BOT.GAZ. 149(1):82-91. 1988. t 1988 by The Universityof Chicago. All rightsreserved. 0006-807 1/88/490 1-0008$02 .00

MORPHOLOGICALVARIATION OF SOMEFLORAL FEATURES OF THE SUBFAMILY () AND THEIRSIGNIFICANCE IN POLLINATIONBIOLOGY

G. S. VARADARAJANAND G. K. BROWN Departmentof Botanyand MarionOwnbey Herbarium, Washington State University,Pullman, Washington 99164-4230; and Departmentof , Universityof Wyoming,Laramie, Wyoming 82071

Scanningelectron and light microscopyobservations of wet-preservedflowers of Bromeliaceaesubfamily Pitcairnioideaeyield new informationon the stigma, petal scales, and septal nectaries.Variations of the stigmatypes are evidentamong several genera. The gross structuralfeatures of the stigmado not indicate definitepollination trends, but the shape of the lobes and papillaeindicate a few specific modes. In pit- cairnioidgenera, petal scales, when functional,may aid in pollinationby accumulatingthe nectarsecreted from the ovary, thus facilitatingits availabilityto the pollinator.Nectaries associated with the gynoecia usuallydisplay tripartite channels in the ovarysepta. Some developmentalchanges of the channelstructure andposition of the ovaryindicate three probable modes of nectarrelease from the gynoeciaof the pitcair- nioids:(1) throughlateral grooves or openings,(2) partlythrough the apicalorifices and partlythrough the dissolvedareas of the spetal channels,and (3) exclusively throughthe apical orifices. Analysis of a wide rangeof floral featuresindicates that ornithophily, chiropterophily, and entomophilyexist in differentPit- cairnioideaelineages.

Introduction Gynoecia of the often contain nectaries in the ovary septa (septal nectaries) and lnvestigations on Bromeliaceae have produced are known to be of taxonomic value in several fam- descriptive and systematically useful data (BROWN ilies (DAUMANN1970; FAHN1982; THORNE1983; and GILMARTIN 1984;BROWN et al. 1984;VARA DAHLGRENet al. 1985) . BUDNOWSKIS ( 1922) ex- DARAJANand BROWN 1985;GILMARTIN and BROWN amination represents the only major study of Bro- 1985,1986;VARADARAJAN 1986a; VARADARAJAN meliaceae septal nectaries. Their morphological and GILMARTIN 1988),and because of its primitive variation and the significance in pollination were status, the subfamily Pitcairnioideae was a major not analyzed until the present work. focus (SMITH 1934;MARCHANT 1967;TOMLINSON The goal of this study is to examine the diversity 1969;BENZING 1980;GILMARTIN and BROVVN1987). of stigma morphology, petal scales, and septal nec- Mostly, the gynoecial traits of Bromeliaceae were taries of the subfamily Pitcairnioideae from wet- described, with a little information on the floral preserved material. features of the Pitcairnioideae (GARDNER 1982; UTLEY 1983;BROWN and GILMARTIN 1984;GIL Material and methods MARTIN and BROWN 1985). The 41 of nine genera of Pitcairnioideae Several floral characteristics (petal scales, nec- were examinedby light microscopy;30 species were taries) were described only from dried and rehy- also examined with scanning electron microscopy drated material, which vwas partly responsible for (SEM) (table 1). All material was field-collected the poor structural detail of floral traits. Petal scales by G. S. VARADARAJANand preserved in FAA (ligule, petal appendages, nectariferous scales, lat- (formaldehyde:acetic acid:ethanol, 1: 1: 18). Sam- eral folds, vertical calli) are relatively frequent in ples of stigmas and ovaries were selected from pre- Bromeliaceae and are diagnostic of several genera anthesis to post-anthesis, and the internal structure (MEZ 1934- 35; SMITH and DOWNS 1974, 1977, of ovaries was examined from freehand cross sec- 1979).Aside from the taxonomic value associated tions. Petal scales were examined from nearly ma- with petal scales, their morphological variation and ture (anthesis) flowers. significance in pollination were not well eluci- Floral parts selected for SEM were transferred dated. from FAA to 0.1 M cacodylate buffer, postfixed in OSO4, dehydrated through an ethanolic series (30%, 50%, 70%, 95%, 100%), dried in a Bomar Manuscript received September 1986; revised manuscript re- critical-point dryer, mounted on aluminum stubs, ceived February 1987. and gold coated with a Technics Hummer-Sputter Address for correspondence and reprints: G. S. VARADARA coater. Flower samples were then examined in an JAN,Arnold Arboretum, Harvard University, 22 Divinity Ave- ETEC Auto Scan U- 1 scanning electron micro- nue, Cambridge, Massachusetts 02138. scope at 20 kV.

