Systematics of Cloiselia (Asteraceae

Systematic Botany (2006), 31(2): pp. 421–431 q Copyright 2006 by the American Society of Plant Taxonomists

Systematics of Cloiselia (Asteraceae, Mutisieae s.l.), a Reinstated Madagascan Genus SANTIAGO ORTIZ Laboratorio de Botańica, Facultade de Farmacia, Universidade de Santiago, 15782 Santiago de Compostela, Galiza-Spain ([email protected])

Delivered by Publishing Technology to: Universidad de Santiago de Compostela IP: 193.144.81.153 on: Mon, 20 Apr 2015 13:54:45 Copyright (c) American Society for Plant Taxonomists. All rights reserved.

Communicating Editor: Thomas G. Lammers ABSTRACT. Studies of the genus Dicoma (Asteraceae, tribe Mutisieae s. 1.) indicate that this taxon as currently defined is paraphyletic, and in fact comprises at least three groups showing marked morphological and anatomical differences. One of these groups is differentiated from Dicoma s. str. by a large number of characters relating to the morphology and anatomy of the phyllaries, corolla, anthers, style, cypsela, and testa. This paper proposes that this group should be considered as a separate genus, for which the name Cloiselia S. Moore has nomenclatural priority. The article presents a systematic study of Cloiselia, which comprises four species: two are new (C. madagascariensis and C. humbertii) and one is a new combination (C. oleifolia). KEYWORDS: comparative morphology, Dicoma, morphology new species, paraphyly, taxonomy.

The genus Cloiselia S. Moore was described by Spencer Moore (1906) for the species Cloiselia carbonaria, endemic to Madagascar. Moore considered this genus to be close to Dicoma Cass., because of achene and pappus morphology, but differing from Dicoma in several ways: a) in its smaller involucre made up of phyllaries with non-spinous apex; b) in the presence of small receptacular paleae; and c) in its flowers with bilabiate corolla. However, Moore’s morphological description was incorrect: Cloiselia carbonaria does not have receptacular paleae, though it does show twin hairs at the base of the cypsela. When the cypsela is extracted from the capitulum, these hairs sometimes adhere (together with the external tissues of the pericarp) to the edge of the receptacle pits and may be mistaken for paleae. In addition, Moore’s description of the corolla as bilabiate is not entirely accurate: the degree of separation of the lobes may vary, but corolla morphology is better described as of ligulate type without extended limb (see below for more details). On the basis of his erroneous morphological characterization, Moore (1906) indicated that Cloiselia should be considered close to the subtribe Gerbereae, and within this subtribe close to the genus Oldenburgia Less. Subsequently, Humbert (1923) transferred the species to the genus Dicoma, and at the same time described a new species, D. oleifolia. He later maintained this taxonomic arrangement (Humbert 1963). More recently, a cladistic analysis of Dicoma and related genera based on morphological data (Fig. 1) concluded that Dicoma carbonaria and D. oleifolia constitute a monophyletic group supported by numerous synapomorphies (Ortiz 2000; Table 1). By contrast, Dicoma as traditionally defined is paraphyletic, becoming monophyletic only if the species of the genus Pasaccardoa Kuntze are included. In line with these results and bearing in mind the marked morphological differences between the components of the different clades mak-

ing up the Dicoma 1 Pasaccardoa group (Table 1), I proposed the separation of this group into monophyletic genera. In a previous publication (Ortiz 2001), I proposed reinstatement of the genus Macledium Cass., and transfered to this genus 20 species previously included in Dicoma. Continuing in the same line, I here propose the reinstatement of the genus Cloiselia, and present a detailed systematic review of this genus. According to my cladistic analysis, Cloiselia is sister to a monophyletic group comprising the genera Macledium, Pasaccardoa and Dicoma s. str. (Fig. 1). My analysis also indicates that the sister of Cloiselia 1 [Macledium, Pasaccardoa 1 Dicoma s. str.] is a clade comprising the genera Pleiotaxis Steetz and Erythrocephalum Benth., this latter including the genus Achyrothalamus O. Hoffm. (Ortiz and Coutinho 2001). From the morphological point of view, one of the most important features of the genus Cloiselia is the presence of a series of characters that appear to be archaic within the family Asteraceae, since they are almost entirely restricted to certain genera of the tribe Barnadesiae and some of the more primitive genera of the South American Mutisieae included in the ‘‘Stenopadus group’’ of Bremer (1994) (‘‘Stifftia group’’ of Panero and Funk 2002; tribe Stifftieae sensu Pruski 2004). However, this relationship may only be apparent, and phylogenetic analyses based on the available molecular data do not support a close relationship between Cloiselia and these basal South American groups within the Asteraceae. Kim et al. (2002), in their phylogenetic analysis of the tribe Mutisieae based on sequencing of the chloroplast DNA marker ndhF, placed Cloiselia carbonaria within a clade including the tribes Tarchonantheae (Tarchonanthus L. and Brachylaena R.Br.) and Cardueae. Funk and Panero (pers. comm.), in a report presented to the First Meeting of the International Compositae Alliance, and later Funk et al. (2005) have proposed a supertree of the family Asteraceae based

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FIG. 1. Principal monophyletic groups recognizable in the clade which includes Dicoma s.l. and Pasaccardoa in the phylogenetic analysis of Ortiz (2000). Heavy line indicates the genus Cloiselia.

