Fig 2 - uploaded by Gerhard Prenner
Content may be subject to copyright.
SEM micrographs of a hermaphrodite flower of Apuleia leiocarpa , specimen Pennington and Rowe 172. Abaxial side is at base unless otherwise noted. a , Frontal view of flower at anthesis with gynoecium in the abaxial median position and two adaxial lateral stamens. b , Gynoecium with ovary wall removed to show ovules. c , d , Longitudinal section of flower base. Asterisk shows the placement of the stipe within the tubular hypanthium. Arrow indicates cavity formed by hypanthium walls. d , Detail of stipe attachment. e , Ovule attached to ovary wall. f , Detail of peltate stigma, abaxial side. A 1⁄4 stamen; C 1⁄4 carpel; o = ovule; P 1⁄4 petal; S 1⁄4 sepal; St 1⁄4 stigma.
Source publication
Apuleia leiocarpa (Vogel) J. F. Macbr. is a South American tree species belonging to the caesalpinioid subfamily of the Leguminosae. Phylogenetic analyses have placed Apuleia into the Dialiinae s.l. clade, with which it shares numerous morphological similarities, including dichasial cymose inflorescences. The genus has also been reported to be andr...
Contexts in source publication
Context 1
... leiocarpa (Vogel) J. F. Macbr. is an andromonoecious South American tree species belonging to the caesalpinioid subfamily of the Leguminosae. Caesalpinioideae possesses the greatest floral morphological diversity of the three legume subfamilies (Lewis et al. 2000), comprising taxa with both actinomorphic and zygomorphic flowers, as well as, particularly within tribe Cassieae, drastic reductions in floral organ number (Tucker 1988 b , 1998). This subfamily, which has been described as the most ‘‘taxonomically prob- lematic’’ of the three (Gasson et al. 2003), contains numerous taxa that have not yet been studied in detail but that may provide clues to floral evolution in the Leguminosae. Apuleia leiocarpa is one such taxon. The only member of its genus according to a recent revision (de Sousa et al. 2010), A. leiocarpa has been placed by phylogenetic analyses into the Dialiinae s.l. clade (Doyle et al. 1997; Kajita et al. 2001; Lewis 2005; Bruneau et al. 2008). Dialiinae s.l. is made up of the Cassieae subtribes Dialiinae and Labicheinae, the latter comprising the Australian genera Labichea Gaud. ex DC and Petalostylis R. Br. The clade is united by its cymose inflorescences (except in Labicheinae), wood lacking in vestured pits, and greatly decreased floral organ numbers—all uncommon features in the Caesalpinioideae as a whole. The precise position of Apuleia within Dialiinae s.l. re- mains uncertain (Bruneau et al. 2008), but the phylogenetic analysis of Bruneau et al. (2008), based on matK exon plus 3 9 -trnK and trnL intron sequences, placed Apuleia and Distemonanthus as sister groups with a high degree of confidence. Koeppen (1978) also suggested a close relationship between Apuleia and the monospecific West African genus Distemonanthus Benth. based on similarities in wood anatomy, spe- cifically, in the presence and deposition of silica bodies. Indeed, Koeppen (1978) goes on to note that there are morphological similarities in the leaves, flowers, and fruits of the two species but does not expand on this observation. Andromonoecy, the form of sex expression seen in the genus Apuleia (Arroyo 1981), which produces both staminate and hermaphrodite flowers, is otherwise unknown in the Dialiinae and rare among legumes. It has been found in ; 4000 species of flowering plants belonging to at least 33 families and appears to have evolved independently numerous times (Miller and Diggle 2003). In some species, andromonoecy is brought about by a late-stage suppression of the gynoecium; the organ is formed but ceases growth prior to maturity and appears stunted or underdeveloped at anthesis (Beavon and Chapman 2011). In other species, however, the female organs are simply not initiated (Tucker 1991). No mention is made in the litera- ture as to which of these staminate flower morphologies is seen in Apuleia . Here, flowers were dissected and observed using a stereomicroscope and scanning electron microscopy (SEM) to examine in detail the floral morphology of A. leiocarpa . A comparison is made with other andromonoecious caesalpinioid legumes, and some of the functional implications of sex expression in ZIMMERMAN ET AL.—FLORAL MORPHOLOGY OF the genus are discussed. Similarities and differences with the Dialiinae clade as a whole are also explored. For SEM, flowers were dissected in 70% ethanol and critical- point dried using an Autosamdri-815B critical-point dryer (Tousimis Research, Rockville, MD). Dried material was then mounted onto specimen stubs using clear nail polish, coated with platinum using an Emitech K550 sputter-coater (Emitech, Ashford, UK), and examined using a Hitachi cold-field emis- sion SEM S-4700-II (Hitachi High Technologies, Tokyo). All SEM work was carried out at the Royal Botanic Gardens, Kew. SEM images were edited using Adobe Photoshop CS5. Floral diagrams and formulas were developed following rec- ommendations by Prenner et al. (2010). Specimens examined under the stereomicroscope were removed from herbarium vouchers and rehydrated in boiling water with a small amount of surfactant and then dehydrated through an ethanol series to 80% ethanol, in which they were dissected and observed using a binocular dissecting mi- croscope (Wild Heerbrugg). These dissections were then used to produce the illustrations used in figure 1. Specimens examined were as follows: G.C.G. Argent 6657, State of Mato Grosso, Amarela ̃ o, Brazil, 1968 (MO); P. Fra- gomemi 11642, Rio Grande do Sul, Brazil, 1968 (MO); R.M. Harley & R. Souza 10720, State of Mato Grosso, Brazil, 1969 (K); Heringer et al. 5426, Bacia do Rio Sa ̃o Bartolmeu, fr., Brazil, 1980 (K); B.B. Klitgaard & F.C.P. Garcia 66, State of Bahia, Brazil, 1994 (MO); Pennington and Rowe 172, Pando, Puerto Oro, Bolivia, 1988 (MO); A.G. Ruiz 217-AGR, Loreto, Maynas Province, Peru, 1965 (MO); Sant’Ana et al. 361, State of Bahia, Brazil, 1993 (MO); R. Va ́squez, R. Ortiz and N. Jaramillo 14369, Loreto, Maynas Province, Peru, 1990 (MO); J.L. Zarucchi & C.E. Barbosa 3739, Vichada, Colombia, 1985 (MO). The bisexual flowers of Apuleia leiocarpa tend to occupy the central (terminal) position in a compound dichasium, as well as some of the central positions in higher-order cymes, while the younger lateral flowers are staminate (fig. 1 a ). The more flowers present on an inflorescence, the more likely the occurrence of multiple bisexual flowers. Figure 1 a represents a smaller but common inflorescence size. Phyllomes subtending the central flower are early cadu- cous, leaving visible scars (fig. 1 a ), while those occurring on lateral flowers are minute and ephemeral. On mature inflorescences, the scars, which occur on the lower portion of the pedicel, are very difficult to discern and are therefore not illustrated in figure 1 a but are shown in the floral diagram (fig. 1 b ). Both floral morphs possess a trimerous calyx and corolla (fig. 1 b , 1 c ). In bisexual flowers, the inner whorls consist of a single pistil and two stamens in the adaxial lateral posi- tions, opposite the adaxial lateral sepals, although additional pistils and stamens are occasionally present (figs. 1 c , 1 d , 2 a ). A longitudinal section of a hermaphrodite flower shows that the gynoecium, which consists of a single carpel, is stipitate and arises from the base of a narrow, tubular hypanthium (fig. 2 b –2 d ), while the perianth and androecium arise from the rim of the hypanthium (fig. 3 c ). The carpel encloses up to four narrow, elongated ovules (fig. 2 b ), which are attached with a short funicle to the ovary wall (fig. 2 e ). The stigma is peltate and covered with short papillae (fig. 2 f ). Staminate flowers of A. leiocarpa do not appear to develop either a functional gynoecium or a vestigial gynoecium. Three stamens (rarely four) develop on the rim of the hypanthium, with the third stamen occupying the volume taken up by the gynoecium in the hermaphrodite flower (fig. 1 b , 3 a , 3 c , 3 d ). At the center of the floral surface, a trichome-filled triangular opening leads to the sunken hypanthium (fig. 3 c , 3 e ), although in some flowers, this develops merely as a three-pointed slit (fig. 2 d ). In cross section, the hypanthium appears to be compressed into three nearly separate chambers (fig. 3 e ); no tissue resembling a suppressed gynoecium is apparent. Anthers de- hisce with longitudinal slits (fig. 3 b ) and release tricolporate pollen grains with microreticulate surfaces (fig. 3 f ). The adaxial surface of the anthers is covered with characteristic hooked trichomes (fig. 3 g ). The basic legume flower is thought to be built on a ground plan of a pentamerous calyx and corolla, two pentamerous whorls of stamens, and a unicarpellate gynoecium, for a total of 21 floral organs (Tucker 2003). The subfamily Caesalpinioideae, which forms a basal grade in the Leguminosae, and in particular the tribe Cassieae, shows the greatest and most frequent deviation from this ground plan, both via organ suppression and, less frequently, complete loss (Tucker 2003; Prenner and Klitgaard 2008). The Dialiinae s.l. clade (Bruneau et al. 2001), which is composed of the two Cassieae subtribes Dialiinae and Labicheinae of Irwin and Barneby (1981) plus the genus Poeppigia C. Presl., displays high levels of organ loss, particularly in the androecium. Several species of the genus Dialium L., e.g., possess only eight organs: five sepals, two stamens, and a carpel. While Dialium represents an extreme, very few species in the clade retain a full set of antepetalous stamens, the vast majority having lost this whorl entirely. Apuleia leiocarpa , with its nine remaining organs, seems to share this characteristic of the clade. Occasionally, a second carpel, with or without additional stamens, is present (fig. 1 d ), a phenomenon noted in certain other caesalpinioid genera, such as Bauhinia L. (Tucker 1988 a ), Ceratonia L. (Tucker 1992), and Dialium (Chakravarty 1969). While a unicarpellate bisexual flower bearing three stamens has been illustrated in Irwin and Barneby’s (1981) revision of Cassieae, this state has not been observed in the many flowers dissected for ...