82 VARADARAJAN& BROWN FLORALFEATURES OF PITCAIRNIOIDEAE 83

Results and discussion in ,Cottendorfa, and . The convolute-bladestigma, type III, previously re- FLORALFEATURES OF PITCAIRNIOIDEAE ported only from the subfamily Tillandsioideae STIGMAMORPHOLOGY. Terminology of the occursin (fig. 7). stigma types follows BROUNand GILMARTIN(1984). Stigmatypes vary within themselvesas well as The most commonly observed stigma type in the withincertain taxa; e.g., species of Brocchiniaex- subfamily is the conduplicate-spiralpattern, type II hibit types I and II (table 2). We confirmreports (f1gS. 1-6, 8-11). The simple-erect type I occurs of a modifiedconduplicate-spiral type (type II) in

,& J 7g:> t- w i58 w *

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FIGS. 1-5.-SEM of variationin stigmamorphology. Fig. 1, Ayensuauaipanensis (Varadarajan 1196). Type II stigma. Arrow indicatesasymmetric lobe of stigma.Note bulbouspapillae (BP) and spiralingrestricted to individuallobes. Figs. 2, 3, Brocchinia acuminata(Varadarajan & Oliva 1159). Two views of a type II stigma. Note tubular,branched papillae (TP). Fig. 4, brevifolia(SEL 82-558). Type II stigma at pre-anthesis.Arrows indicate highly compactstigma lobes. Fig. 5, schreiteri(Varadarajan et al. 1247). Type II stigmaduring post-anthesis. Note pollen grainstrapped within dissected lobes (DL) of stigmabranches. Compare with papillaein othertaxa. r* %l, t ( , s x

- . .S. . *: w @w

t l t

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SslisK Type II stigma at post- Dyckia ragonesei (Varadarajan1218). in stigma morphology.Fig. 6, pollen (P). Fig. 7, Navia splen- FIGS. 6-9. SEM of variation (DL) of stigmalobes with stigmaticlobes. Note dissectedareas nuda (SEL 81-1979). anthesis,displaying the loosened convoluteblades (CB); Fig. 8, 9, Type III stigma duringanthesis with papillateoutgrowths (TP). Fig. dens (Varadarajan1215). mostly the individuallobes. Tubular lobes and duringanthesis. Spiral folding involves noticeablespiral folding of individual Type II stigma Type II stigmaduring anthesis with heterophylla(Varadarajan 1171). of stigma lobes. Pitcairnia papillae(BP) are confinedto edges entirestigmatic apparatus. Bulbous ,wr};9, ;fX 0 ;. 0 0 8.;.:f f X 20'0,llmX < EEWS >E;f2X f# rl^2"tWt

VARADARAJAN& BROWN-FLORAL FEATURESOF PlTCAIRNIOIDEAE 85

FIGS.10-13. Figs. 10, 11, SEM of variation in stigma morphology in . Fig. 10, P. Iaxa (SEL 83-207). A pre-anthesis type II stigma. Arrow indicates stigma lobes that begin to undergo spiraling. Papillae absent at this stage. Fig. 11, P. harmsii (Varadarajanet al. 1245). Type II stigma with highly compacted, spirally folded lobes at anthesis. Bulbous papillae (BP) are confined to edges of stigma lobes. Figs. 12, 13, SEM of petal scales of Deuterocohnia.Note the similarity of scales within the two species. Fig. 12, D. Iongipetala(Varadarajan et al. 1244). Fig. 13, D. haumanEi(Varadarajan et al. 1250).

