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American Journal of Botany 84(3): 285±297. 1997.

A SURVEY OF ANTHER GLANDS IN THE MIMOSOID LEGUME TRIBES PARKIEAE AND MIMOSEAE1

MELISSA LUCKOW2 AND JAMES GRIMES

L. H. Bailey Hortorium, Cornell University, 462 Mann Library, Ithaca, New York 14853; and New York Botanical Garden, Bronx, New York 14058

In a broad survey of anther glands in the mimosoid legume tribes Mimoseae and Parkieae, representatives from 30 genera with anther glands were studied using scanning electron microscopy. Four kinds of anther glands could be distinguished. The -type gland, found in all but four of the genera surveyed, is usually spherical to ellipsoid in shape and often borne on a stipe. The cells making up the gland vary in size among species and are often sculptured. Six different kinds of sculpturing can be recognized: smooth, reticulate, striate, rugulate, scabrate, and papillate. The -type gland is the least specialized, consisting of a simple extension of the connective with irregularly projecting cells. The africana- type gland is borne ventrally between the thecae, the connective extending hump-like over the apex of the anther. The -type gland, found only in the genus Pentaclethra, is distinguished by a median dorsal furrow and a ventral conical structure similar to a food body or osmophore. Anatomical sections revealed two different subtypes within the Piptadenia-type gland. Some glands are composed of a homogeneous matrix of isodiametric cells, whereas others have two layers: a peripheral layer of large radially elongated cells, and a central sphere of smaller isodiametric cells and large air spaces. Some characters of anther glands have clear taxonomic signi®cance, and more detailed surveys within genera will undoubtedly provide additional taxonomic markers.

Key words: anther glands; anther appendages; anther morphology; ; ; Mimoseae; Parkieae.

Anther glands in the Mimosoideae are extensions of (Gymnantherae) of anther glands. Although he was be- the anther connective that have a secretory function ginning to question the reliability of this character by (Chaudhry and Vijayaraghavan, 1992; Endress, 1994). 1875 when his comprehensive treatment of the Mimo- Although connective protrusions are relatively common soideae appeared, Bentham nonetheless recognized the in angiosperms (Endress and Stumpf, 1991), it is less tribe Adenantherae (``usually glanduliferous'') as distinct common that these protrusions are differentiated as se- from the tribe Eumimoseae (``usually without glands''). cretory organs. Among the lower Rosidae, Endress and This classi®cation persisted in one form or another until Stumpf (1991) reported anther glands from Crassulaceae, 1981, when Elias combined the two tribes as the Mi- Cephalotaceae, some Mimosoideae, and some Sapinda- moseae, noting that ¯oral and characters indicated ceae and Rutaceae. Tucker (1996) noted anther append- they did not form natural groups. ages among some papilionoid and caesalpinioid legumes It is surprising, then, that anther glands in the Mimo- as well as in the mimosoids. They have also been re- soideae have been so little studied. Tucker (1988) in her ported from the (Beardsell, Williams, and work on the ¯oral development of pubescens Knox, 1989; Landrum and Bonilla, 1996), Violaceae noted varying expression of anther glands between dif- (Fahn, 1979) and Solanaceae (Sazima et al., 1993). ferent sexual morphs. In male ¯owers, the glands were Until recently, anther glands have ®gured prominently dactyloid and proportionately larger than in perfect ¯ow- in the of the subfamily Mimosoideae. In 1842, ers, and in sterile ¯owers, the staminodia occasionally Bentham recognized two subtribes in the tribe Eumimo- bear only an apical gland. Tucker hypothesized that the seae based on the presence (Adenantherae) or absence glands might serve an elater-like function in addition to acting as attractants. 1 Manuscript received 27 February 1996; revision accepted 26 Sep- Anther glands are usually reported to function in pol- tember 1996. lination (Chaudhry and Vijayaraghavan, 1992; Endress, The authors thank Dr. Shirley Tucker for sharing her pickled material with us, Kew Botanical Garden (K) for both pickled and dried material, 1994), but there is scant evidence to support this asser- the New York Botanical Garden (NY) and the University of Texas at tion. Chaudhry and Vijayaraghavan (1992) studied the Austin (TX) for dried material, the Brooklyn Botanical Garden and the development of anther glands in Prosopis juli¯ora and National Tropical Botanical Garden at Kauai for fresh material for found that they are made up of secretory cells that pro- chemical analysis, Dennis Stevenson for technical supplies and assis- duce a protein/carbohydrate exudate. The cells lyse, and tance, Shirley Tucker and Peter Endress for their careful reviews of this the exudate is passed through cuticular openings to the manuscript, Ed Cope for German translation, Beryl Simpson for sharing her unpublished data on anther glands in Prosopis, and Billie Turner exterior of the gland. Chaudhry and Vijayaraghavan also for suggesting to the ®rst author a number of years ago that micro- noted that anther glands function in pollination by pro- characters in mimosoids might be interesting. We especially thank the viding a food source to attract pollinators. people who took time from their own schedules to collect material for To date there has been no broad comparative study of us: John Freudenstein and Lourdes Rico Arce at Kew, and Dave Lor- the structure of anther glands in the Mimosoideae. The ence at Kauai. This work was supported by a grant to the ®rst author from the President's Council of Cornell Women. objectives of the present study were to: (1) survey the 2 Author for correspondence. FAX: 607-255-7979, e-mail: structure of anther glands in the mimosoid tribes Parkieae [email protected]. and Mimoseae (here referred to as the basal mimosoids) 285 286 AMERICAN JOURNAL OF BOTANY [Vol. 84 using scanning electron microscopy (SEM); (2) examine TABLE 1. Distribution of anther glands in genera of the Parkieae and the internal structure and chemistry of the glands using Mimoseae. Numbers followed by an asterisk indicate that the pres- light microscopy and histochemistry; and (3) to gather ence or absence of anther glands was impossible to determine for one or more species, i.e., the discrepancy between the total number data on mimosoid taxa and a suitable Caesalpinioid out- of species and the number of species with glands is due to lack of group (), which later can be placed in a phylo- data. Double asterisks indicate that the genus is polymorphic for genetic context. anther glands, but that not all species have been examined.

