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Stigma diversity in tropical legumes with considerations on stigma classification.

Introduction

The 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
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Geographic Code:3BRAZ
Date:Mar 1, 2014
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