlier ac- relatively non-porous bark with no auxiliary commodations to dim light and more profligate source of moisture. water use. If the early tillandsioids were tank formers Medina (1974) also questioned a suggestion whose juveniles were comparable to those of previously made by several authors (Schulz modern counterparts, they could have been an- 1930; Tomlinson 1969; Benzing and Burt 1970) cestral to xeric atmospherics. Heterochrony may that atmospheric and vrieseas are well have been the vehicle needed to exploit products of neoteny, their immediate ante- that potential, allowing primitive Tillandsioi- cedents having been native to wetter, darker deae to penetrate the drier parts of the forest habitats. Cited as evidence for heterochrony canopy where tanks cannot provide a reliable were outwardly similar qualities of trichome moisture supply. Unquestionably, absorbing density, leaf succulence, and habit between the trichomes would have facilitated this evolu- young of tank forms and the seedlings and tionary advancement. Medina (1974) made no

This content downloaded from 132.198.9.255 on Thu, 29 Sep 2016 15:34:40 UTC All use subject to http://about.jstor.org/terms 1985] BENZING ET AL.: BROCCHINIA 89 specific comments about trichome evolution. occurrence in wet forests to hundreds of mesic Pittendrigh (1948) stated that he could see no species representing every tillandsioid genus. reason why an absorbing hair would arise Thick layers of loose, white, cuticular wax (fig. where it provided no benefit (under mesic cir- 22) cover the leaves, particularly the bases, of cumstances). The answer may lie in prece- B. tatei and B. reducta, as well as those of several dents in other taxa equipped with foliar im- species in Catopsis and Tillandsia (both Tillands- poundments, and a fuller recognition that ioideae). bromeliad trichomes are involved in nutrient The B. reducta system (habitat preference, nu- as well as moisture uptake. trition, and foliar hairs) suggests that at least Evolutionary implications. The discovery that some bromeliad trichomes have acquired ab- absorbing trichomes are borne by one or more sorptive capacities in the absence of strong species in every subfamily of Bromeliaceae drought selection. Given the impoverished but mandates revision of certain concepts of bro- well-watered substrata supporting this pitcair- meliad evolution. We must now accept the pos- nioid and its numerous animal-trapping asso- sibility that the family prototype was already ciates (e.g., the South American , capable of using its shoots to obtain nutrients ), the impetus for deployment of and moisture. Examination of other vegetative tank leaves bearing absorbing hairs appears features further suggests that Tillandsioideae more closely tied to nutrient than to moisture and Pitcairnioideae (by way of Brocchinia) bear procurement. This suggestion is consistent with more resemblance to one another than either another notion: that impounding shoots arose does to Bromelioideae. So far, all bromelioids in Brocchinia to promote carnivory (McWilliams have proved to be CAM plants (McWilliams 1974). We need not look very far for compara- 1970; Medina and Troughton 1974; Bartholo- ble precedents elsewhere. Foliar impound- mew 1982; Griffiths and Smith 1983), a feature ments and associated absorptive trichomes serve consistent with Pittendrigh's view of the plants in several other families native to moist, subfamily's ancestry. A few are impounding exposed, infertile habitats (e.g., Cephalotacca- terrestrials and epiphytes adapted to deep shade ceae, Nepenthaceae, Sarraceniaceae). In many (e.g., some species of with thin, dis- cases, trap-associated hairs are glandular, pro- colorous leaves; Benzing and Friedman 1981). cessing prey as well as subsequently taking up Others without tanks are native to near-aquatic released nutrients. Similar duality has not been conditions in wet soil (e.g., several reported in a bromeliad, but Picado (1913) did spp.; E. Medina pers. comm.). Here, CAM is record digestive enzymes in the impoundment weak and appears to be relictual or at least rep- fluids of some Costa Rican tillandsioids, a dis- resents an unexpected feature in shoots that covery that requires confirmation under much otherwise are well designed to harvest filtered stricter controls. The unusual acidic character light deep in dense forests. Presumably, noc- (pH approx. 3.0) of B. reducta tank fluids (pers. turnal CO2 fixation in these taxa is a holdover obs.) also is worthy of comment: perhaps the from times when high water use efficiency was pH is lowered by adjacent leaf tissue, possibly more crucial to survival. in conjunction with uptake of certain organic Pitcairnioideae and Tillandsioideae share a solutes as part of a hydrogen ion/amino acid tank habit that is more mesic than that of Bro- co-transport system, or an acid-activated carrier melioideae. Medina et al. (1977) demonstrated complex such as that associated with glands that tank-forming, mesomorphic Brocchinia lining Dionaea muscipula traps (Rea and What- acuminata L. B. Smith, B. micrantha (Baker) Mez, ley 1983). Regardless of why B. reducta tri- B. reducta, and B. tatei L. B. Smith are all C3 chomes were originally modified for nutrient species. Tank habits and epiphytism are asso- uptake, this species certainly has access to ciated in all three subfamilies of Bromeliaceae. abundant animal tissue as a major source of or- Brocchinia acuminata is occasionally epiphytic ganic nitrogen and mineral ions. Most of the while B. tatei is commonly found in tree crowns solid matter in tanks of B. reducta consists of along the El Dorado-Santa Elena Road as one drowned (Givnish et al. 1984). ascends the Escalara to the . Broc- In view of information currently at hand, the chinia tatei is particularly noteworthy for its re- most parsimonious hypothesis for the evolu- markable similarity in leaf texture, habit, and tion of absorptive trichomes in Pitcairnioideae

