Stigma diversity in tropical legumes with considerations on stigma classification.
IntroductionThe stigma is a specialized region, usually located at the carpel apex, variable in shape, size and cell composition (Gifford & Foster, 1989; Fahn, 1990; Raghavan, 1997). It plays a key role in adhesion, recognition and germination of the pollen grain (Maheshwari, 1950; Went & Willemse, 1984; Fahn, 1990; Weberling, 1992; Richards, 1997; Lord & Russell, 2002; Cocucci & Mariath, 2004; Beck, 2005). Stigmatic characteristics, such as shape, occurrence of secretory cells, presence and chemical nature of exudate, and the presence of physical barriers, such as the cuticle and protein pellicle, are important and should be considered in the processes of pollen-pistil interaction (Heslop-Harrison & Shivanna, 1977; Edlund et al., 2004).
The stigma morphology in angiosperms is very diverse, and several studies have described anatomical stigmatic features (see Bell & Hicks, 1976; Dumas et al., 1978; Tilton & Homer, 1980; Heslop-Harrison et al., 1981; Owens & Horsfield, 1982; Verkerke, 1989; Lavin & Delgado, 1990; Owens, 1990; Scribailo & Barrett, 1991; Souza & Moscheta, 1999; Ciampolini et al., 2001; Sanzol et al., 2003; Souza et al., 2003; Sigrist & Sazima, 2004; Spinelli et al., 2005; Carmo-Oliveira & Morretes, 2009; Sage et al., 2009).
Such morphological diversity implies a choice of criteria for stigma classification, such as the shape of stigma lobes, the occurrence of papillae, trichome and exudate (wet or dry stigmatic surface) (Raspail, 1824; Hartig, 1842; Capus, 1878). The broad classification of stigma characterized it as dry (= little or no secretory surface and exudate retained by the cuticle and/or protein pellicle) or wet (= conspicuous secretory surface, and abundant and fluid exudate). In both types of stigma subdivisions based on the arrangement and shape of cells composing the stigmatic surface still occur (Heslop-Harrison & Shivanna, 1977).
Although most studies have followed Heslop-Harrison and Shivanna (1977) for the classification of stigma as wet or dry, further studies increasingly detailed stigmatic morphology and have added other criteria. For example, the chemical nature of the exudate enables the classification of stigma as dry, when exudate is viscous, mainly composed of waxes and proteins, and as wet when exudate is fluid, consisting of lipids, polysaccharides and polyphenols (Dumas, 1978). The observation of intermediate characteristics between the dry and wet stigma types (Heslop-Harrison, 1981; Hiscock, 2000) even led to the adoption of the term "semidry" (Hiscock et al., 2002). Such a stigma has been characterized as having secretory cells, exudate retained by cuticle and/or protein pellicle, which can be ruptured by pressure exerted by exudate or by some physical friction (Heslop-Harrison & Heslop-Harrison, 1983; Lord & Heslop-Harrison, 1984; Tilton et al., 1984).
Among the families studied in terms of stigma morphology, Leguminosae should be emphasized due to its species richness (about 19,000) and great floral diversity (Lewis et al., 2005). The stigma of their representatives has been classified as wet (Heslop-Harrison & Shivanna, 1977) or semidry (Basso-Alves et al., 2011), with no reports of dry-type stigma.
With the goal of checking the stigma morphological diversity in Leguminosae and to evaluate the criteria used in the main classifications of stigma, we compared the stigma morphology in 15 distinct legume lineages.
Materials and Methods
The species examined (Table 1) were included in tribes according to Lewis et al. (2005). Scientific names were confirmed in Tropicos.org (07 Dec. 2012).
Ten floral buds at a stage immediately prior to the anthesis (preanthesis) and ten flowers (anthesis) were used for each species. Fresh materials were observed and dissected on a stereomicroscope and the stigmas removed and fixed for 24 h in buffered formalin (Lillie, 1954) or in Karnovsky solution in 0.075 M phosphate buffer (pH 7.2-7.4) (Karnovsky, 1965).
For stigmatic surface analyses (scanning electron microscopy), the materials were dehydrated in an ethanol series, critical point-dried with liquid C02 in a Bal-Tec CPD 030 apparatus, mounted on aluminum stubs with colloidal carbon, and coated with gold in a Bal-Tec SCD 050 sputter-coater. Observations and images were obtained with Jeol JSM 5200, Jeol JSM 5800LV and Shimadzu SS-550 scanning electron microscopes.
For anatomical analyses and tests for histolocalization of substances (light microscopy), 1.5 to 3 pm thickened longitudinal sections were obtained from samples gradually dehydrated in an ethanol series, embedded in historesin (Gerrits, 1991), and sectioned using a Leica RM 2245 rotary microtome. To obtain 0.5 [micro]m thickened sections, samples were post-fixed in 1 % osmium tetroxide in 0.075 M phosphate buffer (pH 1.2-1 A) for 1 h, gradually dehydrated in an acetone solution, embedded in Araldite 6005 and sectioned using a Leica Reichert Ultracut S ultramicrotome. The anatomical sections were stained with 0.05 % Toluidine blue (O'Brien et al., 1964), Sudan Black B to detect lipids (Jensen, 1962), PAS reagent to detect polysaccharides (O'Brien & McCully, 1981), Aniline Blue Black (Fisher, 1968) and Xylidine Ponceau (Vidal, 1970) to detect proteins. The images were obtained with a Leica DM 5000 B light microscope coupled to a Leica DFC 295 digital camera, with the scale bars at the same optical conditions.
Results
The stigma of the 15 study legumes exhibits quite variable morphology, mainly concerning the diameter, the occurrence of an orifice or a furrow, the coating, the cellular composition, and the occurrence, chemical nature and release mechanism of the exudate (Table 2).
Regarding the stigma diameter vs. diameter of the style apical portion, we found stigma with greater diameter in Bauhinia curvula (Fig. 1a), Hymenaea courbaril (Fig. 1b), Caesalpinia echinata (Fig. 1c), Indigofera lespedezioides (Fig. 1d), Desmodium incanum (Fig. 1e) and Gliricidia sepium (Fig. If); stigma with smaller diameter in Cassia grandis (Fig. 2a), Senegalia polyphylla (Fig. 2b), Swartzia dipetala (Fig. 2c), Taralea oppositifolia (Fig. 2d) and Platycyamus regnelli (Fig. 2e); and stigma with equal diameter in Parkia pedula (Fig. 2f), Inga congesta (Fig. 2g), Crotalaria lanceolata (Fig. 2h) and Tipuana tipu (Fig. 2i). Stigmas larger than 1,000 [micro]m in width are found in Bauhinia curvula (Fig. 1a) and Hymenaea courbaril (Fig. 1b), between 500 and 1,000 [micro]m in Caesalpinia echinata (Fig. 1c) and Cassia grandis (Fig. 2a), and smaller than 500 [micro]m in the other species (Figs, 1d-f and 2b-i, Table 2).
The stigma exhibits a furrow in Bauhinia curvula (Fig. 1a), Hymenaea courbaril (Fig. 1b) and Tipuana tipu (Fig. 3b), and a round and central orifice in Caesalpinia echinata (Fig. 1c), Cassia grandis (Fig. 2a), Senegalia polyphylla (Fig. 2b), Parkia pendula (Fig. 2f), and Inga congesta (Fig. 2g).
A thin cuticle covers the stigma in all species (Fig. 3), except Hymenaea courbaril, in which cuticle is thick at the papillae apex (Fig. 4b). Disrupted cuticle was observed in Bauhinia curvula, Hymenaea courbaril, Caesalpinia echinata, Parkia pendula, Inga congesta, Taralea oppositifolia and Crotalaria lanceolata by means of slits (Fig. 1c, window) or pores (Fig. 2d). In other species (Cassia grandis, Swartzia dipetala, Tipuana tipu, Indigofera lespedezioides, Platycyamus regnelli, Desmodium incanum and Gliricidia sepium), the cuticle remains continuous up to anthesis (Figs. 3a, d and 4c, d). Epicuticular protein pellicle was observed only in Caesalpinia echinata (Fig. 4e), Swartzia dipetala and Taralea oppositifolia.
The stigmatic surface is composed of unicellular simple short trichomes in Hymenaea courbaril (Figs, 1b and 4b); papillose cells in Bauhinia curvula (Figs, 1a and 4a), Caesalpinia echinata (Fig. 1c, window), Gliricidia sepium (Fig. 1f), Taralea oppositifolia (Fig. 2d), Swartzia dipetala (Fig. 3a), Tipuana tipu (Fig. 3b), Indigofera lespedezioides (Fig. 3c), Desmodium incanum (Fig. 3d), and Platycyamus regnelli (Fig. 4c); prismatic cells in Cassia grandis (Fig. 3f), Parkia pendula (Fig. 3g), Senegalia polyphylla (Fig. 3h), and Inga congesta (Fig. 3i). Cuticularized simple trichomes are observed on the stigma margin in Caesalpinia echinata (Fig. 1c), Indigofera lespedezioides (Fig. 1d), Desmodium incanum (Fig. le), Cassia grandis (Fig. 2a), Platycyamus regnelli (Fig. 2e), and Crotalaria lanceolata (Fig. 2h).
