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We thank BRAAM VAN WYK and ToNYABBOTT for their kind help during the visit of A. B. to South Africa and the Splinter-Legat for financial support of this tfip.
Pl. Syst. Evol. 215:141-155 (1999)

--Plant Systernatics and Evolution © Springer-Verlag 1999 Printed in Austria

Androecial development and systematics in F l a c o u r t i a c e a e s. 1. ALEX BERNHARD and PETER K. ENDRESS

Received July 25, 1997; in revised version January 30, 1998 Key words: Flacourtiaceae, Kiggelariaceae, Violales, Linales. - Androecial development, polyandrous flowers. Abstraet: Androecial development of 13 species belonging to six tribes of Flacourtiaceae has been investigated. While in Scolopieae and Flacourtieae the stamens develop centrifugally, in Erythrospermeae, Oncobeae and Pangieae they are initiated in a centripetal sequence or a sequence that is neither distinctly centripetal nor centrifugal. The distribution of these developrnental patterns coincides with the distribution of other characters (e.g. cyanogenic compounds, salicoid leaf teeth) and therefore supports a split of the family into Flacourtiaceae s. str. (containing the Scolopieae, Homalieae, Prockieae, Flacourtieae, Casearieae and Bembicieae) and Kiggelariaceae (with Erythrospermeae, Oncobeae and Pangieae) and is in accordance with results of recent rbcL studies.

The pantropical Flacourtiaceae (in the circumscription of LEM~ 1988) comprises ten tribes with approximately 80 genera and 880 species, many of which have numerous stamens. The family seems to be a heterogeneous group of more or less homogeneous tribes (MmLER 1975, LEMI~ 1988). The family is placed at the base of the Violales by different authors (TAKHTAJAN1980, 1997; CRONQU~Sr1981, 1988; THO~E 1992), whereas it appears in the Linalean-clade in CnASE & al. (1993). The Flacourtiaceae are widely recognized as being of major phylogenetic importance with relations to many other taxa such as Salicaceae GOLYSHEVA1975, HICKEY & WOLVE 1975, MEEUSE 1975, HUBER 1991, CHASE ~ al. 1996, TAKI~XAJAN 1997), Violaceae (MELCttIOR 1964, CRONQUIST 1981), Passifloraceae (DE WILDE 1974, CRONQU~ST1981, HUBER1991, TAKHTAJAN1997), Euphorbiaceae (HVTCHnSSON 1967), Elaeocarpaceae (KEAT~G 1973, MILLER 1975, CRONQUIST 1981, HUBER 1991, TAKHTAJAN1997) and Tiliaceae (HUTCHINSON1967). Despite its orten cited prominent phylogenetic position, structural aspects of the family have received little attention until recently. Studies include pollen structure (ERDTMAYN 1952, KEATIN~ 1973), xylem anatomy (MILLER 1975) and cyanogenic glycosides (SPENCER~ SEIGLER 1985). The most recent comprehensive taxonomic treatment of the Flacourtiaceae (LEMKE 1988) is based on gross