on about 10 chloroplast DNA markers. Funk et al. (2005) placed Cloiselia carbonaria within a clade also including Macledium, Pasaccardoa, and Dicoma, forming part of the new tribe Dicomeae proposed by these authors (Panero and Funk 2002); the seven genera making up this new tribe include most of the African genera previously included in the tribe Mutisieae. These authors’ consideration of Cloiselia 1 Macledium 1 Pasaccardoa 1 Dicoma as a monophyletic clade is in line with my conclusions (Ortiz 2000) noted above. Panero and Funk additionally suggest that Dicomeae and the tribes Tarchonantheae and Carduae together constitute the subfamily Carduoideae. In addition, the preliminary results of our ongoing phylogenetic analysis of the African and some South American representatives of the tribe Mutisieae s.l., using the rDNA marker ITS, confirm that Cloiselia is situated within the Dicomeae clade (unpublished). MATERIALS

AND

METHODS

The present study is based on morphological analysis of specimens from BM, COI, K, LP, MA, MO, and P. The material was studied with the aid of a light microscope. We also studied other micro-morphological and anatomical characters with a compound light microscope. Floral parts were first boiled in water, then placed in Hoyer’s solution (Anderson 1954) for observation. The morphology of the epidermal cell surface of the corolla and corolla twin hairs was classified as per Karis et al. (1992), endothecial cellwall thickening as per Dormer (1962), and testa morphology as per Grau (1980).

RESULTS Vegetative Characters. The genus Cloiselia comprises shrubs and trees of 2–10 m in height, often highly ramified, with branches glabrous to glabrescent, slight-

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ly striate. The leaves are generally fasciculate, sometimes solitary, oblanceolate to spathulate, with rounded apex and entire margin; indumentum variable, from glabrous/glabrescent to moderately tomentose on both surfaces (leaves concolorous) to densely tomentose on the abaxial surface (as in C. oleifolia, with leaves discolorous); marked veining, especially on the abaxial surface; venation pinnate, with secondary veins running more or less parallel for much of their length, so that veining appears parallelinerve (Figs. 5, 6). Reproductive Characters. Capitula solitary (C. madagascariensis, C. oleifolia) or grouped (C. carbonaria, C. humbertii, though may be solitary in these species), on short (C. oleifolia, C. humbertii) or long (C. carbonaria, C. madagascariensis) foliose peduncles, these slender with capitula pendent (C. carbonaria) or relatively stout (C. madagascariensis, C. oleifolia, C. humbertii). Involucre cyathiform to obconic, of 5–9 of deltate to oblong-lanceolate phyllaries, these acute or sometimes somewhat acuminate, slightly pungent, glabrescent to white tomentose. Receptacle flat to slightly concave, alveolate, the pits without border; the hairs sometimes observed on the margins of the pits after extraction of the cypsela, interpreted by Moore (1906) as short paleae, in fact form part of the base of the achene. Each capitulum has 2–8 florets which are markedly longer than the involucre (principally in C. carbonaria, C. madagascariensis and C. humbertii). The corolla is zygomorphic, generally tubular, with 5 lobes, and often with one sinus much longer than the others (C. carbonaria, C. madagascariensis); this type was described as ‘‘ligulate but without expanded limb’’ by Bremer (1994: 52) for Barnadesioideae (and as ‘‘irregularly 5-lobed’’ by Prusky 1997: 266 for Elephanthopus, though in this case the corolla is much less zygomorphic); but in some species corolla morphology may be transitional between this type and the actinomorphic type, in which all the sinuses are long and more or less of the same length; this transitional morphology is seen especially in C. oleifolia, in which many of the florets are almost true actinomorphic, and to lesser extent in C. humbertii (Figs. 5, 6). This type of zygomorphic corolla appears to be primitive, and is seen in several genera of the Barnadesieae, including Barnadesia Mutis, Dasyphyllum Kunth, and Schlechtendahalia Less. Tube base of corolla conspicuously enlarged, bulbous, except in C. humbertii. Corolla epidermal cell cuticle ornamentation ‘‘intestine-like’’ (sensu Karis et al. 1992; i.e. conspicuous longitudinal striation and tranverse undulation). Marginal nerves of the adjacent lobes separate from the corolla base, rather than joined until near the sinuses as is usual in the Asteraceae; this character is seen in some species of Chuquiraga Juss. (Barnadesieae) and Glossarion Maguire & Wurdack and—according to Carlquist (1957) and Bremer (1994)—in Stenopadus S.F.

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TABLE 1. Principal differences between Cloiselia, Dicoma, and Macledium. Apomorphic character states are indicated with an asterisk, in accordance with the analysis of Ortiz (2000). When all character states are apomorphic, the plesiomorphic state is present in other taxa not included in the table.


