Tillandsia Pollination

Tillandsia (sensu Smith and Downs 1977) contains over 500 described species according to the latest count (Luther and Sieff 1996; Chapter 13). This tally will surely grow, although not the size of Tillandsia per se if the views of several authorities prevail. Smith and Downs (1977) listed just 410 species in seven subgenera and one of these segregates, Pseudocatopsis, has already been elevated to Racinaea by Smith and Spencer (1992). Additional components (e.g., subgenus Pseudalcantarea; Beaman and Judd 1996) will likely also prove untenable as currently conceived, in this case owing to convergence on a similar chiropterophilous oral syndrome (Fig. 3.3M). The paraphyletic status of Vriesea and the affinities of several other taxa (e.g., Catopsis and Glomeropitcairnia) that stand well removed from core Tillandsioideae further underscore the need to better resolve Smith and Downs s organization of this subfamily (see Chapters 12 and 13).

Vriesea (two subgenera, >225 species) closely parallel Tillandsia in architecture, geography and ecology, with formal assignment to one or the other taxon based wholly on the presence or absence of petal scales (Fig. 3.1B). Even Smith and Downs (1977) occasionally challenge the utility of their key character (e.g., recognition that T. pabstiana = V. drepanocarpa despite the absence of scales). But whatever the taxonomic fate of Tillandsia vs. Vriesea, populations currently assigned to these two genera and perhaps several others collectively constitute one of the largest assemblages of closely related bromeliads. Moreover, parts of this clade exhibit signs of continuing, active radiation.

Plants representing many different species have been hybridized in culture, and additional combinations are spontaneous (Table 6.2). Frequent sympatry and substantial ecological equivalence, particularly among the epiphytes, further suggest evolutionary youth. Guzmania (>150 species) populate everwet forests of the Colombian Choco with about 40 described species, many sympatric and scarcely distinguishable by vegetative characteristics or substrates. Most important for our purposes,

Table 6.2. Some hybrids involving Tillandsia subgenus Tillandsia

Tillandsia brachycaulos X T. bulbosa T. brachycaulos X T. balbisiana T. brachycaulos X T. capitata T. brachycaulos X T. caput-medusae T. brachycaulos X T. ionantha T. brachycaulos X T. foliosa T. brachycaulos X T. mirabilis

T. fasciculata X T. foliosa T. fasciculataX T. lieboldiana T. 'abellata X Vriesea incurvata T. 'abellataXT. tricolor T. ionantha X T. schiedeana T. punctulata X T. krukof ana T. jalisco-monticola X T. xerographica

Source: After Gardner (1984).

better-known Tillandsia, especially subgenus Tillandsia, provide exceptional opportunity to consider the in uences of pollinators on cladogene-sis, the characteristics of owers, and the integrity of closely related populations.

Subgenus Tillandsia, a primarily Mesoamerican assemblage of >150, mostly epiphytic and often markedly drought-tolerant species, makes up the second largest (after Allardtia) of the formally recognized segregates comprising genus Tillandsia. Flowers with slender, tubular, regular to somewhat zygomorphic corollas, at most aring modestly, characterize the entire subgenus (Fig. 6.1A). Nevertheless, Gardner (1986b) was able to employ shared oral characteristics to differentiate 85 of its member species, plus a few similar taxa from Allardtia, into ve groups preparatory to more extensive study. At issue were reproductive biology and systemat-ics, and especially what appears to be an exceptionally high incidence of multivalent pollination syndromes among members of Group One.

Prominent oral bracts that enclose ower buds and young fruits, the just mentioned narrow petals rolled into a tube, well-insulated, deeply placed nectar, and exerted sexual organs suggest fundamental ornithophily for Group One and perhaps the entire subgenus. Different arrangements prevail elsewhere, especially in much smaller Group Two, which indicate other primary pollinators (Fig. 6.1A). Overall, as many architectures make up what appear to be basic oral themes for the ve groups comprising most of subgenus Tillandsia. Variations on the oral pattern expressed by

Stigma Vriesea

Figure 6.1. Aspects of owers and seeds of Bromeliaceae. (A) Flower structure characteristic of Gardner s (1986b) ve groups of species recognized mostly within Tillandsia subgenus Tillandsia. (B) Flower of Tillandsia punctata demonstrating light-colored petal tips. (C) Plication of stamen lament illustrated from left to right by Tillandsia gardneri, T. stricta and T. aequatorialis. (D) Seed morphology among species of Brocchinia.