MATERIALS AND METHODS No. No. species Total species sam- The SEM study included samples from most genera in the Mimoseae no. with pled/ and Parkieae from which anther glands have been reported, and one Genus species glands SEM genus from the (see Table 1, vouchers in Appendix Parkieae 1). The only genera not examined were (currently being stud- 31 16 3 ied by C. Hughes, Oxford Forestry Institute), and the recently described Pentaclethra 3 3 1 Lemurodendron (Villiers and Guinet, 1989) from Madagascar. Callian- Mimoseae dropsis, reported by HernaÂndez and Guinet (1990) as occasionally hav- 12 12 2 ing an anther appendage, was also omitted as none of the specimens Alantsilodendron 8 5 1 we examined had appendages. Two or more species were examined in Anadenanthera 2 1 1 11 of the genera, in order to provide a rough assessment of variation Calliandropsis 1 1 0 within genera. Samples of ten species were studied from both material 11 10* 3 in liquid and reconstituted dried material to evaluate differences caused Cyclicodiscus 1 1 1 by preservation. It was found that dried material did not differ signi®- 24 1 1 cantly from material in liquid in most characters. An exception was 9 3 2 9 9 2 surface sculpturing of the cells of the anther connective and the anther 27 15** 3 gland, which was somewhat smoother and less distinct in the reconsti- 1 1 1 tuted material. In general, it was possible to score herbarium material Gagnebina 5 5 2 for cell sculpturing with some degree of con®dence, in spite of minor Goldmania ϭ differences due to preservation. Indopiptadenia 1 1 1 Material preserved in FAA (formalin-acetic acid-alcohol) was put Lemurodendron 1 1 0 through an ethanol dehydration series and critical-point dried using a Leucaena 17 5 0 Tousimi critical-point dryer. Samples were then sputter-coated using a Monoschisma ϭ BAL-TEC sputter-coater, and observed on a Hitachi 4500-S SEM. Dried Microlobius 2 2 1 Neptunia 11 7 2 material from herbarium specimens was rehydrated in a 5% solution of 11 6** 1 aerosol, washed, and subsequently subjected to the same treatment as 6 5* 1 the specimens in liquid. Piptadenia 26 25* 2 Terminology describing anther morphology follows Endress and 1 1 1 Stumpf (1991). Walker and Doyle's (1976) terminology to describe 2 2 1 sculpturing of pollen surfaces was used to describe the sculpturing on 1 1 1 the cells of the anther glands, although our usage does not correspond Prosopis 44 34** 3 exactly since there are no perforations in the cell walls of anther glands. Pseudopiptadenia 11 10* 1 Paraf®n sections were made from the anther glands of representative Pseudoprosopis 7 7 1 4 4 1 species from ten different genera, including Adenanthera pavonina, 21 16* 2 Alantsilodendron alluaudianum, Calpocalyx dinklagei, Dichrostachys Tetrapleura 2 2 1 cinerea, Elephantorrhiza goetzei, Gagnebina pervilleana, Piptadenia Xerocladia 1 1 1 viridi¯ora, Prosopis pubescens, Schleinitzia insularum, and Stryphno- 8 6** 1 dendron pulcherrimum. Anthers were put through ethanol and xylene dehydration series, embedded in paraf®n, sectioned, stained using the safranin-fast green method (Johansen, 1940), and examined using light personal communication), and Desmanthus has one re- microscopy. Histochemical tests on four of these genera (see Table 4) cently described species with anther glands (Contreras, included ferric chloride staining for polyphenols (Gahan, 1984), Sudan 1986; Luckow, 1993). In addition to the latter two genera, IV and Nile Blue for lipids (Jensen, 1962), and Coomassie Blue for nine others are polymorphic for the presence of anther proteins (Gahan, 1984). glands: Alantsilodendron, Anadenanthera, Dichrostach- RESULTS ys, Entada, Neptunia, Newtonia, Parkia, Prosopis, and Xylia (Table 1). Calliandropsis, a monotypic genus from Variation in the presence of anther glandsÐAnther Mexico, is reported to have anther glands only rarely and glands are present in the majority of genera in the basal is thus polymorphic within one species (HernaÂndez and tribes of mimosoids, having been recorded from 33 of 38 Guinet, 1990). genera (Table 1). Only ®ve genera are reported always to Lewis and Elias (1981) noted that species of Entada, lack some sort of extension of the anther connective: Au- Dichrostachys, and Gagnebina from Madagascar tend to brevillea, , Kanaloa, and in the lack anther glands, and interpreted this as local special- tribe Mimoseae; and in the tribe Mimoz- ization. Although this generalization is true for Entada ygantheae. All of these are either mono- or ditypic except and Dichrostachys, there are notable exceptions. For ex- Mimosa. Leucaena, although frequently reported to lack ample, the Madagascan species of Xylia have glands, but anther glands, in fact includes ®ve species with connec- one Asian species (sometimes considered a variety of X. tive appendages (C. Hughes, Oxford Forestry Institute, xylocarpa) lacks glands. Species of the Madagascan gen- March 1997] LUCKOW AND GRIMESÐANTHER GLANDS IN MIMOSOID LEGUMES 287

TABLE 2. Characters of anthers from SEM survey. Abbreviations are as follows: AG ϭ anther gland, conn ϭ connective, n. ϭ nearly, int/lat ϭ introrse but with the central part of the connective showing through on the ventral side.