Character

Cloiselia

Dicoma

Macledium

Leaf shape Phyllary central vein Longitudinal dark stripes on the phyllary Phyllary sclerenchymal fibres Innermost phyllaries

*Obovate to oblanceolate Inconspicuous Absent

Ovate to lanceolate *Conspicuous *Present

Ovate to lanceolate Inconspicuous Absent

*Concentrated on the abaxial surface With a scarious margin

*Concentrated on the adaxial surface With a scarious margin

Length of the innermost phyllaries Phyllary pubescence Corolla shape

Longer than the outer

Longer than the outer

Glabrescent to tomentose Zygomorphic

Floret/involucre length relation Disc floret epidermal cell cuticle ornamentation (abaxial surface)

*Floret much longer than the involucre *Conspicuously longitudinally striate and transversely undulate (‘‘intestine-like’’) Absent

Glabrescent to tomentose *Actinomorphic (sometimes with marginal florets true-ray) Floret as long as or slightly longer than the involucre *Conspicuously longitudinally striate and transversely undulate (‘‘intestine-like’’) Absent

*Concentrated on the abaxial surface *More or less entirely scarious *Shorter than the contiguous outer series *Often completely glabrous *Actinomorphic

Long twin glandular hairs on the disc corolla Long simple (not twin) hairs on disc corolla Marginal nerves of adjacent corolla lobes Composition of the marginal vascular tissue of the disc corolla Position of the marginal vascular tissue of the disc corolla Stamen insertion in disc corolla Anther/corolla length relation Adjacent anther tails Pollen surface Style veins Style branches length Style branch vascular tissue Cypsela surface Position of the superficial cypsela glands Position of the cypsela twin hairs Twin hairs base Mature testa surface pattern Pappus/involucre length relation Pappus shape after fruiting

Floret as long as or slightly longer than the involucre *Slightly transversely undulate-striate to nearly smooth *Present

*Present (disc corolla villous) *Separate from the corolla base *Narrow, comprised of fewer vessels and without sclerenchymal fibres Conspicuously submarginal

Absent

*Near the corolla base

At the tube/throat junction

At the tube/throat junction

*Anther protruding beyond the corolla *Connate *Echinate *Four Short Narrow *Conspicuously ribbed *In a continuous layer

Anther not beyond the corolla Free Smooth to slightly granulate Two *Long *Very thick *Conspicuously ribbed *On the ribs

Anther not beyond the corolla Free Smooth to slightly granulate Two Short *Very thick 6 Smooth Absent

*Situated between the ribs

*Situated between the ribs

All around the cypsela

Not bulbous-glandular

Not bulbous-glandular

Perezia type *Pappus overtopping the involucre *Patent

*Dicoma type Pappus and involucre of similar length Erect-patent

*Conspicuously bulbousglandular Gochnatia type Pappus and involucre of similar length Erect-patent

Blake (Stenopadus group), though my own observations of Stenopadus indicate that the nerves are joined near the sinuses. Corolla pink to purple in C. carbonaria and C. madagascariensis, yellowish in C. oleifolia and C. humbertii. Corolla often villous, with long eglandular (not twin) hairs, as in the Barnadesieae, but with a different structure: in Cloiselia the corolla hairs have one or more

Fused until the sinus (rarely well below the sinus) *Narrow, comprised of fewer vessels and without sclerenchymal fibres Conspicuously submarginal

Absent (except at the corolla base in M. spinosum) Fused until the sinus (rarely well below the sinus) Broad, made up of many vessels and surrounded by sclerenchymal fibres *Marginal or almost marginal

long and narrow basal cells, and a very long distal cell, whereas in the Barnadesieae these hairs have a short bulbous proximal cell and a long distal cell (Fig. 2); in Chimantaea Maguire, Steyerm & Wurdack (Stenopadus group) the corolla is also villous, but I have not been able to examine material of this genus for characterization of corolla hair structure. Stamens inserted at


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FIG. 2. Differences between corolla hairs of Cloiselia and the Barnadesieae. Light microscope photographs of the hair base. A. Cloiselia madagascariensis (Chauvet 359 P). B. Barnadesia parviflora Spruce ex Benth. & Hook. (Gentry & Curso de Postgrado en Sistema´tica s.n. MA). Scale bar 5 10 mm.

corolla base, as in some species of Chuquiraga (Barnadesieae), and protruding well beyond the corolla. Filament collar conspicuous and not swollen. Apical appendage apiculate to caudate, anther base caudate and calcarate, anther tails long tapering, with several acute retrorse hairs and (0)2–10 acute antrorse hairs at the apex; adjacent anther tails connate, with hairs sometimes interwoven, an interesting characteristic also seen in Chuquiraga and Dasyphyllum (Barnadesieae) and in the Stenopadus group (Glossarion, Gongylolepis R.H. Schomb., Neblinaea Maguire & Wurdack, Stenopadus, and Stomatochaeta (S.F. Blake) Maguire & Wurdack). Endothecial cells polarized. Style branches short, separate, not curved or slightly curved, with subapical tuft of acute sweeping hairs, with sub-basal group slightly longer than the rest; four stylar nerves, a characteristic that as far as I am aware is not seen in any other species of Asteraceae, in which there are generally two stylar nerves (i.e. Dicoma) (Fig. 3). Style branch nerves narrow. Cypsela turbinate, 8- to 10-ribbed, covered with ascending white to yellowish twin hairs inserted between the ribs; cypsela with superficial glands (Ortiz 2000) in a continuous layer all around the cypsela and without biseriate glands; pericarp with star-shaped crystals. Immature testa (Ortiz 2000) made up of more or less long rectangular crystals oriented in the same direction; mature testa seems to be of Perezia type. Pappus isomorphous, of barbellate bristles, protruding well beyond the involucre (though less far in C. oleifolia), arranged in several series, the inner slightly wider; pappus with two very unusual characteristics for this family, namely bristles reddish to purplish (C. carbonaria, C. madagascariensis) or yellowish (C. oleifolia, C. humbertii), and patent after fruiting.