The stigmatic cells have conspicuous and central nucleus, densely stained cytoplasm and numerous small vacuoles (Fig. 3g-i). Cells with phenolic content were found in Bauhinia curvida (Fig. 4a) and Hymenaea courbaril (Fig. 4b, f). In most species the cells of the stigma are exposed at anthesis, except in Caesalpinia echinata (Fig. 1c), Cassia grandis (Figs. 2a and 3f), and Parkia pendula (Figs. 2f and 3g), in which such cells are hidden in a stigmatic cavity.
The stigma is secretory (Table 2), except in Cassia grandis, (Fig. 3f), Senegalia polyphylla (Fig. 3h) and Caesalpinia echinata (Fig. 4e), species in which exudate was not detected in either the preanthesis and anthesis stage. The stigmatic exudate can be fluid on the surface in Crotalaria lanceolata, Bauhinia curvula (Fig. 4a), Hymenaea courbaril (Fig. 4f), Parkia pendula (Fig. 3g, and 4g), Inga congesta (Figs. 3i and 4h) and Taralea oppositifolia (Fig. 4i) or remain retained under the cuticle in Swartzia dipetala (Fig. 3a), Tipuana tipu (Fig. 3b), Indigofera lespedezioides (Fig. 3c), Desmodium incanum (Fig. 3d), Platycyamus regnelli (Fig. 4c) and Gliricidia sepium (Fig. 4d).
The exudate is predominantly lipid in Parkia pendula, Inga congesta, Swartzia dipetala, Taralea oppositifolia and Gliricidia sepium', protein in Crotalaria lanceolata', lipoprotein in Bauhinia curvula, Hymenaea courbaril, Indigofera lespedezioides and Desmodium incanum', and composed of lipids and polysaccharides in Tipuana tipu and Platycyamus regnelli (Table 2). The release of the exudate is holocrine in Swartzia dipetala (Fig. 3a), Indigofera lespedezioides (Fig. 3c), Desmodium incanum (Fig. 3d), Crotalaria lanceolata (Fig. 3e), Bauhinia curvula (Fig. 4a), Hymenaea courbaril (Fig. 4f), Inga congesta (Fig. 4h) and Taralea oppositifolia (Fig. 4i) and merocrine in Tipuana tipu (Fig. 3b), Platycyamus regnelli (Fig. 4c), Gliricidia sepium (Fig. 4d) and Parkia pendula (Figs. 3g and 4g).
Discussion
Stigma Diversity
Tropical legume flowers exhibited enormous diversity in stigma morphology (see Tables 2 and 3), probably related to the evolutionary history of the group and also to the selective pressure exerted by pollen and pollinators (see Tucker, 1996 and Dulberger et al., 1994).
The wet and semidry types of stigma are predominant in Leguminosae. Most caesalpinoids and mimosoids present wet stigma (see Fig. 5) and most papilionoids present semidry stigma with one reversion to wet condition in Crotalaria (see Fig. 6). The wet stigma seems to be a plesiomorfic character-state whereas the dry and semidry stigmas arose later (see Figs. 5 and 6). The dry stigma arose independently at least in two genera (Cassia and Senegalia) included in different subfamilies (Caesalpinioideae and Mimosoideae, respectively) (see Fig. 5). Only in hardly circumscribed groups as Caesalpinia and Acacia (Lewis et al., 2005) we can found two types of stigma (see Fig. 5), which confirms the taxonomic importance of stigma type. Whether these groups can be characterized by the type of stigma still remains on debate.
According to Dulberger et al. (1994), this large variation in stigmatic features may function as isolating mechanisms between sympatric, visitor-sharing, and concurrently blooming species. Most mellitophilous papilionoids, for example, exhibited stigma with thin and continuous cuticle (see Table 1), which can be ruptured by bees in their visits to flowers exposing the stigmatic surface or the exudate, depending on the species (see Table 2). These features were reported in Trifolium pratense (Heslop-Harrison & Heslop-Harrison, 1983), Vicia faba (Lord & Heslop-Harrison, 1984), Glycine max (Tilton et al., 1984), Cytisus striatus, Retama sphaerocarpa (Rodriguez-Riano et al., 1999), Macroptilium bracteatum, Phaseolus augusti, P. vulgaris, Vigna adenantha (Sovema et al., 2003), Cytisus multiflorus (Rodriguez-Riano et al., 2004), Vigna caracalla (Etcheverry et al., 2008) and Anagy'ris foetida (Valtuena et al., 2008). In the chiropterophilous species studied here the large size stigma of Hymenaea courbaril flower (approximately 1,000 [micro]m, see Table 2) and the large and conspicuous head-like inflorescences of Parkia pendula, with about 1,300 flowers (Hopkins, 1984; Fleming et al., 2009; Oliveira et al., 2006), could be related to the large size of the pollinator. Buzz-pollinated caesalpinoids, such as Cassia grandis (present study) and other members of the subtribe Cassiinae, tribe Cassieae (Dulberger et al., 1994; Tucker, 1996; Marazzi et al., 2007, Arceo-Gomez et al., 2011), share the tubular type of stigma. The majority of study species in this group also exhibits wet stigma (Owens & Lewis, 1989), suggesting that the mechanism of buzz-pollination is related to the type of stigma (wet, dry or semi-dry). However we found a stigma of the dry type in Cassia grandis (see Table 2), indicating that buzz-pollination is rather related to the stigma form and pollen release, caption and deposition on stigma, as previously discussed in Chamaecrista chamaecristoidis (Arceo-Gomez et al., 2011).
Pollen-stigma relationship can be well illustrated in mimosoids since the presence of orifices and furrows on the stigma allows the storage and protection of pollen grains usually grouped into a polyad (16 to 32 grains per polyad), able to fertilize all embryonic sacs in an ovary (Koptur, 1984; Pennington, 1997). Interestingly, even in caesalpinoids, which have no grouped pollen grains, orifices and furrows on the stigma may be related to the large size of pollen grains, ranging from 50 [micro]m in Caesalpinia echinata (Teixeira et al., 2008) and Cassia grandis (Marques-Souza et al., 2002) to 100 [micro]m in Bauhinia curvula (S.P. Teixeira, pers. obs.).
Remarkable Stigmatic Features
It is noteworthy that stigma of all legumes in this study is covered by a cuticle; this structure, however, is poorly described and even disregarded in the literature. This is probably due to the timing of stigma analysis (anthesis, preanthesis) or the presence of an abundant exudate on the stigma surface, which could mask the presence of the cuticle. Thus, it is difficult to know whether a non-cuticularized stigma does exist, especially when stigma is classified as wet.
The cuticle disruption by tears or pores, observed in eight legume species (see Table 2), is likely related to the retaining and slow release of exudate, exposed only at the time of anthesis, ensuring that the stigma becomes receptive up to the time of pollen grain deposition. Other expected functions assumed by the cuticle could be protection against desiccation of the stigmatic exudate or even to the secretory cells in the process of production and release of exudate. Desiccation of stigmatic surface is more pronounced in species occurring in open and dry environments, such as Indigofera lespedezioides, Desmodium incanum and Gliricidia sepium (see Table 1); in these species cuticle is continuous and retains the exudate even during the anthesis (see Table 2). In the night-pollinated and savannic Bauhinia curvula and Hymenaea courbaril (see Table 1), the exudate is exposed by cuticle disruption at night, when the temperatures are milder and relative humidity is higher (see Table 2), avoiding risk of dehydration. In addition, in the wet Tropic species, concealment of exudates can prevent its washing away or dilution by rain (Tucker, 1996).
The simple trichome bordering stigma surface is another interesting structure that seems to assist in the cuticle disruption and even protect the stigma surface by restricting the total exposed area, found in six independent lineages of legumes (see Table 2 and Fig. Id). Another function assigned to this type of trichome is the retention of pollen grains during the preanthesis allowing a later exposure (Westerkamp & Weber 1999). This mechanism, termed secondary pollen presentation, is generally observed in papilionoids (Lavin & Delgado, 1990; Ladd, 1994; Westerkamp & Weber, 1999; Galloni et al., 2007; Etcheverry et al., 2011), and described in some genera addressed here as Cassia (Westerkamp, 2004), Crotalaria (Lavin & Delgado, 1990), Desmodium and Indigofera (Etcheverry et al., 2011). Interestingly to note that most legumes exhibiting secondary pollen presentation also exhibit semidry stigma, suggesting a possible relationship. However, representatives of other families presenting secondary pollen presentation (Howel et al., 1993) exhibit dry (Campanulaceae, Goodeniaceae, Myrtaceae, Polygalaceae, Proteaceae and Rubiaceae), wet (Araceae, Campanulaceae, Myrtaceae and Rubiaceae) (Heslop-Harrison & Shivanna, 1977), or semidry (Asteraceae) (Hiscock, 2000; Hiscock et al., 2002) types of stigma. Guiding the pollen tubes to the style is another function reported for stigma trichomes in literature (Lersten, 2004).
