The genus Trichodesma ( Boraginaceae : Boraginoideae ) in southern Africa

Trichodesma R.Br. is a genus of about 45 species known from tropical and subtropical regions of Africa. Asia and Australia. The group comprises predominantly perennial herbs, the flowers characterized by anthers with prolonged connectives, often twisting above the thecae. and a prominent accrescent calyx. Five species and three subspecies of 7rii hodesma are currently recognized in southern Africa, with T. angustifolium Harv. subsp. argenteum Relief & A.E.van Wyk newly described. These taxa are widespread in southern Africa, occurring in various vegetation types. A key to the species, descriptions, distribution maps and illustrations of various microand macromorphological as well as palvnological features are provided.


INTRODUCTION
Brown described Trichodesma in 1810.a genus well defined by flowers with a deeply divided and strongly accrescent calyx, the absence of fomices, anthers usually with fairly long, soft hairs on the back and conspicuous long, linear, often twisted connectives produced above the thecae.It belongs to the family Boraginaceae estab lished by Jussieu (1789), and subfamily Boraginoideae.This family is characterized amongst others, by coiled, cymose inflorescences, setae with multicellular bases and in most genera, fruit that develop into four nutlets.
The genus Trichodesma R.Br.comprises ± 45 species, known from tropical and subtropical regions of Africa, Asia and Australia (Mabberley 1997).It is currently rep