DISCUSSION In view of the characters detailed above and summarized in Table 1, it seems clear that Cloiselia should be considered a genus separate from Dicoma. Cloiselia—an exclusively African group—shows a few characters that are otherwise almost exclusively seen in certain early diverging South American groups, namely the tribe Barnadesieae and the Stenopadus group of the tribe Mutisieae. A priori, this might be taken to suggest some sort of relationship between Cloiselia and these other groups, but in view of phylogenetic studies (Kim et al. 2002; Panero and Funk 2002; Funk and Panero 2003) relating Cloiselia to other African genera of the Dicoma group (Bremer 1994) (tribe Dicomeae, Panero and Funk 2002), which are close to the Cardueae tribe and thus phylogenetically rather advanced, it must be concluded that these apparently plesiomorphic characters could be a result of isolation and protection from competition, as seen in many other plant and animal lineages on Madagascar. TAXONOMIC TREATMENT CLOISELIA S. Moore in J. Bot. (London) 44: 148 (1906). TYPE: Cloiselia carbonaria S. Moore in J. Bot. (London) 44: 148 (1906). Tree to shrub to 10 m high. Branches nearly rounded to quadrangular, slightly striate, glabrous to glabrescent, with a greyish white tomentum of simple hairs. Leaves simple, alternate to fasciculate, oblanceolate to spathulate, with pseudopetiole; the margins entire; apex rounded, often with a mucro, rarely emarginate; concolorous with both surfaces glabrous or gla-


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FIG. 3. Light microscope photographs showing differences between style of Cloiselia (four nerves) and Dicoma (two nerves). A. Cloiselia humbertii (H. Humbert 11294 P). B. Dicoma anomala Sond. subsp. anomala (M. Silva 3181 COI). Scale bar 5 100 mm.

brescent to 6 densely greyish white tomentose, or discolorous, with the abaxial surface much more densely tomentose than the adaxial. Capitula numerous, solitary or in groups of 2–4, terminal on slender to stout foliose peduncles; involucre cyathiform to obconic, with phyllaries 5–9-seriate, greenish, acute, often slightly pungent, whitish tomentose to glabrescent, the margins not scariose to slightly scariose and entire to shortly serrulate-fimbriate principally towards the apical part. Receptacle flat to slightly concave, alveolate, the pits without border. Florets 2–8 per capitulum. Corolla zygomorphic, often with one sinus much deeper than the others (i.e., corolla ligulate without expanded limb), sometimes nearly actinomorphic, purplish to yellowish, often villous; tube often with an enlarged bulbous basal part; 5 short to long lobes. Stamens with

the entire anthers fully exserted from corolla; filament inserted at the corolla base, with a conspicuous collar; anthers with apiculate to caudate apical appendages; anther base caudate and calcarate, with long tapering tails with several retrorse hairs and a few antrorse hairs basally; tails of adjacent anthers connate. Style with short separate branches not curved or slightly curved, with acute sweeping hairs forming a subapical tuft. Cypselas turbinate, 8- to 10-ribbed, hispid, covered with ascending white to yellowish hairs, these inserted between the ribs; with superficial glands in a continuous layer all around the cypsela; pappus protruding well beyond the involucre, isomorphous, of barbellate purplish to yellowish bristles arranged in several series, the inner slightly wider, patent after fruiting.

Key to the species of Cloiselia. 1. Corollas pink to purple; peduncles generally 5–20 mm long; pappus orange to purplish . . . . . . . . . . . . . . . . . . . . . . . . 2 2. Capitula solitary or in groups of 2–4; peduncles slender 1 mm wide; involucre 6–11 3 4–9 mm, cyathiform to obconic; generally with 25–35 phyllaries arranged in 5–6 rows, innermost phyllaries 4–8 3 1.5–3 mm; (2-)3–4 florets per capitulum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. C. carbonaria 2. Capitula often solitary; peduncles stout 1.5–2 mm wide; involucre 13–18 3 10–20 mm, broadly obconic, generally with 40– 50 phyllaries arranged in 7–8 rows, innermost phyllaries 8–13 3 2–4 mm; (3)4–6 florets per capitulum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. C. madagascariensis 1. Corollas yellowish; peduncles generally 3–6 mm long; pappus yellowish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3. Leaves 3–15 mm wide, oblanceolate to spathulate, conspicuously discolorous; capitula always solitary; involucre 12–13 3 13– 15 mm, broadly obconic, innermost phyllaries 8–10 3 2 mm; 6–8 florets per capitulum; corolla c. 10 mm long, with an enlarged bulbous basal part; pappus of c. 60 bristles up to 7 mm long . . . . . . . . . . . . . . . . . . . . . . . . . 3. C. oleifolia 3. Leaves 1.5–5 mm wide, linear-oblanceolate, 6 concolorous; capitula often paired; involucre 7–10 3 6–9 mm, narrowly obconic, innermost phyllaries 6–7 3 1–1.5 mm; 5–6 florets per capitulum; corolla 12–13 mm long, without an enlarged bulbous basal part; pappus of 100–120 bristles up to 13 mm long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. C. humbertii