B. acuminata(figs. 2, 3) and of a weakly condu- of twistedor spiraledbranches, (3) durationof the plicate-spiral type in B. gilmartinii(VARADARAJAN spiralfolding, and (4) shape and symmetryof the 1986b). The stigma of B. steyermarkiiis similar to individuallobes. type I reported in B. reductaBaker (BROWNand PAPILLAE.Stigma lobes of some taxa are as- GILMARTIN1984). sociated with relatively small, simple, bulbous Variability in types I and II is evident with re- structuresknown as the papillae (fig. 11). These gard to the (1) papillae on the lobes, (2) presence are occasionally tubular (fig. 8), complex, and N.splendens L.B. Smitha ......

TABLE 1 TAXA INCLUDEDIN THESTUDY OF FLORAL FEATURES OF THE SUBFAMILY PITCAIRNIOIDEAE

Taxa Details of voucher Locality : A. uaipanensisL. B. Smitha..... Varadarajan1 196 :Bolivar, AuyanTepui Brocchinia: B. acuminataL. B. Smitha...... Varadarajan& Oliva 1159 Venezuela:Bolivar, La Escalera B. gilmartinfiVaradarajana ...... Varadarajan& Oliva 1158 Venezuela:Bolivar, La Escalera B. steyermarkiiL. B. Smitha..... Varadarajan& Oliva 1164 Venezuela:Bolivar, La GranSabana : C. guianensisK1. ex Bak.a ...... Varadarajan& Oliva 1161 Venezuela:Bolivar, Kavanayan Dezaterocohnia: D. haumaniiCastell.a...... Varadarajanet al. 1250 :Salta, Cafayate D. IongipetalaMeza ...... Varadarajanet al. 1244 Argentina:Cordoba, Sierra Chica D. schreiteriCastell.a...... Varadarajanet al. 1248 Argentina:Salta, Cafayate Dyckia: D. brevifoliaBak.a ...... SEL 82-558b D. niederleiniMeza ...... GSV 0030b Brazil D. ragoneseiCastell.a ...... Varadarajan1218 Argentina:Entre Rios Rio Parana Fosterella: F. elata Luthera...... Holotypeb E. pendulifloraL. B. Smitha..... SEL 024397b Navia. Varadarajan1215 Venezuela:Bolivar, AuyanTepui Pitcairnia: P. andreanaLindena ...... SEL 82-554b P. armataMaurya...... Varadarajan& Gaunchez 1150 Venezuela:.T.F. Amazonas, P. Auyacucho P. brevicalycinaMeza ...... Varadarajan& Ortega 1156 Venezuela:Trujillo, Bocono P. bulbosaL. B. Smitha...... Varadarajan& Guanchez 1143 Venezuela:T. F. Amazonas, P. Auyacucho P. corallinaLinden & Andre .... Varadarajan1 192 Colombia P. crassa L. B. Smith ...... Varadarajanet al. 1292 Bolivia:Nor-Yungas P. ctenophyllaL. B. Smitha..... Varadarajan1195 Venezuela:Bolivar, AuyanTepui P. heterophyllaBeera ...... Varadarajan& Oliva 1171 Venezuela:Aragua, Pittier Natl. Park P. meridensisK1. ex Meza...... Varadarajanet al. 1176 Venezuela:Merida, Paramo de Colorados P. nubigenaPlanch. & Linden . . . Varadarajanet al. 1181 Venezuela:Merida, La Carbonero P. nudaBakera ...... SEL 81-1979b Surinam P. paniculataR. & P...... Varadarajanet al. 1281 Bolivia:Nor-Yungas, Yalosa P. pruinosaH. B. K.a ...... Varadarajan& Guanchez 1147 Venezuela:T. F. Amazonas, P. Auyacucho P. pungensH. B. K...... SEL 016687b P. puniceaScheid...... SEL 80-1590b Mexico Puya: P. aristeguietaeL. B. Smitha.... Varadarajanet al. 1188 Venezuela:Tachira, Paramo de Zumbador P. atra L. B. Smith...... Varadarajanet al. 1274 Bolivia: Sud-Yungas,Unduavi P. ferrugineaL. B. Smitha...... Varadarajanet al. 1272 Bolivia: La Paz, La Florida P. floccosa E. Morr.ex Meza.... Varadarajan& Oliva 1163 Venezuela:Bolivar, La GranSabana P. harmsiiCastell.a ...... Varadarajanet al. 1245 Argentina:Tucuman, Tafi del Valle P. IaxaL. B. Smitha...... SEL 83-207b Bolivia P. Iilloi Castell...... Varadarajan1229 Argentina:Salta, E1Tala P. mirabilisL. B. Smitha...... Varadarajan1230 Argentina:Salta Rio Blanco P. pearcei Mez...... Varadarajanet al. 1286 Bolivia:Nor-Yungas, Yalosa P. stenothrysaMez...... Varadarajan& Canne 1310 Bolivia:La Paz, Sorata P. trianaeBak ...... Varadarajanet al. 1189 Venezuela:Tachira, Paramo de Zumbador P. tristisL. B. Smitha...... Varadarajan& Canne 1306 Bolivia: Cochabamba,Tiraque

