American Journal of Botany 88(2): 185–195. 2001.

FLORAL DEVELOPMENT IN ()1

ANDERS S. BARFOD AND NATALIE W. UHL2

Department of Systematic Botany, Aarhus University, Nordlandsvej 68, DK-8240 Risskov, Denmark; and L. H. Bailey Hortorium, 467 Mann Library, Cornell University, Ithaca, New York 14853 USA

The organogenesis of staminate flower clusters and flowers and some observations on the corresponding pistillate structures of Aphandra natalia are described and compared with those of the other two genera in the Phytelephantoideae (Arecaceae). In Aphandra, staminate flowers are borne in monopodial clusters of mostly four (1–6) flowers. Each flower is surrounded by two pairs of subopposite bracteoles and has two rather indistinctly four-parted whorls of perianth parts. Stamen primordia arise on a shallow apical dome and then centrifugally down the sides of a long, angled, and laterally flattened receptacle. Immediately before the staminate bud opens, the floral receptacle below the androecium rapidly elongates, becoming funnel-shaped, with the bracteoles and a perianth sheath adnate to it forming a pseudopedicel. Epidermal and subepidermal layers of these pseudopedicels split at anthesis and release a great number of raphide idioblasts that resemble the pollen grains in shape and size. It is hypothesized that the idioblasts deter pollen feeding or ovidepositing insects. The phylogenetic implications of these findings are important within the Phytelephantoideae and among palms in general.

Key words: Arecaceae; Aphandra natalia; floral development; monotocotyledons; palms; Phytelephantoideae; pollination; pseu- dopedicel.

Aphandra natalia (Balslev and Henderson) Barfod is a pin- ficult to obtain since large valuable trees must be felled to get a series. Inflo- nate leaved, single-stemmed palm found in Amazonian Ec- rescence stages were obtained from three individuals growing in semi-culti- uador and near the foothills of the . The vated populations near Logron˜o, Province of Morona-Santiago in , the belongs to the subfamily Phytelephantoideae, which includes type locality of Aphandra natalia. The young inflorescences (Figs. 1–4) (Ta- only three small genera and constitutes a morphologically iso- ble 2) were fixed in FAA (formalin-acetic acid-alcohol) in the field and after lated group of dioecious genera within the Palmae (Uhl and 2 d, transferred to storage in nine parts 70% glycerine alcohol to one part Dransfield, 1987). Developmental studies have shown that the 10% glycerine. Prophylls and peduncular bracts (PD bracts) were cut open to phytelephantoid genera have the only monopodial flower clus- facilitate infiltration. ters in the family, a four-parted perianth otherwise known only in only one species of Chelyocarpus (Coryphoideae), and cen- Scanning electron microscopy—The various pistillate and staminate de- trifugal stamen inception. Partial centrifugal stamen develop- velopmental stages were critical point dried in a Biorad CPD-750 Apparatus, ment is known to occur elsewhere only in the genus Eugeis- mounted on stubs with double-adhesive tape, and coated with platinum in an sona (Calamoideae) (Uhl and Moore, 1977; Uhl and Drans- Edwards S150B Sputter Coater. They were studied with a JEOL 840 Scanning Microscope at 20 kV. field, 1984). Balslev and Henderson (1987) originally referred Aphandra natalia to based on the prominent submarginal Clearings—Material for study of vasculature was cleared using a 5% so- lution of NaOH and left overnight in an oven at 50ЊC. After 24 h the NaOH veins on the pinnae and the pedicellate condition of the sta- was changed and we repeated the procedure until clearing was satisfactory. minate flower clusters. Monographic work on the subfamily The material was then rinsed in distilled water and treated with commercial Phytelephantoideae has shown that it is a distinct genus (Bar- bleach to remove any cloudiness. Subsequently preparations were stored in fod, Henderson, and Balslev, 1987; Barfod, 1991) (Table 1) glycerine alcohol. The material was stained in a basic fuchsin solution (1 g and that the structure of the floral pedicel is critical. Devel- of fuchsin and 6 g of solid KOH in 100 mL water) for photographing. opmental studies of the inflorescence and flowers of Aphandra are important for eludication of the pedicel and for comparison RESULTS with developmental patterns previously described for the other genera of Phytelephantoideae (Uhl and Moore, 1977; Uhl and Inflorescence structure—In wild populations of Aphandra Dransfield, 1984). In this study we address three issues in par- natalia the distribution of staminate and pistillate individuals ticular: ontogeny of the staminate flower cluster, stamen in- is almost even. Flowering occurs throughout the year, peaking ception, and the structure of the pedicel of the staminate flow- slightly in February–March (Barfod, 1991). Inflorescences er. Some observations are also presented on the development form in acropetal sequence in the axils of their subtending of the pistillate flower clusters and flowers. . All leaves produced during periods of flowering sub- tend a young inflorescence bud. The pistillate and staminate MATERIALS AND METHODS buds have a similar overall appearance while they are still included in the sheaths of the subtending leaves, but they de- material—Aphandra is exploited for fibers extracted from the velop differently after the peduncular bract (PD bract) breaks bases (Borgtoft Pedersen and Balslev, 1990); developmental material is dif- through the prophyll (Figs. 1–7). In the staminate bud, the PD bract continues to grow and before it splits will attain more 1 Manuscript received 21 December, 1999; revision accepted 27 April 2000. The authors thank Anni Sloth for assistance with laboratory work, SEM, than twice the size of the prophyll. At anthesis the entire in- and electronic processing of the photographs; and the reviewers. Support is florescence is exposed and pendant. The pistillate bud, in con- acknowledged from NSF grant BSR-8806042 to NWU. trast, elongates only a little after the splitting of the prophyll, 2 Author for correspondence (e-mail: [email protected]). the PD bract reaching only about three-quarters the length of 185 186 AMERICAN JOURNAL OF BOTANY [Vol. 88