Position Filament Dorsal Anther size Length ratio Conn. cell Species of stomia attachment furrow (␮m) AG/anther sculpturing Caesalpinioideae latrorse n. basi®xed 1/central 1 800 1:11 smooth Parkieae Parkia multijuga introrse dorsi®xed 2/thecae 1 287 1:6 striate Parkia velutina introrse dorsi®xed 2/thecae 832 1:5 striate introrse dorsi®xed 1/central 1 500 1:3 smooth Mimoseae Adenanthera microsperma introrse dorsi®xed no 430 1:3 striate Adenanthera pavonina introrse dorsi®xed no 743 1:5 striate Alantsilodendron alluaudianum int/lat dorsi®xed no 682 1:5 striate Anadenanthera macrocarpa introrse dorsi®xed no 586 1:3 striate Calpocalyx brevibracteatus introrse dorsi®xed no 744 1:5 striate Calpocalyx dinklagei introrse dorsi®xed no 591 1:3 striate gabunensis introrse dorsi®xed no 400 1:4 striate Desmanthus balsensis introrse dorsi®xed no 353 1:2.5 striate int/lat dorsi®xed no 654 1:4 striate Dichrostachys spicata int/lat dorsi®xed no 646 1:4 smooth Elephantorrhiza elephantina introrse dorsi®xed no 700 1:4 striate Elephantorrhiza goetzei introrse dorsi®xed no 592 1:4 striate Entada mannii introrse dorsi®xed no 400 1:4 striate Entada polystachya introrse n. basi®xed no 654 1:3 striate Entada wahlbergii introrse dorsi®xed no 1 144 1:5 striate Fillaeopsis discophora introrse dorsi®xed no 577 1:4 striate Gagnebina commersoniana introrse dorsi®xed no 1 560 1:13 striate Gagnebina pervilleana introrse dorsi®xed no 1 244 1:10 striate Indopiptadenia oudhensis n. latrorse dorsi®xed no 1 000 1:10 striate Microlobius foetidus introrse dorsi®xed no 480 1:3 striate Neptunia pubescens introrse dorsi®xed no 773 1:5.5 striate Newtonia suaveolens introrse dorsi®xed no 400 1:4 striate Parapiptadenia rigida introrse dorsi®xed no 559 1:4 striate Piptadenia adiantoides introrse dorsi®xed no 445 1:3 striate Piptadenia viridi¯ora introrse dorsi®xed u-shaped 500 1:4 striate Piptadeniastrum africanum n. introrse dorsi®xed no 275 1:2 striate Plathymenia reticulata introrse dorsi®xed no 433 1:3 striate Prosopidastrum mexicanum introrse dorsi®xed no 937 1:5 striate Prosopis africana introrse dorsi®xed no 534 1:2 smooth? Prosopis pubescens introrse dorsi®xed no 682 1:4 striate Prosopis juli¯ora introrse dorsi®xed no 616 1:4 striate Pseudopiptadenia leptostachya introrse dorsi®xed 2/thecae 533 1:2 striate Pseudoprosopis claessensii introrse dorsi®xed no 455 1:2 striate Schleinitzia insularum introrse dorsi®xed 2/thecae 300 1:4 smooth Stryphnodendron pulcherrimum introrse dorsi®xed no 389 1:2.5 striate Stryphnodendron sp. introrse dorsi®xed no 275 1:2.5 striate Tetrapleura tetraptera introrse dorsi®xed no 500 1:3 striate Xerocladia viridiramis introrse dorsi®xed no 533 1:3 striate Xylia torreana introrse dorsi®xed no 609 1:3 striate era Gagnebina and Alantsilodendron do not lack glands independent losses among the New World species as well per se but have a unique kind of appendage (see below), (Luckow and Hopkins, 1995). and Alantsilodendron is polymorphic for appendages within Madagascar. The species of Newtonia lacking an- Variation in morphologyÐMorphological variation of ther glands are found throughout the range of the genus anther glands and anthers among the 30 genera surveyed in Africa. Only Australian species of Neptunia lack an- is summarized in Tables 2 and 3. A complete set of pho- ther glands, except for the widespread aquatic species, N. tographs is available on the World Wide Web at http:// oleracea. Desmanthus and Anadenanthera are the only www.bio.cornell.edu/hortorium/luckow/anther.html. As exclusively New World taxa that are polymorphic for the noted by Endress and Stumpf (1991), mimosoid anthers presence of anther glands. In the few polymorphic genera are, with several notable exceptions, introrse and dorsi- that have been analyzed cladistically, absence of anther ®xed (Table 2, Figs. 3±8). The anthers of bat-pollinated glands represents a secondary loss rather than the prim- species of Parkia are nearly basi®xed, with the ®lament itive condition (Luckow, 1993, 1995; Luckow and Hop- greatly thickened and tucked into a basal fold (Fig. 5). kins, 1995). For example, almost all Old World species Burkea, our sample of Caesalpinioideae, was the only of Parkia have lost anther glands, but there are several species in the survey to have latrorse anthers (Figs. 1, 2), 288 AMERICAN JOURNAL OF BOTANY [Vol. 84

Figs. 1±9. 1±2. Burkea africana (Caesalpinioideae). 1. Anther with latrorse dehiscence. Bar ϭ 600 ␮m. 2. Connective extension. Bar ϭ 150 ␮m. 3. Ventral view of an anther of Piptadeniastrum africanum. The gland is relatively large as compared to the size of the anther. Bar ϭ 150 ␮m. 4. Ventral view of an anther of Indopiptadenia oudhensis having nearly latrorse dehiscence. The gland is relatively small as compared to the size of the anther. Bar ϭ 375 ␮m. 5. Dorsal view of anther of Parkia platycephala. Note the lateral furrows between the thecae and the connective. Bar ϭ 429 ␮m. 6. Dorsal view of an anther of Piptadenia viridi¯ora. There is a U-shaped furrow between the thecae and the connective, and March 1997] LUCKOW AND GRIMESÐANTHER GLANDS IN MIMOSOID LEGUMES 289

TABLE 3. Characters of anther glands from SEM survey. Abbreviations are as follows: AG ϭ anther gland, APP ϭ appendiculate, PIP ϭ Piptadenia- type gland, PENT ϭ Pentaclethra-type gland, GAGN ϭ Gagnebina-type gland, PRO ϭ Prosopis africana-type gland, NA ϭ not applicable, Dolabri ϭ Dolabriform, UNS ϭ unsculptured, Sculp ϭ Sculptured. The column labelled ``AG cell edges'' refers to whether there is a large unsculptured edge to each anther gland cell, or whether the gland is sculptured throughout. A question mark indicates that there was a problem scoring the character due to preservation.