Context 2
... leiocarpa (Vogel) J. F. Macbr. is an andromonoecious South American tree species belonging to the caesalpinioid subfamily of the Leguminosae. Caesalpinioideae possesses the greatest floral morphological diversity of the three legume subfamilies (Lewis et al. 2000), comprising taxa with both actinomorphic and zygomorphic flowers, as well as, particularly within tribe Cassieae, drastic reductions in floral organ number (Tucker 1988 b , 1998). This subfamily, which has been described as the most ‘‘taxonomically prob- lematic’’ of the three (Gasson et al. 2003), contains numerous taxa that have not yet been studied in detail but that may provide clues to floral evolution in the Leguminosae. Apuleia leiocarpa is one such taxon. The only member of its genus according to a recent revision (de Sousa et al. 2010), A. leiocarpa has been placed by phylogenetic analyses into the Dialiinae s.l. clade (Doyle et al. 1997; Kajita et al. 2001; Lewis 2005; Bruneau et al. 2008). Dialiinae s.l. is made up of the Cassieae subtribes Dialiinae and Labicheinae, the latter comprising the Australian genera Labichea Gaud. ex DC and Petalostylis R. Br. The clade is united by its cymose inflorescences (except in Labicheinae), wood lacking in vestured pits, and greatly decreased floral organ numbers—all uncommon features in the Caesalpinioideae as a whole. The precise position of Apuleia within Dialiinae s.l. re- mains uncertain (Bruneau et al. 2008), but the phylogenetic analysis of Bruneau et al. (2008), based on matK exon plus 3 9 -trnK and trnL intron sequences, placed Apuleia and Distemonanthus as sister groups with a high degree of confidence. Koeppen (1978) also suggested a close relationship between Apuleia and the monospecific West African genus Distemonanthus Benth. based on similarities in wood anatomy, spe- cifically, in the presence and deposition of silica bodies. Indeed, Koeppen (1978) goes on to note that there are morphological similarities in the leaves, flowers, and fruits of the two species but does not expand on this observation. Andromonoecy, the form of sex expression seen in the genus Apuleia (Arroyo 1981), which produces both staminate and hermaphrodite flowers, is otherwise unknown in the Dialiinae and rare among legumes. It has been found in ; 4000 species of flowering plants belonging to at least 33 families and appears to have evolved independently numerous times (Miller and Diggle 2003). In some species, andromonoecy is brought about by a late-stage suppression of the gynoecium; the organ is formed but ceases growth prior to maturity and appears stunted or underdeveloped at anthesis (Beavon and Chapman 2011). In other species, however, the female organs are simply not initiated (Tucker 1991). No mention is made in the litera- ture as to which of these staminate flower morphologies is seen in Apuleia . Here, flowers were dissected and observed using a stereomicroscope and scanning electron microscopy (SEM) to examine in detail the floral morphology of A. leiocarpa . A comparison is made with other andromonoecious caesalpinioid legumes, and some of the functional implications of sex expression in ZIMMERMAN ET AL.—FLORAL MORPHOLOGY OF the genus are discussed. Similarities and differences with the Dialiinae clade as a whole are also explored. For SEM, flowers were dissected in 70% ethanol and critical- point dried using an Autosamdri-815B critical-point dryer (Tousimis Research, Rockville, MD). Dried material was then mounted onto specimen stubs using clear nail polish, coated with platinum using an Emitech K550 sputter-coater (Emitech, Ashford, UK), and examined using a Hitachi cold-field emis- sion SEM S-4700-II (Hitachi High Technologies, Tokyo). All SEM work was carried out at the Royal Botanic Gardens, Kew. SEM images were edited using Adobe Photoshop CS5. Floral diagrams and formulas were developed following rec- ommendations by Prenner et al. (2010). Specimens examined under the stereomicroscope were removed from herbarium vouchers and rehydrated in boiling water with a small amount of surfactant and then dehydrated through an ethanol series to 80% ethanol, in which they were dissected and observed using a binocular dissecting mi- croscope (Wild Heerbrugg). These dissections were then used to produce the illustrations used in figure 1. Specimens examined were as follows: G.C.G. Argent 6657, State of Mato Grosso, Amarela ̃ o, Brazil, 1968 (MO); P. Fra- gomemi 11642, Rio Grande do Sul, Brazil, 1968 (MO); R.M. Harley & R. Souza 10720, State of Mato Grosso, Brazil, 1969 (K); Heringer et al. 5426, Bacia do Rio Sa ̃o Bartolmeu, fr., Brazil, 1980 (K); B.B. Klitgaard & F.C.P. Garcia 66, State of Bahia, Brazil, 1994 (MO); Pennington and Rowe 172, Pando, Puerto Oro, Bolivia, 1988 (MO); A.G. Ruiz 217-AGR, Loreto, Maynas Province, Peru, 1965 (MO); Sant’Ana et al. 361, State of Bahia, Brazil, 1993 (MO); R. Va ́squez, R. Ortiz and N. Jaramillo 14369, Loreto, Maynas Province, Peru, 1990 (MO); J.L. Zarucchi & C.E. Barbosa 3739, Vichada, Colombia, 1985 (MO). The bisexual flowers of Apuleia leiocarpa tend to occupy the central (terminal) position in a compound dichasium, as well as some of the central positions in higher-order cymes, while the younger lateral flowers are staminate (fig. 1 a ). The more flowers present on an inflorescence, the more likely the occurrence of multiple bisexual flowers. Figure 1 a represents a smaller but common inflorescence size. Phyllomes subtending the central flower are early cadu- cous, leaving visible scars (fig. 1 a ), while those occurring on lateral flowers are minute and ephemeral. On mature inflorescences, the scars, which occur on the lower portion of the pedicel, are very difficult to discern and are therefore not illustrated in figure 1 a but are shown in the floral diagram (fig. 1 b ). Both floral morphs possess a trimerous calyx and corolla (fig. 1 b , 1 c ). In bisexual flowers, the inner whorls consist of a single pistil and two stamens in the adaxial lateral posi- tions, opposite the adaxial lateral sepals, although additional pistils and stamens are occasionally present (figs. 1 c , 1 d , 2 a ). A longitudinal section of a hermaphrodite flower shows that the gynoecium, which consists of a single carpel, is stipitate and arises from the base of a narrow, tubular hypanthium (fig. 2 b –2 d ), while the perianth and androecium arise from the rim of the hypanthium (fig. 3 c ). The carpel encloses up to four narrow, elongated ovules (fig. 2 b ), which are attached with a short funicle to the ovary wall (fig. 2 e ). The stigma is peltate and covered with short papillae (fig. 2 f ). Staminate flowers of A. leiocarpa do not appear to develop either a functional gynoecium or a vestigial gynoecium. Three stamens (rarely four) develop on the rim of the hypanthium, with the third stamen occupying the volume taken up by the gynoecium in the hermaphrodite flower (fig. 1 b , 3 a , 3 c , 3 d ). At the center of the floral surface, a trichome-filled triangular opening leads to the sunken hypanthium (fig. 3 c , 3 e ), although in some flowers, this develops merely as a three-pointed slit (fig. 2 d ). In cross section, the hypanthium appears to be compressed into three nearly separate chambers (fig. 3 e ); no tissue resembling a suppressed gynoecium is apparent. Anthers de- hisce with longitudinal slits (fig. 3 b ) and release tricolporate pollen grains with microreticulate surfaces (fig. 3 f ). The adaxial surface of the anthers is covered with characteristic hooked trichomes (fig. 3 g ). The basic legume flower is thought to be built on a ground plan of a pentamerous calyx and corolla, two pentamerous whorls of stamens, and a unicarpellate gynoecium, for a total of 21 floral organs (Tucker 2003). The subfamily Caesalpinioideae, which forms a basal grade in the Leguminosae, and in particular the tribe Cassieae, shows the greatest and most frequent deviation from this ground plan, both via organ suppression and, less frequently, complete loss (Tucker 2003; Prenner and Klitgaard 2008). The Dialiinae s.l. clade (Bruneau et al. 2001), which is composed of the two Cassieae subtribes Dialiinae and Labicheinae of Irwin and Barneby (1981) plus the genus Poeppigia C. Presl., displays high levels of organ loss, particularly in the androecium. Several species of the genus Dialium L., e.g., possess only eight organs: five sepals, two stamens, and a carpel. While Dialium represents an extreme, very few species in the clade retain a full set of antepetalous stamens, the vast majority having lost this whorl entirely. Apuleia leiocarpa , with its nine remaining organs, seems to share this characteristic of the clade. Occasionally, a second carpel, with or without additional stamens, is present (fig. 1 d ), a phenomenon noted in certain other caesalpinioid genera, such as Bauhinia L. (Tucker 1988 a ), Ceratonia L. (Tucker 1992), and Dialium (Chakravarty 1969). While a unicarpellate bisexual flower bearing three stamens has been illustrated in Irwin and Barneby’s (1981) revision of Cassieae, this state has not been observed in the many flowers dissected for ...