TABLE 1. Diagnostic table.

Ammandra decasperma Aphrandra natalia macrocarpa Phytelephas aequatorialis Pistillate inflorescence No. of flowers per inflorescence 6–10 30–50 5–25 15–25 No. of sepaloid bracts 0? 4–6 4–6 4–6 No. of perianth segments 7–10 7–9 5–8 6–9 No. of carpels 6–9 6–8 4–5 5–6

Staminate inflorescence Length of rachis 30–60 100–170 30–60 90–150 Axis of flower cluster at anthes- present indistinguishable indistinguishable indistinguishable isa No. of flowers per cluster b 6–9 4 (Ϫ5) 4 (Ϫ5) 4 (Ϫ5) Pedicel pseudopedicel?c pseudopedicelc indistinguishable pedicel Distribution of idioblasts concentrated in even even even blisters Idioblast released at anthesis yes yes no no No. of sepaloid bracts 0? 4 4 4 No. of perianth segments 8? 8 8 8 Shape of male receptacle at an- elongated, recurved elongated, dome flat to dome shaped widened, flat thesis shaped Stamen inception centrifugal? centrifugal, sequential centrifugal, sequential centrifugal, in 2 phases No. of stamens 300–500 400–650 150–300 500–700 Length of filament at anthesis 0.1–0.2 2.5–3 3–9 6–10 Length of anthers at anthesis 0.5 3–3.5 4–6.5 3–5 Pistillode ϩ/Ϫ present absent absent absent Size and shape of pollen grain 45–55, rounded 60–70, elliptic 55–65, elliptic to 80, elongate elongate Pollen grain aperture monoporate monosulcate monosulcate monosulcate a The individual pseudopedicels or pedicels of the flowers of Aphandra natalia and Phytelephas aequatorialis are fused, thus forming a pseudo- axis. b Aberrant number in parentheses. c Pseudopedicel formed by fusion and elongation of the perianth and the receptacle (see text). the prophyll. The rachis of the pistillate inflorescence is much comes adpressed to the rachis with the posterior flower partly shorter, and the flowers remain closely bunched. At anthesis, hidden (Fig. 19A). they are partly contained in the PD bract, which splits longi- tudinally along the abaxial side to expose only the tips of long Organogenesis of staminate flower clusters and flowers— strap-shaped perianth parts and stigma branches (Fig. 19C). In the earliest developmental stages available to us, the flower cluster sites are covered by their subtending bracts. Removal Structure of the staminate flower cluster—The staminate of the bract exposes a lentil-shaped apical dome in each flower inflorescence of Aphandra natalia breaks through the PD bract cluster (Fig. 16). The two bracts that subtend the lateral flow- in the evening and finishes development overnight. Elongation ers (Fig. 16: A, B) are clearly discernible (ba and bb), whereas proceeds at up to 10 cm/h until the rachis has attained a length the subtending bracts of the posterior and anterior flowers, of 100–170 cm at anthesis the following day. The staminate respectively, are not visible in distal view. The apices of the flowers are gathered in 200–300 spirally arranged and densely four flowers are flattened to slightly dome-shaped (Fig. 17: A, inserted clusters (Figs. 6, 19A). The individual clusters have B, and D). In distal outline, they appear three- to four-lobed mostly four (1–6) flowers. Lower, stalklike parts of the flowers because of primordial bulges (Fig. 18, 19D). On the lateral are united to varying degrees and taper proximally to a com- flowers, a pair of subopposite bracteoles develops first, slightly mon attachment (Figs. 8, 19A). The basal clusters have fewer displaced relative to the plane of symmetry (Figs. 16, 19: 1b, flowers, usually two or three, and a number of solitary flowers 2b, 1a, 2a). The posterior member of this pair is usually visible are always present at the apex of the inflorescence. Each clus- before the anterior one. On the posterior flower of the cluster, ter is subtended by a bract that differs in shape and size from the first-formed pair of subopposite bracteoles can be distin- deltoid and is ϳ3 cm long at the base of the rachis to a narrow, guished in lateral positions (Fig. 16: 1c, 2c). The anterior floral few millimetre wide rim near the apex. primordium is partly hidden under the basal part of the bract The flower cluster usually consists of two pairs of subop- that subtends the entire flower cluster. posite flowers (Fig. 8). Rarely, one or two more flowers de- Each floral apex produces an additional pair of subopposite velop distal to these. The lower pair of flowers are in lateral bracteoles, perpendicular to the first formed ones (Fig. 19D). positions and the upper two flowers are smaller and in anterior In Fig. 15 (3a, 3b), a bracteole is formed at a latero-posterior and posterior postions. The receptacle of the anterior flower is position, and the opposite one in a latero-anterior position (4a, narrower than those of the lateral ones (Fig. 8), and the pos- 4b). The former appears first and attains a larger size than any terior flower never attains the size of the others. All flowers of the remaining bracts. Later in ontogeny, the two pairs of are sessile (Figs. 6, 7) until late in ontogeny when a curved subopposite bracteoles are adnate to the receptacle as it be- stalk develops, and the cluster bends over and ultimately be- comes elongate. Their presence in the mature flower is ob- February 2001] BARFOD AND UHL—FLORAL DEVELOPMENT IN APHANDRA 187