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morphology and on results of the works mentioned above. A phylogenetic analysis based on rbcL sequences of representative genera of most of the tribes suggests that the family splits into three major clades (CHASE & al. 1996). This finding coincides with the distribution of salicoid leaf teeth (HICKEY& WOLFE 1975, NANDI & al. 1998), cyanogenic glycosides and vessel element anatomy (CHASE & al. 1996). The only studies concerning androecium development in Flacourtiaceae by ENDRESS & VOSER (1975) and RONSE DECRAENE& SMETS (1992) include only one and four species respectively. VAN HEEL (1977) reports the direction of stamen initiation for Oncoba spinosa. In accordance to the position of the Flacourtiaceae in the order Violales, the sequence of statuen initiation is described as centrifugal (VAN HEEL 1977, CRONQUIST 1981, RONSE DECRAENE & SMETS 1992) or neither distinctly centrifugal nor centripetal (ENDRESS& VOSER 1974). The systematic significance of a centrifugal as opposed to a centripetal sequence of stamen initiation in angiosperms was emphasized by CORNER (1946). CRONQUIST (1957) discussed this pattern as characteristic for larger systematic units. Since then the assessment of the significance of developmental characters, especially the mode and sequence of statuen initiation has become more difficult, because different studies have shown that the direction of stamen initiation does not necessarily characterize larger taxa. MAYR (1969) and LErNS (1988) reported that the Lythraceae are centrifugal in contrast to the centripetal Myrtaceae in the same order Myrtales (CONTI & al. 1996). Loasaceae (LEnsS & WINHARD 1973, HUFFORD 1990) and Hamamelidaceae (ENDRESS1976) each show both sequences in different genera. Although the developmental sequence may show variability at different taxonomic levels, it is predominantly stable in larger groups with polyandrous flowers. Therefore this character remains useful in systematics if it is not considered in isolation. The aim of the present study is (1) to contribute more developmental data to the knowledge of the Flacourtiaceae, (2) to compare these data with the intrafamilial distribution of other characters and (3) with the most recent phylogenetic hypotheses based on rbcL studies. Materials

and methods

The flowers were fixed in FAA and then stored in 70% ethanol. For SEM micrographs the specimens were dehydrated through an acetone seiles, critical-point dried and sputtered with gold. The following taxa were investigated (tribes after LEM~ 1988): Erythrospermeae: Camptostylus mannii (OLIv.) GILG,SCHöNENBERGER10, Cameroon. C. ovaIis (OLw.) CHIPP,SCHöNENBERaER52, Cameroon. Oncobeae: Lindackeria dentata (OLIV.)GinG, ENDRESS97--25, Ivory Coast. - Caloncoba echinata (OLIv.) GILG, ENDRESS 1139, cult. Honduras. - C. gIauca (P. BEAUV.) GILa, SCHöNENBERGER49, Cameroon. Pangieae: Kiggelaria africana L., BERNHARD110, South Africa. Scolopieae: Pseudoscolopia polyantha GING, BERN•AaO 107, South Africa. Phyllobotryon soyauxianum BAmL., SCHöNENBEaaZR121, Cameroon. Flacourtieae: Flacourtia indica (BuRM. F.) MERR., ENDRESS 3025, India. - Idesia polycarpa MAXIM.,BERNHARD112, Botanical Garden of the University of Zurich (BGZ). -

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Poliothyrsis sinensis OLIV., BERNHARD 111, BGZ. - Xylosma congesta (Lour.) MERR., B~RNHARD115, BGZ.

Casearieae: Casearia silvana SCnLTR.,ENDRESS6019, New Caledonia.