Context 3
... leiocarpa (Vogel) J. F. Macbr. is an andromonoecious South American tree species belonging to the caesalpinioid subfamily of the Leguminosae. Caesalpinioideae possesses the greatest floral morphological diversity of the three legume subfamilies (Lewis et al. 2000), comprising taxa with both actinomorphic and zygomorphic flowers, as well as, particularly within tribe Cassieae, drastic reductions in floral organ number (Tucker 1988 b , 1998). This subfamily, which has been described as the most ‘‘taxonomically prob- lematic’’ of the three (Gasson et al. 2003), contains numerous taxa that have not yet been studied in detail but that may provide clues to floral evolution in the Leguminosae. Apuleia leiocarpa is one such taxon. The only member of its genus according to a recent revision (de Sousa et al. 2010), A. leiocarpa has been placed by phylogenetic analyses into the Dialiinae s.l. clade (Doyle et al. 1997; Kajita et al. 2001; Lewis 2005; Bruneau et al. 2008). Dialiinae s.l. is made up of the Cassieae subtribes Dialiinae and Labicheinae, the latter comprising the Australian genera Labichea Gaud. ex DC and Petalostylis R. Br. The clade is united by its cymose inflorescences (except in Labicheinae), wood lacking in vestured pits, and greatly decreased floral organ numbers—all uncommon features in the Caesalpinioideae as a whole. The precise position of Apuleia within Dialiinae s.l. re- mains uncertain (Bruneau et al. 2008), but the phylogenetic analysis of Bruneau et al. (2008), based on matK exon plus 3 9 -trnK and trnL intron sequences, placed Apuleia and Distemonanthus as sister groups with a high degree of confidence. Koeppen (1978) also suggested a close relationship between Apuleia and the monospecific West African genus Distemonanthus Benth. based on similarities in wood anatomy, spe- cifically, in the presence and deposition of silica bodies. Indeed, Koeppen (1978) goes on to note that there are morphological similarities in the leaves, flowers, and fruits of the two species but does not expand on this observation. Andromonoecy, the form of sex expression seen in the genus Apuleia (Arroyo 1981), which produces both staminate and hermaphrodite flowers, is otherwise unknown in the Dialiinae and rare among legumes. It has been found in ; 4000 species of flowering plants belonging to at least 33 families and appears to have evolved independently numerous times (Miller and Diggle 2003). In some species, andromonoecy is brought about by a late-stage suppression of the gynoecium; the organ is formed but ceases growth prior to maturity and appears stunted or underdeveloped at anthesis (Beavon and Chapman 2011). In other species, however, the female organs are simply not initiated (Tucker 1991). No mention is made in the litera- ture as to which of these staminate flower morphologies is seen in Apuleia . Here, flowers were dissected and observed using a stereomicroscope and scanning electron microscopy (SEM) to examine in detail the floral morphology of A. leiocarpa . A comparison is made with other andromonoecious caesalpinioid legumes, and some of the functional implications of sex expression in ZIMMERMAN ET AL.—FLORAL MORPHOLOGY OF the genus are discussed. Similarities and differences with the Dialiinae clade as a whole are also explored. For SEM, flowers were dissected in 70% ethanol and critical- point dried using an Autosamdri-815B critical-point dryer (Tousimis Research, Rockville, MD). Dried material was then mounted onto specimen stubs using clear nail polish, coated with platinum using an Emitech K550 sputter-coater (Emitech, Ashford, UK), and examined using a Hitachi cold-field emis- sion SEM S-4700-II (Hitachi High Technologies, Tokyo). All SEM work was carried out at the Royal Botanic Gardens, Kew. SEM images were edited using Adobe Photoshop CS5. Floral diagrams and formulas were developed following rec- ommendations by Prenner et al. (2010). Specimens examined under the stereomicroscope were removed from herbarium vouchers and rehydrated in boiling water with a small amount of surfactant and then dehydrated through an ethanol series to 80% ethanol, in which they were dissected and observed using a binocular dissecting mi- croscope (Wild Heerbrugg). These dissections were then used to produce the illustrations used in figure 1. Specimens examined were as follows: G.C.G. Argent 6657, State of Mato Grosso, Amarela ̃ o, Brazil, 1968 (MO); P. Fra- gomemi 11642, Rio Grande do Sul, Brazil, 1968 (MO); R.M. Harley & R. Souza 10720, State of Mato Grosso, Brazil, 1969 (K); Heringer et al. 5426, Bacia do Rio Sa ̃o Bartolmeu, fr., Brazil, 1980 (K); B.B. Klitgaard & F.C.P. Garcia 66, State of Bahia, Brazil, 1994 (MO); Pennington and Rowe 172, Pando, Puerto Oro, Bolivia, 1988 (MO); A.G. Ruiz 217-AGR, Loreto, Maynas Province, Peru, 1965 (MO); Sant’Ana et al. 361, State of Bahia, Brazil, 1993 (MO); R. Va ́squez, R. Ortiz and N. Jaramillo 14369, Loreto, Maynas Province, Peru, 1990 (MO); J.L. Zarucchi & C.E. Barbosa 3739, Vichada, Colombia, 1985 (MO). The bisexual flowers of Apuleia leiocarpa tend to occupy the central (terminal) position in a compound dichasium, as well as some of the central positions in higher-order cymes, while the younger lateral flowers are staminate (fig. 1 a ). The more flowers present on an inflorescence, the more likely the occurrence of multiple bisexual flowers. Figure 1 a represents a smaller but common inflorescence size. Phyllomes subtending the central flower are early cadu- cous, leaving visible scars (fig. 1 a ), while those occurring on lateral flowers are minute and ephemeral. On mature inflorescences, the scars, which occur on the lower portion of the pedicel, are very difficult to discern and are therefore not illustrated in figure 1 a but are shown in the floral diagram (fig. 1 b ). Both floral morphs possess a trimerous calyx and corolla (fig. 1 b , 1 c ). In bisexual flowers, the inner whorls consist of a single pistil and two stamens in the adaxial lateral posi- tions, opposite the adaxial lateral sepals, although additional pistils and stamens are occasionally present (figs. 1 c , 1 d , 2 a ). A longitudinal section of a hermaphrodite flower shows that the gynoecium, which consists of a single carpel, is stipitate and arises from the base of a narrow, tubular hypanthium (fig. 2 b –2 d ), while the perianth and androecium arise from the rim of the hypanthium (fig. 3 c ). The carpel encloses up to four narrow, elongated ovules (fig. 2 b ), which are attached with a short funicle to the ovary wall (fig. 2 e ). The stigma is peltate and covered with short papillae (fig. 2 f ). Staminate flowers of A. leiocarpa do not appear to develop either a functional gynoecium or a vestigial gynoecium. Three stamens (rarely four) develop on the rim of the hypanthium, with the third stamen occupying the volume taken up by the gynoecium in the hermaphrodite flower (fig. 1 b , 3 a , 3 c , 3 d ). At the center of the floral surface, a trichome-filled triangular opening leads to the sunken hypanthium (fig. 3 c , 3 e ), although in some flowers, this develops merely as a three-pointed slit (fig. 2 d ). In cross section, the hypanthium appears to be compressed into three nearly separate chambers (fig. 3 e ); no tissue resembling a