The stigmatic exudate plays an important role in the rehydration of the pollen grain, especially in those long-lived grains, classified by Pacini and Hesse (2004), Pacini et al. (2006) and Pacini (2010) as orthodox, which suffer great dehydration at the time of anther ripening and are commonly found in tropical species. Interestingly, no exudate was found in Caesalpinia echinata, Cassia grandis and Senegalia polyphylla stigmas, contradicting the wide classification of legume stigma as wet (Heslop-Harrison & Shivanna, 1977; Owens, 1990).
Stigma and Breeding Systems
The different types of stigma have been related with particular breeding systems (Endress, 1994; Heslop-Harrison & Shivanna, 1977). The dry type of stigma seems to be related to the sporophytic self-incompatibility systems, and the wet type of stigma to the gametophytic systems. This relationship is hardly found in Leguminosae based on the fact that self-incompatibility is spread in the three subfamilies (see Baker & Harris, 1957; Arroyo, 1981; Koptur, 1984; Bawa et al., 1985). If we attend to the investigated species here, apart from self-incompatible species (Bauhinia curvula--Munin et al., 2008; Cassia grandis--Agostini & Sazima, 2003; Caesalpinia echinata--Borges et al., 2009; Hymenaea courbaril--Bawa, 1974; and Indigofera lespedezioides--pers. obs.), we can also found self-compatible species in genera as Arachis, Stylosanthes (Arroyo, 1981), Dahlstedtia (Teixeira et al., 2001), Crotalaria (Jacobi et al., 2005), Anagyris (Valtuena et al., 2008), Trifolium (Speroni et al., 2009) and Desmodium (Etcheverry et al., 2010). Future experimental studies should be carried on legumes to better check whether there is a relationship between incompatibility mechanism and stigma type.
Stigma and Mechanisms Avoiding Self-pollination
The semidry type of stigma found in papilionoids (see Table 3) is probable involved in mechanisms that avoid self-pollination. The simple trichomes around the stigma and the stigmatic cuticle represent a physical barrier avoiding the contact among flower's own pollen and the stigma (see examples above on "Stigma diversity"). Whether any contact occurs between the pollen and stigma, chemical mechanisms may promote the recognition or inhibition of the pollen grains of the same flower (Silva & Goring, 2001; Nasrallah, 2002; Hiscock & McInnis, 2003; Nasrallah, 2005; Mcclure & Franklin-Tong, 2006), but rather at style or ovary levels than at stigma in case of legume species. The follow species illustrated this phenomenon: Acacia retinodes (Gibbs & Bianchi, 1999), A. Senegal (Tandon et al., 2001), Adenocarpus complicatus, Caesalpinia calycina, C. eriostachys, Calliandra calothyrsus, Cytisus grandiflorus, C. multiflorus (Gibbs & Bianchi, 1999; Rodriguez-Riano et al., 2004), Dalbergia retusa (Seavey & Bawa, 1986), D. miscolobium (Gibbs & Sassaki, 1998), Dipteryx odorata (Maues et al., 2004). D. panamaensis (Seavey & Bawa, 1986), Genista hirsuta (Gibbs & Bianchi, 1999), Hymenaea stigonocarpa (Gibbs et al., 1999), Lotus corniculatus, Medicago sativa, Myrospermum frutescens (Gibbs & Bianchi, 1999), Myrospermum pubescens (Seavey & Bawa, 1986), Strongylodon macrobotrys, Swartzia apetala (Gibbs & Bianchi, 1999).
Other mechanisms avoiding self-pollination as spatial separation (herkogamy) and temporal separation (dichogamy) (Barrett, 2003; Webb & Lloyd, 1986; Lloyd & Webb, 1986) are hardly related to the stigma type in legumes in part due to the few experimental studies found in literature for this group. Examples of herkogamic legumes are Hymenaea courbaril (Bawa, 1974), Bauhinia curvula (Munin et al., 2008) and Trifolium polymorphum (Speroni et al., 2009); and dichogamic legumes are Acacia conferta, A. dealbata, A. iteaphylla, A. mearnsii, A. retinodes, A. subulata (Kenrick & Knox, 1981), A. Senegal (Tandon et al., 2001), Pseudopiptadenia contorta, P leptostachya (Pires & Freitas, 2008), Bauhinia championii, B. corymbosa and B glauca (Lau et al., 2009).
Stigma Classification
The proposed classifications to define the types of stigma (compare Heslop-Harrison & Shivanna, 1977; Dumas, 1978; Heslop-Harrison, 1981; Hiscock, 2000; Hiscock et al., 2002) are polarized into dry and wet, with varying criteria for classification according to each author. More conflicting criteria are used to define the semidry type, exemplified in species of most tribes of Papilionoideae (see Table 3) and detailed in Trifolium pratense (Heslop-Harrison & Heslop-Harrison, 1983), Vicia faba (Lord & Heslop-Harrison, 1984), Glycine max (Tilton et al., 1984), Erythrina, Macroptilium and Mucuna species (Basso-Alves et al., 2011).
The first finding of stigma having intermediary characteristics of both dry and wet types (Heslop-Harrison, 1981) did not prevent subsequent studies in Leguminosae from continuing to classify stigma as wet (see Table 3), following Heslop-Harrison and Shivanna (1977). It was only in 2002 that Hiscock et al. named this type of stigma as semidry in some species of Asteraceae, whose main criterion employed, i.e., the presence of an exudate retained by a continuous cuticle (Hiscock, 2000; Hiscock et al., 2002), enabled authors to utilize the new proposed term in legumes (see Basso-Alves et al., 2011).
Another criterion that generates conflicts in stigma classification is the phase chosen to perform the analysis. Most studies describing the stigma at the time of anthesis (see Table 3 for references), when the cuticle is often already broken and exudate exposed or drained. Also, we must consider that there are differences in the timing of release of exudate into the extracellular environment and that exudate may already fill the intercellular spaces and be retained by the cuticle at the time immediately prior to anthesis. More detailed studies in the secretory process (sensu Fahn, 1979) of stigma during late floral stages of development would improve the level of description and also the classification of the stigma in angiosperms.
In conclusion, our data indicate that the stigma should be classified into dry, semidry and wet and we propose to standardize the stigma classification as follow: dry stigma if there is no exudate at preanthesis or anthesis; wet stigma if there is free flowing exudate at preanthesis or anthesis; and semidry stigma if there is exudate contained by a continuous cuticle covering the stigmatic surface, at either preanthesis or antesis. Thus, for an accurate stigma classification we should take into account morphology, floral phase, and exudates analyses, employing techniques for surface study under stereomicroscopy and scanning electron microscopy, and for anatomical and chemical studies under light microscopy. For the next researches, it would be interesting to convert stigma size and shape, for example, into continuous variables which could allow a more confident stigma classification.
DOI 10.1007/s 12229-014-9131-5
Acknowledgments We thank to Fundacao de Amparao a Pesquisa do Estado de Sao Paulo (process numbers 2002/11834-5, 2008/57487-0 and 2009/01057-0), Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (process numbers 142876/2008-9, 301960/2009-7 and 152759/2010-7), and Coordenaqao de Aperfeiqoamento de Pessoal de Nivel Superior (Proex) for financial support; Edmarcio S. Campos (FCFRP/USP), Maria Dolores S. Ferreira (FMRP/USP), Paulo D. Frighetto (FMRP/USP), Rodrigo F. Silva (FFCLRP/USP) and Adriane C, S, Sprogis (IB/UN1CAMP) for technical assistance; and Dewey Litwiller (University of Saskatchewan, Saskatoon, Saskatchewan, Canada) for English review.