AG cell AG AG size size AG cell AG cell Cell Species type Stalk AG shape (␮m) (␮m) sculpturing edges planes Caesalpinioideae Burkea africana APP NA NA 165 21 Smooth NA One Parkieae Parkia multijuga PIP Stipitate Spheroid 206 19 Smooth NA One Parkia velutina PIP Stipitate Spheroid 183 21 Smooth NA One Pentaclethra macroloba PENT Sessile Spheroid 550 28 Smooth NA One Mimoseae Adenanthera microsperma PIP Stipitate Spheroid 150 48 Scabrate UNS One Adenanthera pavonina PIP Stipitate Spheroid 150 57 Scabrate UNS One Alantsilodendron alluaudianum GAGN NA NA 136 21 Striate Sculp Many Anadenanthera macrocarpa PIP Stipitate Spheroid 180 25 Rugulate Sculp One Calpocalyx brevibracteatus PIP Stipitate Dolabri 142 31 Rugulate UNS One Calpocalyx dinklagei PIP Stipitate Dolabri 166 27 Rugulate UNS One Cylicodiscus gabunensis PIP Stipitate Spheroid 100 27 Rugulate Sculp One Desmanthus balsensis PIP Stipitate Spheroid 125 20 Scabrate Sculp One Dichrostachys cinerea PIP Stipitate Spheroid 162 21 Striate UNS One Dichrostachys spicata PIP Stipitate Spheroid 170 23 Striate UNS One Elephantorrhiza elephantina PIP Stipitate Spheroid 188 27 Scabrate Sculp One Elephantorrhiza goetzei PIP Stipitate Spheroid 130 17 Scabrate UNS One Entada wahlbergii PIP Sessile Spheroid 214 30 ? Sculp One Entada mannii PIP Stipitate Spheroid 113 24 Rugulate UNS One Entada polystachya PIP Sessile Spheroid 214 21 Rugulate UNS One Fillaeopsis discophora PIP Sessile Spheroid 133 27 Rugulate Sculp One Gagnebina commersoniana GAGN NA NA 118 34 Rugulate Sculp Many Gagnebina pervilleana GAGN NA NA 122 26 Striate Sculp Many Indopiptadenia oudhensis PIP Sessile Spheroid 96 22 Rugulate Sculp One Microlobius foetidus PIP Stipitate Ovoid 155 27 Rugulate Sculp One Neptunia pubescens PIP Stipitate Clavate 137 20 Rugulate Sculp One Newtonia suaveolens PIP Stipitate Spheroid 100 20 Rugulate UNS One Parapiptadenia rigida PIP Stipitate Spheroid 144 18 Reticulate UNS One Piptadenia adiantoides PIP Sessile Spheroid 133 20 Rugulate UNS One Piptadenia viridi¯ora PIP Stipitate Spheroid 127 21 Rugulate Sculp One Piptadeniastrum africanum PIP Sessile Spheroid 175 30 Rugulate UNS One Plathymenia reticulata PIP Stipitate Spheroid 133 25 Rugulate Sculp One Prosopidastrum mexicanum PIP Stipitate Spheroid 187 17 Rugulate Sculp One Prosopis africana PRO Sessile Triangular 257 25 Papillate Sculp One Prosopis pubescens PIP Stipitate Ovoid 175 28 Rugulate Sculp One Prosopis juli¯ora PIP Stipitate Ovoid 120 23 Rugulate Sculp One Pseudopiptadenia leptostachya PIP Stipitate Spheroid 133 16 Rugulate UNS One Pseudoprosopis claessensii PIP Stipitate Ellipsoid 227 38 Scabrate UNS One Schleinitzia insularum PIP Stipitate Clavate 75 15 Rugulate Sculp One Stryphnodendron pulcherrimum PIP Stipitate Dolabri 167 21 Rugulate Sculp One Stryphnodendron sp. PIP Stipitate Dolabri 100 16 Rugulate Sculp One Tetrapleura tetraptera PIP Stipitate Spheroid 155 41 Scabrate UNS One Xerocladia viridiramis PIP Sessile Obconic 133 23 Rugulate Sculp One Xylia torreana PIP Stipitate Ellipsoid 182 30 Smooth? ? Many although anthers of the mimosoid Indopiptadenia (Fig. 4) dorsal surface of the anther where the thecae meet the are nearly latrorse. Dichrostachys and Alantsilodendron connective (Fig. 5); in Piptadenia viridi¯ora, these fur- often have the anther sacs displaced laterally, such that rows are continuous and form a U-shaped structure (Fig. the connective is visible on the ventral side between the 6). A single median dorsal furrow, common in the Cae- thecae (Fig. 8), and the stomia are thus somewhat lateral. salpinioideae (see Endress and Stumpf, 1991), was seen In several genera, there are two distinct furrows on the among the mimosoids only in Pentaclethra (see Fig. 30).