NoTE.-Voucherspecimens in LAB, LAP, MO, PORT, SEL, US, VEN, and WS. a Taxaprocessed for SEM. b Taxa cultivatedat the Selby BotanicalGardens, Florida. AyensuaBrewcariaDyckiaNavia ...... 1 III3... II 1(flabelliform (Ib)(I,II II ) [III?]C)

VARADARAJAN& BROWN FLORALFEATURES OF PITCAIRNIOIDEAE 87

TABLE 2 tions of several Pitcairnia and Puya species (Pit- TAXONOMICDISTRIBUTION OFTHE STIGMA TYPES cairnia pulverulenta R. & P., P. schultzei Harms, INTHE SUBFAMILY PITCAIRNIOIDEAE Puya hofstenii Mez). Petal scales generally occur at the bases of petals (figs. 12-22) and may have NO. species originated from simple vertical folds along the in- Genera examined Stigma type(s)a terior face of the petal (e.g., Puya floccosa; fig. 14). Petal scales may be a pair of earlike lobes (fig. 15) flanking the base of the filaments near petal Brocchinia ...... 3 I (ICd), II (IICd) margins. More often, petal scales are solitary, ob- Cottendorfia ...... 1 I long, and tongue-shaped with variable sizes, as in Deuterocohnia ...... 3 II (IIC) several species of Pitcairnia (fig. 16). Occasion- ally, petal scales develop crenations (figs. 17, 18) ...... (IIC) Fosterella ...... 2 I (IC) or lacerations (figs. 12, 13) or complex distal mod- ...... (ISCIIC) ifications (figs. 20-22).

Pitcairnia ...... 15 II (IICd) Puya ...... 12 II (IIC) ...... (IIb)

NOTE. Stigma types are unknown for Abromeitiella and . Stigma types indicated in parentheses include other reports.

a Definition according to BROWNand GILMARTIN(1984). From SMITH( 1984) . c From MEZ(1934-1935). From BROWNand GILMARTIN(1984). 'vX (#;l}@ branched(figs. 2, 3). Papillae are distinguishedfrom 17. the dissected or laceratedportions of the stigma (fig. 20.L, S) and are not discernible until anthesis (fig. 10). 14.tS O.5 cm At post-anthesis, the papillae are characterized by 1 m m a moist, sticky surface entangled with pollen. COMPACTIONOF THESTIGMA BRANCHES De- scribing the degree of compaction of stigma lobes is very subjectiveas it depends on the size and shape of the individual lobes. Two general types of com- paction of the lobes are characterized during an- thesis. In the first type, the individual lobes are 1; Wn 154 18. 1; conduplicately folded (figs. 1, 8) with little or no l spiraling of the whole stigmatic apparatus. In the I cm I cm 21.1; second type, conduplication of the lobes is highly compact and involves the lobes as well as the en- lmm tire stigma unit in the spiral folding (fig. 11). DURATIONOF THE SPIRAL FOLDING. Compaction and spiral folding of the lobes begin prior to an- thesis (figs. 1, 9, 1 1), are completed during stigma receptivity, and are relaxed at post-anthesis (figs. 5, 6). Because of these structural changes during 16. / 22g development, one must exercise caution in inter- | j I c m _ m preting stigma morphology. I cm 1 m SHAPE AND SYMMETRYOF THE INDIVIDUAL FIGS. 14-22. Diagrams illustrating the variable morphol- LOBES. Stigma branches may be ovate (fig. 3), ogy of petal scales. Figs. 17 and 20-22 are reproduced from lanceolate, spathulate (fig. 9), or sagittate (fig. 6), SMITHand DOWNS( 1974), with permission (copyright 1974, The New York Botanical Garden). Fig. 14, Puya floccosa and in some stigmas, one of the lobes is asym- (Varadarajan& Oliva 1163). Petal scales represented as ver- metric because of a slight extension of one limb tical folds (arrows) on the interior of petals. Figs. 15-22, Di- (fig. 1). versity of petal scales in Pitcairnia.Fig. 15, P. brevicalycina PETALSCALES. Petal scales are diagnostic for (Varadarajan& Ortega 1156); fig. 16, P. crassa (Varadarajan et al. 1292); fig. 17, P. caricifolia;fig. 18, P. meridensis Abromeitiella,, and Deuterocohnia. Yet, (Varadarajanet al. 1176); fig. 19, P. nubigena(Varadarajan they show a high degree of instability in occur- et al. 1181);fig. 20, P. heterophylla;fig. 21, P. pungens;fig. rence, especially among the species and popula- 22, P. filispina. 88 BOTANICALGAZETTE [MARCH