Results

Camptostylus mannii (Erythrospermeae). In Camptostylus mannii bisexual and male flowers occur. The flowers have a diameter of c. 4 c m at anthesis. The perianth consists of three sepals, the formation of which leads to a triangular floral pilmordium, and seven to ten petals. The petals are arranged in two seiles. An outer seiles of three and an inner seiles of six to seven petals. The increase in organ number in the inner seiles of petals results by double or triple positions in each sector (see ENDRESS 1996). The term "dédoublement" is avoided here because of its developmental connotation. The approximately 190 stamens are irregularly arranged on the slightly convex receptacle. The gynoecium is unilocular with four to five parietal placentae. Statuen initiation begins at the periphery of a low ring meilstem and continues in centripetal direction to the centre (Fig. 1A-C). Camptostylus ovalis (Erythrospermeae). In Camptostylus ovalis bisexual and male flowers occur. The male flowers have a diameter of c. 2.5 cm at anthesis. The calyx consists of three sepals. As in C. mannii, the floral pilmordium becomes triangular in outline by the formation of the calyx. The corolla consists of ten petals in two seiles, an outer seiles of three and an inner seiles of seven petals. The inner seiles shows double and triple positions as in C. mannii. The approximately 50 stamens are irregularly arranged on the flat receptacle. In male flowers the gynoecium is lacking. Androecial initiation begins at the periphery of the receptacle and proceeds in centripetal direction to its centre (Fig. 1D-F). Lindackeria dentata (Oncobeae). The flowers of Lindackeria dentata are commonly bisexual. They have a diameter of c. 2.5 cm at anthesis. The perianth consists of three sepals and six to ten petals. The increase in organ number may be interpreted as a double or triple position in different sectors of the inner petal whorl. The c. 30 stamens are arranged in three irregular seiles. The gynoecium has three to four carpels with parietal placentation. Statuen initiation begins at the periphery of the receptacle and proceeds in centilpetal direction to the floral center (Fig. 2A-D). Caloncoba echinata (Oncobeae). In Caloncoba echinata bisexual and male flowers occur. The flowers have a diameter of c. 2-3 cm at anthesis. The perianth consists of a calyx with three sepals and a corolla with seven to eight petals in two seiles, an outer seiles consisting of three and an inner seiles consisting of four to five organs. As in the investigated species of Camptostylus, the increase in organ number results by double position in one or two sectors. The approximately 100 stamens are in about three irregular seiles. The number of stamens increases from ten to fifteen in the innermost to about 25 in the outermost series. The gynoecium has three to four carpels with parietal placentation. It is rudimentary in male flowers.

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Fig. 1. Floral buds showing different stages of androecial development. A-C Camptostylus mannii; A, B sepals removed, C sepals and petals removed, the androecium shows slight imprints of the petals. D-F Camptostylus ovalis, sepals removed. Bars: A-C 150 gin, D-F 100 gm

Initiation of the stamens takes place on a flat ring meristem. The first initiated primordia at the periphery of the receptacle alternate with the petals. The further stamens appear almost simultaneously without a clear centrifugal or centripetal direcfion (Fig. 2E-H) (see also ENDRESS & VOSER (1975). Caloncoba glauca (On•obeae). The bisexual flowers of Caloncoba glauca have a diameter of c. 7-12 cm at anthesis. The perianth consists of three sepals and

Fig. 2. Floral buds from above, showing different stages of androecial development. A-D Lindackeria dentata; A, B sepals removed, C, D sepals and petals partially or completely removed. E-H Caloncoba echinata. Bars: A - H 100m

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12-15 petals in two seiles, an outer seiles consisting of three and an inner series consisting of nine to twelve organs. The high number of organs in the inner seiles results by triple or quadruple positions. The approximately 400 stamens (more than 500 in male flowers) are irregularly arranged on the slightly concave receptacle. The gynoecium has five carpels with parietal placentation. Initiation of the stamens begins on a flat ring primordium at the periphery of the receptacle. The first initiated large pilmordia alternate with the petals (Fig. 3A). This is followed by a second set of two to three much smaller primordia in each sector alternating with these first organs (Fig. 3B), The further stamens appear almost simultaneously (Fig. 3B-D). Kiggelaria africana (Pangieae). Kiggelaria africana is dioecious. The male flowers have a diameter of c. 1 cm at anthesis. The perianth consists of five sepals and five petals. The petals have a contorted aestivation; they have an oblong scale at their base. The ten to twelve stamens are arranged in more or less two series, which become more and more irregular as development progresses. In male flowers the gynoecium is lacking. The stamens ailse more or less simultaneously (Fig. 3E-G). Flacourtia indica (Flacourtieae). Flacourtia indica is dioecious. The male flowers have a diameter of c. 0.5 cm at anthesis. The perianth consists of four sepals, which never fully enclose the bud. Petals are lacking. In male flowers the approximately 60 stamens are irregularly arranged on a slightly convex receptacle. The bases of the filaments are surrounded by an irregularly grooved nectailferous tissue. The gynoecium is lacking. Stamen pilmordia start to develop from the floral centre. The formation of the androecium proceeds on the expanding receptacle in centilfugal direction to the periphery (Fig. 4A-C). Idesia polycarpa (Flacourtieae). The male flowers of Idesia polycarpa have a diameter of c. 1.3 cm at anthesis. The perianth consists of five sepals. Petals are lacking. In male flowers the approximately 60 stamens are placed in three irregular seiles. The number of stamens increases from about ten to twelve in the innermost to about 20 in the middle and 30 in the outermost seiles. A rudimentary gynoecium is present. Androecial initiation begins on a ring meristem with the stamens of the innermost, and continues in centrifugal direction to the outermost seiles. The stamens within each seiles develop more or less simultaneously (Fig. 4D-F). Poliothyrsis sinensis (Flacourtieae). Poliothyrsis sinensis is monoecious. The male flowers have a diameter of c. 0.9 cm at anthesis. The perianth consists of five sepals. Petals are lacking. In male flowers the approximately 25 stamens are in three irregular seiles. A rudimentary gynoecium is present. Androecial initiation begins with the formation of a low ring pilmordium. On the ring primordium the c. eight stamens of the innermost series arise more or less simultaneously. On one side the primordia are retarded due to pressure of the sepals (Fig. 5A). The initiation of the stamens of the outer series starts with the stamens that alternate with those of the innermost seiles (Fig. 5B). Additional stamens of the third seiles arise in a more or less irregular sequence (Fig. 5C). Xylosma congesta (Flacourtieae). Xylosma congesta is dioecious. The male flowers have a diameter of c. 0.6 cm at anthesis. The perianth consists of four sepals