MATERIALS AND METHODS
Herbarium specimens of Trichodesma in BFLU.BM.BOL.COI.E. GRA.J. K. NBG.NH.NMB.NU, PRE.PRU.SAM and WIND (acronyms as in Holmgren et al. 1981) were examined to gather data on morphological characters, phenology and distribution.Specimens of taxa occurring outside southern Africa that were exam ined.are not cited.This was supplemented by field work which included observations on the effect of fire on plants of T. physaloides in the Pretoria National Botani cal Garden, where this species occurs naturally.Pollen and various plant parts were studied with an 1SI-SX-25 scanning electron microscope.Measurements of pollen grains were done from acetolysed grains mounted in glycerine jelly.Acetolysis followed the standard method of Erdtman (1960).africanum L. When De Candolle (1846) revised the genus, he recognized eight species.In the description of T. africanum, De Candolle mentioned that it was collect ed by Thunberg and by Drêge in the 'Cape of Good Hope', the first southern African record for the genus.De Candolle also included Friedrichsthalia physaloides Fenzl.a species previously described from the Sudan.Wright (1904) noted that T. physaloides (Fenzl) A.DC. also occurred in the Transvaal.South Africa.He added a third southern African species, T. angustifolium, described by Harvey (1859).but was not aware of T. zey lanicum (Burm.f.) R.Br.. today also known from southern Africa, although originally described from Sri Lanka (Ceylon), and most probably introduced to the region by man.Two species, T. africanum and T. angustifolium, were recognized in the flora of South West Africa (now Namibia) by Friedrich-Holzhammer (1967).Herman (1993) listed five species and a subspecies for southern Africa, namely T. africanum, T. angustifolium, T. arenicola Giirke, T. physaloides, T. zeylanicum and T. amba cense Welw.subsp.hockii (De Wild.)Brummitt.How ever, specimens from southern Africa previously identi fied as T. arenicola, proved to be T. ambacense Welw.subsp.hockii.In the present paper we recognize five species and three subspecies of Trichodesma in southern Africa, namely T. africanum (L.) Lehm., T. ambacense Welw.subsp.hockii (De Wild.)Brummitt, T. angustifoli um Harv.subsp.angustifolium, T. angustifolium Harv.subsp.argenteum Retief & A.E.van Wyk subsp.nov., T. physaloides (Fenzl) A.DC. and T. zeylanicum (Burm.f.) R.Br.Brummitt (1990), in his account on Trichodesma for the Flora zambesiaca (FZ) region, recognized the same species for the FZ region except for T. africanum, a species with a disjunct distribution between the FSA region, Angola and North Africa, and which is not known in the region.T. zeylanicum, T. physaloides and T. amba cense extend further north into Africa, supplemented by other species (Verdcourt 1991).
TRIBAL DELIMITATION De Candolle (1846) assigned Trichodesma to the tribe 'Borrageae' and subtribe Cynoglosseae.a classification followed by most subsequent authors, for example Hooker (1885), Giirke (1897), Baker & Wright (1905), Brand (1921), Melchior (1964) and Hilger (1985).In 1941 Zakirov placed Trichodesma in a tribe of its own.Trichodesmeae.recognized by Riedl (1967) and is also accepted in the present contribution.Trichodesma is well defined by a combination of floral and palynological characters: deeply divided and strongly accrescent calyx; the absence of tomices in the corolla tube: anthers that usually have fairly long, soft hairs on the back: and con spicuous long, linear, often twisted connectives above the thecae.Pollen of the genus shows essentially no interspecific differences, is isopolar, tricolporate and with a nodular tectum.This pollen type is strikingly dif ferent from that of most genera of the tribe Cynoglosseae in which the grains are heterocolpate and the tectum psilate (Retief & Van Wyk 1999a. b).Avetisian (1956) agreed with Zakirov in removing Trichodesma from the tribe Cynoglosseae.based on the structure of its flowers and fruits, because the pollen grains of the genus have nothing in common with those of the Cynoglosseae.
Pollen morphology thus strongly supports the recogni tion of the separate tribe, Trichodesmeae.
Members of Trichodesma differ significantly from each other in nutlet morphology (see note on fruit mor phology).However, the presence of glochidia on the outer surface of the nutlets of T. africanum and T. angus tifolium could be used to argue that the placement of Trichodesma in its own tribe is not justified, because glochidia also occur on the outer nutlet surface of Cynoglossum and Afrotysonia.The types of glochidia found in Trichodesma, however, differ from those of Cynoglossum and Afrotysonia.Hilger (1985) studied the development and morphology of flowers and fruits of 23 species of the Cynoglosseae and Eritrichieae.and com mented on the implications of his findings on the tax onomy of these groups.He found that in most Cynoglosseae the nutlets are initially positioned with their disc (the flat base) parallel to the basal area (the nectary disc) of the gynoecium.Subsequent growth in a vertical direction brings the nutlets to their final oblique position.In both species of Trichodesma studied by Hilger, he observed that the nutlets are, from the begin ning, in an oblique position.This can also be used to sup port the recognition of a separate tribe for this genus.
Two other genera are assigned to the tribe Tricho desmeae, namely Caccinia Savi and Suchtelenia Kar.ex Meisn.(Riedl 1967).Giirke (1897) separated five genera using the accrescent calyx, either enclosing the fruit or expanded, as the key character: Trichodesma, Such telenia, Caccinia, Brachybotrys Maxim, ex Oliv.and Heliocarya Bunge.Heliocarya is regarded as congeneric with Caccinia (Mabberley 1997) and Brachybotrys belongs to the tribe Trigonotideae (Riedl 1997).Such telenia has 6-heterocolpate pollen grains, showing simi larity to pollen of members of Heliotropioideae, Cynoglosseae, Eritrichieae and Myosotideae.The triaperturate pollen grains of Trichodesma and Caccinia, on the other hand, show similarity to pollen of the subfami lies Wellstedioideae and Ehretioideae.The tribe Trichodesmeae can be regarded as 'primitive' within the subfamily Boraginoideae, showing similarities to various other genera within the Boraginaceae s.I.The family is sometimes treated as two separate entities, Boraginaceae s. str.and Ehretiaceae.but various characteristics sup port the recognition of one family divided into several subfamilies (Retief & Van Wyk 1999c).

Habit
Trichodesma is a genus of perennial and annual herbs or subshrubs.T. africanum is the only southern African species that is usually annual or occasionally biennial.This growth form can be correlated with its distribution in arid and desert regions where fast growth under opti mal conditions is essential.
The other species are perennial herbs or subshrubs occurring in summer rainfall regions, mainly in grassland and savanna.They are subjected to winter drought and also to regular natural fires and frost.Grassland species are usually quick in responding to the effects of fire (smoke, change in temperature and the release of nutri ents), and plants may sprout a number of inflorescences.With sturdy, often very old, fire-resistant rootstocks and mass seed production by fire-stimulated flowering, these species are well-adapted to survive unfavourable condi tions.Most examples of fire-stimulated flowering plants do flower in the absence of fire, but not as profusely as when subjected to fire.It was, however, observed that unbumed plants of T physaloides did not flower at all or produced only a few inflorescences, as opposed to burned plants of the species in the same grassland that sprouted and produced inflorescences abundantly after a natural fire (Figure 1 A, B).Burning of this particular piece of grass land under controlled circumstances to remove moribund and/or unacceptable grass material had no effect on the number of flowers produced, because the intensity of the fire was too low.A cool or low-intensity fire of less than 1 000 kJ/s/m is usually applied (Trollope 1992).