SEPTALNECTARIES. The septal nectaries of Bromeliaceae correspond to the "labrynthinecom- mon nectarial cavity" type sensu SCHMID(1985). Architecture of the septal nectaries varies in su- perior and inferior ovaries (BUDNOWSKI1922). Pit- cairnioid flowers are uniquely suited for examining this variation as the ovaries range from fully su- perior to completely inferior. Septal nectaries of pitcairnioids usually consist of three longitudinal systems of channels in the septa that are connected I mm with the axis by a median component (figs. 24, 23. 26). The channels originate at the ovary base and open through orifices at the top. The orifices are small slits or rounded pores (BUDNOWSKI1922). Triradiatechannels sometimes extend to the style and exhibit vertical folds and twists, appearing as convolutions, branches, and undulations in some corosssections (fig. 25). The surface of the septal nectaries is lined by variable amounts of glandular tissue. Glandulartissue and the contents of the se- cretion of Pitcairnioideae may correspond to those of some Liliaceous members (FAHN1949, 1952; FAHNand BENOUAICHE1979). Our observations of the septal nectaries from representatives of Pitcairnioideae with superior, semi-inferior, and inferior ovaries confirm some structuralvariations reported by BUDNOWSKI(1922), I mm e.g., the number of nectariferous channels, ori- 24. fices. In taxa with superior ovaries (Deuterocohnia schreiteri,Dyckia ragonesei, and Fosterellaelata), six nectariferous channels are discernible radially during the very early stages of flower develop- ment. Three channels oriented toward the septa probably constitute the primary nectariferous sys- tem. The remainder, oriented toward the placenta, may be the secondarynectariferous system (fig. 24). The latter channels are discernible only in the ova- ries of pre-anthesis flowers. In some superior ova- t S N ries (Naviasplendens, Cottendorfa guianensis) and semi-inferior to inferior ovaries (Pitcairniahetero- phylla, Puya harmsii, fig. 27), the nectaries in- 0.2 5 mm clude only the septal channels in all developmental 25. stages examined. FIGS.23-25.-Cross sections of septal nectaries (SN) from The number, orientation, persistence of the nec- pre-anthesis flowers. Fig. 23, Puyafloccosa (Varadarajan & tariferouschannels, and ovary position indicate three Oliva 1163), example of a superior ovary. G = grooves. Fig. modes of nectar release from the ovary. In superior 24, Puya harmsEi(Varadarajan et al. 1245), semi-inferior ovary. Arrows indicate likely additional nectariferous channels (AC). ovaries with six radial channels or three septal Note the thick receptaculartissue (R). Fig. 25, Navia splendens channels (fig. 27), nectar release to the exterior by (Varadarajan1215) with convoluted channels of septal nectar- the dissolution of the septal channels seems likely. es. The ovary surface is mostly grooved, and the sep- tal channels break open at the grooves (figs. 23, 28). Guided by the grooves, nectar flows from the transferredinto the locule via the placentaltissue septal channels to the ovary base, where it finally and (2) throughthe dissolved areas of the septal accumulates. channels(fig. 28). From the locule, nectarflows Placental channels lose their morphological throughthe apical orifices of the ovary. The dis- identity at anthesis as they become integrated with solutionof the septal channelscauses the individ- the placental tissue. Although the actual route of ual carpelsto partfrom one another,leading to a nectar flow from these channels is not well under- superficialapocarpy (fig. 28). stood, it appears that their secretions are partly (1) Nectar release from the semi-inferior/inferior g.e - Ow . w r e ;- ' 4 .;sr v>4 .* 2 l .ts l wt-- i