Figure 6.1. Aspects of owers and seeds of Bromeliaceae. (A) Flower structure characteristic of Gardner s (1986b) ve groups of species recognized mostly within Tillandsia subgenus Tillandsia. (B) Flower of Tillandsia punctata demonstrating light-colored petal tips. (C) Plication of stamen lament illustrated from left to right by Tillandsia gardneri, T. stricta and T. aequatorialis. (D) Seed morphology among species of Brocchinia.

all members of Group One demonstrate continuing capacity to evolve as changing environments reorder the advantages of relying on one vs. other kinds of fauna, or so it seems.

Certain Tillandsia also demonstrate the in uence of rooting medium and plant size on breeding system and ower morphology. The most diminutive forms (e.g., T. capillaris, T. recurvata), those species that tend to colonize twigs consistent with their small stature, also often display much reduced, autogamous owers (Fig. 3.3C). These species consistently set self-seeds, sometimes by cleistogamy (T. capillaris; Gilmartin and Brown 1985), perhaps because they lack capacity to entice fauna to fertilize enough of what are already reduced numbers of ovules in miniaturized capsules. Anthers in several cases form a hood above the stigma that at once prevents outcrossing and assures fruit set (Till 1992a). Additional members of this highly neotenic subgenus produce showy owers that emit powerful perfumes (e.g., T. crocata, T. myosura).

Sel ng also occurs in subgenus Tillandsia, and most conspicuously where monocarpy rather than small size or ephemeral substrates mandates that most ovules become seeds (e.g., T. utriculata in Group Two; Fig. 6.1A). However, variations on the basic oral plan of Tillandsia subgenus Tillandsia Group One offer superior opportunity to learn about the evolution of reproductive biology because several of Gardner s Mexican subjects illustrate recent or on-going change in this system (Gardner 1982, 1986a). Sometimes geographic distributions and ecology indicate what may be related adaptation involving aspects of subjects other than their owers.

Circumstantial evidence suggests that pollinators currently isolate many co-occurring populations, and that they also fostered much speciation within oversized Group One. Tillandsia andrieuxii (lavender corolla, diurnal anthesis) and T. erubescens (chartreuse, nocturnal), for example, exhibit such close overall similarity that Mez (1934 35) considered them varieties of the second taxon. Tillandsia parryi illustrates a similar pattern with accompanying changes in ecology that indicate additional change, perhaps even cladogenesis. Epiphytes quite similar to T. parryi collected near Monterey, Mexico and described as T. sueae (Ehlers 1991), and similar plants growing south of Xilitla in San Luis Potosi State, ower just once (monocarp) and display lavender corollas that open in midmorning (Gardner 1982). However, specimens east of the city of San Luis Potosi occur as iteroparous lithophytes equipped with chartreuse petals that separate at dusk. Winter vs. summer owering further suggests dependence on different kinds of pollen carriers.

Certain members of subgenus Tillandsia attract the same kinds of polli nators using different variations on the same basic oral syndrome. Populations comprising Group One serviced by nocturnal visitors lack fragrances, whereas species elsewhere in the same taxon (Group Three), especially night- owering T. heterophylla, produce powerful perfumes. Appropriate timing and color clearly suffice for fruit set in Group One, perhaps rendering osmophores functionally redundant and an unnecessary investment. Lavender petals among certain members of Group One become more re ective, hence visible in dim light, simply by accumulating less anthocyanin (e.g., T. seleriana).