Leaf
Infraspecific taxa of Trichodesma differ remarkably in the indumentum of the leaf blade.The leaf trichome complement of the southern African members of Trichodesma consists of setae with multicellular bases, and simple, unbranched hairs.T. physaloides and T. ambacense subsp.hockii have flat, large-based setae, but differ in the structure of the setae (Figure 2A, B, D, E). T. ambacense subsp.hockii (Figure 2D) has slender setae, orientated in different directions, whereas T. physaloides (Figure 2E) has shorter, attenuate setae, ori entated more or less in a direction parallel to the midrib.Upper leaf surfaces of the taxa concerned are relatively densely hairy (Figure 2A, C, H), whereas the lower leaf surfaces of T. physaloides (Figure 2B), T. ambacense subsp.hockii, T. angustifolium subsp.angustifolium and T. africanum (Figure 21) are sparsely hairy, with setae scattered on the midribs and along the veins.T. angusti folium subsp.angustifolium is characterized by an indu mentum of appressed setae, orientated in a direction par allel to the midrib and varying in length and in size at the base, with distinct spaces between the trichomes.The leaf surfaces of T. angustifolium subsp.argenteum (Figure 2C, F) are silver-grey, covered with a dense layer of setae on both surfaces, a feature distinguishing this taxon from all other southern African taxa of Tricho desma.The outline of the multicellular bases of the setae is not circular, but slightly asymmetrical.Leaves of T. zeylanicum (Figure 2G) are characterized by a lower surface that is densely hairy, with mainly sim ple, small hairs, but also with scattered setae along the midrib and some veins.The upper surface is covered by setae of which the large, 2-layered multicellular bases are ± circular in outline, with much smaller setae in between (Figure 2H).T. africanum has a spinose indumentum with stiff setae on the lower surface (Figure 21).Cells of the multicellular base of the setae are narrower compared to those of T. zeylanicum.The upper surface of T. africanum is characterized by well-spaced setae with a prominent row of swollen cells at the point where the seta and multicellular base join.Cells of the multicellu lar bases of the older leaves are impregnated with silica and some calcium, giving them a spotted appearance.

Flower
Various flower characters in Trichodesma are taxonomically significant.Anthers with connectives lengthe ning into usually twisted appendages above the thecae, distinguish the genus from all other southern African members of the family (Figure 3A, B).Long, shaggy hairs (Figure 3A, C, F) are present on the dorsal surfaces of the connectives, whereas the inside of the thecae are glabrous (Figure 3F).The subglobose stigma displays two types of receptive surfaces (Figure 3D, E, G, H). T. angustifolium has papillae with prominent contiguous caps (distal swellings) and crenulate margins (Figure 3D,  E).Papillae without distinct caps occur in the other taxa studied (Figure 3G, H).Corolla lobes are often twisted (Figure 31) and acuminate to long-acuminate.The colour of the lobes is usually shades of blue except for T. physa loides which has white lobes with a brownish rim.
A prominent feature of the flower in Trichodesma is the calyx which is strongly accrescent when in fruit  (Figure 4).T. physaloides and T. ambacense subsp.hockii are characterized by a single mature nutlet with a persistent style.The style is initially gynobasic, but due to abortion of three ovules, it becomes orientated side ways.These single nutlets, together with the calyx and style are shed from the plant.This type of nutlet disper sal also occurs in Cryptantha flava (A.Nels.)Payson, another member of the Boraginaceae.According to Casper & Wiens (1981), the abortion of three of the four ovules may be an adaptation for dispersal by wind, the entire floral structure serving as a relatively light disper sal unit.The attached, accrescent, papery calyx may aug ment the buoyancy of nutlets in air currents and increase the dispersal distance.In the case of T. africanum it can be speculated that the spinose indumentum of the calyx protects the nutlets, allowing them to mature before any damage can be done by herbivores.