Fig. 3. Floral buds from above, showing different stages of androecial development. A-D Caloncoba glauca; A, sepals removed, B-D sepals and petals partly or completely removed, C, the androecium shows imprints of the petals. E-G Kiggelaria africana, sepals and petals removed. Bars: A - C 150 gin, D 250 gm, E - G 100 gm

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Fig. 4. Floral buds from above, showing different stages of androecial development. A - C Flacourtia indica; A one sepal removed. C sepals removed. D - F Idesia polycarpa, sepals removed. Bars: A, B 50 gm, C-F 100 um

in two decussate pairs. Petals are lacking. The approximately 15 stamens are commonly in an inner series of four stamens, opposite the sepals, and two irregular outer series. The bases of the filaments are surrounded by irregularly grooved nectariferous tissue. In male flowers the gynoecium is lacking. Androecial development begins with the formation of an inner pair of stamens opposite to the outer sepals (Fig. 5D). Subsequently, a pair of stamens opposite the

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Fig. 5. Floral buds from above, showing different stages of androecial development. A-C Potiothyrsis sinensis, sepals removed. D-F Xylosma congesta; D, E sepals removed, B sepals partly removed. Bars: A-C 100 gm, D 30 gm, E, F 40 gm

inner sepals arises (Fig. 5D, E). Therefore the first formed two pairs of stamens show a centripetal direction of initiation. Since the outer series o f stamens arise later, the sequence of androecial initiation as a whole is centrifugal as in the other members of the Flacourtieae. The stamens of the outer series are initiated in a more or less irregular sequence (Fig. 5F). Pseudoscolopia polyantha (Scolopieae). The flowers of Pseudoscolopia polyantha are bisexual. They have a diameter of c. 1.5 cm at anthesis. The

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Fig. 6. Floral buds from above, showing different stages of androecial development. A-C Pseudoscolopia polyantha; A, B sepals removed, C sepals and petals removed. D-F Phyllobotryon soyauxianum, sepals and petals removed. Bars: A, B 50 gm, C, E 100 gm, D, 70 gin, F 150 gm perianth consists of four sepals and four petals in two series. The approximately 40 stamens are arranged in three irregular series. The number of stamens increases from about nine in the innermost to about 17 in the middle and in the outermost series. The gynoecium is bicarpellate with parietal placentation. Stamen initiation begins on a flat ring primordium with the stamens of the innermost series and continues in centrifugal direction to the peripheral series (Fig. 6A-C).