Tillandsia streptophylla uses the same basically ornithophilous syndrome (large oral bracts, exerted sexual appendages, tubular corolla, extensive nectar production) to signal crepuscular and night iers with densely lepi-dote, light pink oral bracts. Deep purple- owered T. punctulata may do the same even more subtly by displaying a lightly pigmented, exerted style with matching petal tips (Fig. 6.1B). Little impetus may exist to augment with odors or other major investments a possibly minor backup arrangement needed only to commit the few gynoecia overlooked by the diurnal pollinators (birds for T. punctata) that these species target more expensively and conspicuously (large, bright red and green oral bracts).

A widely shared feature of oral development may predispose many Tillandsia subgenus Tillandsia species to high fruit set and mixed-paternity progeny. Diurnal owers typically last about 48 h, extending access to fauna active after sundown. Similarly, owers that open during the night tend to remain turgid into the following day. Related embellishments to attract night or day iers vary with the example. Tillandsia roland-gosselinii represents one extreme by relying on a brilliant, parrot-like combination of a large, bright red scape and slick green oral bracts to promote seed set. For good measure, and normally as a prelude to lavender owers in similarly colored relatives, the entire shoot becomes scarlet. Finally, and incongruously, emerging petals add a relatively faint, pale chartreuse signal just before sunrise.

Gardners use of oral characters to segregate 85 species into ve groups revealed ecological correlates, some of which may constrain oral evolution. Most members of Group One occupy arid habitats, i.e., belong to ecological Type Five, or, if equipped with thinner leaves that impound moisture (Type Four), constitute relatively xeromorphic members of that assemblage. Soft, green, essentially glabrous foliage more consistent with conditions in everwet forests prevails through Groups Two and Three. However, most of these plants exhibit nocturnal or diurnal anthesis respectively. No comparable information exists for Groups Four or Five (only one or two species in each), nor are enough data available to speak with authority about timing for primarily ornithophilous and diurnal Group One.

Factors other than pollinators in uence the evolution of the ower, and possibly did so in Tillandsia. Aridity and extended anthesis in addition to frequent dependence on birds may explain some of the distinguishing oral characteristics shared by members of Group One. All of these plants possess distally broadened and attened stamen laments that, combined with an apically narrowed corolla, may deter all but legitimate pollinators those with long mouth parts like hummingbirds (Fig. 6.1). Alternatively, aridity, speci cally its capacity to concentrate nectar enough to impede extraction, rather than gate-keeping explains the same morphology.

Protogyny prevails in Group One as it does through most of the rest of the subgenus. Anthers fail to reach the exerted and precocious stigma except in some autogamous populations where mature organs of both types extend the same distance beyond the corolla (Fig. 6.1A). Occasionally, the two-tiered con guration lasts only a few hours as if to encourage allogamy after which elongating laments brush self-pollen against any stigma that remains receptive. Fewer than every ower favors autogamy by this mechanism in still other species (e.g., T. achyrostachys, T. concolor, T. capitata, T. matudae), perhaps to relieve plants unable to mature every potential capsule. Benzing and Davidson (1979) determined that specimens of T. paucifolia bearing the largest numbers of fruits in Florida invested exceptionally large proportions of their N and P there, enough to slow the growth of the next ramet compared with subjects with some barren owers.

Mixed oral syndromes may help account for the relatively frequent spontaneous hybridizations among some members in Group One (Table 6.2). Tillandsia punctulata, with its white-tipped, purple corolla, noctural anthesis and bird-attracting bracts, often crosses with diurnal, green- owered (prominent green laments) T. krukoffiana in the highlands north of Puebla, Mexico. However, conclusions about the importance of owers and pollinators vs. agencies more remote to this outcome are best drawn within a broader context. Intensive agriculture in Mexico and Central America beginning about 4000 5000 bp may have encouraged gene exchange among Tillandsia subgenus Tillandsia populations through the activities of pollinators that foraged more selectively in pre-agrarian habitats (Gardner 1984).