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Marina Fernanda Bortolin Costa (1,3) * Juliana Villela Paulino (2,3) * Cristina Ribeiro Marinho (1,3) * Viviane Gonsalves Leite (2,3) * Giseli Donizete Pedersoli (2,3) * Simone Padua Teixeira (3,4)
(1) Programa de Pos-Graduacao em Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, Sao Paulo, Brazil
(2) Programa de Pos-Gradua<;ao em Biologia Comparada, Faculdade de Filosofia, Ciencias e Letras de Ribeirao Preto, Universidade de Sao Paulo, Av. Bandeirantes 3900, 14040-901 Ribeirao Preto, Sao Paulo, Brazil
(3) Departamento de Ciencias Farmaceuticas, Faculdade de Ciencias Farmaceuticas de Ribeirao Preto, Universidade de Sao Paulo, Av. do Cafe, s/n, Ribeirao Preto, Sao Paulo 14040-903, Brazil
(4) Author for Correspondence; e-mail: spadua@fcfrp.usp.br
Published online: 25 February 2014
Table 1 Information of studied legume species
Species Subfamily Tribe Collect site
(24) Bauhinia C Cercideae Campo Grande,
curvula Benth. MS, Brazil
(7,18) Hymenaea C Detarieae Ribeirao Preto,
courbaril L. SP, Brazil
(1,19) Cassia C Cassieae Ribeirao Preto,
grandis L. f. SP, Brazil
(4,19) Caesalpinia C Caesalpinieae Ribeirao Preto,
echinata Lam. SP, Brazil
(11,9) Parkia pendula M Mimoseae Rio de Janeiro,
(Willd.) Benth. ex Walp. RJ, Brazil
(19,25) Senegalia M Acacieae Ribeirao Preto,
polyphylla (DC.) Britton SP, Brazil
(2,13) Inga congesta M Ingeae Niteroi, RJ,
T. D. Penn. Brazil
(8,12,22) Swartzia P Swartzieae Ilheus, BA,
dipetala Willd. ex Vogel Brazil
(28) Taralea P Dipterygeae Belem, PA,
oppositifolia Aubl. Brazil
(14,16) Crotalaria P Crotalarieae Campinas, SP,
lanceolata E. Mey. Brazil
(6,21) Tipuana tipu P Dalbergieae Ribeirao Preto,
(Benth.) Kuntze SP, Brazil
(3,10,23) Indigofera P Indigofereae Ribeirao Preto,
lespedezioides Kunth SP, Brazil
(5,20) Platycyamus P Millettieae Ribeirao Preto,
regnelli Benth. SP, Brazil
(9,16,27) Desmodium P Desmodieae Ribeirao Preto,
incanum (SW.) DC. SP, Brazil
(15,17,26,29) Gliricidia P Robinieae Ribeirao Preto,
sepium (Jacq.) Kunth SP, Brazil
ex Walp.
Species Voucher Flabitus
(24) Bauhinia S.P. Teixeira et al. subshrub
curvula Benth. 59 (SPFR)
(7,18) Hymenaea S.P. Teixeira et al. tree
courbaril L. 45 (SPFR)
(1,19) Cassia S.P. Teixeira et al. tree
grandis L. f. 65 (SPFR)
(4,19) Caesalpinia S.P. Teixeira tree
echinata Lam. 67 (SPFR)
(11,9) Parkia pendula H.C. Lima 5693 tree
(Willd.) Benth. ex Walp. (RB)
(19,25) Senegalia S.P. Teixeira et al. tree
polyphylla (DC.) Britton 28 (SPFR)
(2,13) Inga congesta J.V. Paulino et al. shrub/tree
T. D. Penn. 2, 3 (SPFR)
(8,12,22) Swartzia J.V. Paulino et al. tree
dipetala Willd. ex Vogel 7, 8, 9, 10
(SPFR)
(28) Taralea J.C. Freitas 233 tree
oppositifolia Aubl. (IAN)
(14,16) Crotalaria S.P. Teixeira et al. herb
lanceolata E. Mey. 66 (SPFR)
(6,21) Tipuana tipu S.P. Teixeira 51 tree
(Benth.) Kuntze (SPFR)
(3,10,23) Indigofera M.S. Ogasawara s/n subshrub/shrub
lespedezioides Kunth (SPFR 9926)
(5,20) Platycyamus S.P. Teixeira et al. tree
regnelli Benth. 54(SPFR)
(9,16,27) Desmodium S.P. Teixeira et al. prostrate or
incanum (SW.) DC. 64 (SPFR) suberect herb
(15,17,26,29) Gliricidia S.P. Teixeira 62 tree
sepium (Jacq.) Kunth (SPFR)
ex Walp.
Species Environment Pollinator
(24) Bauhinia Cerrado, border regions moth
curvula Benth. and treefall gaps
(7,18) Hymenaea Cerrado and dry forest bat
courbaril L.
(1,19) Cassia secondary forest and primary pollen
grandis L. f. "Terra firme" forest bee
(4,19) Caesalpinia Atlantic Rain Forest, inside nectar
echinata Lam. of dense primary "Terra firme" bee
forest
(11,9) Parkia pendula Amazon Rain Forest and bat
(Willd.) Benth. ex Walp. Atlantic Rain Forest,
"Terra firme" high forest,
inside of dense forest
(19,25) Senegalia primary and secondary nectar
polyphylla (DC.) Britton forests bee
(2,13) Inga congesta inside and edge of the
T. D. Penn. Atlantic Rain Forest
(8,12,22) Swartzia Riparian forest bee
dipetala Willd. ex Vogel probably
(28) Taralea Amazon Rain Forest
oppositifolia Aubl.
(14,16) Crotalaria ruderal nectar
lanceolata E. Mey. bee
(6,21) Tipuana tipu nectar
(Benth.) Kuntze bee
(3,10,23) Indigofera "Cerrado" (grassland and probably
lespedezioides Kunth savanic intermediary bee
formations)
(5,20) Platycyamus Semideciduous montane forest nectar
regnelli Benth. bee
(9,16,27) Desmodium ruderal nectar
incanum (SW.) DC. bee
(15,17,26,29) Gliricidia Savanna and agroforest systems nectar
sepium (Jacq.) Kunth bee
ex Walp.
Symbols: C Caesalpinioideae, M Mimosoideae, P Papilionoideae. Empty
cells indicate missing information. References: (1) Agostini &
Sazima, 2003; (2) Andreata et al., 2008; (3) Boff, 2008; (4) Borges
et al., 2009; (5) Bortoluzzi, 2000; (6) Carvalho & Marchini, 1999;
(7) Dunphy et al.. 2004; (8) Flores & Rodrigues, 2010; (9)
Gavilanes & D'Angieri Filho, 1991; (10) Gemmill-Herren, 2007; (11)
Hopkins, 1984; (12) J. G. Jardim (pers. comm.); (13) J. V. Paulino
(pers. comm.); (14) Jacobi et al., 2005; (15) Kiill & Drumond,
2001; (16) Kissmann & Groth, 1999; (17) Llamas, 2003; (18)
Lopez-Forment, 1985; (19) Lorenzi, 2002; (20) Marangon et al.,
2003; (21) Martins & Oliveira, 2001; (22) Moco & M. C. B. Pinheiro,
1999; (23) Moreira & Tozzi, 1997; (24) Munin et al., 2008; (25)
Nogueira-Neto, 2002; (26) Vargas, 1987; (27) Schlindwein, 1998;
(28) V. G. Leite (pers. comm.); (29) Waited et al., 2004
Table 2 Stigma morphological features in studied legume species
Stigma size
(length vs. Cuticle
Species width-[micro]m) continuity
Bauhinia curvula 3,240 x 2,590 Disrupted by slit
Hymenaea courbaril 750 x 1,083 Dismpted by slit
Cassia grandis 500 x 420 Continuous
Caesalpinia echinata 500 x 650 Dismpted by slit
Parkia pendula 50 x 138 Dismpted by slit
Senegalia polyphylla 30 x 20 Dismpted by slit
Inga congesta 260 x 230 Dismpted by slit
Swartzia dipetala 200 x 160 Continuous
Taralea oppositifolia 400 x 240 Disrupted by pore
Crotalaria lanceolata 330 x 160 Dismpted by slit
Tipuana tipu 310 x 200 Continuous
Indigofera lespedezioides 160 x 130 Continuous
Plalvcyamus regnelli 140 x 100 Continuous
Desmodium incanum 150 x 110 Continuous
Gliricidia sepium 430 x 400 Continuous
Protein Stigmatic surface
Species pellicle
Secretory Marginal Depth
trichomes
Bauhinia curvula - + - Shallow
Hymenaea courbaril - + - Shallow
Cassia grandis - - + Deep
Caesalpinia echinata + - + Deep
Parkia pendula - + - Deep
Senegalia polyphylla - - - Shallow
Inga congesta - + - Shallow
Swartzia dipetala + + - Shallow
Taralea oppositifolia + + - Shallow
Crotalaria lanceolata - + + Shallow
Tipuana tipu - + - Shallow
Indigofera lespedezioides - + + Shallow
Plalvcyamus regnelli - + + Shallow
Desmodium incanum - + + Shallow
Gliricidia sepium - + - Shallow
Exudate
Species
Site of Chemical nature
accumulation
Bauhinia curvula Intracellular Lipoprotein
Hymenaea courbaril Intracellular Lipoprotein
Cassia grandis
Caesalpinia echinata
Parkia pendula Intercellular Lipid
Senegalia polyphylla
Inga congesta Intercellular Lipid
Swartzia dipetala Intercellular Lipid
Taralea oppositifolia Lipid
Crotalaria lanceolata Intracellular Protein
Tipuana tipu Intercellular Lipid and polysaccharide
Indigofera lespedezioides Intercellular Lipoprotein
Plalvcyamus regnelli Intercellular Lipid and polysaccharide
Desmodium incanum Intercellular Lipoprotein
Gliricidia sepium Intercellular Lipid
Exudate
Species
Releasing Releasing
mechanism time
Bauhinia curvula Holocrine Anthesis
Hymenaea courbaril Holocrine Anthesis
Cassia grandis
Caesalpinia echinata
Parkia pendula Merocrine Preanthesis
Senegalia polyphylla
Inga congesta Holocrine Preanthesis
Swartzia dipetala Holocrine Preanthesis
Taralea oppositifolia Holocrine Anthesis
Crotalaria lanceolata Holocrine Anthesis
Tipuana tipu Merocrine Preanthesis
Indigofera lespedezioides Holocrine Preanthesis
Plalvcyamus regnelli Merocrine Preanthesis
Desmodium incanum Holocrine Preanthesis
Gliricidia sepium Merocrine Preanthesis
Symbols: + = present, - = absent, empty cells = not defined
Table 3 Stigma comparative classifications of legume species
studied here and by other authors according to four main
criteria found in the literature
Subfamily/Tribe/Species Author's
classification
Caesalpinioideae
Cercideae
(19)Cercis chinensis Bunge wet
(19)Cercis griffithii Boiss. wet
(19)Cercis occidentalis A. wet
Gray
(19)Cercis siliquastrum L. wet
(19)Bauhinia aculeata L. wet
(19)Bauhinia acuminata L. wet
(19)Bauhinia binala Blanco wet
(19)Bauhinia blakeana Dunn wet
(19)Bauhinia candicans Benth. wet
(= Bauhinia forjicata subsp.