1. CLOISELIA CARBONARIA S. Moore in J. Bot. (London) 44: 148 (1906). Dicoma carbonaria (S. Moore) Humbert in Me´m. Soc. Linn. Normandie 25: 149 (1923).- TYPE: MADAGASCAR. Toliara: Fort-Dauphin, Cloisel 35 (holotype: BM!; isotype: P!). Tree to shrub 4–10 m high. Branches subterete, slightly striate, glabrous to glabrescent, with a greyish

white tomentum of simple hairs. Leaves (1–)2.5–6.5 3 (0.2–)0.4–1(–1.7) cm, greenish, alternate to fasciculate, oblanceolate to spathulate, with a pseudopetiole 3–25 mm long; the margins entire; apex rounded, often with a mucro to 0.5 mm long, rarely emarginate; often concolorous, with both surfaces glabrous or glabrescent to 6 densely greyish white tomentose, sometimes slightly

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FIG. 4. A–F. Closelia madagascariensis—A. Branch with capitulum. B. Leaf. C. Capitula. D. Phyllary. E. Floret. F. Cypsela with pappus. G. Cloiselia carbonaria, branch with florets. A–F drawn from Leandri 3668 (P), G drawn from Service de Conservation des Soils de Madagascar 19169SF (P).


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FIG. 5. A–F. Closelia humbertii—A. Branch with capitula. B. Leaf. C. Capitulum. D. Phyllary. E. Floret. F. Cypsela with pappus. G. Cloiselia oleifolia, branch with florets. A–F drawn from Humbert 11294 (P), G drawn from Service des Eaux et Foreˆts de Madagascar 3636SF (P).


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FIG. 6. Distribution of Cloiselia. C. carbonaria (vertical lines). C. madagascariensis (horizontal lines). C. oleifolia (dots). C. humbertii (black).

discolour, with the abaxial surface more densely tomentose. Capitula often pendant, solitary or in groups of 2–4 on the ends of slender, foliose peduncles 4–20 3 1 mm; involucre (6–)7–11 3 4–7(–9) mm, cyathiform to obconic, with (20)25–35(50) phyllaries, 5–6-seriate, greenish, acute, whitish tomentose to glabrescent, the margins slightly scariose and shortly serrulate-fimbriate principally distally; outermost phyllaries (0.7–)1.5– 2.5 3 (0.7–)1–2 mm, deltoid; middle phyllaries 1.5–5 3 (1–)1.5–2.5(–3) mm, deltoid to oblong-lanceolate, erect; innermost phyllaries 4–7(–8) 3 1.5–3 mm, longer than outer phyllaries, oblong-lanceolate, erect. Receptacle flat to slightly concave. Florets (2–)3–4 per capitulum. Corolla (9–)17–22 3 2–3 mm, strongly zygo-

morphic, often with one sinus much longer than the others, pink to purple, often with hairs; tube 3–14 mm, basally enlarged, bulbous; lobes 1–14 mm long. Stamens exserted 3–20 mm beyond the corolla; filament 10–12 mm long; collar c. 0.5 mm long; anthers 16–17(– 18) mm long; apical appendages 4–5 mm long, apiculate to caudate, apiculum 0.3–0.8 mm; anther tails 6– 7 mm long, with retrorse hairs up to 1 mm long and (0)3–10 antrorse hairs at the tip. Style 23–27 mm long, branches c. 1 mm long, with sweeping hairs forming an abaxial subapical tuft covering a surface c. 0.3 mm long. Cypselas 4–5 3 3(–4) mm, covered with 0.5–2 mm long hairs; pappus exserted (8.5–)12–17 mm beyond the involucre, made up of 120–180 barbellate red-


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dish to purple bristles, 3–4-seriate, the longest bristles 17–20 mm long, the shortest 5–10 mm long; barbellae c. 0.1–0.2 mm long (Fig. 4). Species with reddish to purplish florets and pappi, characterized by its capitula with small involucres arranged in groups on slender, often pendant, peduncles. The most similar species to C. carbonaria is C. madagascariensis. Cloiselia carbonaria occurs in bush and forests in a large area in the south of Masdagascar, in the provinces of Toliara and Fianarantsoa (Fig. 6). Vernacular Names. Varomamony, totsivonimbary, pisopiso, farimau. Representative Specimens Examined. MADAGASCAR. Fianarantsoa: Ambatomainty, Decary 9296 (K, P). Toliara: Antanimora, Betaly Forest, Decary 2957 (P, K, BM); Antanimora, Sonave, Service des Eaux et Forets de Madagascar 7741SF (P); 10 Km S of Antanimora, Service des Eaux et Forets de Madagascar 4193SF (P); Fort Dauphin, Andohahely, Dumetz 1340 (P, K); W of Fort Dauphin, Anarafito, Service des Eaux et Forets de Madagascar 1219 SF (P); W of Fort Dauphin; 5 kms NW of Tsimilofo, Willing 1 (MO); between Amboasary and Fort Dauphin, Keraudren-Aymonin & Aymonin 24851 (P); Amboasary, J. Bosser 10218 (P); Ambovombe, Bekiria, Mandrau Valley, Decary 9239 (P, K, BM); W of Ambovombe, near Ampanihy, Service des Eaux et Forets de Madagascar 8474SF (P, K, MO); NW of Ambovombe, Ambaliandro, Decary 9211 (P, K); km 44 on the road Toliara-Ihosy, L. Bernardi 11422 (K, FT); Behara, Ramarokoto Forest, Conservation des Re´serves Naturelles et Parcs Nationaux de Madagascar 3406 RN (P); Mahafaly Plateau, Onilahy, Humbert 2663 (P); Beza Mahafaly Reserve, near Betioky, P.B. Phillipson 2357 (MO, P); Beza Mahafaly Reserve, near Betioky, Van der Werff, Malcomber, B. Gray & Rapanarivo 12699 (K, MO, UPS); Fangidraty, Decary 9329 (P); between Tsimelaha and Ambatohabo, Andohahela National Park, P. Hoffmann, Ranaivojaona, Ralimanana & Randriamampionona 151 (K).