This content downloaded from 132.198.9.255 on Thu, 29 Sep 2016 15:34:40 UTC All use subject to http://about.jstor.org/terms 90 SYSTEMATIC BOTANY [Volume 10 would cast the foliar hair of B. reducta as an odologies designed to reveal adaptive and eco- adjunct to the tank habit, not as a high-speed, logical aspects of its phylogeny. nutrient-garnering device tot aid a tankless ancestor gain nourishment from passing pre- ACKNOWLEDGMENTS. We wish to thank A. J. Gil- cipitation (as Pittendrigh suggested was true martin and S. Gardner for constructive criticism dur- ing the early stages of this manuscript's preparation, for Tillandsioideae). Since there is as yet no and Grady Webster and the anonymous reviewer for evidence for absorbing trichomes in non-im- helpful comments in their evaluations. This work was pounding pitcairnioids, the absorptive capacity supported by National Science Foundation Grant DEB of the Brocchinia trichome is best viewed as a 8100100. mechanism that evolved to acquire nutrients released from impounded animal prey or de- LITERATURE CITED grading vegetable debris in the fashion of ex- tant tank bromelioids and tillandsioids. Early Aso, K. 1909. Konnen Bromeliaceen durch die tillandsioids may have followed a similar adap- Schuppen der Blatter Salze aufnehmen? Flora tive sequence, or they and an equally ancient 100:447-450. BARTHOLOMEW, D. 1982. Environmental control of Brocchinia relative could have inherited com- carbon assimilation and dry matter production mon trichome qualities and habit from a single by . Pp. 278-294 in Crassulacean acid ancestor. In either instance, shield elaborations metabolism, eds. I. P. Ting and M. Gibbs. Rock- came later as tillandsioid trichomes evolved the ville, Maryland: American Society of Plant Phys- capacity to absorb moisture and solutes with- iologists. out benefit of long-term contact with tank BENZING, D. H. 1980. The biology of the bromeliads. fluids. Similar elaborations apparently have not Eureka, California: Mad River Press. developed in Pitcairnioideae. Convergence, of and K. M. BURT. 1970. Foliar permeability course, remains a plausible alternative. The among twenty species of the Bromeliaceae. Bull. bromeliad trichome design is not unique; many Torrey Bot. Club 97:269-279. and W. E. FRIEDMAN. 1981. Patterns of foliar other lineages have evolved foliar hairs capa- pigmentation in Bromeliaceae and their adaptive ble of solute exchange. At least one, the salt- significance. Selbyana 5:224-240. excreting appendage of halophytic Statice and A. PRIDGEON. 1983. Foliar trichomes of (Plumbaginaceae), is remarkably similar in Pleurothallidinae (Orchidaceae): Functional sig- structure to that of Tillandsioideae (fig. 14; nificance. Amer. J. Bot. 70:173-180. Liphschitz and Waisel 1982). Whether conver- and A. RENFROW. 1971a. The significance of gence or parallelism explains their similarities, photosynthetic efficiency to habitat preference Pitcairnioideae and Tillandsioideae appear to and phylogeny among tillandsioid bromeliads. be more closely related than previously Bot. Gaz. 132:19-30. and . 1971b. Significance of the pat- thought. terns of CO2 exchange to the ecology and phy- Brocchinia and tillandsioid genera, especially logeny of the Tillandsioideae (Bromeliaceae). Glomeropitcairnia, should be compared for evi- Bull. Torrey Bot. Club 98:322-327. dence of close evolutionary relationship, with and . 1980. The nutritional dynamics foliar hairs as a major focal point. Those borne of Tillandsia circinnata in southern and the by various pitcairnioids, particularly brocchi- origin of the "air plant" strategy. Bot. Gaz. 141: nias lacking well-developed tanks, must be 165-172. examined more closely for attributes that pro- , J. SEEMANN, and A. RENFROW. 1978. The fo- mote fitness and for similarities with compa- liar epidermis in Tillandsioideae (Bromeliaceae) rable tillandsioid appendages. Attempts to use and its role in habitat selection. Amer. J. Bot. 65: characters of major ecological import in studies 359-365. , K. HENDERSON, B. KESSEL, and J. SULAK. 1976. of bromeliad evolution should continue. Adap- The absorptive capacities of bromeliad tri- tive radiation throughout Bromeliaceae was ac- chomes. Amer. J. Bot. 63:1009-1014. companied by major changes related to prob- COUTINHO, L. M. 1965. Algumas informacoes s6bre lems of resource acquisition in diverse and often a capacidade ritmica diaria da fixaq-ao e acumu- very stressful environments. This family pro- laq5o do CO2 no escure em epifitas e erbaceas vides an unusual opportunity for functional terrestres da mata pluvial. Botanica 21:397-408. analysis as well as for more traditional meth- GARDNER, C. S. 1982. A systematic study of Tillandsia

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