Uniform chromosome numbers indicate a minor role for polyploidy during the history of Tillandsia beyond subgenus Diaphoranthema (Chapter 9). Genetic analyses (see below) of several populations of

Mexican Tillandsia ionantha (Group One) and T. recurvata (subgenus Diaphoranthema), except for a single triallelic locus in the latter (Soltis et al. 1987), and Kress et al.s (1990) less comprehensive analysis (three enzymes) of Florida T. recurvata, T. usneoides and T. recurvata, support this hypothesis. Distributions in many instances (e.g., T. fasciculata, T. utricu-lata) across Mesoamerica into northern South America, and included ranges of numerous close, more insular relatives (see below), accord with comparative youth and recent colonizations of separated habitats.

Capacity to readily adopt different pollinators to service often self-compatible owers and oral morphology conducive to spontaneous autogamy (e.g., T. recurvata) probably assisted the exceptional radiation demonstrated by the size of Tillandsia subgenus Tillandsia. Outlying populations of several species (e.g., T. balbisiana, T. 'exuosa in Florida) regularly set self-fruit, perhaps as founders did to establish populations. Breeding systems even shift across short distances. Southernmost Florida Tillandsia balbisiana, for example, produces bright red oral bracts, whereas members of isolated outlying colonies farther north at about mid-peninsula develop little color, yet mostly ripen abundant seeds.

Floral syndromes that unambiguously target insects also characterize Tillandsia subgenus Tillandsia. Tillandsia utriculata (Group Two) initiates anthesis after dark with owers bearing large, creamy petals further distinguished by an apical twist (Fig. 6.1A). The lateral aperture exposes the style and six stamens with circular, uniformly slender laments. Anthers attach in versatile rather than basi xed fashion, supposedly to promote sphingophily (moth pollination; Vogel 1969). Self-compatibility probably describes all T. utriculata, and sometimes this bromeliad requires no assistance to reproduce. Certain populations in northeastern Mexico mature relatively low percentages of gynoecia (average 33% at seven locations; Gardner 1982,1984), while plants in Florida with similar owers, but paler bracts, set nearly every fruit. Breeding systems in these outlying populations may re ect depauperate faunas, or, again, bottlenecks effected by autogamous founders.

Like those of Group One, members of Group Three possess large primary bracts, perhaps owing to a bird-serviced ancestry. Pigmentation usually follows suit (e.g., T. imperialis, T. ponderosa, T. deppeana), but not ower structure, which better matches another group of visitors. Characteristically basi xed anthers exceed the lengths of those presented by members of the other four groups, and more pollen is produced. Diurnal anthesis and corolla shape also signal melittophily (bee pollination). Firm lavender petals curve gently or roll back to provide a credible landing site for medium-sized visitors (Fig. 6.1A).

Petals of zygomorphic- owered T. multicaulis, rather than curving downward to expose the anthers, twist apically to provide access to nectar and pollen along one side of the corolla tube much like many Pitcairnia species (Fig. 3.4K). One petal rolls down the side of the T. deppeana ower to again furnish a landing site, presumably for Hymenoptera. Tillandsia heterophylla (Group Three) alone in subgenus Tillandsia stands out for its large, leafy-green, glaucous oral bracts that presumably help guide moths to the pale, spreading corolla. A spicy, sweet fragrance complements this sphingophilous arrangement.

Gardner also attributed phalaenophily (pollination by moths) to Tillandsia tortilis and T. lepidosepala, in part because small, densely lepi-dote (light-scattering) shoots characterize both species. Imbricate oral bracts project a dull, rose-pink hue to highlight the protruding, re exed, moss-green petals surrounding the uniquely included stigma and conspicuous yellow anthers (Fig. 6.1A). Abundant pollen produced precociously indicates protandry, a second novelty for subgenus Tillandsia. A long ex-ible scape (T. tortilis), or characteristic orientation on rocky substrates for shorter-stemmed T. lepidosepala, positions owers downward.

