Bonnetiaceae

Bonnetiaceae (Bartl.) L. Beauvis. ex Nakai in Bull. Tokyo Sci. Mus. 22:25 (1948).

A.L. Weitzman, K. Kubitzki, and P.F. Stevens

More or less subpachycaulous small to mediumsized trees and shrubs. Leaves convolute, spiral, crowded towards apex of branches, with close, ascending lateral veins, margins serrulate, initially setulose, estipulate; petiole short or 0. Flowers single, or more or less cymose inorescences; pedicels with 2 prophylls or several bracts; owers bisexual, cyclic; sepals 5, unequal, free, quincuncial; petals 5, contorted, free; stamens numerous; laments slender, free, or basally connate into 5 antepetalous bundles; anthers short, basixed; fasciclode + or 0; ovary 3(5)-locular, with numerous orderly arranged ovules on biseriate axile placentae; stylodia free or united into a branched or simple style; stigmas papillate. Fruits septicidal capsules with a persistent central column; seeds with scanty endosperm; embryo straight. Three genera and about 40 species, northern South America, West Indies, Southeast Asia, West Malesia, Moluccas and New Guinea. Vegetative Morphology and Anatomy. Bonnetiaceae are stout-stemmed shrubs or usually small trees with few branches. The smallest species, Bonnetia ahogadoi, is notable for its trailing and rooting inorescence axis which also acts as a stolon (Fig. 10), whereas Ploiarium alterniorum, a small, stilt-rooted tree, may grow up to 25 m high on swampy peat soil in Johore (Corner 1978). The terminal bud usually lacks scales, axillary buds are small, and branching appears to be sylleptic, although in B. ahogadoi growth of the main axis appears to be rhythmic (Steyermark 1984) and there are scales at the base of agelliform inorescence shoots. The leaves remain rolled up as the bud elongates, and are more or less sessile and usually have a distinct but not very prominent midrib. The plants are completely glabrous, except for tiny colleters found in the leaf axils. The leaf margin is usually minutely serrulate and only rarely entire but, in the juvenile stage, it is always provided with minute setae which fall off during leaf expansion

but persist in the tiny, revolute leaves of Bonnetia roraimae. Archytaea and Ploiarium have vascularised, disciform structures borne immediately inside the margin and on the lower surface of the blade and in its upper one-third. Venation is often eucamptodromous, sometimes more or less brochidodromous or parallelodromous. The phellogen in the stem is surcial in origin, that in the root is initiated 3 or 4 layers deep in the cortex. There are brachysclereids in the stem cortex, a sheath of bres in the pericyclic position, and groups of bres in the secondary phloem (see also van Tieghem 1885). The heartwood is dark reddish brown and heavy. Vessel elements are solitary, of medium length, and their perforations are simple/transverse; uniseriate rays are of upright cells, and multiseriates (24 cells wide) consist of procumbent cells with uniseriate extensions of upright cells; axial parenchyma is scanty paratracheal, and bres are mostly thick-walled. Xylem parenchyma forms an adaxial cap on the vessels. Nodes are trilacunar in Bonnetia, unilacunar in Archytaea and Ploiarium. The separate traces are visible in leaf scars although, in taxa such as Bonnetia ahogadai, traces are more or less conuent in the outer part of the cortex. Ploiarium has an arcuate midrib bundle, that of other taxa is more complex, the tissue on the adaxial side in particular being irregularly arranged. Vascular bundles are embedded, and the marginal setae of Archytaea and Ploiarium, but not those of Bonnetia, are associated with vascular tissue. Stomata are anomocytic and an adaxial hypodermis is sometimes present. The leaf anatomy of Bonnetia is remarkable: the epidermis is often mucilaginous and its cells bulge and intrude between the mesophyll cells; foliar sclereids are widespread in the mesophyll; and the leaf midrib and all veins including the terminal veinlets are surrounded by an endodermis of thin-walled cells provided with Casparian strips (Maguire 1972; Dickison and Weitzman 1996; Weitzman and Stevens 1997).