← the gland is short-stipitate. Bar ϭ 150 ␮m. 7. Dorsal view of an anther of Piptadenia adiantoides that lacks furrows. The gland is sessile. Bar ϭ 150 ␮m. 8. Ventral view of an anther of Dichrostachys spicata. The thecae are separated and the connective is visible between them. The anther gland is spherical and long-stipitate. Bar ϭ 150 ␮m. 9. Anther gland of Pseudoprosopis claessensii, which is stipitate and ellipsoid in shape. Bar ϭ 150 ␮m. 290 AMERICAN JOURNAL OF BOTANY [Vol. 84

Figs. 10±18. 10. Anther gland of Neptunia pubescens, which is sunken below the thecae at anthesis and is clavate in shape. Bar ϭ 75 ␮m. 11. Dolabriform, stipitate anther gland of Stryphnodendron sp. Bar ϭ 50 ␮m. 12. Spherical, stipitate anther gland of Adenanthera pavonina. The cells making up the gland are relatively large. Bar ϭ 120 ␮m. 13. Anther gland of Prosopidastrum mexicanum consisting of many small cells. Bar ϭ 85 ␮m. 14. Reticulate sculpturing on the cells of the anther gland of Parapiptadenia rigida. Bar ϭ 15 ␮m. 15. Scabrate sculpturing on the cells of the anther gland of Adenanthera pavonina. Bar ϭ 15 ␮m. 16. Smooth anther gland cells of Parkia velutina. Bar ϭ 15 ␮m. 17. Striate sculpturing on the cells of the anther gland of Gagnebina pervilleana. Bar ϭ 15 ␮m. 18. Rugulate sculpturing on the cells of the anther gland of Neptunia pubescens. Bar ϭ 15 ␮m. March 1997] LUCKOW AND GRIMESÐANTHER GLANDS IN MIMOSOID LEGUMES 291

Four distinct kinds of anther glands can be recognized smooth varies continuously among genera. It was thought in the lower mimosoids (Table 3), which we have called that this character might re¯ect different developmental the Piptadenia type, the Gagnebina type, the Prosopis stages, but an examination of anther glands from young africana type, and the Pentaclethra type of glands. buds to mature ¯owers demonstrated that such is not the 1) The Piptadenia type is the most common, being case (Figs. 19, 20). found in all but four of the genera surveyed. The anther 2) The Gagnebina type. In contrast to the ``stalked- glands are most often spherical in shape (Figs. 3, 4±8), sphere'' morphology of the Piptadenia type of gland, the but may also be ellipsoid (Fig. 9), clavate (Fig. 10), or Malagasy endemics Gagnebina and Alantsilodendron dolabriform (Fig. 11). They are usually borne on a stalk have an elongate conical appendage formed by the ex- (Figs. 6, 8±12), which varies in length among and within tension of the connective (Figs. 21±23). The cells of the genera. The longest stipe occurs in Dichrostachys (Fig. appendage grow outward in several planes, forming 8); occasionally the gland may be completely sessile (Fig. unique ®nger-like projections (Figs. 17, 22). This is un- 7). The stipe also varies in degree of differentiation from like typical anther gland cells, which project uniformly the main body of the gland. In Dichrostachys (Fig. 8), from the surface (e.g., Fig. 12). The cells of anther glands the cells of the stipe are greatly elongated, whereas in of Xylia (Fig. 24) may also project outward in several Pseudoprosopis (Fig. 9) they are smaller than the gland planes, similar to those of the Gagnebina type. The cells cells and rectangular in outline. In other species, the stalk of the Gagnebina-type appendage are usually striate gradually widens distally to form the gland, and is only throughout, lacking the smooth borders seen on many poorly differentiated from it (Fig. 10). In many species, Piptadenia-type glands, but may be smooth toward the anther glands are caducous, and the structure of the stipe apex of the appendage (Fig. 22). Burkea (Caesalpinioi- is probably intimately related to the degree of persistence deae) has a connective extension similar to that in Gag- of the gland on the anther. nebina, but the cells do not project from the surface and The Piptadenia-type anther gland ranges in size from are smooth throughout (Figs. 1, 2). 75 to 227 ␮m, most species falling within the range of 3) The Prosopis africana type. In contrast to other spe- 100±200 ␮m (Table 3). Although this range is relatively cies of Prosopis that display the typical Piptadenia-type narrow, the size of the anthers varies among genera, and stalked-sphere morphology (Fig. 28), Prosopis africana thus the relative proportions of these structures, expressed has very unusual morphology of the anthers and anther here as a ratio of anther gland/anther length (Table 2). gland (Figs. 25±27). The anther is V-shaped, in contrast For example, the anther glands of Piptadeniastrum (Fig. to the typical mimosoid anther in which the thecae are 3) and Indopiptadenia (Fig. 4) do not differ greatly in borne more or less parallel to one another (Figs. 3, 4). absolute size (122 and 96 ␮m, respectively), but the rel- The stomia do not extend above the shoulder as in most ative proportions are quite different. In Piptadeniastrum, species (e.g., Fig. 4), but are short and form small pockets the glands are nearly as conspicuous as the anthers (1:2 on the ventral surface (Fig. 25). The connective extends length ratio), but in Indopiptadenia the glands are quite hump-like over the apex of the anther and the sessile small relative to the anther (1:10 length ratio). anther gland is borne ventrally between the thecae (Figs. Among species, cells of the anther gland also vary in 25, 26). In all other species of mimosoids examined, the size (and thus the number of cells making up the gland) gland was either apical or dorsal (e.g., Figs. 3±8). The and surface characteristics. Exceptionally large cells are gland is a triangular-shaped ¯ap in rehydrated material, found in a group of Old World genera, including Aden- although it is likely to be different in fresh or preserved anthera (Figs. 12, 15), Calpocalyx, and Tetrapleura. At ¯owers. A drawing in Flora of Tropical East Africa the other end of the spectrum is Prosopidastrum mexi- (Brenan, 1959, p. 34) depicts the connective as forming canum, with very many small cells making up the gland a triangular hood over an in¯ated bulbous gland, and it epidermis (Fig. 13). may be that the this triangular ¯ap is in¯ated in fresh Five kinds of sculpturing of the cell surfaces can be material. However, the drawing is not consistent with our distinguished in the Piptadenia-type gland (Table 3): re- observations of the shape of the connective, and the de- ticulate (Fig. 14), scabrate (Fig. 15), smooth (Fig. 16), piction of the dorsal view of the anther also disagrees striate (Fig. 17), and rugulate (Fig. 18). Reticulate sculp- with our observations. Prosopis africana is the only spe- turing is rare, found only in the genus Parapiptadenia. cies in which the sculpturing on the cells of the anther Completely smooth surfaces are also rare, and are for the gland were found to be papillate (Fig. 27). most part con®ned to the putatively basal lineages of mi- 4) The Pentaclethra type. Pentaclethra macroloba has mosoids, e.g. Parkia and Pentaclethra. The surfaces of exceptionally large anthers and glands, nearly twice as the cells of most species are striate. The striations may large as any other species examined (Figs. 29±32, Tables be nearly parallel to one another and continuous (scored 2, 3). The dorsal side of both the anther and the gland as striate) or broken up and at angles (scored as rugulate). has a median furrow (Fig. 30). Median dorsal furrows are These tend to grade into one another, and may vary with- characteristic of the Caesalpinioideae, and they were not in a single individual. The results in Table 3 refer to the observed in any other mimosoids in this study. The gland state in the majority of the cells within a sample or group is sessile, and the cell surfaces are completely smooth. of samples. In a few species, the rugulae are very smooth The most striking feature is a specialized conical struc- and are scored as scabrate (Fig. 15). ture similar to a food body or osmophore borne on the In many genera, the edges of the cells are smooth, and ventral surface of the gland just above the anther sacs sculpturing is con®ned to the central part of the cell (Figs. (Figs. 31, 32). Such a structure was not seen elsewhere 19, 20), whereas in others the entire cell surface is sculp- in the Mimosoideae. tured (Figs. 17, 18). The proportion of the cell that is Changes in the cells of anther glands at different de- 292 AMERICAN JOURNAL OF BOTANY [Vol. 84