pruinosa (Vogel) Fortunato &
Wunderlin)
(19)Bauhinia c.f. wet
commersoniana
(19)Bauhinia corymbosa Roxb. wet
(23)Bauhinia curvula wet
(19)Bauhinia divaricata L. wet
(19)Bauhinia faberi Oliv. wet
(= Bauhinia brachycarpa Benth.)
(19)Bauhinia forjicata Link wet
(19)Bauhinia galpinii N.E.Br. wet
(19)Bauhinia glabra Jacq. wet
(19)Bauhinia jenningsii P. wet
Wilson
(19)Bauhinia macrantha Oliv. wet
(= Bauhinia petersiana subsp.
macrantha (Oliv.)
Brummitt & J.H. Ross
(19)Bauhinia monandra Kurtz wet
(19)Bauhinia pentandra wet
(Bong.) Steud.
(19)Bauhinia rufa Bong. Steud wet
(19)Bauhinia taitensis Taub. wet
(19)Bauhinia tomentosa L. wet
(19)Bauhinia sp. wet
(19)Bauhinia Ihonningii wet
Schum.
Detarieae
wet
(19)Phyllocarpus riedelii
(= Barnebydendron riedelii
(Tul.) J.H. Kirkbr.)
(19)Daniellia ogea (Harms) wet
Holland
(19)Peltogyne paniculata wet
Benth.
(23)Hymenaea courbaril wet
(19)Hymenaea parvifolia Huber wet
(19)Baikiaea insignis Benth. wet
(19)Copaifera langsdorffii wet
Desf.
(19)Copaifera sp. wet
(19)Cynometra alexandri C.H. wet
Wright
(19)Tamarindus indica L. wet
(19)Intsia bijuga (Colebr.) wet
Kuntze
(19)Afzelia bella Harms wet
(19)Afzelia bipindensis Harms wet
(19)Afzelia quanzensis Welw. wet
(19)Brodriguesia santosii wet
Cowan
(19)Zenkerella capparidacea wet
(Taub.) J. Leonard
(19)Hymenostegia afzelii wet
(01 iv.) Harms
(19)Schotia africana wet
(= Leonardoxa africana
(Baill.) Aubrev.)
(19)Elizabetha speciosa Ducke wet
(19)Brownea x crawfordii S. wet
Watson
(19)Macrolobium angustifolium wet
(Benth.) Cowan
(19)Paramacnolobium wet
coeruleum (Taub.) Leonard
(19)Berlinia coriacea Keay wet
(19)Berlinia grandiflora wet
(Vahl) Hutch. & Dalziel
(19)Berlinia sp. aff. B. wet
craibiana Baker f.
(19)Berlinia sp. aff. B. wet
exfoliatum Baker f.
(19)Gilbertiodendron dewevrei wet
(De Wild.) J. Leonard
(19)Isoberlinia doka Craib wet
& Stapf
(19)Brachystegia hoehmii wet
Taub.
(19)Brachystegia eurycoma wet
Haims
(19)Brachystegia fascifolia wet
Harms
(19)Brachystegia nigerica wet
Hoyle & A.P.D. Jones
(19)Brachystegia spiciformis wet
Benth.
(19)Brachystegia stipulata wet
De Wild.
Cassieae
(19)Duparquetia orchidacea wet
Baill.
(19)Poeppigia prvcera C. wet
Presl
(19)Mendoravia dumaziana wet
Capuron
(19)Dialium orientate wet
Baker f.
(23)Cassia grandis dry
Caesalpinieae
(19)Gleditsia caspica Desf. wet
(= Gleditsia caspia Desf.)
(19)Gleditsia japonica Miq. wet
(19)Gleditsia koraiensis Miq. wet
(=Gleditsia japonica Miq.)
(20)Cordeauxia edulis Hemsl. wet
(20)Ptervlobium stellatum wet
(Forssk.) Brenan
(20)Caesalpinia cassioides wet
Willd.
(20)Caesalpinia decapetala wet
(Roth) Alston
(23)Caesalpinia echinata diy
(20)Caesalpinia erianthera wet
Chiov.
(20)Caesalpinia J'errea wet
C. Mart.
(20)Caesalpinia paucijlora wet
(Griseb.) C. Wright
(20,21)Caesalpinia wet
pulcherrima (L.) Sw.
(20)Caesalpinia sappan L. wet
(20)Caesalpinia spinosa wet
(Molina) Kuntze
(20)Caesalpinia vesicaria L. wet
(20)Caesalpinia sp. wet
(20)Caesalpinia gilliesii wet
(Hook.) D. Dietr.
(20)Cenostigma gardnerianum wet
Tul.
(20)Cenostigma macrophyllum wet
Tul.
(20)Wagatea spicata wet
(= Moullava spicata (Dalzell)
Nicolson)
(20)Moldenhawera aff. wet
cuprea Pohl
(20)Moldenhawera sp. wet
(20)Jacqueshuberia wet
amplifoliola Cowan
(19)Peltophorum pterocarpum wet
(DC.) K. Heyne
(20)Parkinsonia aculeata L. wet
(20)Delonix elata (L.) Gamble wet
(20)Delonix regia wet
(Hook.) Raf.
(20)Dimorphandra vernicosa wet
Benth.
(20)Stachyothyrsus sp. wet
(20)Campsiandra angustifolia wet
Benth.
Mimosoideae
Mimoseae
(23)Parkia pendula wet
Acacieae
(11)Acacia baileyana
F. Muell.
(13)Acacia conferta Benth. wet
(11)Acacia diffusa Lindl.
(= Acacia genistifolia Link)
(13)Acacia iteaphylla Benth. wet
(26)Acacia mangium Willd. wet
x A. auriculiformis Benth.
(11,14)Acacia retinodes wet
Schltdl.
(28)Acacia Senegal L. wet
(Willd.)
(11,13)Acacia subulata Bonpl. wet
(23)Senegalia polyphylla dry
Ingeae
(8)Calliandra sp.
(23)Inga congesta (= Ajfonsea wet
bullata Benth.)
Papilionoideae
Swartzieae
(23)Swartzia dipetala semidry
Dipterygeae
(23)Taralea oppositifolia semidry
Thermopsideae
(31)Anagvris foetida L.
Crotalarieae
(7)Crotalaria juncea L. wet
(4)Crotalaria micans Link
(23)Crotalaria lanceolata wet
Genisteae
(12)Lupinus nanus var. wet
latifolius Benth. Ex Torn
(= Lupinus nanus Benth.)
(6)Cytisophyllum
sessilifolium (L.) O. Lang
(6)Laburnum anagyrvides
Medik.
(6)Cytisus hirsutus L.
(6)Cytisus scoparius
(L.) Link
(24)Cytisus striatus (Hill)
Rothm.
(24)Retama sphaerocarpa (L.)
Boiss.
(6)Genista januensis Viv.
(6)Genista radiata (L.) Scop
(6)Genista tinctoria L.
(6)Spartium junceum L.
Dalbergieae
(23)Tipuana tipu semidry
Indigofereae
(23)Indigofera lespedezioides semidry
Millettieae
(25)Platycyamus regnellii semidry
Phaseoleae
(25)Canavalia gladiata
(Jacq.) DC.
(25)Canavalia virosa (Roxb.)