VARADARAJAN& BROWN FLORALFEATURES OF PITCAIRNIOIDEAE 89 19881

*' '} te; ',,' \ .' jh ovaries is slightly different from the above ac- count. Completeepigyny results from the recep- taculartissue overgrowingthe ovary, beyond the -,'i Ai..*. _. ,,;v , ^.... level of origin of the gynoecium (ESAU 1977). Sometimes,the relativeposition of the inferiorovary is furthercomplicated by the developmentof an epigynous tube (e.g., Ayensua). All the pitcair- nioid inferiorovaries investigatedhave only three septal channels. Unlike the superiorovaries, the receptaculartissue peripheralto the ovarywall and b Ws R .t b , > jo S -- o ; e - X sometimesthe epigynoustube of an inferiorovary Mi, -ยข>...,(:J..,.'.;,^. i 200'"m'.l are conceivablythe mainbarrier to the nectarflow to the exterior.The only remainingoutlet for the nectarof these semi-inferioror inferiorovaries is, therefore,the apicalorifices. Persistence of the septal channelsduring the post-anthesisstages of the in- feriorovaries provides evidence for the above ex- planation.

FLORALMORPHOLOGY AND OBSERVATIONS ONTHE POLLINATION BIOLOGY TypeII stigmaof Pitcairnioideaevaries so widely that more than a single pollinationsystem seems probable. The highly compact, conduplicately folded,spathulate stigma lobes (fig. 11 ) with dense papillaeare frequentin relativelylarge (often 6 cm long), tubular,scarlet to red, zygomorphicflowers of Pitcairniawith abundantnectar (P. corallina, P. meridensis,P. nubigena). These features, in combinationwith a fairly compacttype II stigma, diurnalanthesis, tubular and/or reflexed flowers, hardflower wall, stiff filaments, and stylar base stronglyindicate bird pollination (PROCTOR and YEO 1972). Type II stigmawith semicompactlobes with or withoutpapillae (fig. 1) also occursin large, night blooming,white, tubularblossoms. These actino- morphicflowers occasionally produce strong odors at night and are aggregatedon massive, terminal inflorescencesconspicuously demarcated from the surroundingfoliage (Ayensuauaipanensis, Puya aristeguietae).These features indicate bat polli- nation(PROCTOR and YEO 1972). Type I or type II stigmas with ovate to lanceo- late, somewhatloosely folded stigmalobes lacking papillae(fig. S) are characteristicof several rela- tively small (often S cm long), diurnal,white, yel- low, green, actinomorphicflowers with moderate amountsof nectar.These flowers are mostly pro- duced on lax, panicledinflorescences (B. steyer- FIGS.26-28. SEM of cross sections of ovariesdisplaying markii,C. guianensis,Deuterocohnia longEpetala, detailsof septal nectaries.Fig. 26, (SEL 83-207). Septalnectaries with a medianchannel (M) and three septal D. schreiteri,F. elata, Pitcairnia brevicalycina) channels(SC), a typicalpre-anthesis structure in most superior and may indicateinsect pollination(PROCTOR and ovaries. Fig. 27, Pitcairnia ctenophylla (Varadarajan1195). YEO 1972). Septalchannels (SC) are evidentas semi-inferior/inferiorovary The degree of compactionof the lobes and pa- matures.R = receptaculartissue. Fig. 28, Puya tristis (Var- adarajan& Canne1306). Septalnectaries with superiorovary pillae may be morereliable in indicatinga specific duringanthesis. Note the dissolvedareas of the channelslead- pollinationtype thanthe gross morphologicaltype ing to superficialapocarpy. D = undissolvedchannel. of stigma,especially when consideredin conjunc- 9o BOTANICALGAZE l l E [MARCH tion with the , blooming times, flower sible differences in modes of nectar release from color, and symmetry. well-developed nectariferous system(s), evident in Petal scales and septal nectaries provide some varying ovary positions, associated with a wide indirect clues as to the nectar production, storage, range of zygomorprhic, tubular, colored flowers and release associated with some pollination types. (Pitcairnia and Puya) are apparently linked to bird MCWILLIAMS(1974) suggested that