Figs. 1–2. Young pistillate inflorescences of Aphandra natalia still contained inside the prophyll and peduncular bract. 1. Stage VII (see Table 2). Prophyll removed. Note the emarginate peduncular bract. The inflorescence axis is revealed through a ‘‘window’’ cut on the abaxial face of the peduncular bract. Some of the anterior sterile bracts below the rachis have been removed in this preparation. 2. Stage IV (see Table 2). Prophyll and peduncular bract removed. Note the large lateral sterile bracts. The long stigmatic branches (darker) are more than twice as long as the perianth segments (lighter) in this stage. Figure Abbreviations: SB ϭ bract subtending flower cluster; ba, bb, bc, bd ϭ bracts subtending flowers; A ϭ apex of first formed flower; B ϭ apex of second formed flower; C ϭ apex of posterior flower (third in formation); D ϭ apex of anterior flower (fourth in formation); the order of formation of the subopposite bracteoles are indicated by numbers, e.g., 1a, 2a, 3a, 4a; the direction of the hypothesized twist of the of the apical dome due to spatial constraint is indicated by arrows. scured because only the apices are free and they are displaced The occurrence of a pistillode is variable. Andrew Hender- to positions immediately below the perianth (Fig. 25). son et al. collected in 1990, staminate material from a popu- The perianth is initiated in two alternating, more or less lation of Aphandra natalia in Acre, Brazil (Henderson et al. four-merous whorls. The primordia of the first whorl appear 1657 [NY, AAU, BH]). The material made available to us was as bulges between the bracteoles (Fig. 15). Members of the sampled from a bud immediately before the splitting of the second whorl appear almost simultaneously, but slightly above PD bract. close to the base of the rachis all had large the first whorl and opposite the bracteoles. As the flower in- pistillodes visible to the unaided eye, consisting of rudimen- creases in size, the presence of two whorls is obscured. In the tary carpels extended apically in long slender stigmatic mature flower there is a variable number of long, deltoid peri- branches. In some of the young stages of the inflorescences anth segments, and sepals and petals are indistinguishable collected at Logron˜o, solitary flowers near the apex produce (Fig. 19C). After the origin of the perianth members, the floral hairy processes up to 1 cm long arising from the middle of receptacle increases in height (Fig. 21). Inner perianth seg- the receptacle. These, however, appear to be staminodial in ments are closely appressed. When the apex is ϳ650 ␮m in origin. diameter, the first stamens arise in an incomplete ring around Late in staminate organogenesis, after stamen inception has the central part of the apical dome (Fig. 21). Stamen primordia stopped but immediately before splitting of the PD bract, the are initially round but become irregularly angled by close ap- lower part of the floral receptacle, sheathed in adnate and con- pression as they enlarge. The sides of the expanding apical nate perianth bases, undergoes zonal growth to form a stalk dome are indented and flattened by the appressed perianth seg- that we have designated as a pseudopedicel. At maturity the ments (Fig. 21). Subsequent stamen primordia arise in irreg- epidermis and one or more subepidermal layers of the pseu- ular groups along these edges (Fig. 22), in more or less cen- dopedicel become split and the surface acquires a fuzzy ap- trifugal order, with those primordia that are covered by peri- pearance due to a covering of broken cells (Figs. 11, 12). anth parts often arising and enlarging later than more exposed Raphide-containing idioblasts very similar to the pollen grains ones. in shape and size are released from the split layers in great 188 AMERICAN JOURNAL OF BOTANY [Vol. 88