Figs. 19±27. 19±20. Cells of the anther gland of Dichrostachys cinerea prior to anthesis (19) and postanthesis (20). Notice the perforations in the cells in the postanthesis gland. Bars ϭ 15 ␮m. 21. Ventral view of an anther of Alantsilodendron alluaudianum. The connective is visible between the thecae, and there is a small connective extension. Bar ϭ 275 ␮m. 22±23. Connective extension of Gagnebina pervilleana. The cells of the appendage grow outward in several planes. Bars ϭ 50 and 20 ␮m, respectively. 24. Anther gland of Xylia torreana in which the cells are also nonplanar. The cells of the stalk are smaller and more regularly arranged than those of the anther gland. Bar ϭ 100 ␮m. 25±27. Anther and gland of Prosopis africana. 25. Ventral view of V-shaped anther showing pocket-like stomia. Bar ϭ 200 ␮m. 26. Triangular anther gland borne March 1997] LUCKOW AND GRIMESÐANTHER GLANDS IN MIMOSOID LEGUMES 293 velopmental stages were observed in Dichrostachys ci- DISCUSSION nerea and Schleinitzia insularum. The cells of D. cinerea lose turgor as they mature (Figs. 19, 20), and cracks ap- Phylogenetic implicationsÐThe anther appendage of pear in the smooth areas of the cells at anthesis (Fig. 20). Burkea (Caesalpinioideae) is relatively simple when com- Anther gland cells of S. insularum also lose turgor as they pared to those in the Mimosoideae, consisting of an ex- mature (Figs. 33, 34), but the cells collapse at anthesis tension of the connective, the cells not well differentiated (Fig. 35). Although this collapse may appear somewhat relative to the rest of the anther (Figs. 1, 2). In contrast similar to the ®nger-like projections in the Gagnebina to most mimosoids, the anthers are latrorse and there is type of gland (Figs. 21±23), the cells of the latter actually no surface sculpturing on the cells of either the connec- grow outward in several planes, even in young buds. tive or anther appendage. It is not clear that any secretory function is associated with the connective extension. Variation in anatomy and histochemistryÐLight mi- It is tempting to consider the Gagnebina-type gland as croscopy revealed two anatomical subtypes within the ``primitive'' within the mimosoids, and possibly transi- Piptadenia type of gland. The Piptadenia subtype, ob- tional between Burkea and the rest of the mimosoids, served in Dichrostachys, Elephantorrhiza, Piptadenia, because of its simple appendage-like structure. However, Prosopis, Schleinitzia, and Stryphnodendron, has cells there are notable differences, such as the projection of that are isodiametric and of nearly equal size throughout the cells in different planes and surface sculpturing on (Figs. 36±38). The epidermal cells are not well differ- the cells in the mimosoid genera. Furthermore, based on entiated from those at the center of the gland, nor are recent phylogenetic analyses (Luckow, 1995), the Gag- there any large intercellular spaces. Most cells contain nebina-type gland could be viewed as a modi®cation of areas that stain red in safranin/fast green (Fig. 38), and the Piptadenia-type gland, a hypothesis strengthened by these are largest in the peripheral cells. These areas are the anatomical similarities between the two types. Thus, presumed to be vacuoles, as a red-staining nucleus is also it seems unlikely that appendages in Burkea are homol- visible in some cells. ogous with those in the Mimosoideae. The Adenanthera subtype, found in Adenanthera and Pentaclethra is usually considered to be basal among Calpocalyx, consists of two well differentiated layers of the mimosoids, linking them to the Caesalpinioid genus cells (Figs. 39, 40). The cells of the epidermal layer are . Both the anther and the gland of Penta- relatively large (ഠ 50 ϫ 20 ␮m) and radially elongated. clethra have features suggestive of the Caesalpinioideae, They also contain red-staining inclusions. The center of the including relatively large size of the anther and a median gland consists of smaller isodiametric cells with large in- dorsal furrow. Using Burkea as an , it is also tercellular spaces (Fig. 40). It is unlikely that the air spaces likely that smooth surfaces on the anther connective and are artifacts, as the overall structure of these glands is very gland cells are ``primitive'' features. similar to that observed in the Myrtaceae by Beardsell, Wil- Nevertheless, the gland of Pentaclethra has many liams, and Knox (1989). In none of the species examined unique characters not seen in any other genera, such as with light microscopy was any well-developed vascular tis- the bizarre conical structure on the ventral surface. The sue observed in the anther gland or stalk. function of this structure is unknown. Pentaclethra ma- The anatomy of the Gagnebina type of anther gland is croloba is reported to be beetle-pollinated (Kress and most similar to the Piptadenia-type, consisting of a ho- Beach, 1994), and it may be that the gland functions in mogenous matrix of cells (Figs. 41, 42). The cells of the scent production and emission. Alternatively, ant asso- appendage of Alantsilodendron alluaudianum stain ciations have been reported for this species (Bennett and heavily, as do the connective cells, indicating that they Breed, 1985), and the conical structure may be some sort probably contain signi®cant amounts of tannins (Fig. 41). of food body. Studies are currently underway to inves- Additional histochemical tests for polyphenols (Ferric tigate these hypotheses. Chloride), lipids (Nile blue, Sudan IV), and proteins Our work provides further evidence that the tribe Par- (Coomassie Blue) showed no reaction with the vacuolar kieae (Pentaclethra ϩ Parkia) is not a natural group. The contents (Table 4). The cell walls of both the connective only feature of the anther gland that the two genera share and the anther glands showed a positive reaction with is smooth surfaces on the cells making up the gland. The ferric chloride in three species, indicating that they prob- Piptadenia-type gland of Parkia is typical of the tribe ably contain tannins. In most cases, the reactions of the Mimoseae. Furthermore, one of the more unusual fea- cell walls of the anther glands paralleled those of the tures of the anther glands of Parkia, lateral dorsal furrows connective, and a positive reaction probably indicates at the junction of the connective with the thecae, is not their derivation from the tissue of the connective rather seen in Pentaclethra, but is found in other genera in the than having any functional signi®cance. Given the overall tribe Mimoseae. negative reactions to the histochemical tests in Table 4, Among some genera of the Mimoseae, characters of it seems likely that the vacuoles contain either carbohy- the anther glands demonstrate close correspondence to drates or perhaps terpenoids. Gas chromatographic stud- previously proposed phylogenetic hypotheses. For ex- ies are currently underway to more precisely characterize ample, anther glands of Adenanthera, Pseudoprosopis, the chemistry of the anther glands. and Tetrapleura are composed of exceptionally large