Wight & Am. (= Canavalia
cathartica Thouars)
(2)Mucuna japira A.M.G. semidry
Azevedo, Agostini & Sazima
(2)Mucuna urens (L.) Medik semidry
(29)Butea monosperma wet
(Lam) Taub.
(7)Cajanus cajan (L.) Millsp. wet
(2)Erythrina crista-galli L. semidry
(2)Erythrina speciosa Andrews semidry
(2)Erythrina velutina Willd. semidry
(30)Glycine max (L.) Merr. wet
(21)Vigna adenantha (G. Mey.)
Marechal& al.
(5)Vigna caracalla (L.)
Verde.
(7)Vigna radiata (L.) wet
R. Wilczek
(7)Vigna unguiculata wet
(L.) Walp.
(27)Phaseolus augustii Harms
(18)Phaseolus vulgaris L. wet
(27)Phaseolus vulgaris var.
aborigineus (Burkart)
Baudet
(2)Macroptilium atropurpureum semidry
(DC.) Urb.
(27)Macroptilium bracteatum
(Nees & C. Mart.) Marechal
& Bau
(2)Macroptilium erythmloma semidry
(Benth.) Urb.
Desmodieae
(23)Desmodium incanum semidry
Loteae
(6)Hippocrepis comosa L.
(6)Securigera securidaca (L.)
Degen & Dorfl.
(6)Coronilla emerus L.
(= Hippocrepis emerus
subsp. emerus (L.) Lassen)
(6)Coronilla varia L.
(= Securigera varia (L.)
Lassen)
(6)Anthyllis vulneraria L.
(6)Lotus comiculatus L.
(6)Dorycnium hirsutum
(L.) Ser.
Robinieae
(23)Gliricidia sepium semidry
(6)Robinia pseudoacacia L.
Galegeae
(6)Astragalus glycyphyllos L.
(6)Colutea arborescens L.
(9)Clianthus puniceus wet
(G. Don) Lindl.
Hedysareae
(6)Hedysarum coronarium L.
(16)Hedysarum glomeralum wet
F. Dietr.
(6)Onobrvchis viciifolia
Scop.
Cicereae
(1)Cicer arietinum L. wet
Trifolieae
(10)TrifoIium pratense L. wet
(3,15)Medicago saliva L.
Fabeae
(17)Vicia faba L.
Subfamily/Tribe/Species Heslop- Dumas
Harrison and (1978)
Shivanna
(1977)
Caesalpinioideae
Cercideae
(19)Cercis chinensis Bunge wet wet
(19)Cercis griffithii Boiss. wet wet
(19)Cercis occidentalis A. wet wet
Gray
(19)Cercis siliquastrum L. wet wet
(19)Bauhinia aculeata L. wet wet
(19)Bauhinia acuminata L. wet wet
(19)Bauhinia binala Blanco wet wet
(19)Bauhinia blakeana Dunn wet wet
(19)Bauhinia candicans Benth. wet wet
(= Bauhinia forjicata subsp.
pruinosa (Vogel) Fortunato &
Wunderlin)
(19)Bauhinia c.f. wet wet
commersoniana
(19)Bauhinia corymbosa Roxb. wet wet
(23)Bauhinia curvula wet wet
(19)Bauhinia divaricata L. wet wet
(19)Bauhinia faberi Oliv. wet wet
(= Bauhinia brachycarpa Benth.)
(19)Bauhinia forjicata Link wet wet
(19)Bauhinia galpinii N.E.Br. wet wet
(19)Bauhinia glabra Jacq. wet wet
(19)Bauhinia jenningsii P. wet wet
Wilson
(19)Bauhinia macrantha Oliv. wet wet
(= Bauhinia petersiana subsp.
macrantha (Oliv.)
Brummitt & J.H. Ross
(19)Bauhinia monandra Kurtz wet wet
(19)Bauhinia pentandra wet wet
(Bong.) Steud.
(19)Bauhinia rufa Bong. Steud wet wet
(19)Bauhinia taitensis Taub. wet wet
(19)Bauhinia tomentosa L. wet wet
(19)Bauhinia sp. wet wet
(19)Bauhinia Ihonningii wet wet
Schum.
Detarieae
wet wet
(19)Phyllocarpus riedelii
(= Barnebydendron riedelii
(Tul.) J.H. Kirkbr.)
(19)Daniellia ogea (Harms) wet wet
Holland
(19)Peltogyne paniculata wet wet
Benth.
(23)Hymenaea courbaril wet wet
(19)Hymenaea parvifolia Huber wet wet
(19)Baikiaea insignis Benth. wet wet
(19)Copaifera langsdorffii wet wet
Desf.
(19)Copaifera sp. wet wet
(19)Cynometra alexandri C.H. wet wet
Wright
(19)Tamarindus indica L. wet wet
(19)Intsia bijuga (Colebr.) wet wet
Kuntze
(19)Afzelia bella Harms wet wet
(19)Afzelia bipindensis Harms wet wet
(19)Afzelia quanzensis Welw. wet wet
(19)Brodriguesia santosii wet wet
Cowan
(19)Zenkerella capparidacea wet wet
(Taub.) J. Leonard
(19)Hymenostegia afzelii wet wet
(01 iv.) Harms
(19)Schotia africana wet wet
(= Leonardoxa africana
(Baill.) Aubrev.)
(19)Elizabetha speciosa Ducke wet wet
(19)Brownea x crawfordii S. wet wet
Watson
(19)Macrolobium angustifolium wet wet
(Benth.) Cowan
(19)Paramacnolobium wet wet
coeruleum (Taub.) Leonard
(19)Berlinia coriacea Keay wet wet
(19)Berlinia grandiflora wet wet
(Vahl) Hutch. & Dalziel
(19)Berlinia sp. aff. B. wet wet
craibiana Baker f.
(19)Berlinia sp. aff. B. wet wet
exfoliatum Baker f.
(19)Gilbertiodendron dewevrei wet wet
(De Wild.) J. Leonard
(19)Isoberlinia doka Craib wet wet
& Stapf
(19)Brachystegia hoehmii wet wet
Taub.
(19)Brachystegia eurycoma wet wet
Haims
(19)Brachystegia fascifolia wet wet
Harms
(19)Brachystegia nigerica wet wet
Hoyle & A.P.D. Jones
(19)Brachystegia spiciformis wet wet
Benth.
(19)Brachystegia stipulata wet wet
De Wild.
Cassieae
(19)Duparquetia orchidacea wet wet
Baill.
(19)Poeppigia prvcera C. wet wet
Presl
(19)Mendoravia dumaziana wet wet
Capuron
(19)Dialium orientate wet wet
Baker f.
(23)Cassia grandis dry dry
Caesalpinieae
(19)Gleditsia caspica Desf. wet wet
(= Gleditsia caspia Desf.)
(19)Gleditsia japonica Miq. wet wet
(19)Gleditsia koraiensis Miq. wet wet
(=Gleditsia japonica Miq.)
(20)Cordeauxia edulis Hemsl. wet wet
(20)Ptervlobium stellatum wet wet
(Forssk.) Brenan
(20)Caesalpinia cassioides wet wet
Willd.
(20)Caesalpinia decapetala wet wet
(Roth) Alston
(23)Caesalpinia echinata dry dry
(20)Caesalpinia erianthera wet wet
Chiov.
(20)Caesalpinia J'errea wet wet
C. Mart.
(20)Caesalpinia paucijlora wet wet
(Griseb.) C. Wright
(20,21)Caesalpinia wet wet
pulcherrima (L.) Sw.
(20)Caesalpinia sappan L. wet wet
(20)Caesalpinia spinosa wet wet
(Molina) Kuntze
(20)Caesalpinia vesicaria L. wet wet
(20)Caesalpinia sp. wet wet
(20)Caesalpinia gilliesii wet wet
(Hook.) D. Dietr.
(20)Cenostigma gardnerianum wet wet
Tul.
(20)Cenostigma macrophyllum wet wet
Tul.
(20)Wagatea spicata wet wet
(= Moullava spicata (Dalzell)
Nicolson)
(20)Moldenhawera aff. wet wet
cuprea Pohl
(20)Moldenhawera sp. wet wet
(20)Jacqueshuberia wet wet
amplifoliola Cowan
(19)Peltophorum pterocarpum wet wet
(DC.) K. Heyne
(20)Parkinsonia aculeata L. wet wet
(20)Delonix elata (L.) Gamble wet wet
(20)Delonix regia wet wet
(Hook.) Raf.
(20)Dimorphandra vernicosa wet wet
Benth.
(20)Stachyothyrsus sp. wet wet
(20)Campsiandra angustifolia wet wet
Benth.
Mimosoideae
Mimoseae
(23)Parkia pendula wet wet
Acacieae
(11)Acacia baileyana wet wet
F. Muell.
(13)Acacia conferta Benth. wet wet
(11)Acacia diffusa Lindl. wet wet
(= Acacia genistifolia Link)
(13)Acacia iteaphylla Benth. wet wet
(26)Acacia mangium Willd. wet wet
x A. auriculiformis Benth.