TABLE 2. Measurements of developmental stages of the pistillate and inflorescence bud differs from its staminate homologue by staminate inflorescences of Aphandra natalia. having an emarginate apex (Figs. 1, 5). The rachis of the in- florescence resembles the staminate but bears only ϳ20 soli- Length of pro- Length of PDa Distance between Length of phyll (cm) bract (cm) (mm) rachis (mm) tary, spirally arranged, pistillate flowers, each in the axil of a Pistillate series bract. It is noteworthy that two subopposite pairs of bracteoles Stage IX 5.5 3 5 2 are present below each flower. In fully developed flowers, the Stage VIII 12 3 8 5 bracteoles can be distinguished from the perianth segments by Stage VII 25 4 10 5 being smaller and less fleshy. In Fig. 1, the youngest stage Stage VI 29 5 15 6 available, the subtending bract, four bracteoles, and the peri- Stage V 31 5.5 19 7 anth of the pistillate flowers are already elongate. The central Stage IV 35 6.3 20 7 Stage III 35 8.5 20 9 whitish bulges in individual flowers are the multicarpellate gy- Stage II 39 10.5 25 10 noecia. The flowers in stage number VII of our collection have Staminate series I free carpel primordia that are conduplicate. The carpel pri- Stage VIII 3 1.8 10 10 mordia are present before the initiation of the staminodes, Stage VII 6.5 4.5 18 20 which first appear as a single series of primordia surrounding Stage VI 23 14 35 30 the gynoecium, a second whorl eventually forming on the out- Stage V 32 8 55 40 Stage IV 36 10 50 45 side. Stage III 36 12 50 60 The development of the pistillate perianth is irregular. Our Stage II 36 15 52 80 collections did not comprise the earliest stages of perianth in- Stage I cut 24 80 155 ception, but the sizes and insertion of the segments suggest Staminate series II that more than one whorl is involved. Whereas the first-formed 40 61 92 360 segments are uniform in shape and in size, additional segments 42 62 105 370 usually form on the abaxial side of the flower. This phenom- a PD ϭ peduncular bract. enon, possibly related to asymmetrical expansion of the apex, was also observed in R. and P. (Bar- fod, 1991). numbers. They remain trapped in the epidermal shreds on the Early in organogenesis, the apices of the carpels elongate. surface where they mix with pollen grains at anthesis (Figs. The resulting stigmatic branches become longer than the peri- 12, 13). anth segments as can be determined from the material shown When the inflorescence breaks through the peduncular bract, in Figs. 1 and 2. The stylar portion of the gynoecium elongates 400–650 stamens have been produced. A narrow zone of the continuously until anthesis when the stigmatic branches are floral receptacle above the perianth and below the stamen- surrounded by the apices of the long perianth segments. At bearing part remains naked (Figs. 9, 12). this time the style length ranges between 20 and 25 cm and the stigmatic branches are 4–5 cm long (Fig. 19C). Vascular anatomy—The large number of collateral bundles supplying each flower varies with the size and developmental DISCUSSION stage. As the floral apex expands longitudinally and in diam- eter the bundles curve towards the periphery and anastomose This study confirms that in staminate flowers of Aphandra, frequently (Fig. 10). two pairs of sepaloid bracteoles develop before the perianth on each floral apex (Barfod, 1991), that the floral apex expands Pistillate inflorescence and flowers: structure and in width and height during stamen development, and that sta- development—Stages of pistillate organs were incomplete but men development is for the most part centrifugal (Uhl and some observations were possible. The PD bract of the pistillate Moore, 1977). The stalk of the staminate flower was deter-

Figs. 3–4. Developmental stages of staminate and pistillate inflorescences of Aphandra natalia enclosed by the prophyll and the peduncular bract. The Roman numerals indicate the consecutive order in which the buds were removed from the crown. They are referred to in Table 2 and throughout the text. 3. Staminate series (from left to right, stages I–VII). Besides the stages shown here two additional stages were collected for study: one immediately before splitting of the PD bract, and one immediately before anthesis. 4. Pistillate series (from left to right, stages I–IX). February 2001] BARFOD AND UHL—FLORAL DEVELOPMENT IN APHANDRA 189

Figs. 5–9. Developmental stages of the staminate inflorescence of Aphandra natalia. 5. Stage VI. The prophyll and peduncular bract have both been split open along their flattened rims. Note that the prophyll is much larger than the peduncular bract. The latter is pointed and not notched like its pistillate homologue in Fig. 1. 6. Stage III. Note the sessile flower clusters. At this stage the pseudopedicels have not formed. The two large lateral sterile bracts at the base are homologous to similar bracts found in the pistillate inflorescence (Fig. 2). 7. Stage VI. Rachis showing the two sterile lateral bracts at the base and the black tips of the bracts subtending the flower clusters. 8. Monopodial cluster of four flowers. The stamens have been removed to reveal the uneven size and shape of the receptacles. 9. Adaxial side of a fully developed lateral flower of a cluster. Note the irregular borderline between the perianth fused to the receptacle and the naked peripheral zone of the apical dome. Raphide idioblasts are visible on the pseudopedicel stalk as tiny luminescent spots. 190 AMERICAN JOURNAL OF BOTANY [Vol. 88

Figs. 10–13. Preparations of the staminate flowers of Aphandra natalia at anthesis. 10. Section of cleared flower stained to show the vascular bundles. 11. SEM preparation showing the borderline between the naked, glabrous peripheral zone of the apical dome (upper half of picture) and split superficial layers of the pseudopedicel covered by masses of pollen grains and raphide idioblasts. 12. Detail of Fig. 11 showing the surface of pseudopedicel. Note the mixture of pollen grains and raphide idioblasts almost indistinguishable in shape and size. 13. LM preparation of the pollen grains and raphide idioblasts scraped from the surface of the psudopedicel. February 2001] BARFOD AND UHL—FLORAL DEVELOPMENT IN APHANDRA 191