Bonnetiaceae

37

Inorescence and Flowers. Inorescences are lateral, and several species appear to have axillary owers. However, these are probably reduced inorescences, and the pedicels bear 2several bracts along their length, sometimes very close to the calyx. The sepals of Bonnetia, and perhaps also Ploiarium, are terminated by setae very like those found on the leaf margins. The petals are predominantly white or pink. Whether or not the androecium of Bonnetia is fasciculate needs study; fascicles have been reported (e.g. Steyermark 1984) but their existence at least, as evident in later bud or ower has been questioned (Kobuski 1948; PFS, pers. obs.). It is not known if the fasciclodes of Ploiarium secrete nectar; otherwise, there are no reports of nectar from the family (Dickison and Weitzman 1998). Pollen Morphology. Pollen is 28 to almost 60 m long, oblate-spheroidal, tricolporate with wide colpi and circular ora. Sometimes, as in B. lancifolia, the colpi are fused at the poles, leaving a triangular polar space. There are costal colpi in Archytaea and Ploiarium, and all taxa have costal pori. The nexine, 0.54 m thick, is thicker than the sexine, which is nely reticulate (Erdtman 1952; Maguire 1972; Steyermark 1984; Salgado-Laboriau and Villar de Seoane 1992). Seed. The seeds are quite small, and Corner (1976) suggested that the seed coat of Ploiarium is probably endotestal, although its development has not been studied. Exotestal cells are thin-walled and polygonal, endotestal cells are usually isodiametric, low, and with sinuous anticlinal walls, lignication is extensive and there are numerous narrow plasmodesmata. Ploiarium alternifolium has rather elongated endotestal cells, and the anticlinal walls of those of Archytaea are almost straight. There is a thin, persistent layer of endoperm surrounding the straight embryo. Although the cotyledons are generally small, those of Bonnetia range from 1/21/6 the length of the embryo. Germination is epigeal (Ploiarium). Phytochemistry. Bonnetiaceae are rich in xanthones with various substitution patterns, and bixanthones and anthraquinone xanthones have been reported from Ploiarium (Kubitzki et al. 1978; Bennett et al. 1990). Xanthones are also richly diversied in Clusiaceae and Hypericaceae (Bennett and Lee 1989).

Family Circumscription and Afnities. When the exudate-producing genus Neotatea and the anther gland-bearing genera around Kielmeyera and Caraipa are removed from Bonnetiaceae, as suggested by Weitzman and Stevens (1997), the family becomes very homogeneous. Although in the past members of the family have been included in the intermediate zone between Theaceae and Clusiaceae/Hypericaceae, the former are now in Ericales, and possession of xanthones, oral morphology, testa anatomy, etc., all link Bonnetiaceae with Clusiaceae/Hypericaceae. The combination of characters of wood anatomical characters presented above sets Bonnetiaceae apart from Theaceae, with which Baretta-Kuipers (1976) compared them, and also Guttiferae and Hypericaceae. Gene sequence analyses by Savolainen, Fay et al. (2000) and Gustafsson et al. (2002) conrm the close relationship of Bonnetiaceae with Clusiaceae/Hypericaceae. The inclusion of Ploiarium in Malvales (Savolainen, Fay et al. 2000) was probably due to a mistaken identication, since i.a. the distinctive seed coat anatomy of Archytaea is quite unlike that of Malvales. Elatinaceae have also often been considered as possibly related to Bonnetiaceae, agreeing in testa anatomy and a number of other features, but molecular data place them sister to Malpighiaceae (Davis and Chase 2004); whether or not that family is close to Bonnetiaceae, etc., is unclear. Distribution and Habitats. The two closely related, small genera Archytaea and Ploiarium are disjunct between Southeast Asia/Malesia and northern South America, whereas Bonnetia is restricted to continental South America, with one species on Cuba. Archytaea prefers open habitats, often by creeks, always on nutrient-poor soil, ranging from lowland to mid-altitudes. Bonnetia is most speciose in the Guayana Highland and its surroundings, where 27 species are found, all but one (B. paniculata) of which are endemic to this region. Most of them have only a limited altitudinal range, with the majority preferring the mesothermic/submicrothermic belt (1,2002,700 m; Huber 1988), but Bonnetia crassa spans a belt of 2,000 m. With increasing altitude, the bonnetias tend to be of lower stature. Bonnetia ahogadoi is a low shrublet growing at localized sites on peat in rock depressions of the Chimat Massif in Venezuela