Floral variety exceeding that present in subgenus Tillandsia occurs elsewhere in Tillandsia and the rest of Tillandsioideae. Unequivocal chiropte-rophily in at least two versions and entomophily and ornithophily, much as previously described, appear repeatedly, as do additional mixed and more exclusive syndromes for insects and birds (Fig. 3.3). Powerful fragrances, included rather than exerted sexual appendages, widely ared white, yellow and lavender corollas, small, dull bracts, and continuously green shoots characterize most of the allogamous Anoplophytum, Diaphoranthema and Phytarrhiza species also known as the fragrant tillandsias (Fig. 3.3A,F,I). Catopsis (>20 species) seems to lack capacity to produce anthocyanins, and its usually modest-sized, white to yellow owers (Fig. 3.3H) often emit pleasant fragrances during the day (e.g., C. paniculata) or night (e.g., C. nutans). Many Guzmania and Vriesea species t the ornithophilous syndrome, as does Mezobromelia (four species).

Van Sluys and Stotz (1995) provided one of the most comprehensive accounts of ornithophily involving Tillandsioideae by observing Vriesea neoglutinosa in an open habitat within the Reserva Forestal de Linhares of Espirito Santo State, Brazil. Records were kept for large and smaller clumps of plants over a ve-day interval during the approximately one-month period that local plants owered. Tubular, odorless owers subtended by red bracts opened before 06.00 hours and secreted nectar most copiously in the morning and again later in the day before the corollas with ered. Four species of birds exploited this resource, with greater attention accorded by territorial Amazilia mbriata and Polytmus guainumbi than trap-lining Chlorostilbon aureoventris and Phaethornis idaliae. Visitation peaked during the morning, but continued through the afternoon. Patches offering the fewest owers received the fewest visits (range 1 7 per day). Small compared with large patches also experienced signi cantly fewer visits per in orescence (1.33 vs. 1.79). Capsules ripened by plants in small patches contained fewer seeds than those obtained from the larger clumps (152.6 vs. 180.5). Similar values obtained by Snow and Snow (1986) for epiphytic V. incurva and V. jonghei in Atlantic Forest led them to conclude that pollen supply limited local seed production.

Utley (1983) and Vogel (1969) studied Central American thecophylloid Vriesea species (part of section Xiphion), many notable for bat-attracting, unusually large, pale, wide-mouthed owers featuring hood-like arrangements of stamens with oversized anthers (see Fig. 3.5E for a Brazilian Xiphion). Heavy nocturnal odors help advertise for pollinators, while the large green bracts primarily protect buds and developing fruits. According to Utley, derived forms (e.g., V. vietoris, V. leucophylla, V. hainesiorum) abandoned bats, adopting instead brightly colored in orescences and diurnal anthesis to utilize birds. Tubular corollas and symmetrical androe-cia further differentiate ornithophilous from chiropterophilous forms. Grant (1995a,b) erected genus Werauhia to recognize the close relationship and distinctness of these unusually large-bodied Tillandsioideae.

Vriesea of the Organ mountains of southeastern Brazil constitute another exceptionally broad radiation within Tillandsioideae far south of the ranges of most Tillandsia subgenus Tillandsia. While ornithophily prevails in this second group as well (e.g., V. carinata, V. erythrodactylon with red/orange bracts and green to yellow petals; Table 6.1), other species lure unrecorded fauna with fragrant day or night owers often subtended by green, deep carmine or dry, brown oral bracts. Mixed systems characterize several of the more ornamental species as in Mesoamerica. Vriesea philippo-coburgii bears reddish bracts and yellow day owers with pleasant aromas, suggesting versatile syndromes designed for bees and birds as in some Tillandsia (e.g., T. imperialis).

Night- owering taxa lack bright pigments, producing instead pale to dark corollas associated with odd scents never reported for Tillandsia. Flowers of Vriesea longiscapa open at dusk and emit a yeasty grease aroma; those of nocturnal V. regnellii display even larger, 3 5 cm, ared, pale corollas sprinkled with wine-red dots accompanied by another disagreeable odor. Nocturnal Vriesea unilateralis seems oddly disadvantaged if it has to compete for the same fauna given its lack of re ective bracts, a ared corolla or a strong scent.