suppressed gynoecium is apparent. Anthers de- hisce with longitudinal slits (fig. 3 b ) and release tricolporate pollen grains with microreticulate surfaces (fig. 3 f ). The adaxial surface of the anthers is covered with characteristic hooked trichomes (fig. 3 g ). The basic legume flower is thought to be built on a ground plan of a pentamerous calyx and corolla, two pentamerous whorls of stamens, and a unicarpellate gynoecium, for a total of 21 floral organs (Tucker 2003). The subfamily Caesalpinioideae, which forms a basal grade in the Leguminosae, and in particular the tribe Cassieae, shows the greatest and most frequent deviation from this ground plan, both via organ suppression and, less frequently, complete loss (Tucker 2003; Prenner and Klitgaard 2008). The Dialiinae s.l. clade (Bruneau et al. 2001), which is composed of the two Cassieae subtribes Dialiinae and Labicheinae of Irwin and Barneby (1981) plus the genus Poeppigia C. Presl., displays high levels of organ loss, particularly in the androecium. Several species of the genus Dialium L., e.g., possess only eight organs: five sepals, two stamens, and a carpel. While Dialium represents an extreme, very few species in the clade retain a full set of antepetalous stamens, the vast majority having lost this whorl entirely. Apuleia leiocarpa , with its nine remaining organs, seems to share this characteristic of the clade. Occasionally, a second carpel, with or without additional stamens, is present (fig. 1 d ), a phenomenon noted in certain other caesalpinioid genera, such as Bauhinia L. (Tucker 1988 a ), Ceratonia L. (Tucker 1992), and Dialium (Chakravarty 1969). While a unicarpellate bisexual flower bearing three stamens has been illustrated in Irwin and Barneby’s (1981) revision of Cassieae, this state has not been observed in the many flowers dissected for ...
Context 4
... leiocarpa (Vogel) J. F. Macbr. is an andromonoecious South American tree species belonging to the caesalpinioid subfamily of the Leguminosae. Caesalpinioideae possesses the greatest floral morphological diversity of the three legume subfamilies (Lewis et al. 2000), comprising taxa with both actinomorphic and zygomorphic flowers, as well as, particularly within tribe Cassieae, drastic reductions in floral organ number (Tucker 1988 b , 1998). This subfamily, which has been described as the most ‘‘taxonomically prob- lematic’’ of the three (Gasson et al. 2003), contains numerous taxa that have not yet been studied in detail but that may provide clues to floral evolution in the Leguminosae. Apuleia leiocarpa is one such taxon. The only member of its genus according to a recent revision (de Sousa et al. 2010), A. leiocarpa has been placed by phylogenetic analyses into the Dialiinae s.l. clade (Doyle et al. 1997; Kajita et al. 2001; Lewis 2005; Bruneau et al. 2008). Dialiinae s.l. is made up of the Cassieae subtribes Dialiinae and Labicheinae, the latter comprising the Australian genera Labichea Gaud. ex DC and Petalostylis R. Br. The clade is united by its cymose inflorescences (except in Labicheinae), wood lacking in vestured pits, and greatly decreased floral organ numbers—all uncommon features in the Caesalpinioideae as a whole. The precise position of Apuleia within Dialiinae s.l. re- mains uncertain (Bruneau et al. 2008), but the phylogenetic analysis of Bruneau et al. (2008), based on matK exon plus 3 9 -trnK and trnL intron sequences, placed Apuleia and Distemonanthus as sister groups with a high degree of confidence. Koeppen (1978) also suggested a close relationship between Apuleia and the monospecific West African genus Distemonanthus Benth. based on similarities in wood anatomy, spe- cifically, in the presence and deposition of silica bodies. Indeed, Koeppen (1978) goes on to note that there are morphological similarities in the leaves, flowers, and fruits of the two species but does not expand on this observation. Andromonoecy, the form of sex expression seen in the genus Apuleia (Arroyo 1981), which produces both staminate and hermaphrodite flowers, is otherwise unknown in the Dialiinae and rare among legumes. It has been found in ; 4000 species of flowering plants belonging to at least 33 families and appears to have evolved independently numerous times (Miller and Diggle 2003). In some species, andromonoecy is brought about by a late-stage suppression of the gynoecium; the organ is formed but ceases growth prior to maturity and appears stunted or underdeveloped at anthesis (Beavon and Chapman 2011). In other species, however, the female organs are simply not initiated (Tucker 1991). No mention is made in the litera- ture as to which of these staminate flower morphologies is seen in Apuleia . Here, flowers were dissected and observed using a stereomicroscope and scanning electron microscopy (SEM) to examine in detail the floral morphology of A. leiocarpa . A comparison is made with other andromonoecious caesalpinioid legumes, and some of the functional implications of sex expression in ZIMMERMAN ET AL.—FLORAL MORPHOLOGY OF the genus are discussed. Similarities and differences with the Dialiinae clade as a whole are also explored. For SEM, flowers were dissected in 70% ethanol and critical- point dried using an Autosamdri-815B critical-point dryer (Tousimis Research, Rockville, MD). Dried material was then mounted onto specimen stubs using clear nail polish, coated with platinum using an Emitech K550 sputter-coater (Emitech, Ashford, UK), and examined using a Hitachi cold-field emis- sion SEM S-4700-II (Hitachi High Technologies, Tokyo). All SEM work was carried out at the Royal Botanic Gardens, Kew. SEM images were edited using Adobe Photoshop CS5. Floral diagrams and formulas were developed following rec- ommendations by Prenner et al. (2010). Specimens examined under the stereomicroscope were removed from herbarium vouchers and rehydrated in boiling water with a small amount of surfactant and then dehydrated through an ethanol series to 80% ethanol, in which they were dissected and observed using a binocular dissecting mi- croscope (Wild Heerbrugg). These dissections were then used to produce the illustrations used in figure 1. Specimens examined were as follows: G.C.G. Argent 6657, State of Mato Grosso, Amarela ̃ o, Brazil, 1968 (MO); P. Fra- gomemi 11642, Rio Grande do Sul, Brazil, 1968 (MO); R.M. Harley & R. Souza 10720, State of Mato Grosso, Brazil, 1969 (K); Heringer et al. 5426, Bacia do Rio Sa ̃o Bartolmeu, fr., Brazil, 1980 (K); B.B. Klitgaard & F.C.P. Garcia 66, State of Bahia, Brazil, 1994 (MO); Pennington and Rowe 172, Pando, Puerto Oro, Bolivia, 1988 (MO); A.G. Ruiz 217-AGR, Loreto, Maynas Province, Peru, 1965 (MO); Sant’Ana et al. 361, State of Bahia, Brazil, 1993 (MO); R. Va ́squez, R. Ortiz and N. Jaramillo 14369, Loreto, Maynas Province, Peru, 1990 (MO); J.L. Zarucchi & C.E. Barbosa 3739, Vichada, Colombia, 1985 (MO). The bisexual flowers of Apuleia leiocarpa tend to occupy the central (terminal) position in a compound dichasium, as well as some of the central positions in higher-order cymes, while the younger lateral flowers are staminate (fig. 1 a ). The more flowers present on an inflorescence, the more likely the occurrence of multiple bisexual flowers. Figure 1 a represents a smaller but common inflorescence size. Phyllomes subtending the central flower are early cadu- cous, leaving visible scars (fig. 1 a ), while those occurring on lateral flowers are minute and ephemeral. On mature inflorescences, the scars, which occur on the lower portion of the pedicel, are very difficult to discern and are therefore not illustrated in figure 1 a but are shown in the floral diagram (fig. 1 b ). Both floral morphs possess a trimerous calyx and corolla (fig. 1 b , 1 c ). In bisexual flowers, the inner whorls consist of a single pistil and two stamens in the adaxial lateral posi- tions, opposite the adaxial lateral sepals, although additional pistils and stamens are occasionally present (figs. 1 c , 1 d , 2 a ). A longitudinal section of a hermaphrodite flower shows that the gynoecium, which consists of a single carpel, is stipitate and arises from the base of a narrow, tubular hypanthium (fig. 2 b –2 d ), while the