38

A.L. Weitzman, K. Kubitzki, and P.F. Stevens

Fig. 10. Bonnetiaceae. Bonnetia ahogadoi. A Habit. B Leaf. C Flower. D Androecium and gynoecium. E Anther. F Ovary, transversal section. G Capsule at beginning of dehiscence.

H Two valves of dehiscent capsule with adherent seeds and persistent columella. I Seeds, various positions. (Drawing by B. Manara; Steyermark 1984)

at an altitude of about 2,100 m (Huber 1992). Ploiarium grows in the lowland, often close to the sea, and on swampy peaty soil (Corner 1978) or on nutrient-poor white sand in the heath forests of Borneo. Uses. The wood is durable and in Asia/Malesia locally used for constructions, but is not a commercial timber.

Genera of Bonnetiaceae 1. Ploiarium Korthals

Ploiarium Korthals, Verh. Nat. Gesch. Bot., ed. Temminck: 135 (1840); Kobuski, J. Arnold Arb. 31:196207 (1950), rev.

Key to the Genera

1. Androecium not fasciculate; ovary 3(4)-locular 3. Bonnetia Androecium 5-fasciculate; ovary 5-locular 2 2. Flowers in 3many-owered inorescences; sepals and stamens caducous; style simple 2. Archytaea Flowers solitary; sepals and stamens persistent; stylodia 5, free to base 1. Ploiarium

Trees, sometimes vast, or shrubs. Flowers solitary; pedicels ancipitous, increasing in diameter towards apex; sepals caducous; nectary glands 5, alternating with petals; stamens numerous, caducous, in 5 antesepalous fascicles; ovary 5-locular; stylodia 5, free to base, persistent. Capsule dehiscing from the base; seeds linear; endosperm eshy. Three species, from Cambodia through Malay Peninsula to Sumatra, Borneo and Halmahera. 2. Archytaea Mart.
Archytaea Mart. in Mart. & Zucc., Nov. Gen. Sp. Pl. 1:116 (1826); Weitzman & Stevens, BioLlania Esp. 6:556557 (1997); Weitzman, Fl. Venez. Guayana 9:310313 (2005).

Bonnetiaceae

39

Small trees or shrubs. Inorescences axillary, 3 many-owered; peduncles ancipitous, increasing in diameter towards apex; pedicels midway with prophylls; sepals persistent; nectary glands 5, alternate with petals; stamens numerous, persistent, in 5 antesepalous fascicles; ovary 5-locular; style simple, persistent. Seeds numerous, linear, imbricate, exalbuminous. Two species, in the Guayana sandstone region and adjacent lowlands of northern South America. 3. Bonnetia Mart. Fig. 10

Bonnetia Mart. in Mart. & Zucc., Nov. Gen. Sp. Pl. 1:114 (1826), nom. cons.; Kobuski, J. Arnold Arb. 29:393413 (1948), rev.; Weitzman, Fl. Venez. Guayana 9:313324 (2005). Neblinaria Maguire (1972). Neogleasonia Maguire (1972) except N. duidae (Kobuski & Steyerm.) Maguire Acopanea Steyerm. (1984).