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Fig. 7. Casearia silvana, floral buds showing different stages of androecial development, A from above, sepals removed, B, C sepals removed. Bars: A 50 ~tm, B, C 200 ~tm

PhyUobotryon soyauxianum (Scolopieae). The flowers of Phyllobotryon soyauxianum are bisexual. They have a diameter of c. 1.7 cm at anthesis. The perianth consists of three sepals and four petals. The approximately 75 stamens are arranged in three to four irregular seiles. In bud the anthers become irregular in shape due to crowding. The gynoecium is tricarpellate with parietal placentation. Initiation of the stamens begins on a flat ring meristem with the innermost seiles and proceeds in centrifugal direction to the periphery (Fig. 6D-F). Casearia silvana (Casearieae). The flowers of Casearia silvana are bisexual. They have a diameter of c. 0.7 cm at anthesis. The perianth consists of five sepals. Petals are lacking. The ten to thirteen stamens are in a single seiles. An equal number of hairy scales alternate with the stamens (Fig. 7B). The gynoecium is tricarpellate with parietal placentation. The stamens seem to arise simultaneously around the massive gynoecium primordium. (Fig. 7A). The scales that alternate with the stamens seem to appear only much later, when stamen development is rar advanced (Fig. 7C).

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Discussion

Flacourtiaceae s. 1. (in the circumscription by LEMKE 1988) were variously characterized as having a centrifugal stamen initiation (CRONQUISV 1981, ROYSE DECRAE~ & SMETS 1992). The present study, however, shows that both, centrifugal and centripetal stamen initiation do occur in this family. A centripetal sequence or an almost simultaneous initiation of stamens is found in the tribes Erythrospermeae and Oncobeae, whereas a centrifugal initiation of stamens is shown by Scolopieae and Flacourtieae. No correlation could be found between the sequence of stamen initiation and other floral characters that might reveal a cause for the respective sequences. The distribution of the direction of androecium development coincides well with the distribution of other characters. Therefore these data imply the division of the different tribes of Flacourtiaceae into at least two groups. In group 1, containing Erythrospermeae, Oncobeae and Pangieae, cyanogenic glycosides are present (SeENCER & SnCLER 1985), perforation plates of the tracheary elements are often scalariform or a combination of scalariform and simple, and they have medium sized to large intervascular pits (MALER 1975); members of these tribes have no salicoid leaf teeth (NAYoI & al. 1998). The close relationship of Oncobeae and Erythrospermeae is, in addition, confirmed by the distinctive pattern of petal initiation found in these two tribes. The relationship was also emphasised by GILQ (1925) by uniting these tribes (which were recognised earlier by WARBUa~ 1894), primarily based on flower morphology, into one large Oncobeae. As an exception in the Oncobeae, the genus Oncoba itself turns out to have characters that do not fit with the characters expected in a typical representative of this tribe. The stamens in Oncoba spinosa are initiated in a centrifugal sequence (VAN HEEL 1977). The genus lacks cyanogenic compounds present in the other Oncobeae genera (SPENCER & SnaLER 1985) and it shows salicoid leaf teeth, which are abseht in the tribe elsewhere (NAyoI & al. 1998). Furthermore, the ovules of Oncoba spinosa are orthotropous whereas they are anatropous in Caloncoba spp., Camptostylus spp., Dasylepis brevipedicellata, Scotellia mimfiensis and Lindackeria dentata (Oncobeae) (VAY HEEL 1977). However gross morphology lead H t r c & Bm~~ZLER (1997) to unite the genera Caloncoba, Camptostylus, Lindackeria, Paraphyadanthe and Xylotheca with Oncoba. In group 2, containing Flacourtieae, Homalieae, Scolopieae, Prockieae, Casearieae and Bembicieae, cyanogenic glycosides are lacking (SPZYCER & SEI~LER 1985); the perforation plates of the tracheary elements are often simple or a combination of scalariform and simple, and they have small intervascular pits (MALER 1975); the leaves of many members have salicoid teeth (NANDI & al. 1998); the tribes Scolopieae, Flacourtieae, and Homalieae have pollen which can scarcely be distinguished (KEATrNG 1973). LEMrd~ (1988) recognized three distinct groups within the Flacourtiaceae, based on morphological, palynological, anatomical and biochemical characters. This grouping with Berberidopsideae, Erythrospermeae, Oncobeae and Pangieae in a first, Scolopieae, Homalieae and Prockieae in a second and Flacourtieae, Casearieae and Bembicieae in a third group is not in contradiction to the grouping