Sazima et al. (1995) con rmed chiropterophily for six Vriesea species native to Brazil s Atlantic Forest. Flower color ranges from cream (V. gigantea), through yellow (e.g., V. sazimae), to brownish red (V bituminosa). Stiff, tubular corollas always are more than those of their bird-pollinated relatives, open at dusk and begin to collapse by midmorning (Fig. 3.5E). Anthers bend to the lower side except for V. gigantea where the display remains radial. Flowers distichously inserted on spikes or branched in o-rescences with divergent or secund orientations emit nectar tainted with garlic-like odors. Subtending bracts exhibit shades of green, with or without dark spots, to deep carmine.

All three of the species with opposite- owered spikes secrete abundant mucilage, perhaps to deter nectar thieves. Two species of long-tongued, small glossophagine bats visited one to all six of these bromeliads. Hummingbirds sometimes harvested residual nectar from withered owers after dawn. Additional vrieseas representing section Xiphion and recently resurrected Alcantarea with similar oral syndromes indicate even wider use of bats through this complex of primarily rock and bark-dwelling Tillandsioideae (Fig. 3.3J). Some larger- owered Alcantarea attract larger bats, including the stenodermatine frugivore Artibeus lituratus.

Andean Guzmania rival Mesoamerican Tillandsia and Brazilian Vriesea as subjects to investigate interesting aspects of bromeliad pollination. Ecuadorian Guzmania alcantareoides parallels certain other bat-pollinated Tillandsioideae, including Alcantarea (Fig. 3.3J) and Tillandsia subgenus Pseudalcantarea (e.g., T. viridi'ora; Fig. 3.3M; Beaman and Judd 1996). Large white owers that open at night further advertise by smelling like slightly spoiled cabbage. Stamens with outsized anthers, that along with the petals droop limply by morning, distinguish this species from homopla-sious relatives. Bat-attracting Guzmania present either smaller, widely ared, white, cream or pale green corollas with a conventionally arranged androecium (e.g., G. coriostachys, G. fosteriana) or, like G. mucronata, feature a larger, campanulate, green corolla enclosing anthers arrayed somewhat like those of thecophylloid Vriesea (Luther 1993).

Other species clearly attract other kinds of pollinators, or they defy assignments to any of the recognized categories. North Andean Guzmania wittmackii, a day- owering, close relative of G. alcantareoides, produces a brilliantly colored in orescence to catch the attention of birds, demonstrating once again the plasticity of the oral syndrome in Tillandsioideae, as does wide-ranging Guzmania monostachia (autogamous in Florida, mostly allogamous and more brightly colored beyond). Additionally, some Guzmania species exhibit combinations of oral characteristics about as incongruous as those presented by certain Tillandsia and Vriesea. For example, white owers that open around midnight and close soon after dawn accompany bright orange-rose oral bracts in Ecuadorian Guzmania kentii.

Summarizing brie y, Tillandsioideae, especially as demonstrated by the Tillandsia/Vriesea complex and Guzmania, repeatedly co-opted widely available pollen carriers that require speci c plant form and function to manipulate to set seeds. And where monocarpy, small plant size or ephemeral substrates mandate substantial fecundity, lineages sometimes abandoned pollinators entirely. However, the evolutionary pathways that link the oral syndromes remain largely unexplored. Reconstructed phylogenies would increase insights on historical events and underlying determinants, for example the extent to which past conditions of owers and in ores-cences limited options for pollen dispersal later.

At this point, nonrandom distributions of oral syndromes among related lineages suggest that the oral biology of ancestors in uenced outcomes in descendants, i.e., operated as phylogenetic constraints. Vriesea psittacina, the type species for its genus, attracts birds, as do many of what appear to be its closest relatives (e.g., V. carinata), whereas a second group of conspeci cs that includes many Vriesea section Xiphion species (now Werauhia) depend primarily on bats. Many members of a third, natural assemblage of about 15 saxicolous species former Vriesea species (genus Alcantarea) also native to southeastern Brazil mostly attract day- ying insects with large, perfumed, yellow-petaled owers (Fig. 3.3J). To what degree do these patterns re ect inherent barriers to arrangements that would promote fruit set by other kinds of pollinators?

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