perianth and androecium arise from the rim of the hypanthium (fig. 3 c ). The carpel encloses up to four narrow, elongated ovules (fig. 2 b ), which are attached with a short funicle to the ovary wall (fig. 2 e ). The stigma is peltate and covered with short papillae (fig. 2 f ). Staminate flowers of A. leiocarpa do not appear to develop either a functional gynoecium or a vestigial gynoecium. Three stamens (rarely four) develop on the rim of the hypanthium, with the third stamen occupying the volume taken up by the gynoecium in the hermaphrodite flower (fig. 1 b , 3 a , 3 c , 3 d ). At the center of the floral surface, a trichome-filled triangular opening leads to the sunken hypanthium (fig. 3 c , 3 e ), although in some flowers, this develops merely as a three-pointed slit (fig. 2 d ). In cross section, the hypanthium appears to be compressed into three nearly separate chambers (fig. 3 e ); no tissue resembling a suppressed gynoecium is apparent. Anthers de- hisce with longitudinal slits (fig. 3 b ) and release tricolporate pollen grains with microreticulate surfaces (fig. 3 f ). The adaxial surface of the anthers is covered with characteristic hooked trichomes (fig. 3 g ). The basic legume flower is thought to be built on a ground plan of a pentamerous calyx and corolla, two pentamerous whorls of stamens, and a unicarpellate gynoecium, for a total of 21 floral organs (Tucker 2003). The subfamily Caesalpinioideae, which forms a basal grade in the Leguminosae, and in particular the tribe Cassieae, shows the greatest and most frequent deviation from this ground plan, both via organ suppression and, less frequently, complete loss (Tucker 2003; Prenner and Klitgaard 2008). The Dialiinae s.l. clade (Bruneau et al. 2001), which is composed of the two Cassieae subtribes Dialiinae and Labicheinae of Irwin and Barneby (1981) plus the genus Poeppigia C. Presl., displays high levels of organ loss, particularly in the androecium. Several species of the genus Dialium L., e.g., possess only eight organs: five sepals, two stamens, and a carpel. While Dialium represents an extreme, very few species in the clade retain a full set of antepetalous stamens, the vast majority having lost this whorl entirely. Apuleia leiocarpa , with its nine remaining organs, seems to share this characteristic of the clade. Occasionally, a second carpel, with or without additional stamens, is present (fig. 1 d ), a phenomenon noted in certain other caesalpinioid genera, such as Bauhinia L. (Tucker 1988 a ), Ceratonia L. (Tucker 1992), and Dialium (Chakravarty 1969). While a unicarpellate bisexual flower bearing three stamens has been illustrated in Irwin and Barneby’s (1981) revision of Cassieae, this state has not been observed in the many flowers dissected for ...
Context 5
... leiocarpa (Vogel) J. F. Macbr. is an andromonoecious South American tree species belonging to the caesalpinioid subfamily of the Leguminosae. Caesalpinioideae possesses the greatest floral morphological diversity of the three legume subfamilies (Lewis et al. 2000), comprising taxa with both actinomorphic and zygomorphic flowers, as well as, particularly within tribe Cassieae, drastic reductions in floral organ number (Tucker 1988 b , 1998). This subfamily, which has been described as the most ‘‘taxonomically prob- lematic’’ of the three (Gasson et al. 2003), contains numerous taxa that have not yet been studied in detail but that may provide clues to floral evolution in the Leguminosae. Apuleia leiocarpa is one such taxon. The only member of its genus according to a recent revision (de Sousa et al. 2010), A. leiocarpa has been placed by phylogenetic analyses into the Dialiinae s.l. clade (Doyle et al. 1997; Kajita et al. 2001; Lewis 2005; Bruneau et al. 2008). Dialiinae s.l. is made up of the Cassieae subtribes Dialiinae and Labicheinae, the latter comprising the Australian genera Labichea Gaud. ex DC and Petalostylis R. Br. The clade is united by its cymose inflorescences (except in Labicheinae), wood lacking in vestured pits, and greatly decreased floral organ numbers—all uncommon features in the Caesalpinioideae as a whole. The precise position of Apuleia within Dialiinae s.l. re- mains uncertain (Bruneau et al. 2008), but the phylogenetic analysis of Bruneau et al. (2008), based on matK exon plus 3 9 -trnK and trnL intron sequences, placed Apuleia and Distemonanthus as sister groups with a high degree of confidence. Koeppen (1978) also suggested a close relationship between Apuleia and the monospecific West African genus Distemonanthus Benth. based on similarities in wood anatomy, spe- cifically, in the presence and deposition of silica bodies. Indeed, Koeppen (1978) goes on to note that there are morphological similarities in the leaves, flowers, and fruits of the two species but does not expand on this observation. Andromonoecy, the form of sex expression seen in the genus Apuleia (Arroyo 1981), which produces both staminate and hermaphrodite flowers, is otherwise unknown in the Dialiinae and rare among legumes. It has been found in ; 4000 species of flowering plants belonging to at least 33 families and appears to have evolved independently numerous times (Miller and Diggle 2003). In some species, andromonoecy is brought about by a late-stage suppression of the gynoecium; the organ is formed but ceases growth prior to maturity and appears stunted or underdeveloped at anthesis (Beavon and Chapman 2011). In other species, however, the female organs are simply not initiated (Tucker 1991). No mention is made in the litera- ture as to which of these staminate flower morphologies is seen in Apuleia . Here, flowers were dissected and observed using a stereomicroscope and scanning electron microscopy (SEM) to examine in detail the floral morphology of A. leiocarpa . A comparison is made with other andromonoecious caesalpinioid legumes, and some of the functional implications of sex expression in ZIMMERMAN ET AL.—FLORAL MORPHOLOGY OF the genus are discussed. Similarities and differences with the Dialiinae clade as a whole are also explored. For SEM, flowers were dissected in 70% ethanol and critical- point dried using an Autosamdri-815B critical-point dryer (Tousimis Research, Rockville, MD). Dried material was then mounted onto specimen stubs using clear nail polish, coated with platinum using an Emitech K550 sputter-coater (Emitech, Ashford, UK), and examined using a Hitachi cold-field emis- sion SEM S-4700-II (Hitachi High Technologies, Tokyo). All SEM work was carried out at the Royal Botanic Gardens, Kew. SEM images were edited using Adobe Photoshop CS5. Floral diagrams and formulas were developed following rec- ommendations by Prenner et al. (2010). Specimens examined under the stereomicroscope were removed from herbarium vouchers and rehydrated in boiling water with a small amount of surfactant and then dehydrated through an ethanol series to 80% ethanol, in which they were dissected and observed using a binocular dissecting mi- croscope (Wild Heerbrugg). These dissections were then used to produce the illustrations used in figure 1. Specimens examined were as follows: G.C.G. Argent 6657, State of Mato Grosso, Amarela ̃ o, Brazil, 1968 (MO); P. Fra- gomemi 11642, Rio Grande do Sul, Brazil, 1968 (MO); R.M. Harley & R. Souza 10720, State of Mato Grosso, Brazil, 1969 (K); Heringer et al. 5426, Bacia do Rio Sa ̃o Bartolmeu, fr., Brazil, 1980 (K); B.B. Klitgaard & F.C.P. Garcia 66, State of Bahia, Brazil, 1994 (MO); Pennington and Rowe 172, Pando, Puerto Oro, Bolivia, 1988 (MO); A.G. Ruiz 217-AGR, Loreto, Maynas Province, Peru, 1965 (MO); Sant’Ana et al. 361, State of Bahia, Brazil, 1993 (MO); R. Va ́squez, R. Ortiz and N. Jaramillo 14369, Loreto, Maynas Province, Peru, 1990 (MO); J.L. Zarucchi & C.E. Barbosa 3739, Vichada, Colombia, 1985 (MO). The bisexual flowers of Apuleia leiocarpa tend to occupy the central (terminal) position in a compound dichasium, as well as some of the central positions in higher-order cymes, while the younger lateral flowers are staminate (fig. 1 a ). The more flowers present on an inflorescence, the more likely the occurrence of multiple bisexual flowers. Figure 1 a represents a smaller but common