Figs. 14–18. Staminate inflorescence of Aphandra natalia. Development of the flower cluster. 14. Stage VII. Part of an inflorescence rachis with flower clusters in different stages. Numbers indicate the ontogenetic sequence from 1 (youngest cluster) to 12 (oldest cluster). 15. Stage VII. Cluster number 10 in Fig. 14. The perianth primordia (asterisks) are visible. 16. Stage VIII. 17. Stage VII. Cluster number 1 in Fig. 14. Latero-distal view. 18. Stage VII. Detail showing cluster number 1 in Fig 14. Distal view. 192 AMERICAN JOURNAL OF BOTANY [Vol. 88

Staminate flower cluster—Uhl and Dransfield (1984) sug- gested that in Phytelephas aequatorialis (syn. Palandra ae- quatorialis), the four bract-like appendages surrounding the perianth in the pistillate flowers are homologous to the four bracts that subtend the flowers of the staminate cluster and termed them ‘‘bracteoles.’’ Aphandra differs from P. aequa- torialis in that four bract-like appendages are also present be- low the perianth on each staminate flower. Barfod (1991) re- ferred to these as sepaloid bracts. The four first-formed brac- teoles on each staminate floral axis and the four bracteoles, or sepaloid bracts, of the pistillate flower are homologous. Thus, the homology is between the pistillate flower and a single flower of the staminate cluster. The extra bracteoles might sug- gest a more branched staminate flower cluster in Aphandra.

Stamen inception—In multistaminate palms, floral recep- tacles expand to accommodate more stamens, the shape of the receptacle and pattern of origin of primordia varying in dif- ferent groups (Uhl and Moore, 1980). The three genera of phytelephantoid palms are distinguished by bizarre differences in receptacle shape during stamen initiation. Floral develop- ment of two species of Phytelephas has been studied. In Phy- telephas aequatorialis the staminate flowers are pedicellate from early in organogenesis; the pedicels are true stalks, not pseudopedicels as in Aphandra. When the first stamen pri- mordia originate, the receptacle in P. aequatorialis is ϳ800 ␮m in diameter and relatively flat. Stamen inception occurs rapidly in two phases. During a first phase, the entire apex becomes covered by primordia except for a marginal meriste- matic area. Although the primordia surrounding the center are larger, Uhl and Moore (1977) did not observe any apices with a single ring of primordia. In the second phase, the stamen primordia develop in centrifugal order in radial rows along the meristematic periphery and thereby increase the size of the apex. At this stage, a pistillode was observed in some flowers. Five to seven hundred stamens are usually produced in each staminate flower. In Phytelephas macrocarpa, the staminate clusters and flow- ers are sessile, the flowers remaining sessile throughout de- velopment. At the time of inception of the first stamens, the receptacle is ϳ550 ␮m wide and slightly curved with a raised Fig. 19. (A) Part of a mature staminate inflorescence showing four-merous apex. Two types of meristem are active, either simultanously flower clusters; each flower with numerous stamens. (B) A young staminate or in succession. One produces a limited number of stamen flower dissected from an unopened bud; note the sterile bracts and perianth primordia at early stages of stamen inception, apparently in a segments surrounding the closely appressed stamen primordia, and the large proximal bract which subtends the flower cluster. (C) A pistillate flower at centripetal pattern (Uhl and Moore, 1977). The remaining sta- anthesis showing strap-shaped sepaloid bracteoles at the base, the staminodes, mens are produced in a centrifugal sequence by the peripheral long perianth segments, and sinuous stigmatic branches. (D) Diagram of sta- meristem, which is active throughout organogenesis. Pistillo- minate flower cluster of Aphandra natalia to show the approximate configu- des were not observed. The number of stamens formed in each ration of bracts and bracteoles. Note the slightly displaced position of the staminate flower varies from 150 to 300. bracteoles of the lateral flowers, probably due to spatial constraint in the In species of Phytelephas and in Aphandra the receptacles developing floral apices. are shallow domes in early ontogenetic stages. The receptacle expands in diameter but only slightly in height in both species mined to be structurally unique and designated as a pseudo- of Phytelephas. In Aphandra natalia, however, the receptacle pedicel, which consists of an enlarged, more or less funnel- also elongates, becoming somewhat funnel-shaped, with sta- shaped floral receptacle with an adnate perianth tube. The men primordia originating centrifugally along the angled and small tips of the perianth members are free distally. The epi- flattened sides, often partly under the perianth segments. At dermis and one or more underlying layers of the pseudopedicel anthesis a naked zone remains between the level of insertion contain large raphide idioblasts, resembling the pollen grains of perianth segments and the stamen-bearing part of the re- in shape. The raphides are freed by disintegration of the epi- ceptacle. Our evidence is not conclusive as to whether there dermal cells and become mixed with pollen grains on the sur- is a short centripetal phase previous to centrifugal stamen in- face of the pseudopedicel at anthesis. Comparison with other ception in Aphandra. In some apices studied one to six pri- genera of the Phytelephantoideae and further consideration of mordia may develop later in the center of the flower as sug- these findings are given below. gested by the presence of inner bulges. They do not differ from February 2001] BARFOD AND UHL—FLORAL DEVELOPMENT IN APHANDRA 193