Pollen
Pollen studies revealed no significant differences between the species of Trichodesma included in this study, a finding that is in agreement with Brummitt (1982).Pollen grains of the genus are isopolar, radially symmetrical, tricolporate, subspheroidal, with P = 7.0-11.5Mm, E = 6.0-9.5 pm, P/E = 1.1-1.2(Figure 5A-F).The shape of the pollen grains in polar view is ± triangular, with convex mesocolpia and sunken apertures (Figure 5B).The equatorial view is elliptic to rounded with protruding ora; grains are angulaperturate (Figure 5A, C).Long apertures, extending over about 4/5 of the length of the polar axis, are characteristic of the grains.They are comparatively narrow with acute ends and the margins are not conspicuously different.Ora are coarse ly granular, with endo-apertures lalongate (Figure 5D).The tectum is nodular with nodules ± of the same size (Figure 5E), sometimes absent in the vicinity of the ora (Figure 5C, D).As noted in the discussion on the tribal delimitation of the genus, some authors prefer to classify  (Retief & Van Wyk 1999a).

Fruit
In Boraginaceae fruit characters are often used to dis tinguish species.Brand (1921) recognized six sections in Trichodesma, based on the outer surface morphology of the nutlets.Members of four sections are present in southern Africa, similar to the diversity reported by Verdcourt (1991) 61).