2. Cloiselia madagascariensis S. Ortiz, sp. nov.— TYPE: MADAGASCAR. Toliara: Environs de Toliara, La Table, alt. 0–200 m, bush with euphorbies, 4 November 1960, J. Leandri 3668 (holotype: P!; isotypes: K!, MO!). A C. carbonaria S. Moore differt involucris obconicis, maioribus, phyllariis manifeste longioribus—intimis, praesertim—capitulisque nulla exceptione solitariis, pedunculo insertis latiore, rigido, lignificato. Shrub to tree to 5 m high. Branches subterete, slightly striate, glabrous to glabrescent, with a greyish white tomentum of simple hairs, especially on young branches. Leaves (0.8–)2–3.5 3 0.2–0.9 cm, greenish, alternate to often fasciculate, oblanceolate to spathulate, with a pseudopetiole (2–)3–10(–15) mm long; the margins entire; apex rounded, often with a mucro to 0.3 mm long; often concolorous, with both surfaces 6 densely greyish white tomentose, sometimes slightly discolorous, with the abaxial surface more densely tomentose. Capitula often solitary, terminal on stout, curved, foliose peduncles (3–)5–13(–15) 3 1.5–2 mm; involucre 13–18 3 (10–)13–17(–20) mm, broadly obconic, with (35)40– 50(60) phyllaries, (6)7–8(9)-seriate, light white-green, acute, slightly pungent, whitish tomentose, the margins not scariose to very narrowly scariose, shortly ser-

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rulate principally distally; outermost phyllaries 1–2.5 3 0.5–2.5 mm, deltoid, erect-patent; middle phyllaries 1.5–8 3 1.5–4(–5) mm, deltoid to oblong-lanceolate, erect; innermost phyllaries (8–)9–13 3 2–3(–4) mm, conspicuously longer than outer phyllaries, oblonglanceolate, erect. Receptacle 6 flat. Florets (3)4–6 per capitulum. Corolla (18–)20–23 3 2–4 mm, strongly zygomorphic, often with one sinus much longer than the others, pink to orange-red, often with hairs; tube 6– 16(–18) mm, basally enlarged, bulbous; lobes 0.3–15 mm long. Stamens exserted 17–18 mm beyond the corolla; filament 11–13(–15) mm long; collar c. 0.5–0.7 mm long; anthers 14–18 mm long; apical appendages 4–4.5 mm long, apiculate-caudate, apiculum 0.3–0.7 mm; anther tails (4.5–)6–7 mm long, with retrorse hairs up to 1 mm long and (0)2–5 antrorse hairs at the tip. Style 21–28 mm long, branches 0.5–1 mm long, with sweeping hairs forming a subapical tuft covering a surface c. 0.3–0.7 mm long. Cypselas 2.5–5 3 (–2)3– 5 mm, covered with 0.5–2.5 mm long hairs; pappus exserted (7–)9–12(–14) mm beyond the involucre, made up of 100–150 barbellate orange to purplish bristles, 3(4)-seriate, the longest bristles 16–21 mm long, the shortest 3–4 mm long; barbellae c. 0.2 mm long (Fig. 4). Species with reddish to purplish florets and pappi, characterized by its capitula with large involucres generally solitary on stout peduncles. The most similar species to C. madagascariensis is C. carbonaria. Cloiselia madagascariensis is restricted to the area of Toliara (Toliara province) in SW Madagascar (Fig. 6) where it occurs in bush with euphorbias and in spiny forests. Vernacular Names. Varimamona. Representative Specimens Examined. MADAGASCAR. Toliara: 15 km E of Toliara along road Nationale 7, Schatz, Baum, Villiers & Klackenberg 1772 (P, K, MO); 15 km of Toliara on road N7, Montagne de La Table, Civeyrel 1207 (K); Toliara, La Table, Morat & Raharimalala 7929 (P); Table-Toliara, F. Chauvet 359 (P, K); near Toliara, near the coast on the track to St. Agustin, J. Leandri 3730 (P, K); Toliara, St. Agustin, Service des Eaux et Forests de Madagascar 12441SF (P) (This specimen presents smaller capitula than is usual in this species); St. Augustin-Mamoroka, Peltier 1296 (P).