Figs. 20–25. Staminate inflorescence. Stamen inception and development. 20. Stage VII. Floral apex of a lateral member of a flower cluster. The perianth segments are irregular in size and shape and indistinguishable from the bracteoles. The apex is covered by stamen primordia except for a naked center. Note that some of the inner primordia seem to develop later than the adjacent outer ones. 21. Stage VII. Floral apex with the perianth segments removed. Note the impressions left by these in the apex and stamen primordia arising in irregular groups along their edges. 22. Stage VII. Floral apex with some of the perianth segments removed, and stamen primordia differing in size and shape. Some stamen primordia are in the process of splitting as indicated by white arrows. 23. Stage VII. Close-up showing the naked center of the floral apex. 24. Stage VI. Distal view of the rachis showing details of adjacent four-flowered clusters. Note the irregular perianth segments. 25. Stage IV. A flower cluster in lateral view (anterior flower to the left, lateral flower to the right). The pseudopedicel of the lateral flower is partly developed at this stage; bracteoles are indicated by white arrows. 194 AMERICAN JOURNAL OF BOTANY [Vol. 88 the surrounding stamen primordia in shape, only in size. The where similar carpel primordia become fused laterally later in bulges observed could represent the carpel primordia, but that development, the ventral sutures remaining open throughout remains to be demonstrated. A similar developmental pattern (Uhl and Dransfield, 1984). The presence of two pairs of se- was considered partial centrifugal development in Phytelephas paloid bracts below the perianth has been noted. Two indistinct macrocarpa (Uhl and Moore, 1977, fig. 18). four-parted perianth whorls are followed by a ring of condu- In the third genus, Ammandra, the receptacle at anthesis is plicate carpel primordia. In P. aequatorialis carpels became irregularly chunky and becomes expanded basally to cover the laterally connate, but ventral sutures remain open and the sin- perianth apices on the abaxial side of the flower. The stamen gle ovule of each carpel is initiated directly on the floral axis, filaments are much shorter, and the anthers are smaller than in in a position that might be considered axillary to the carpel. the other phytelephantoid genera (Barfod, 1991). Button- At maturity the gynoecium of all phytelephantoid genera has shaped pistillodes, inserted in shallow depressions and usually a central, cone-shaped receptacle, histologically distinguished caducous at anthesis, are almost universally present. Anatom- by large parenchyma cells and scattered tannins. Similar gyn- ical sections of the fully developed flowers show that most of oecial structure is found elsewhere in the family only in the the major trunk bundles extend to about three-fourths the genera of the Calamoideae, where the receptacle is different height of the flower and then curve toward the periphery and in shape and histology. extend downward (Uhl and Moore, 1977), suggesting centrif- Staminodes in Aphandra originate in two whorls, the first ugal initiation. No other observations of stamen inception have whorl next to the carpel primorida and a second outside the been made. Up to 1200 stamens have been recorded in A. first. Uhl and Moore (1977) demonstrated the same kind of dasyneura (Burret) Barfod (Barfod, 1991), the highest number centrifugal staminodial inception in the pistillate flowers of in the family. Phytelephas aequatorialis.