petal scales may or bat pollination (VARADARAJAN1986a, 1987). help in keeping the nectar in suitable position within MCWILLIAMS( 1974) listed the studies dealing the floral tube for the pollinator. However, our ob- with hummingbirdpollination of bromeliads. READ servations suggest that, while some petal scales are (1969) documentedhummingbird pollination in one apparently "nectariferous," others are vestigial. Pitcairnia species and SNOWand SNOW(1980) in Pitcairniabrevicalycina has yellow flowers with another. REESand ROE (1980) discussed the nu- or without petal scales (fig. 15). Three populations tritional relationships between birds and Puya. In of this species examined in Venezuela displayed a addition, there are several instances in Pitcairnioi- simple type of petal scales (fig. 14), accumulating deae where the strategies for entomophily and chi- little nectar. In contrast, P. heterophylla,a taxon ropterophily are evident. In Abromeitiella, Broc- widely known from several areas of tropical Amer- chinia, Cottendorfia, Deuterocohnia, Dyckia, ica, had scarlet-red flowers with petal scales (fig. Fosterella, and a few other genera, insect polli- 20) and abundant nectar. Although the amount of nation may be widespread. Within Pitcairnia and nectar was determined by crude methods, it is ap- Puya, however, a wide range of floral features parentthat modes of pollination differed in the two (massive, cylindrical , reflexed species. The former, with a relatively simple type flowers, zygomorphy, epigyny, carination of se- of petal scales and low amounts of nectar, may be pals) strongly indicates a variety of pollination a bee flower; the latter, with a petal scale with mechanisms. These are perhaps significant in the complex distal modifications and abundantnectar, adaptive radiation of Pitcairnia and Puya exten- may be a moth flower. While petal scales could sively in . possibly assist in accumulating nectar in P. hete- rophylla,they may be simply vestigial in P. brevi- Acknowledgments calycina(VARADARAJAN 1987). Complexity of petal scale morphology does not We thank Drs. A. J. GILMARTIN,J. H. LARSEN, necessarily provide reliable indications for nectar JR., and two anonymous reviewers for their con- storagecapacity. Even a pair of simple vertical folds structive criticisms of earlier drafts of the manu- on petals of some P. floccosa populations (fig. 14) script; and C. BILOS,J. CANNE,J. CRISCI,C. CRIS- may be nectariferous,although they apparentlylack TOBAL,D. DIAZ,T. F. DI FULVIO,J. DUGARTE,F. any glandular linings. Other floral structures may GUANCHEZ,A. HUNZIKER,H. LUTHER,G. MOR- substitutefor petal scales for storing the nectar. This ILLO,R. NEUMANN,L. NOVARA,F. OLIVA,F. OR- is indicatedby the coherent, swollen filament bases TEGA,A. SCHININI,J. SOLOMON,B. STERGIOS,J. of Dyckiathat possibly function as a nectar storage STEYERMARK,and F. VERVOORSTfor their help and site in the absence of petal scales. assistance during fieldwork. We thank USHAVAR- Septal and placental nectaries of Bromeliaceae, ADARAJANand LINDAKIBLER for typing the manu- examined by BUDNOWSKI(1922) primarily from a script and C. DAVITTfor technical assistance with taxonomic viewpoint, were not elucidated from the SEM. A National Science Foundation Doctoral perspective of pollination. Septal nectaries consti- Dissertation Improvement Grant (BSR-8306999) tute the internal secretory and storage system of supported G. S. VARADARAJANs field research. nectar especially significant to the bromeliad blos- Partial supports for the work were obtained from a soms adapted to entomophily, ornithophily, and National Science Foundation grant (BSR-8407573) chiropterophily (MEEUSE1961; FAEGRIand VAN and a Washington State University graduate school DERPIJL 1971; PROCTORand YEO 1972). The pos- research fellowship.

LITERATURECITED

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