3. Cloiselia oleifolia (Humbert) S. Ortiz, comb. nov.— Dicoma oleifolia Humbert in Me´m. Soc. Linn. Normandie, Bot. 25: 306 (1923) as ‘‘oleaefolia’’.—TYPE: MADAGASCAR. Mahajanga: Forest of Manomba, sandy plateau, February 1892, Douliot s.n. (syntype: P!). Proximity of Bedanga near Soalala (Ambongo), bare hills, May 1902, Perrier de la Bathie 1428 (syntype: P!). Near Mahavavy, hills not far from the sea, June 1903, Perrier de la Bathie 1428 bis (syntype: P!, chosen here as lectotype). Between la Betsiboke and la Mahavevy, hills not far from the sea, 1914, Perrier de la Bathie 7314 (syntype: P!). Shrub 2–4 m high. Branches subterete to almost qua-


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drangular, slightly striate, glabrous to covered with a greyish white tomentum of simple hairs, especially on young branches. Leaves (0.8–)1–4 3 0.3–1.5 cm, mostly fasciculate, oblanceolate to spathulate, with a pseudopetiole 0.2–10 mm long; the margins entire; apex rounded, often with a mucro to 0.3 mm long, sometimes emarginate; conspicuously discolorous, with the adaxial surface greenish, glabrous to glabrescent, the abaxial surface with a dense whitish tomentum of simple hairs mixed with wax. Capitula solitary on stout, short, erect-patent, tomentose, foliose peduncles 4–6 (–25) 3 1–2 mm; involucre 12–13 3 13–15 mm, broadly obconic, with 30–40 phyllaries, 5–6-seriate, acute to slightly acuminate, slightly pungent, white tomentose, the margins entire to very shortly serrulate principally distally; without scariose margin; outermost phyllaries 1.5–2.5 3 0.7–1.5 mm, deltoid, erect-patent; middle phyllaries 2.5–8 3 1.5–2.5 mm, deltoid to oblong-lanceolate, erect; innermost phyllaries 8–10 3 2 mm, conspicuously longer than outer phyllaries, oblong-lanceolate, erect. Receptacle 6 flat to concave. Florets 6–8 per capitulum. Corolla 10 3 2.5 mm, slightly zygomorphic, yellowish, often with hairs, tube 2.5 mm, basally enlarged; lobes 7–10 mm long. Stamens exserted c. 11 mm beyond the corolla; filament 8 mm long; collar c. 0.3 mm long; anthers 9.5 mm long; apical appendages 3.5 mm long, apiculate-caudate; anther tails 3.5–4 mm long, with retrorse hairs up to 0.5 mm long and c. 5 antrorse hairs at the tip. Style 15–15.5 mm long, branches c. 0.5 mm long, with sweeping hairs forming a subapical tuft covering a surface c. 0.3–0.4 mm long. Cypselas 2–2.2 3 1–1.3 mm, covered with 0.5–1.5 mm long hairs; pappus exserted 4–6 mm beyond the involucre, made up of c. 60 barbellate, yellowish bristles, 3(–4)-seriate, the longest bristles 6.5–7 mm long, the shortest 1 mm long; barbellae c. 0.1–0.2 mm long (Fig. 5). Species with yellowish florets and pappi, characterized by its broad, discolorous leaves and its solitary capitula with broad involucres. The most similar species to C. oleifolia is C. humbertii. Cloiselia oleifolia occurs on bare, siliceous and limestone hills and plateaus along a coastal strip in central and northwest Madagascar, in Mahajanga province (Fig. 6). Vernacular Names. Hazontifa. Representative Specimens Examined. MADAGASCAR. Mahajanga: Mahajanga, Madroibe, Kaudern s.n. (S); Bekapika, Service des Eaux et Forests de Madagascar 3636SF (P); Tambohorano, Decary 8022 (P); near Soalala, Decary 7818 (P).

4. Cloiselia humbertii S. Ortiz, sp. nov.—TYPE: MADAGASCAR. Toliara: Beroroha, Mangoky and de L’Isahaina valley, sandy soils, alt. 200 m, October 1933, H. Humbert 11294 (holotype: P!; isotype: K!). A C. oleifolia (Humbert) S. Ortiz differt foliis linearibus, concoloribus, capitulisque minoribus, plerumque