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proposed here. TAKHTAJAN(1997) adopts LEMKE'S classification but he excludes the Bembicieae and the Berberidopsideae and classifies them as families of their own. CORN~R (1976) divides the family into a Flacourtia group and a Hydnocarpus group. His Flacourtia group, diagnosed by the seed morphological character, presence of a fibrous exotegmen, consists of LEMKE'S (1988) Erythrospermeae, Oncobeae, Scolopieae, Flacourtieae and Casearieae and thus violates the grouping implied by the other characters cited above and the developmental data presented here. VAN HEEL'S (1979) study of seed anatomy does not corroborate CORNER'S (1976) division of Flacourtiaceae. According to a phylogenetic analysis based on rbcL sequences (CHASE• al. 1996) the family splits into three major clades. Clade 1 with Bembicieae, Casearieae, Flacourtieae and Scolopieae reflects out group 2. Clade 2 containing Pangieae and Achariaceae and clade 3 containing Oncobeae and Lacistemataceae cannot be commented on by this study as they include families not investigated here, but they are supported as consisting of taxa that are different from our group 2. Another result by CHASE & al. (1996) is the inclusion of Salicaceae in Flacourtiaceae s. str. HALLmR(1908) was the first to propose a close relafionship of Salicaceae and Flacourtiaceae. Other anthors have also discussed potential relationship between these two families. For a general overview see MEEUSE (1975). Vegetative anatomy and leaf morphology of both families have been investigated by METCALFE & CHALK (1950), GOLYSHEVA (1975) and HICKEY 8¢ WOLZZ (1975); aspects of seed anatomy by CORNER (1976). In Salicaceae androecium development is centrifugal (KAUE 1995) as found here for Flacourtiaceae s. str., which supports the results by CHASE & al. (1996). The available data support the arrangement of the components of Flacourtiaceae s. 1. in at least two separate groups as proposed by NANDI & al. (1998). According to them Flacourtiaceae s. str. include Flacourtieae, Homalieae, Scolopieae, Casearieae, Bembicieae and the genus Oncoba (in the circumscription of LEMr,Z 1998) while Erythrospermeae (containing all genera of LEMI~'S Erythrospermeae and Oncobeae except for Oncoba) and Pangieae are in their Kiggelariaceae. Despite the various uncommon features revealed by different studies it seems to be too preliminary to separate the genus Oncoba from the other genera of Oncobeae. Therefore, at the present stage two families are proposed as follows: (1) Flacourtiaceae s. str. with Flacourtieae, Homalieae, Scolopieae, Prockieae, Casearieae and Bembicieae and (2) Kiggelariaceae with Erythrospermeae, Oncobeae and Kiggelarieae (Kiggelarieae represents the Pangieae in the circumscription by LEMKE 1988). While the separation of these two families seems to be quite well established by a number of characters from different fields, the position and composition of some tribes (e.g. Bembicieae) is still uncertain. We thank BRAAMVANWYK and ToNYABBOTTfor their kind help during the visit of A. B. to South Africa and the Splinter-Legat for financial support of this tfip. We are indebted to JÜRG S¢HÖNENBERGERwho provided most valuable material from Cameroon and to MARK CHASEwho made available unpublished results of an rbcL analysis. We also thank URS JAUCHfor his assistance with the SEM.

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