PHYTOGEOGRAPHY
Trichodesma is widespread in southern Africa (Figure 7) where members occur in various vegetation types, -íÁ ranging from grassland and savanna to succulent shrubland, mainly in the Savanna and Grassland Biomes.All southern African species extend further north into Africa.
Trichodesma angustifolium subsp.argenteum, occur ring in the northern parts of Namibia, is the only taxon endemic to the FSA region.Brummitt (1985) described a new Trichodesma species from the volcanic regions of Kenya, T. marsabiticum Brummitt, which is very similar in facies to T. angustifolium, and can be regarded as a vicariant of the southern African species, which differs in calyx and corolla characters.T. angustifolium subsp.angustifolium itself is disjunct in distribution in southern Africa (Figure 9), and its current occurrences may repre sent relicts of a once much wider distribution.Brummitt (1985) considered that an early record of the species from Bulawayo in Zimbabwe should be disregarded unless modem collections can substantiate it.
The floristic connection between the dry areas of southern Africa, especially Namibia, and northeastern tropical Africa is well known, and is ascribed to a socalled arid corridor which connected the two regions at various times in the past (Verdcourt 1969;De Winter 1971;Thulin & Johansson 1996).T. africanum and T. angustifolium are examples of species confined to arid climatic conditions: in Africa it is known from arid parts of southern Africa, Angola and North Africa, thus belonging to the disjunct Afro-arid element.
The genus Trichodesma occurs in all six phytogeographical regions of southern Africa recognized by White (1983): Zambesian region, Kalahari-High veld Transition Zone, Karoo-Namib Region, Tongaland-Pondoland Region, Afromontane Region and Cape Region.T. physa loides occurs mainly in the Afromontane floristic region which extends from the northern parts of Africa to south ern Africa along the eastern mountain ranges.The Afro montane region comprises a series of isolated highland areas and is well represented in eastern Africa from Yemen to South Africa, but is also present in the Cameroon (Denys 1980).The region in southern Africa is character ized by numerous small forest patches in a grassland or fynbos matrix.The edges, or ecotones between forests and grasslands are usually sharp (typically just over a few metres) and are mainly maintained by both natural and more anthropogenic fires.T. ambacense subsp.hockii, closely related to T physaloides, is found in some regions where T physaloides occurs but is also found in regions such as Nigeria (see Brummitt 1985).
Annual and perennial herbs, often with annual stems from a woody rootstock, variously hairy.Leaves simple, opposite, subopposite or alternate, basal leaves usually opposite and petiolate, upper ones alternate and sessile or all leaves sessile, diminishing in size towards inflor escences; blade variously shaped, entire; stipules absent.Inflorescence a scorpioid, cymose panicle, bracteate, usually terminal.Flowers bisexual, regular, pedicellate, calyx, corolla and stamens usually 5-merous.Calyx deeply divided to base or lobes loosely adherent along lower margin, finely setulose on abaxial side, variously hairy on adaxial side; lobes ovate or narrowly ovate, sometimes winged, base rounded to cordate, apex acute, acuminate or cuspidate, strongly accrescent and papery in fruit.Corolla blue or white; tube campanulate or funnel-shaped, naked in throat, but with gibbosities between lobe sinuses; lobes ovate to broadly triangular, apex trun cate or acute to acuminate, sometimes cuspidate, often spreading or reflexed.Stamens arising from base or from throat of corolla tube, sessile or filaments shorter than 1 mm and broader than long; anthers linear-oblong or lin ear-lanceolate, with long hairs on back, connectives pro longed above anthers, often twisted together at apex, usually exserted.Ovary 4-lobed, with a single ovule in each loculus; style persistent, gynobasic, terete, narrow ing above; stigma subglobose, papillate, papillae with or without distinct caps, caps with crenulate margins.Fruit either 4 nutlets or by abortion 1; nutlets ovoid, planocon vex or biconvex, smooth or variously ornamented.
The name Trichodesma alludes to the twisted hairs or awns that terminate the anthers; Greek thrix, trikhos = hair and desme = a band or bundle (Tólken 1986).Brand (1921) divided the genus into six sections but his taxonomy and nomenclature have been queried since.Some of the rather striking differences could be consid ered almost of generic importance (Verdcourt 1991), but we found no supporting palynological differences to justify this view in agreement with Brummitt (1982).Five species and three subspesies are recognized in south ern Africa.Southern African species of Trichodesma rep resent the following four sections: • Sect.Trichodesma: Riedl: 225 (1967).
Fruit of four nutlets, ovoid-cup-shaped with distinct serrate margins and glochidiate hairs on outer face, i.e. base of cup; outer face convex, inner face concave, ser rate margin also with glochidia; gynobase pyramidal with four strongly concave sides, each with ± winged margin, verrucose (T.africanum).
Although different infraspecific taxa of T. zeylanicum have been described, the species does not warrant subdi vision in southern Africa.In Australia the species does show differences and three forms are recognizable (Randall 1993).
Trichodesma africanum is a rather plastic species with small leaves and much-branched inflorescences under arid climatic conditions, compared to large leaves and less branched inflorescences when growing in the shade of boulders or during times of above-average rainfall.The different varieties recognized by Brand (1921) and El- Hadidy & Boulos (2000) are not upheld here, but this needs further attention.
Perennial herb or subshrub, up to 1.2 m high, with a woody rootstock, appressed hairy throughout, with setae orientated parallel to midrib of leaves.Stems erect or decumbent-ascending; setae variable in size or of ± equal length; epidermis often flaking off in older plants.Leaves shortly petiolate or blades decurrent; blade linear to narrowly elliptic to linear-elliptic, 20-50 x (1.5-) 3.0-6.0(-15.0)mm, base narrowly cuneate, apex acute, surfaces with setae dense or with spaces in between; petiole up to 3 mm long.Inflorescences terminal at ends of main stems and also terminal on lateral branches, lowermost flowers occasionally solitary in leaf axils.Calyx setulose, winged, ± 11 x 4 mm in flower, ± 25 x 20 mm in fruit, base cordate, apex long-acute.Corolla pinkish in young stage, changing to blue or mauve, fading white; tube cylindric to slightly campanulate, ± 9-15 mm long; lobes triangular, ± 5.5 x 4 mm, long-acuminate, often twisted.Fruit of 4 nutlets; nutlets glochidiate, ± 5-6 mm long; glochidia usually coalescing at base to form dis tinct rim.
Distinguishing characters: resprouting perennial, stems, inflorescences and calyces appressed hairy; leaf blades linear to narrowly elliptic; calyx winged, ± 25 x 20 mm in fruit; nutlets with several-barbed glochidia; glochidia usually coalescing at their bases to form a dis tinct rim.The prominent silver-grey to greyish green indumen tum is reflected in the specific epithet: 'argenteum' = sil ver.The difference in the density of the setae on the leaf surfaces, distinguishes the two subspecies.This distinc tion is further supported by habitat differences.

Key to subspecies
Flowering time: November to April.Distinguishing characters: indumentum tomentose, silvery grey to grey ish green; setae densely packed; usually on lime soils.Distribution: northern part of Namibia (Figure 9).Habitat: grassland, savanna, margins of pans, road verges; usually in grey, lime-rich soils.
Flowering time: August to November.Figure 10.

SPECIMENS EXAMINED (southern Africa only)
Numbers in brackets signify the identity of the speci mens: ( 1
Trichodesma in the tribe Cynoglosseae but the tricolpo rate pollen of the genus supports its placement in the sep arate tribe Trichodesmeae.Pollen grains of members of the tribe Cynoglosseae are usually heterocolpate, quite different from those of Trichodesma.The similarity in pollen morphology between Trichodesma and Cordia, does not support the separation of the Boraginaceae into two separate families