inflorescence size. Phyllomes subtending the central flower are early cadu- cous, leaving visible scars (fig. 1 a ), while those occurring on lateral flowers are minute and ephemeral. On mature inflorescences, the scars, which occur on the lower portion of the pedicel, are very difficult to discern and are therefore not illustrated in figure 1 a but are shown in the floral diagram (fig. 1 b ). Both floral morphs possess a trimerous calyx and corolla (fig. 1 b , 1 c ). In bisexual flowers, the inner whorls consist of a single pistil and two stamens in the adaxial lateral posi- tions, opposite the adaxial lateral sepals, although additional pistils and stamens are occasionally present (figs. 1 c , 1 d , 2 a ). A longitudinal section of a hermaphrodite flower shows that the gynoecium, which consists of a single carpel, is stipitate and arises from the base of a narrow, tubular hypanthium (fig. 2 b –2 d ), while the perianth and androecium arise from the rim of the hypanthium (fig. 3 c ). The carpel encloses up to four narrow, elongated ovules (fig. 2 b ), which are attached with a short funicle to the ovary wall (fig. 2 e ). The stigma is peltate and covered with short papillae (fig. 2 f ). Staminate flowers of A. leiocarpa do not appear to develop either a functional gynoecium or a vestigial gynoecium. Three stamens (rarely four) develop on the rim of the hypanthium, with the third stamen occupying the volume taken up by the gynoecium in the hermaphrodite flower (fig. 1 b , 3 a , 3 c , 3 d ). At the center of the floral surface, a trichome-filled triangular opening leads to the sunken hypanthium (fig. 3 c , 3 e ), although in some flowers, this develops merely as a three-pointed slit (fig. 2 d ). In cross section, the hypanthium appears to be compressed into three nearly separate chambers (fig. 3 e ); no tissue resembling a suppressed gynoecium is apparent. Anthers de- hisce with longitudinal slits (fig. 3 b ) and release tricolporate pollen grains with microreticulate surfaces (fig. 3 f ). The adaxial surface of the anthers is covered with characteristic hooked trichomes (fig. 3 g ). The basic legume flower is thought to be built on a ground plan of a pentamerous calyx and corolla, two pentamerous whorls of stamens, and a unicarpellate gynoecium, for a total of 21 floral organs (Tucker 2003). The subfamily Caesalpinioideae, which forms a basal grade in the Leguminosae, and in particular the tribe Cassieae, shows the greatest and most frequent deviation from this ground plan, both via organ suppression and, less frequently, complete loss (Tucker 2003; Prenner and Klitgaard 2008). The Dialiinae s.l. clade (Bruneau et al. 2001), which is composed of the two Cassieae subtribes Dialiinae and Labicheinae of Irwin and Barneby (1981) plus the genus Poeppigia C. Presl., displays high levels of organ loss, particularly in the androecium. Several species of the genus Dialium L., e.g., possess only eight organs: five sepals, two stamens, and a carpel. While Dialium represents an extreme, very few species in the clade retain a full set of antepetalous stamens, the vast majority having lost this whorl entirely. Apuleia leiocarpa , with its nine remaining organs, seems to share this characteristic of the clade. Occasionally, a second carpel, with or without additional stamens, is present (fig. 1 d ), a phenomenon noted in certain other caesalpinioid genera, such as Bauhinia L. (Tucker 1988 a ), Ceratonia L. (Tucker 1992), and Dialium (Chakravarty 1969). While a unicarpellate bisexual flower bearing three stamens has been illustrated in Irwin and Barneby’s (1981) revision of Cassieae, this state has not been observed in the many flowers dissected for ...
Similar publications
The evolution of floral morphology in the monocot order Zingiberales shows a trend in which androecial whorl organs are progressively modified into variously conspicuous "petaloid" structures with differing degrees of fertility. Petaloidy of androecial members results from extensive laminarization of an otherwise radially symmetric structure. The g...
Citations
... Also, in the mature dry forest of Chamela, Mexico, more than half of the species recorded were hermaphrodites (54 %; Bullock 1985). This representation is explained by the dominance of the Fabaceae family in dry forests; this family is composed of hermaphrodite species (Banda-R et al. 2016), although some species may be in a transitional stage to monoecy (andromonoecious; Ortiz et al. 2003, Nair et al. 2004, Casimiro-Soriguer et al. 2013, Zimmerman et al. 2013). On the other hand, tree composition of hermaphrodites differed greatly between conserved and the other three habitats evaluated, probably due to limitations in dispersal and establishment: in this landscape, 66 % of the hermaphrodite species registered as ≥ 2.5 cm DBH were also found in the seed rain of early successional environments (Martínez-Garza et al. 2011), therefore, they seem to have low dispersal limitation (failure of seeds to reach a site; Terborgh et al. 2011). ...
Background:
Obligate outcrossing species (such as dioecious species) are more vulnerable to habitat fragmentation than self-compatible hermaphrodite trees.
Questions:
What is the effect of restoration intervention in the populations of dioecious, monoecious, and hermaphrodite tree species in permanent agricultural landscapes?
Study site and dates:
8-year-old restoration settings in the seasonally dry tropical forest in Sierra de Huautla Biosphere Reserve, Morelos, Mexico.
Methods:
We measure richness and density of dioecious, monoecious, and hermaphrodite tree species with Diameter at Breast Height ≥ 2.5 cm in perturbed, 8-year-old restoration settings (plantings and natural succession) and conserved habitats.
Results:
Overall habitats, 2,042 trees from 46 species in 18 families were identified; the highest percentage of species and trees were hermaphrodites (63 % of species and 78 % of trees), the lowest percentage of species were monoecious (9 %) and the lowest percentage of trees (10 %) were dioecious. In the plantings were registered the largest number of species (37 species) and in the conserved habitat the largest number of trees (852 trees). Density and richness of dioecious, monoecious, and hermaphrodite species did not differ by habitat, contrary to our predictions. For dioecious trees, the restored and conserved habitats showed similar composition heterogeneity. Composition of hermaphrodites in agricultural landscapes differed the most with the conserved habitat.
Conclusions:
Dioecious and monoecious species are favored in agricultural landscapes due to their use value. Selection of species for restoration plantings should consider sexual systems of trees to recover not only forest structure but also ecosystem function.
... Moreover, they found that staminate flowers of S. berlandieri produced more stamens than did perfect flowers, which differs from our observations of Albizia, which has significantly more stamens in perfect flowers, and Mimosa, with no significant difference. Zimmerman et al. (2013) analyzed the unusual trimerous floral morphology of Apuleia leiocarpa J.F. Macbr., an andromonoecious tree (recently placed in the new subfamily Dialioideae by LPWG (2017)). They found that inflorescences produce about four times as many staminate flowers as perfect flowers per head, an observation at odds with previous studies that found perfect-to-staminate ratios ranging from 2:1 up to 15:1 (cited in Zimmerman et al. 2013). ...
... Zimmerman et al. (2013) analyzed the unusual trimerous floral morphology of Apuleia leiocarpa J.F. Macbr., an andromonoecious tree (recently placed in the new subfamily Dialioideae by LPWG (2017)). They found that inflorescences produce about four times as many staminate flowers as perfect flowers per head, an observation at odds with previous studies that found perfect-to-staminate ratios ranging from 2:1 up to 15:1 (cited in Zimmerman et al. 2013). Moreover, in contrast to previously studied andromonoecious legumes, such as Caesalpinia (Caesalpinioideae), Anthonotha (Detarioideae), and Bauhinia (Cercidioideae), gynoecial development in Apuleia is suppressed early in ontogeny. ...