(11,14)Acacia retinodes wet wet
Schltdl.
(28)Acacia Senegal L. wet wet
(Willd.)
(11,13)Acacia subulata Bonpl. wet wet
(23)Senegalia polyphylla dry dry
Ingeae
(8)Calliandra sp. wet wet
(23)Inga congesta (= Ajfonsea wet wet
bullata Benth.)
Papilionoideae
Swartzieae
(23)Swartzia dipetala wet wet
Dipterygeae
(23)Taralea oppositifolia wet wet
Thermopsideae
(31)Anagvris foetida L. wet wet
Crotalarieae
(7)Crotalaria juncea L. wet wet
(4)Crotalaria micans Link wet wet
(23)Crotalaria lanceolata wet wet
Genisteae
(12)Lupinus nanus var. wet wet
latifolius Benth. Ex Torn
(= Lupinus nanus Benth.)
(6)Cytisophyllum wet wet
sessilifolium (L.) O. Lang
(6)Laburnum anagyrvides wet wet
Medik.
(6)Cytisus hirsutus L. wet wet
(6)Cytisus scoparius wet wet
(L.) Link
(24)Cytisus striatus (Hill) wet wet
Rothm.
(24)Retama sphaerocarpa (L.) wet wet
Boiss.
(6)Genista januensis Viv. wet wet
(6)Genista radiata (L.) Scop wet wet
(6)Genista tinctoria L. wet wet
(6)Spartium junceum L. wet wet
Dalbergieae
(23)Tipuana tipu wet wet
Indigofereae
(23)Indigofera lespedezioides wet wet
Millettieae
(25)Platycyamus regnellii wet wet
Phaseoleae
(25)Canavalia gladiata wet wet
(Jacq.) DC.
(25)Canavalia virosa (Roxb.) wet wet
Wight & Am. (= Canavalia
cathartica Thouars)
(2)Mucuna japira A.M.G. wet wet
Azevedo, Agostini & Sazima
(2)Mucuna urens (L.) Medik wet wet
(29)Butea monosperma wet wet
(Lam) Taub.
(7)Cajanus cajan (L.) Millsp. wet wet
(2)Erythrina crista-galli L. wet wet
(2)Erythrina speciosa Andrews wet wet
(2)Erythrina velutina Willd. wet wet
(30)Glycine max (L.) Merr. wet wet
(21)Vigna adenantha (G. Mey.) wet wet
Marechal& al.
(5)Vigna caracalla (L.) wet wet
Verde.
(7)Vigna radiata (L.) wet wet
R. Wilczek
(7)Vigna unguiculata wet wet
(L.) Walp.
(27)Phaseolus augustii Harms wet wet
(18)Phaseolus vulgaris L. wet wet
(27)Phaseolus vulgaris var. wet wet
aborigineus (Burkart)
Baudet
(2)Macroptilium atropurpureum wet wet
(DC.) Urb.
(27)Macroptilium bracteatum wet wet
(Nees & C. Mart.) Marechal
& Bau
(2)Macroptilium erythmloma wet wet
(Benth.) Urb.
Desmodieae
(23)Desmodium incanum wet wet
Loteae
(6)Hippocrepis comosa L. wet wet
(6)Securigera securidaca (L.) wet wet
Degen & Dorfl.
(6)Coronilla emerus L. wet wet
(= Hippocrepis emerus
subsp. emerus (L.) Lassen)
(6)Coronilla varia L. wet wet
(= Securigera varia (L.)
Lassen)
(6)Anthyllis vulneraria L. wet wet
(6)Lotus comiculatus L. wet wet
(6)Dorycnium hirsutum wet wet
(L.) Ser.
Robinieae
(23)Gliricidia sepium wet wet
(6)Robinia pseudoacacia L. wet wet
Galegeae
(6)Astragalus glycyphyllos L. wet wet
(6)Colutea arborescens L. wet wet
(9)Clianthus puniceus wet wet
(G. Don) Lindl.
Hedysareae
(6)Hedysarum coronarium L. wet wet
(16)Hedysarum glomeralum wet wet
F. Dietr.
(6)Onobrvchis viciifolia wet wet
Scop.
Cicereae
(1)Cicer arietinum L. wet wet
Trifolieae
(10)TrifoIium pratense L. wet wet
(3,15)Medicago saliva L. wet wet
Fabeae
(17)Vicia faba L. wet wet
Subfamily/Tribe/Species Heslop- Hiscock
Harrison (2000),
(1981, 2000) Hiscock et
al., (2002)
Caesalpinioideae
Cercideae
(19)Cercis chinensis Bunge wet wet
(19)Cercis griffithii Boiss. wet wet
(19)Cercis occidentalis A. wet wet
Gray
(19)Cercis siliquastrum L. wet wet
(19)Bauhinia aculeata L. wet wet
(19)Bauhinia acuminata L. wet wet
(19)Bauhinia binala Blanco wet wet
(19)Bauhinia blakeana Dunn wet wet
(19)Bauhinia candicans Benth. wet wet
(= Bauhinia forjicata subsp.
pruinosa (Vogel) Fortunato &
Wunderlin)
(19)Bauhinia c.f. wet wet
commersoniana
(19)Bauhinia corymbosa Roxb. wet wet
(23)Bauhinia curvula wet wet
(19)Bauhinia divaricata L. wet wet
(19)Bauhinia faberi Oliv. wet wet
(= Bauhinia brachycarpa Benth.)
(19)Bauhinia forjicata Link wet wet
(19)Bauhinia galpinii N.E.Br. wet wet
(19)Bauhinia glabra Jacq. wet wet
(19)Bauhinia jenningsii P. wet wet
Wilson
(19)Bauhinia macrantha Oliv. wet wet
(= Bauhinia petersiana subsp.
macrantha (Oliv.)
Brummitt & J.H. Ross
(19)Bauhinia monandra Kurtz wet wet
(19)Bauhinia pentandra wet wet
(Bong.) Steud.
(19)Bauhinia rufa Bong. Steud wet wet
(19)Bauhinia taitensis Taub. wet wet
(19)Bauhinia tomentosa L. wet wet
(19)Bauhinia sp. wet wet
(19)Bauhinia Ihonningii wet wet
Schum.
Detarieae
wet wet
(19)Phyllocarpus riedelii
(= Barnebydendron riedelii
(Tul.) J.H. Kirkbr.)
(19)Daniellia ogea (Harms) wet wet
Holland
(19)Peltogyne paniculata wet wet
Benth.
(23)Hymenaea courbaril wet wet
(19)Hymenaea parvifolia Huber wet wet
(19)Baikiaea insignis Benth. wet wet
(19)Copaifera langsdorffii wet wet
Desf.
(19)Copaifera sp. wet wet
(19)Cynometra alexandri C.H. wet wet
Wright
(19)Tamarindus indica L. wet wet
(19)Intsia bijuga (Colebr.) wet wet
Kuntze
(19)Afzelia bella Harms wet wet
(19)Afzelia bipindensis Harms wet wet
(19)Afzelia quanzensis Welw. wet wet
(19)Brodriguesia santosii wet wet
Cowan
(19)Zenkerella capparidacea wet wet
(Taub.) J. Leonard
(19)Hymenostegia afzelii wet wet
(01 iv.) Harms
(19)Schotia africana wet wet
(= Leonardoxa africana
(Baill.) Aubrev.)
(19)Elizabetha speciosa Ducke wet wet
(19)Brownea x crawfordii S. wet wet
Watson
(19)Macrolobium angustifolium wet wet
(Benth.) Cowan
(19)Paramacnolobium wet wet
coeruleum (Taub.) Leonard
(19)Berlinia coriacea Keay wet wet
(19)Berlinia grandiflora wet wet
(Vahl) Hutch. & Dalziel
(19)Berlinia sp. aff. B. wet wet
craibiana Baker f.
(19)Berlinia sp. aff. B. wet wet
exfoliatum Baker f.
(19)Gilbertiodendron dewevrei wet wet
(De Wild.) J. Leonard
(19)Isoberlinia doka Craib wet wet
& Stapf
(19)Brachystegia hoehmii wet wet
Taub.
(19)Brachystegia eurycoma wet wet
Haims
(19)Brachystegia fascifolia wet wet
Harms
(19)Brachystegia nigerica wet wet
Hoyle & A.P.D. Jones
(19)Brachystegia spiciformis wet wet
Benth.
(19)Brachystegia stipulata wet wet
De Wild.
Cassieae
(19)Duparquetia orchidacea wet wet
Baill.
(19)Poeppigia prvcera C. wet wet
Presl
(19)Mendoravia dumaziana wet wet
Capuron
(19)Dialium orientate wet wet
Baker f.