The pseudopedicel—Floral stalks or pedicels vary among Pollination—Several studies have been undertaken on the the phytelephantoid genera. Both sessile and pedicellate flow- pollination of phytelephantoid palms. Barfod, Henderson, and ers occur in Phytelephas. The stalked condition of the stami- Balslev (1987) and Barfod (1991) studied Phytelephas macro- nate flower cluster was used to separate the genus Palandra carpa ssp. tenuicaulis Barfod in Amazonian Ecuador and con- from Phytelephas (Cook, 1927), but the character was found cluded that several insect groups mediate pollen transfer. It is variable among the species of Phytelephas, and Palandra has noteworthy that beetles of the families Staphylinidae, Nituli- since been placed in synonomy (Barfod, 1991). It is notewor- dae, and Curculionidae were all ovipositing in the staminate thy that in Phytelephas tumacana Cook, the clusters in the inflorescence. At the time of anthesis, they had perforated the middle and proximal part of the inflorescence are composed receptacle completely. Bernal and Ervik (1996) described the of four (rarely five) flowers that are sessile to subsessile, floral biology and pollination of Phytelephas seemannii Cook whereas a number of solitary flowers are always present at the in . Pollination is mostly carried out by species of apex with pedicels up to 7 mm long (Barfod, 1991). In other pollen-eating and predating staphylinids. One particular spe- species of Phytelephas, as in P. macrocarpa, all flowers are cies of the genus Amazoncharis reproduces in the male inflo- sessile. Here also Ammandra differs in having stalked stami- rescences by constructing egg chambers in the fleshy recep- nate flowers borne in clusters of up to nine on a 1.5–3 cm tacles of the flowers. This reproductive behavior resembles long branch. The floral stalk appears to be a short branch, but that of beetles in the closely related subtribe Gyrophaenina that this requires confirmation by developmental and anatomical feed on the spores and reproduce in fleshy mushrooms. studies. Aphandra natalia is pollinated mainly by Baridinae (Cole- In Aphandra the pseudopedicel is a special structure, an optera) that feed on pollen and, in contrast to the situation in elongate floral receptacle with an adnate and connate perianth other phytelephantoid species, prefer the pistillate rather than tube. Several characters appear associated with the pedicellate staminate inflorescence for oviposition (Ervik, 1992). The condition. The rapid expansion of the pseudopedicel may help pseudopedicel may play a key role in the interaction with the generate the pressure that is needed for the flower-bearing tis- visiting insects. The raphide idioblasts that are released from sues to break through the PD bract. Secondly, such rapid in- the hypodermal layers in great numbers could be detrimental crease in size may contribute to the heating of the bud above to the larvae. Their similarity in size and shape to the pollen ambient temperature during pollination. Thirdly, the epidermis grains are striking (Figs. 12, 13). A simple bio-assay could be disintegrates releasing raphide idioblasts at the same time as designed to demonstrate whether the pollinating insects are pollen grains are shed, and the idioblasts and pollen intermin- able to distinguish between the two. gle, covering the surface of the pseudopedicel. In Ammandra Ervik, Tollsten, and Knudsen (in press) have analyzed the raphide idioblasts are also found in great numbers, not scat- floral scent of Ammandra decasperma, A. dasyneura, Aphan- tered in subepidermal layers as in Aphandra, but inside blister- dra natalia, Phytelephas aequatorialis, P. macrocarpa ssp. like structures that occur scattered on the pedicel and the re- tenuicaulis and P. seemannii. Their results show that the major ceptacle as well. The blisters rupture at anthesis to release the constituents of the floral scents of the three genera are of com- idioblasts. As in Aphandra the idioblasts resemble the rounded pletely different biochemical origin. The floral scent of Aphan- pollen grains in size and shape. Such idioblasts may help to dra is unusual in being dominated by a pyrazine. The presence deter pollen feeding and perforation of pedicels and recepta- of this compound could explain the absence in Aphandra na- cles for ovipositing. talia of Derelomini and Mystrops that are common visitors in all Phytelephas species studied as well as in many other palm Pistillate flower clusters and flowers—Except for the num- and cyclanth species (Henderson, 1986; Gottsberger, 1991; Er- ber of flowers in the inflorescence (see Table 1), structure and iksson, 1994). development of the pistillate flower clusters and flowers in Aphrandra are like those found for Phytelephas aequatorialis Phylogenetic implications—Cladistic analyses based on February 2001] BARFOD AND UHL—FLORAL DEVELOPMENT IN APHANDRA 195 morphology and restriction site fragments found the Phytele- al., 1995) has clearly demonstrated that these groups are only phantoideae monophyletic (Barfod, 1991; Uhl et al., 1995). remotely related to each other. The respective pollination syn- The group is strongly supported by a number of synapomor- dromes of the cyclanthoid genus Cardulovica and the phyt- phies, although some of the characters are found elsewhere elephantoid genera are very similar. Both groups are beetle throughout the family, such as the multicarpellate condition pollinated, and they share the following features: nocturnal (some species of Attalea), attached to an extension of flowering, color, scent and temperature elevation (Barfod and the receptacle (Eugeissona), floral buds open (e.g., Ceroxylon), Henderson, 1987; Barfod, 1991; Gottsberger, 1991; Eriksson, and the breaking up of the mesocarp into corky processes 1994). Their similarities appear to represent a striking example (e.g., Manicaria, Pelagodoxa, Sommiera, and Johanneste- of convergent evolution in response to uniform selection pres- ijsmannia). sures in similar habitats. Barfod (1991) used morphological data to infer relation- LITERATURE CITED ships among genera of the Phytelephantoideae. An outgroup was assembled representing the major evolutionary lineages BALSLEV, H., AND A. HENDERSON. 