Although it is yet to be conclusively established, floral features of many legumes of the mimosoid clade suggest the existence of a highly wasteful late-acting form of genetic self-incompatibility. We evaluated the role this may have played in the evolution of aggregated pollen, restricted stigmas, and polycarpelly in these plants by first investigating the reproductive biology of two species from the southeastern United States: Mimosa microphylla and Albizia julibrissin. Insights gained from detailed study of their reproductive biology informed a wider, critical review of reproductive characters in other members of the clade. Descriptions of the flowers and inflorescences of the two southeastern U.S. species fail to define clearly the functional situation, including that both species are andromonoecious. Pollen of M. microphylla is released as tetrads, whereas polyads of 16 pollen grains characterize A. julibrissin. Diameters of the cup-like stigmas are constrained so that typically only one or a few tetrads or one polyad will fit. These features are consistent with a syndrome involving, in its fullest manifestation, low fruit set, restriction of stigmatic surfaces, pollen aggregation, reduction of ovule number, and polycarpelly. We interpret all of these unusual features as adaptations to circumvent a highly wasteful (of pollen and ovules) form of late-acting self-incompatibility in which rejection of self-pollen occurs in the ovary. These adaptations reduce the likelihood of a mixed load of self- and cross-pollen being delivered. Enhanced efficiency of pollen transfer may also contribute to the evolution of aggregated pollen, but this explanation fails to account for the other unusual features of this syndrome.
... Of the 17 genera of Dialioideae, only five have been ontogenetically studied; the addition of two complete series and a broad comparative compilation from the literature and herbarium data will help in the understanding of floral evolution in this group. Zimmerman, Prenner & Bruneau (2013a) presented the final floral developmental stages for Apuleia. The authors pointed out features, such as the absence of carpels primordia in the staminate flowers and the internal division of the hypanthium into three chambers, and also suggested andromonoecy as a strategy for increasing the dispersion of pollen. ...
... Uncinate trichomes, already found by Zimmerman et al. (2013aZimmerman et al. ( , 2013b and Tucker (1998), in the final stages of development of Apuleia and Dialium were observed here on the anthers, filaments and sepals of Apuleia, even at intermediate developmental stages, but were not observed in Martiodendron fluminense, which, like M. elatum and M. mediterraneum, has glabrous anthers. On the other hand, M. excelsum and M. parviflorum have pubescent anthers (Koeppen & Iltis, 1962;Falcão et al., unpubl. ...
... The ontogenetic studies made for the subfamily thus far have shown the absence of organs from initiation as a main developmental pathway to organ and whorl reductions (Tucker, 1998;Zimmerman et al., 2013aZimmerman et al., , 2013b. Inferences relating this character to the 'increasing sterility' hypothesis in the evolution of Dialioideae have been made by Zimmerman et al. (2017). ...
The goal of this study was to better understand the origin and development of flowers and inflorescences in the newly established subfamily Dialioideae, an unusual and morphologically variable clade of Fabaceae due to its varied levels of floral reduction. We present here the complete ontogenetic series for two species characterizing different levels of floral reduction: Apuleia leiocarpa, an andromonoecious species with trimerous flowers; and Martiodendron fluminense, a species lacking the inner whorl of stamens. We also performed a literature review and herbarium specimen survey of the inflorescence and floral morphology of the other 15 genera in Dialioideae. Among the exclusive traits of Apuleia found here are the absence of two sepals and petals from initiation, the simultaneous initiation of the sepals (never before documented for Dialioideae), the absence of carpel initiation in staminate flowers and the formation of the carpel in the staminal whorl of monoclinous flowers, with the presence of a nectariferous hypanthium in both flower types. In Martiodendron the two exclusive traits are the heteromorphic development of stamens of the outer whorl, with the abaxial one being the last to elongate, and the possible initiation of an inner staminal whorl, which stops developing immediately thereafter and is no longer visible at anthesis. Among the potential synapomorphies for the subfamily are the absence of bracteoles and a pair of bracts subtending a triad of flowers or inflorescence axes, the distichous anthotaxy of the thyrsoid inflorescences, the bidirectional initiation of the sepals and the simultaneous initiation of the stamens.
... Staminate flowers are known in some Leguminosae. The most relevant are unisexual flowers of Gleditsia with hairy sepaloid petals and long hypanthium, but they have no more than ten stamens, like several other unisexual or andromonoecious legumes (e.g., Hou et al. 1996;Larsen et al. 1980;Ross 1998;Tucker 2003;Xu et al. 2010;Zimmerman et al. 2013). Polysymmetric polystaminate flowers are present in many mimosoid legumes (currently interpreted as a clade of Caesalpinioideae: LPWG 2017). ...
The late Eocene ambers provide plethora of animal and plant fossils including well-preserved angiosperm flowers from the Baltic amber. The Rovno amber from NW Ukraine resembles in many aspects the Baltic amber; however, only fossilized animals and some bryophytes have yet been studied from the Rovno amber. We provide the first detailed description of an angiosperm flower from Rovno amber. The flower is staminate with conspicuous hypanthium, double pentamerous perianth and whorled androecium of 24 stamens much longer than the petals. Sepals are sparsely pubescent and petals are densely hirsute outside. The fossil shares important features with extant members of Prunus subgen. Padus s. l. (incl. Laurocerasus, Pygeum and Maddenia), especially with its evergreen paleotropical species. It is described here as a new species Prunus hirsutipetala D.D.Sokoloff, Remizowa et Nuraliev. Our study provides the first convincing record of fossil flowers of Rosaceae from Eocene of Europe and the earliest fossil flower of Prunus outside North America. Our record of a plant resembling extant tropical species supports palaeoentomological evidences for warm winters in northwestern Ukraine during the late Eocene, as well as suggesting a more significant role of tropical insects in Rovno amber than inferred from Baltic amber.
... and Cynometra L. (Tucker, 2001) and for Isoberlinia Craib & Stapf ex Holland and Microberlinia Tucker (2002). In the other subfamilies it also appears that they do not overlap, as in Cercis L. (Cercidoideae; Tucker, 1984), in the members of Dialioideae studied so far (see Zimmermann, Prenner & Bruneau, 2013) and in Cassia L., Senna Mill. and Chamaecrista Moench (Tucker, 1996). ...
We evaluated the floral development of Hymenaea verrucosa, the only African species of the genus. This species has unusual floral features, such as a tetramerous calyx, a corolla with three normal and two vestigial petals, and stamens of different sizes. We analysed floral buds and flowers under scanning electron microscopy and light microscopy. The results indicated that sepals initiate helically and the petals initiate simultaneously, but the two abaxial ones develop more rapidly. In the intermediate stage, the abaxial petals stop growing and the three adaxial ones continue to develop until anthesis. Ten stamens of different sizes are distributed in two whorls, in which the antesepalous stamens are initiated before the carpel in a modified unidirectional order and the antepetalous stamens are initiated in a simultaneous order after the carpel. We speculate that the difference in size between the stamens may be related to changes in floral architecture due to the availability of space provided by the abortion of the abaxial petals. The ovary has glandular and non-glandular trichomes that overlie a broad base and a stipe with central insertion. Several secretory structures were found: secretory cavities; papillose phenolic epidermis; mucilaginous idioblasts; secretory trichomes; and an annular nectary. The calyx is tetramerous as result of fusion of the two adaxial sepals. The two vestigial abaxial petals and a more pronounced growth of the abaxial stamens characterize the flower as zygomorphic.
... In Tripetaleia (Ericaceae), the androecium and petals become trimerous as to become spatially accommodated with the ovary (Nishino 1988). Space reduction is responsible for the difference between staminate and pistillate flowers in Apuleia (Leguminosae): the trimerous pistillate flowers have two stamens, while staminate flowers have three stamens, with the abaxial stamen occupying the space of the ovary (Zimmerman et al. 2013). The strict arrangement of eight stamens in Sapindaceae and Tropaeolaceae (Fig. 4g) follows a similar pattern, linked with a trimerous gynoecium. ...