← below a hump-like connective that extends over the apex of the anther. Bar ϭ 85 ␮m. 27. Papillate sculpturing on the cells of the anther gland. Bar ϭ 15 ␮m. 294 AMERICAN JOURNAL OF BOTANY [Vol. 84

Figs. 28±35. 28. Anther of Prosopis juli¯ora. Note the typical stipitate Piptadenia-type morphology. Bar ϭ 231 ␮m. 29±32. Anther and gland of Pentaclethra macroloba. 29. Ventral view of the anther and gland. Bar ϭ 500 ␮m. 30. Dorsal view showing dorsal furrow on both anther and gland. Bar ϭ 500 ␮m. 31. Anther gland with unique conical structure. Bar ϭ 200 ␮m. 32. Closer view of the conical structure on the ventral surface of the gland. Bar ϭ 75 ␮m. 33±35. Anther gland of Schleinitzia insularum before (33) and after (34, 35) anthesis. The cells collapse at maturity. Bars ϭ 50 ␮m in Figs. 33 and 34 and 15 ␮m in Fig. 35. March 1997] LUCKOW AND GRIMESÐANTHER GLANDS IN MIMOSOID LEGUMES 295

Figs. 36±42. 36±37. Paraf®n sections of an anther (36) and anther gland (37) of Piptadenia viridi¯ora. The anther gland is homogeneous throughout, with many small isodiametric cells. Bars ϭ 1 mm in Fig. 36, 60 ␮m in Fig. 37. 38. Anther gland of Prosopis pubescens which also consists of a homogeneous layer of cells. Note the red-staining inclusions in the cells. Bar ϭ 30 ␮m. 39±40. Anther glands of Calpocalyx dinklagei. There are two layers of cells: a peripheral layer of large radially elongated cells with red inclusions and an internal sphere of smaller isodiametric cells with large air spaces between them. Bars ϭ 2 mm in Fig. 39 and 60 ␮m in Fig. 40. 41. Anther glands of Alantsilodendron alluaudianum. The projecting, ®nger-like cells of the anther glands stain very dark in safranin/fast green. Bar ϭ 90 ␮m. 42. The anther gland of Gagnebina pervilleana is composed of a homogeneous layer of cells. Note the septae between the pollen grains. Bar ϭ 100 ␮m. 296 AMERICAN JOURNAL OF BOTANY [Vol. 84