Trees or shrubs. Flowers solitary or up to three on axillary peduncles or occasionally arranged in loose panicles with ancipitous or terete peduncles; sepals persistent; stamens very numerous, persistent, the laments adnate to the base of the ovary and otherwise free; anthers dehiscing longitudinally or by two pores at the base; ovary 3(4)-celled; stylodia 3, or style simple and then sometimes apically branched. Seeds linear, elongated above and below into a small membranous wing. About 29 species, mainly in the Guayana highland and adjacent regions, with B. paniculata Spr. ex Benth. extending along the Andes to Peru, B. stricta (Nees) Nees & Mart. along the Atlantic coast southwards to Rio de Janeiro, and B. cubensis (Britton) Howard in Cuba.

Selected Bibliography
Baretta-Kuipers, T. 1976. Comparative wood anatomy of Bonnetiaceae, Theaceae and Guttiferae. In: Baas, P., Bolton, A.M., Catling, D.M. (eds) Wood structure in biological and technological research. Leiden Botanical Series 3, pp. 76101.

Bennett, G.J., Lee, H.-H. 1989. Xanthones from Guttiferae. Phytochemistry 28:967998. Bennett, G.J., Lee, H.-H., Lowrey, T.K. 1990. Novel metabolites from Ploiarium alternifolium: a bixanthone and two anthraquinolyxanthones. Tetrahedron Lett. 31:751754. Corner, E.J.H. 1976. See general references. Corner, E.J.H. 1978. The freshwater swamp-forest of South Johore and Singapore. Gard. Bull. suppl. 1. Singapore: Government Printers. Davis, C.C., Chase, M.W. 2004. Elatinaceae are sister to Malpighiaceae, and Peridiscaceae are members of Saxifragales. Amer. J. Bot. 91:262273. Dickison, W.C., Weitzman, A.L. 1996. Comparative anatomy of the young stem, node and leaf of Bonnetiaceae, including observations on a foliar endodermis. Amer. J. Bot. 83:405418. Dickison, W.C., Weitzman, A.L. 1998. Floral morphology and anatomy of Bonnetiaceae. J. Torrey Bot. Soc. 125:268286. Erdtman, G. 1952. See general references. Gustafsson, M.H.G., Bittrich, V., Stevens, P.F. 2002. Phylogeny of Clusiaceae based on rbcL sequences. Intl J. Pl. Sci. 163:10451054. Huber, O. 1988. Guayana highlands versus Guayana lowlands, a reappraisal. Taxon 37:595614. Huber, O. 1992. La vegetacin. In: Huber, O. (ed.) El macizo de Chimat. Caracas: Todtmann, pp. 161177. Kobuski, C.E. 1948. Studies in the Theaceae, XVII. A review of the genus Bonnetia. J. Arnold Arb. 29:393413. Kubitzki, K., Mesquita, A.A.L., Gottlieb, O.R. 1978. Chemosystematic implications of xanthones in Bonnetia and Archytaea. Biochem. Syst. Ecol. 6:185187. Maguire, B. 1972. Bonnetiaceae. In: The Botany of the Guyana Highland. Part IX. Mem. New York Bot. Gard. 23:131165. Prakash, N., Lau, Y.Y. 1976. Morphology of Ploiarium alternifolium and the taxonomic position of Ploiarium. Bot. Notiser 129:279285. Salgado-Laboriau, M.L., Villar de Seoane, L. 1992. Contribucin a la ora polnica de los tepuyes. In: Huber, O. (ed.) El macizo de Chimat. Caracas: Todtmann, pp. 219236. Savolainen, V., Fay, M.F. et al. 2000. See general references. Steyermark, J.A., 1984. Theaceae (Bonnetiaceae), pp. 323 330. In: Flora of the Venezuelan Guayana, I. Ann. Missouri Bot. Gard. 71:297340. van Tieghem, Ph. 1885. Second mmoire sur les canaux scrteurs des plantes. Ann. Sci. Nat. VII, Bot. 1:596; see particularly Ternstroemiaces, pp. 4346. Weitzman, A.L., Stevens, P.F. 1997. Notes on the circumscription of Bonnetiaceae and Clusiaceae, with taxa and new combinations. BioLlania Edic. Esp. 6:661 564.