Flower morphology results from the interaction of an established genetic program, the influence of external forces induced by pollination systems, and physical forces acting before, during and after initiation. Floral ontogeny, as the process of development from a meristem to a fully developed flower, can be approached either from a historical perspective, as a "recapitulation of the phylogeny" mainly explained as a process of genetic mutations through time, or from a physico-dynamic perspective, where time, spatial pressures, and growth processes are determining factors in creating the floral morphospace. The first (historical) perspective clarifies how flower morphology is the result of development over time, where evolutionary changes are only possible using building blocks that are available at a certain stage in the developmental history. Flowers are regulated by genetically determined constraints and development clarifies specific transitions between different floral morphs. These constraints are the result of inherent mutations or are induced by the interaction of flowers with pollinators. The second (physico-dynamic) perspective explains how changes in the physical environment of apical meristems create shifts in ontogeny and this is reflected in the morphospace of flowers. Changes in morphology are mainly induced by shifts in space, caused by the time of initiation (heterochrony), pressure of organs, and alterations of the size of the floral meristem, and these operate independently or in parallel with genetic factors. A number of examples demonstrate this interaction and its importance in the establishment of different floral forms. Both perspectives are complementary and should be considered in the understanding of factors regulating floral development. It is suggested that floral evolution is the result of alternating bursts of physical constraints and genetic stabilization processes following each other in succession. Future research needs to combine these different perspectives in understanding the evolution of floral systems and their diversification.
... In some species, e.g., Gleditsia triacanthos L. (Tucker, 1991) and Apuleia leiocarpa (Vogel) J.F. Macbr. (Zimmerman et al., 2013), female reproductive organs are completely absent in male flowers. In others, the gynoecium is progressively limited in response to mineral nutrition, water availability, or overall fruit set on the plant (Gibbs et al., 1999;Zimmerman et al., 2013;Beavon and Chapman, 2011). ...
... (Zimmerman et al., 2013), female reproductive organs are completely absent in male flowers. In others, the gynoecium is progressively limited in response to mineral nutrition, water availability, or overall fruit set on the plant (Gibbs et al., 1999;Zimmerman et al., 2013;Beavon and Chapman, 2011). In the former case, andromonoecy may be genetically pre-determined, while in the latter case ontogenetic changes later in development may limit gynoecial development. ...
Passiflora incarnata is a functionally andromonoecious clonal wildflower, native to the southeastern United States, whose primary pollinator is the carpenter bee, Xylocopa virginica. While recent studies looking at reproductive ecology in P. incarnata have classified flowers as one of two morphs (male or hermaphroditic) based on stylar deflexion, preliminary field studies conducted in Tennessee indicated there were five distinct morphs present (three male, two hermaphroditic), supported by stylar deflexion, floral size, and pistil development. The present study sought to test the hypothesis that five distinct floral morphs are present in P. incarnata by sampling 13 floral characters, and to document variation in nectar constituents, volume, and concentration across the five morphs. Five well-established individual plants were examined at three sites in Cookeville, Tennessee. Two-factor permuted analysis of variance of 13 floral characteristics with floral morph and individual plants as factors suggested that morph:plant interactions explained 6%, individual plant explained 18%, and floral morph explained 36% of variation in floral characteristics. Nectar sampling indicated that all morphs produced nectar comprised exclusively of sucrose. Nectar volume generally increased with floral morph size, while nectar concentration decreased. NMDS analysis indicated that four of the five hypothesized morphs were supported as distinct, with morphs 4a and 4b best classified as submorphs due to substantial overlap. The supported morphs are best distinguished by ovary width, ovary length, style length, and stigma width. These findings support a hypothesis that the morphs result from variation in developmental arrest during floral ontogeny. The ecological implications of the morphs and nectar variation are considered for X. virginica with suggestions for additional studies.
... Andromonoecy (i.e. the coexistence of hermaphrodite and male flowers on the same plant) can arise at different stages of development. It may arise early by the lack of female organ initiation (Zimmerman et al., 2013) or late by the suppression of the gynoecium (Beavon and Chapman, 2011;Ajani et al., 2016). As developmental studies are lacking, it will be interesting to compare the developmental pathways of hermaphrodite and male flowers in Cruciata. ...
... On the other hand, early determination of sexual morphs has also been reported (e.g. Apuleia in the Leguminosae; Zimmerman et al., 2013), suggesting that andromonoecy in the respective species is an evolutionarily stable strategy and insen-sitive to environmental factors. It is thus obvious that different evolutionary forces are involved in andromonoecy. ...
The Rubiaceae is characterized by considerable diversity in floral features. To shed light on the variation of floral developmental patterns in Rubiaceae, a comparative study was carried out on pentamerous flowers of Rubia tinctorum L. and tetramerous flowers of Cruciata (Cruciata laevipes Opiz.; Cruciata glabra (L.) Ehrend.), two herbaceous genera of the tribe Rubieae. We aim to study the mechanism responsible for meristic variation and to discuss the expression of andromonoecy in C. laevipes. Developmental peculiarities include the time overlap in the initiation of petal and stamen whorls in Cruciata, the lack of calyx, and a very weak sympetaly in all species examined. Our results show that changes in initial meristem size can play a significant role in meristic variation. The late expression of gender differentiation in C. laevipes may be an explanation for the plasticity of andromonoecy in response to the environmental changes.
... Trimerous flowers of Apuleia leiocarpa J.F. Macbr. (Leguminosae) also arise as a result of a reduction from a monosymmetric flower (Zimmerman et al., 2013). An increase of the merism of the perianth will generally not happen without affecting the androecium, contrary to the gynoecium ( Fig. 3d; Table 2). ...
... As noted by previous authors (Chakravarty, 1969;Tucker, 1998) and by ourselves with respect to Apuleia (Zimmerman et al., 2013), it is not uncommon in Dialiinae for flowers to develop extra organs in any of their whorls. Here, we have found extra sepals and carpels in D. orientale, as well as extra stamens in D. orientale and D. pentandrum. ...
... Among Dialiinae, synchronous petal formation was also reported for P. labicheoides (Tucker, 1998). Outside the clade, synchronous organ formation is frequently seen in mimosoids (Ramirez-Domenech and Tucker, 1990) and was also found in the sepals (Prenner, 2004d) and in the petal whorl of some papilionoids such as Daviesia cordata (Prenner, 2004a) and Lespedeza thunbergii (Prenner, 2004c; for more examples, see also Table 1 in Prenner, 2013). This shows that synchronous organ formation is a repeatedly occurring theme among legumes which is found more frequently in some groups than in others. ...
... Tucker (1988) notes that cases of outright loss are most prevalent in caesalpinioids, and in particular in various Cassieae groups and in tribe Detarieae. Among papilionoid legumes, organ loss can also be found in Dalea candida (Amorpheae), in which the inner stamen whorl is lost (McMahon and Hufford, 2002) and in Abrus precatorius, in which the adaxial stamen of the inner whorl is lost (Prenner, 2013). These anomalous cases show that while ontogenetic themes such as organ loss seem to occur more frequently in caesalpinioids, they also occur sporadically in the other two subfamilies. ...
The Caesalpinioideae are widely variable in their floral ontogeny, and among caesalpinioids, members of the polyphyletic tribe Cassieae are particularly diverse. Within the Cassieae, the monophyletic Dialiinae clade is also marked by a high degree of organ loss, particularly in the largest genus, Dialium. The purpose of this work is to explore the ontogeny of several previously undocumented species of the diverse Dialiinae clade, with the goal of building amore complete picture of floral development and evolution in this group and especially within Dialium. We have documented the floral ontogeny of six species of the Dialiinae; four from Dialium, aswell as Poeppigia procera andMendoravia dumaziana.Mode and timing of organ initiation weremostly consistent across the Dialium species studied. With the exception of Dialium dinklagei, which undergoes helical calyx initiation, all flowers initiated sepals bidirectionally. In the instances of both gains and losses of floral organs in Dialium, one trend is apparent — an absence of abaxial organs. Gains in both sepals and stamens occur in the adaxial median position, while stamens and petals which are lost are always the ventral-most organs. Organ initiation in Poeppigia and Mendoravia is unlike that seen in Dialium. Poeppigia shows a ventral to dorsal unidirectional sepal initiation, while both Poeppigia and Mendoravia display near-synchronous initiation of the corolla and staminal whorls. The taxa examined here exemplify the apparent lack of developmental canalisation seen in caesalpinioid legumes. This ontogenetic plasticity is reflective of the morphological diversity shown by flowers across the subfamily, representing what has been described as an “experimental” phase in legume floral evolution.