TABLE 4. Results of histochemical tests on the anther glands of four prehensive studies of the anther glands in these genera genera. Rxn ϭ reaction. may shed light on the relationships among their species. Although a phylogenetic analysis of the basal mimosoids Ferric Nile Coomassie Species chloride blue Sudan IV blue is needed to unequivocally assess the homology of anther Dichrostachys Cell walls Cell walls Cell walls Cell walls glands among the genera, it seems likely that the Piptad- Elephantorrhiza No Rxn. Cell walls No. Rxn. Cell walls enia-type gland represents a developmentally homologous Prosopis Cell walls No. Rxn. No. Rxn. No. Rxn. structure. The uniqueness of the anther gland of Pentacleth- Schleinitzia Cell walls No. Rxn. No. Rxn. Cell walls ra, as well as the overall similarity of the anthers to those of other Caesalpinioideae, suggest it may not be homolo- gous to those of the rest of the Mimosoideae. cells with scabrate sculpturing (Table 3, Figs. 9, 12, 15). Functional considerationsÐAt least four hypotheses These genera, along with the genus Amblygonocarpus for the function of anther glands in the Mimosoideae can (which lacks anther glands), were united as the Aden- be proposed. The hypothesis that has been advanced most anthera group by Lewis and Elias (1981). often is that they act as a food reward for pollinators, i.e., Likewise, our results accord well with recent work on that the insect pollinates the ¯ower while eating the the Xylia, Dichrostachys, and Leucaena groups (Harris et glands (Chaudhry and Vijayaraghavan, 1992). A second al., 1994; Luckow, 1995). For example, the clavate shape hypothesis, suggested by Endress (1994), is that anther of the anther glands of Neptunia and Schleinitzia (Table 3) glands exude a sticky substance that attaches pollen to is consistent with general ideas of relationship between the bodies of ¯oral visitors. Another possibility is that these taxa (Luckow, 1995). In this study, the Gagnebina- anther glands could function to protect the developing type gland is found only in Alantsilodendron and Gagne- anthers and ovaries from insect predators. The glands bina, two genera considered to be closely related based on form a mass of tissue at the apex of the ¯ower in bud, other data. The unusual nonplanar arrangement of cells of and the glands are often caducous at anthesis, suggesting the Gagnebina-type gland occurs also in Xylia (Fig. 22), that they might function prior to anthesis. A fourth hy- recently considered an outgroup to the other two genera. pothesis, recently suggested by Landrum and Bonilla The closely related genera Dichrostachys (Fig. 7) and (1996), is that anther glands might function to attract pol- Alantsilodendron (Fig. 19) have the unusual feature of a linators as well as provide a reward. This is supported by connective visible on the ventral side between the thecae. several lines of evidence from our own work. The Ad- Prosopis africana has consistently been recognized as enanthera type of anatomy is very similar to that seen in anomalous within the genus, and has been placed in its the osmophores of other which function in the pro- own section (Bentham, 1875; Burkart, 1976). Unlike oth- duction and emission of odor. Vogel (1990) characterized er species of Prosopis, P. africana lacks stipular spines osmophores as having large papillate epidermal cells, and and brachyblasts, has internally glabrous petals, and pol- internal aeration via intercellular spaces, both features of len with costae (Guinet, 1969). Guinet (1969) considered the Adenanthera type of gland. Sazima et al. (1993) re- it to be closest to Entada or Newtonia, based on char- ported this anatomical structure in the elaborated anther acters of the pollen. Our observations con®rm the unique- connectives of Cyphomandra (Solanaceae), which pro- ness of P. africana. Many characters, such as the V- duce perfume as a ¯oral reward for euglossine bees. The shaped anther, the small stomia, and the structure of the unique structure of the gland of Pentaclethra is likewise anther gland, are singular not just within Prosopis, but very suggestive of an osmophore. within the Mimoseae as a whole. It is not clear from the present data exactly how anther In a few cases, characters of the anther glands suggest glands function in the Mimoseae, nor what the actual novel hypotheses of relationship that need to be explored mode of secretion might be. Given the morphological and further. For example, the anatomy of the anther glands of anatomical diversity observed, it might be that all of the Calpocalyx and Adenanthera is similar and quite differ- above hypotheses are valid, and anther glands serve dif- ent from that of the other genera examined (Figs. 39, 40). ferent purposes in different taxa. We are currently col- Calpocalyx was considered most closely related to Xylia lecting additional chemical data as well as ®eld obser- in Lewis and Elias' scheme (1981), but these data indi- vations of insect visitors in order to test these hypotheses. cate that it may be related to the Adenanthera group. A more exhaustive survey of the anatomy of the relevant LITERATURE CITED genera is needed to demonstrate this. Piptadenia and Entada show remarkable infrageneric BEARDSELL, D. V., E. G. WILLIAMS, AND R. B. KNOX. 1989. The struc- variation in characters of both the anthers and glands (Ta- ture and histochemistry of the and anther secretory tissue of bles 2, 3). The two species of Piptadenia examined dif- the ¯owers of calycina (Lindl.) Stapf (Myrtaceae). Australian Systematic Botany 37: 65±80. fered in the shape of the anther, the presence of a U- BENNETT, B., AND M. D. BREED. 1985. On the association between shaped dorsal furrow de®ning the thecae, the anther Pentaclethra macroloba (Mimosaceae) and Paraponera clavata glands being stipitate or sessile, and the amount of the (Hymenoptera: Formicidae) colonies. Biotropica 17: 253±255. cell surface that is sculptured. The three species of En- BENTHAM, G. 1842. Notes on Mimoseae, with a short synopsis of spe- tada varied in many of the same characters (anther shape, cies. Journal of Botany (Hooker) 4: 323±418. glands stipitate or sessile, and amount of sculpturing) as . 1875. Revision of the suborder Mimoseae. Transactions of the Linnean Society, London 30: 335±664. well as in the size of the anthers. Infrageneric variation BRENAN, J. P. M. 1959. Flora of tropical East Africa: Leguminosae in the structure of anther glands has also been reported subfamily Mimosoideae. Crown Agents for Oversea Governments for Schleinitzia (Nevling and Niezgoda, 1978), and com- and Administration, London. 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