(23)Cassia grandis dry dry
Caesalpinieae
(19)Gleditsia caspica Desf. wet wet
(= Gleditsia caspia Desf.)
(19)Gleditsia japonica Miq. wet wet
(19)Gleditsia koraiensis Miq. wet wet
(=Gleditsia japonica Miq.)
(20)Cordeauxia edulis Hemsl. wet wet
(20)Ptervlobium stellatum wet wet
(Forssk.) Brenan
(20)Caesalpinia cassioides wet wet
Willd.
(20)Caesalpinia decapetala wet wet
(Roth) Alston
(23)Caesalpinia echinata dry dry
(20)Caesalpinia erianthera wet wet
Chiov.
(20)Caesalpinia J'errea wet wet
C. Mart.
(20)Caesalpinia paucijlora wet wet
(Griseb.) C. Wright
(20,21)Caesalpinia wet wet
pulcherrima (L.) Sw.
(20)Caesalpinia sappan L. wet wet
(20)Caesalpinia spinosa wet wet
(Molina) Kuntze
(20)Caesalpinia vesicaria L. wet wet
(20)Caesalpinia sp. wet wet
(20)Caesalpinia gilliesii wet wet
(Hook.) D. Dietr.
(20)Cenostigma gardnerianum wet wet
Tul.
(20)Cenostigma macrophyllum wet wet
Tul.
(20)Wagatea spicata wet wet
(= Moullava spicata (Dalzell)
Nicolson)
(20)Moldenhawera aff. wet wet
cuprea Pohl
(20)Moldenhawera sp. wet wet
(20)Jacqueshuberia wet wet
amplifoliola Cowan
(19)Peltophorum pterocarpum wet wet
(DC.) K. Heyne
(20)Parkinsonia aculeata L. wet wet
(20)Delonix elata (L.) Gamble wet wet
(20)Delonix regia wet wet
(Hook.) Raf.
(20)Dimorphandra vernicosa wet wet
Benth.
(20)Stachyothyrsus sp. wet wet
(20)Campsiandra angustifolia wet wet
Benth.
Mimosoideae
Mimoseae
(23)Parkia pendula wet wet
Acacieae
(11)Acacia baileyana - -
F. Muell.
(13)Acacia conferta Benth. wet wet
(11)Acacia diffusa Lindl. - -
(= Acacia genistifolia Link)
(13)Acacia iteaphylla Benth. wet wet
(26)Acacia mangium Willd. intermediate semidry
x A. auriculiformis Benth.
(11,14)Acacia retinodes wet wet
Schltdl.
(28)Acacia Senegal L. wet wet
(Willd.)
(11,13)Acacia subulata Bonpl. wet wet
(23)Senegalia polyphylla dry dry
Ingeae
(8)Calliandra sp. wet wet
(23)Inga congesta (= Ajfonsea wet wet
bullata Benth.)
Papilionoideae
Swartzieae
(23)Swartzia dipetala intermediate semidry
Dipterygeae
(23)Taralea oppositifolia intermediate semidry
Thermopsideae
(31)Anagvris foetida L. intermediate semidry
Crotalarieae
(7)Crotalaria juncea L. wet wet
(4)Crotalaria micans Link wet wet
(23)Crotalaria lanceolata wet wet
Genisteae
(12)Lupinus nanus var. intermediate semidry
latifolius Benth. Ex Torn
(= Lupinus nanus Benth.)
(6)Cytisophyllum intermediate semidry
sessilifolium (L.) O. Lang
(6)Laburnum anagyrvides intermediate semidry
Medik.
(6)Cytisus hirsutus L. intermediate semidry
(6)Cytisus scoparius intermediate semidry
(L.) Link
(24)Cytisus striatus (Hill) intermediate semidry
Rothm.
(24)Retama sphaerocarpa (L.) intermediate semidry
Boiss.
(6)Genista januensis Viv. intermediate semidry
(6)Genista radiata (L.) Scop intermediate semidry
(6)Genista tinctoria L. intermediate semidry
(6)Spartium junceum L. intermediate semidry
Dalbergieae
(23)Tipuana tipu intermediate semidry
Indigofereae
(23)Indigofera lespedezioides intermediate semidry
Millettieae
(25)Platycyamus regnellii intermediate semidry
Phaseoleae
(25)Canavalia gladiata intermediate semidry
(Jacq.) DC.
(25)Canavalia virosa (Roxb.) intermediate semidry
Wight & Am. (= Canavalia
cathartica Thouars)
(2)Mucuna japira A.M.G. intermediate semidry
Azevedo, Agostini & Sazima
(2)Mucuna urens (L.) Medik intermediate semidry
(29)Butea monosperma intermediate semidry
(Lam) Taub.
(7)Cajanus cajan (L.) Millsp. intermediate semidry
(2)Erythrina crista-galli L. intermediate semidry
(2)Erythrina speciosa Andrews intermediate semidry
(2)Erythrina velutina Willd. intermediate semidry
(30)Glycine max (L.) Merr. intermediate semidry
(21)Vigna adenantha (G. Mey.) intermediate semidry
Marechal& al.
(5)Vigna caracalla (L.) intermediate semidry
Verde.
(7)Vigna radiata (L.) intermediate semidry
R. Wilczek
(7)Vigna unguiculata intermediate semidry
(L.) Walp.
(27)Phaseolus augustii Harms intermediate semidry
(18)Phaseolus vulgaris L. intermediate semidry
(27)Phaseolus vulgaris var. intermediate semidry
aborigineus (Burkart)
Baudet
(2)Macroptilium atropurpureum intermediate semidry
(DC.) Urb.
(27)Macroptilium bracteatum intermediate semidry
(Nees & C. Mart.) Marechal
& Bau
(2)Macroptilium erythmloma intermediate semidry
(Benth.) Urb.
Desmodieae
(23)Desmodium incanum intermediate semidry
Loteae
(6)Hippocrepis comosa L. intermediate semidry
(6)Securigera securidaca (L.) intermediate semidry
Degen & Dorfl.
(6)Coronilla emerus L. intermediate semidry
(= Hippocrepis emerus
subsp. emerus (L.) Lassen)
(6)Coronilla varia L. intermediate semidry
(= Securigera varia (L.)
Lassen)
(6)Anthyllis vulneraria L. intermediate semidry
(6)Lotus comiculatus L. intermediate semidry
(6)Dorycnium hirsutum intermediate semidry
(L.) Ser.
Robinieae
(23)Gliricidia sepium intermediate semidry
(6)Robinia pseudoacacia L. intermediate semidry
Galegeae
(6)Astragalus glycyphyllos L. intermediate semidry
(6)Colutea arborescens L. intermediate semidry
(9)Clianthus puniceus intermediate semidry
(G. Don) Lindl.
Hedysareae
(6)Hedysarum coronarium L. intermediate semidry
(16)Hedysarum glomeralum intermediate semidry
F. Dietr.
(6)Onobrvchis viciifolia intermediate semidry
Scop.
Cicereae
(1)Cicer arietinum L. intermediate semidry
Trifolieae
(10)TrifoIium pratense L. intermediate semidry
(3,15)Medicago saliva L. intermediate semidry
Fabeae
(17)Vicia faba L. intermediate semidry
Taxa are cited according to their systematic position in Lewis et
al. (2005). References: (1) Baird et al., 1988; (2) Basso-Alves et
al., 2011; (3) Brink & Cooper, 1936; (4) Etcheverry et al., 2003;
(5) Etcheverry et al., 2008; (6) Galloni et al., 2007; (7) Ghosh &
Shivanna, 1982; (8) Greissl, 2006; (9) Heenan, 1998; (10)
Heslop-Harrison & Heslop-Harrison, 1983; (11) Jobson et al.,
1983; (12) Juncosa & Webster, 1989; (13) Kenrick & Knox, 1981; (14)
Knox et al., 1989; (15) Kreitner & Sorensen, 1984; (16) LasHerasetal.,
2001; (17) Lord & Heslop-Harrison, 1984; (18) Lord & Webster, 1979;
(19) Owens & Lewis, 1996; (20) Owens, 1990; (21) Owens et al.,
1995; (22) Pedersoli et al., 2010; (23) present study; (24)
Rodriguez-Riano et al., 1999; (25) Sahai, 2009; (26) Somsathapomkul
& Owens, 1998; (27) Sovema et al., 2003; (28) Tandon et al.,
2001; (29) Tandon et al., 2003; (30) Tilton et al., 1984; (31)
Valtuena et al., 2008
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| Author: | Costa, Marina Fernanda Bortolin; Paulino, Juliana Villela; Marinho, Cristina Ribeiro; Leite, Viviane |
|---|---|
| Publication: | The Botanical Review |
| Article Type: | Report |
| Geographic Code: | 3BRAZ |
| Date: | Mar 1, 2014 |
| Words: | 11871 |
| Previous Article: | A survey of karyological phenomena in the Juncaceae with emphasis on chromosome number variation and evolution. |
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