1987. A new Ammandra (Palmae) from within the palms according to Uhl and Dransfield (1987). Flo- Ecuador. Systematic Botany 12: 501–504. BARFOD, A. S. 1991. A monographic study of the subfamily Phytelephan- ral characters were emphasized by weighting procedures. The toideae. Opera Botanica 104: 1–76. result was ambiguous due to lack of a likely sister group, but ———, A. HENDERSON, AND H. BALSLEV. 1987. A note on the pollination the cladogram favored had Aphandra and Phytelephas as a of Phytelephas microcarpa (Palmae). Biotropica 19: 191–192. clade with Ammandra as sister group. One problem of weight- BERNAL, R., AND F. ERVIK. 1996. Floral biology of the dioecious palm Phy- ing in favor of floral characters is that these are often the result telephas seemannii in Colombia: an adaptation to staphylinid beetles. of coevolutionary relationships and therefore do not necces- Biotropica 28: 682–696. BORGTOFT PEDERSEN, H., AND H. BALSLEV. 1990. Ecuadorean palms for sarily reflect phylogeny. The findings of this study further cor- agroforestry. AAU reports 23: 1–122. robate an Aphandra–Phytelephas clade. The early, sessile on- CHASE, M. W., D. W. STEVENSON, P. WILKIN, AND P. J. RUDALL. 1995. togenetical stages of the staminate flowers of Aphandra na- Monocot Systematics: a combined analysis. In P. J. Rudall et al. [eds.], talia are very similar to similar stages in Phytelephas macro- : systematics and evolution, 685–730. Royal Botanic carpa. This similarity applies to number of flowers per cluster, Gardens, Kew, Richmond, Surrey, UK. COOK, O. F. 1927. New genera and species of Ivory Palms from Colombia, stamen inception, length of the flower-bearing axis, and shape Ecuador and Peru. Journal of the Washington Academy of Sciences 17: and vasculature of the receptacle. Subsequent development, 218–230. however, is very different. DAHLGREN, R., H. T. CLIFFORD, AND P. F. YEO. 1985. The families of the This study further supports the circumscription of Aphandra monocotyledons: structure, evolution, and . Springer Verlag, based on several characters of the staminate flower, in partic- Berlin, Germany. ular the presence of four sepaloid bracteoles, the shape of the DAVIS, J. I. 1995. A phylogenetic structure for the monocotyledons, as in- ferred from chloroplast dna restriction site variation and a comparison floral receptacle, and a structurally unique pseudopedicel. Sta- of measures of clade support. Systematic Botany 20: 503–527. men number, and the morphology and number of pistillate ERIKSSON, R. 1994. The remarkable weevil pollination of the neotropical flowers per inflorescence, are also different (Table 1). Cardulovicoideae (Cyclanthaceae). Plant Systematics and Evolution 189: The relationship of the phytelephantoid genera to other 75–81. palms is not yet clear. Some trees (Uhl et al., 1995) based on ERVIK, F. 1992. Notes on the phenology and pollination of the dioecious palms Mauritia flexuosa (Calamoideae) and Aphandra natalia (Phytele- morphological and molecular characters resolved the Ceroxy- phantoideae) in Ecuador. In W. Barthlott et al. [eds.], Animal-plant in- leae as a sister group. A chloroplast DNA (cpDNA) restriction teractions in tropical environments, 7–12. Zoologisches Forschungsinsti- fragment analysis that compares representatives of the three tut und Museum Alexander Koenig, Bonn, Germany. phytelephantoid genera with a joint outgroup of 12 taxa is ERVIK, F., L. TOLLSTEN, AND J. T. KNUDSEN. In press. Floral scent chemistry currently underway to further seek a likely sister group. Sev- and pollination ecology in phytelephantoid palms (Arecaceae). Plant Sys- eral of the gene trees generated using simple parsimony and tematics and Evolution. GOTTSBERGER, G. 1991. Pollination of some species of the Carludovicoideae, Nypa as a functional outgroup have Ceroxylon as sister group. and remarks on the origin and evolution of the Cyclanthaceae. Botanis- Tribe Ceroxyleae in the ceroxyloid palms has a Gondwanic che Jahrbu¨cher fu¨r Systematik 113: 221–235. distribution pattern with representatives in the Juan Fernandes HENDERSON, A. 1986. A review of pollination studies in the Palmae. Botan- Islands, northern , Madagascar, and Australia. ical Review 52: 221–259. UHL, N. W., AND J. DRANSFIELD. 1984. Development of the inflorescence, In general the group is less specialized than the Phytelephan- androecium, and gynoecium with reference to palms. In R. A. White and toideae, but further research is necessary to establish this re- W. C. Dickison [eds.], Contemporary problems in plant anatomy, 397– lationship. The Phytelephantoideae is of primary importance 449. Academic Press, New York, New York, USA. in understanding evolutionary trends within the palm family. ———, AND H. E. MOORE, JR. 1977. Centrifugal stamen initiation in phy- The superficial resemblance of inflorescences and flowers with telephantoid palms. American Journal of Botany 64: 1152–1161. ———, AND ———. 1980. Androecial development in six polyandrous gen- certain cyclanthaceous groups such as Cardulovica is note- era representing five major groups of palms. Annals of Botany, London worthy. The phytelephantoid palms share with members of this 45: 57–75. genus, strong floral dimorphy, monopodial flower clusters, ———, AND ———. 1987. Genera Palmarum. L.H. Bailey Hortorium and pseudopedicels, a multistaminate condition, four-merous floral International Palm Society. Allen Press, Lawrence, Kansas, USA. whorls, spicate inflorescences, and lack of vessels in the stem ———, J. I. DAVIS, M. A. LUCKOW, K. S. HANSEN, AND J. J. DOYLE. 1995. Phylogenetic relationships among palms: cladistic analyses of morpho- (Dahlgren, Clifford, and Yeo, 1985). There are, however, nu- logical and chloroplast DNA restriction site variation. In P. J. Rudall et merous differences, and comparative analysis of restriction al. [eds.], Monocotyledons: systematics and evolution, 623–661. Royal fragments (Davis, 1995) as well as DNA sequences (Chase et Botanic Gardens, Kew, Richmond, Surrey, UK.