geminis, donatis floribus paucioribus, cypselis minoribus pappoque breviore. Shrub to shrublet. Stem ramified; the branches subterete, glabrous. Leaves 1.5–5 3 0.1–0.5 cm, mostly fasciculate, rarely alternate, linear-oblanceolate, with a pseudopetiole 2–20 mm long; the margins entire; apex rounded, often with a mucro to 0.2 mm long; 6 concolorous, glabrous to greyish white tomentose-araneose, sometimes with the abaxial surface more densely tomentose. Capitula often paired on short, stout, erectpatent, whitish-tomentose, foliose peduncles 3–5 3 (1–)1.5(–2) mm; involucre (7–)8–9(–10) 3 6–7(–9) mm, narrowly obconic, with 35–40 phyllaries, (7–)8(–9)-seriate, acute, slightly pungent, with a lax white tomentum, the margins shortly serrulate-fimbriate principally distally, not scariose; outermost phyllaries 0.5–1 3 0.3–0.7 mm, deltoid, erect-patent; middle phyllaries 1– 5 3 1–2 mm, deltoid to oblong-lanceolate, erect; innermost phyllaries 6–7 3 1–1.5 mm, conspicuously longer than outer phyllaries, oblong-lanceolate, erect; receptacle concave. Florets 5–6 per capitulum. Corolla 12–13 3 2 mm, zygomorphic, yellowish, with hairs, tube 3– 4 mm, without enlarged bulbous basal part; tube 3–4 mm; lobes 9–10 3 0.5 mm long. Stamens exserted 10– 11 mm beyond the corolla; filament 8–9 mm long; collar c. 0.7 mm long; anthers 9–10 mm long; apical appendages 3–4 mm long, conspicuously apiculate-caudate, apiculum 0.5–0.7 mm; anther tails 3.5–4 mm long, with retrorse hairs up to 0.8 mm long and 3–5 antrorse hairs at the tip. Style 13 mm long, branches 0.5 mm long, with sweeping hairs forming a subapical tuft covering a surface c. 0.4 mm long. Cypselas 2.5–3 3 2.5–3 mm, covered with 0.3–2 mm long hairs; pappus exserted 7–9 mm beyond the involucre, made up of 100–120 barbellate, yellowish bristles, 3–5-seriate, the longest bristles 12–13 mm long, the shortest 1.5 mm long; barbellae c. 0.1–0.2 mm long (Fig. 5). Species with yellowish florets and pappi, characterized against C. oleifolia by its narrow, concolorous leaves and its often paired capitula with narrow involucres. Cloiselia humbertii is known only from the type locality near Beroroha (province of Toliara) (Fig. 6), where it occurs on sandy soils. ACKNOWLEDGEMENTS. Our thanks go to Manuel Laıńz for the Latin diagnoses, to Luis G. Orellana for the illustrations, to G. Norman for the English translation, and to the keepers of the cited herbaria for the loan of study material. This work has been supported in part by the CGL2005-06878-01/BOS project.

LITERATURE CITED BREMER, K. 1994. Asteraceae. Cladistics & classification. Portland: Timber Press. CARLQUIST, S. 1957. Anatomy of Guayana Mutisieae. Memoirs of the New York Botanical Garden 9: 441–476. DORMER, K. J. 1962. The fibrous layer in the anthers of Compositae. New Phytologist 61: 150–153. FUNK, V. A., R. J. BAYER, S. KEELEY, R. CHAN, L. WATSON, B. GE-


2006]


MEINHOLZER, E. SCHILLING, J. L. PANERO, B. G. BALDWIN, N. T. GARCIA-JACAS, A. SUSANNA, and R. K. JANSEN. 2005. Everywhere but Antarctica: Using a supertree to understand the diversity and distribution of the Compositae in: Proceedings of a Symposium on Plant Diversity and Complexity Patterns— Local, Regional and Global Dimensions, eds. I. Friis and H. Balslev. Copenhagen: The Royal Danish Academy of Sciences and Letters. GRAU, J. 1980. Die Testa der Mutisieae und ihre systematische Bedeutung. Mitteilungen (aus) der Botanischen Staatssammlung Mu¨nchen 16: 269–332. HUMBERT, H. 1923. Les Composeés de Madagascar. Me´moires de la socie´te´ linneéne de Normandie. Botanique 25: 1–334. ———. 1963. Flore de Madagascar et des Comores. Plantes vasculaires. Famille 189. Composeés.Vol. 2. Paris. KARIS, P. O., M. KA¨LLERSJO¨, and K. BREMER. 1992. Phylogenetic analysis of the Cichorioideae (Asteraceae), with emphasis on the Mutisieae. Annals of the Missouri Botanical Garden 79: 416– 427. KIM, H.-G., S. C. KEELEY, P. S. VROOM, and R. K. JANSEN. 1998. Molecular evidence for an African origin of the Hawaiian endemic Hesperomannia (Asteraceae). Proceedings of the National Academy of Sciences USA 95: 15440–15445. ———, D. J. LOCKERMAN, and R. K. JANSEN. 2002. Systematic im-

431

plications of ndhF sequence variation in the Mutisieae (Asteraceae). Systematic Botany 27: 598–609. MOORE, S. 1906. Alabastra Diversa.-Part XIII. Journal of Botany (London) 44: 145–154. ORTIZ, S. 2000. A phylogenetic analysis of Dicoma Cass. and related genera (Asteraceae: Cichorioideae: Mutisieae) based on morphological and anatomic characters. Annals of the Missouri Botanical Garden 87: 459–481. ———. 2001 The reinstatement of the genus Macledium Cass. (Asteraceae, Mutisieae): morphological and phylogenetic arguments. Taxon 50: 733–744. ——— and A. P. COUTINHO. 2001. Achyrothalamus reduced to Erythrocephalum (Asteraceae, Mutisieae). Taxon 50: 389–403. PANERO, J. L. and V. A. FUNK. 2002. Toward a phylogenetic subfamilial classification for the Compositae (Asteraceae). Proceedings of the Biological Society of Washington 115: 909–922. PRUSKI, J. F. 1989. Compositae of the Guayana Highland, II: novelties in Gongylolepis and Stenopadus (Mutisieae). Annals of the Missouri Botanical Garden 76: 993–1003. ———. 1997. Asteraceae. Pp. 177–774 in Flora of the Venezuelan Guayana, eds. J. A. Steyermark, P. E. Berry and B. K. Holst. St. Louis: Missouri Botanical Garden Press. ———. 2004. Missouri Botanical Garden, Research; Asteraceae (Compositae). St. Louis: Missouri Botanical Garden Press.