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The subfamily Mutisioideae (Asteraceae).

Introduction

In the taxonomic history of the family Asteraceae, two significant classification systems, one by Cassini (1819) and the other by Bentham (Bentham & Hooker, 1873), were proposed. Cassini (1816, formally 1819) established 19 tribes, among them the Mutisieae and Nassauvieae. Bentham (Bentham & Hooker, 1873) proposed a system of 13 tribes, including the tribe Mutisieae (as Mutisiaceae), which was divided into five subtribes. Bentham's system mostly prevailed years, with changes in the circumscription of the subtribes (e.g., Hoffmann, 1894; Cabrera, 1961, 1977; Hansen, 1990; Bremer, 1994; Table 1), until recent years with the appearance of molecular phylogenies.

Cassini (1816, 1819) proposed the tribe Mutisieae to include the genera with bilabiate corollas considered by Lagasca (1811) in his Chaenanthophorae and by de Candolle (1812) in his Labiatiflorae. Cassini emphasized the style characteristics over the corolla morphology and established two related tribes: Mutisieae and Nassauvieae. The tribe Mutisieae included genera with short style branches internally uniformly covered by stigmatic papillae and externally covered by short hairs: "... ses deux stigmatophores courts, non divergentes, un peu arques en dedans, demi-cylindriques, arrondies au sornmet qui est un peu epaissi; leur face interne plane porte deux tres-petits bourrelets stigmatiques marginaux confluens au sommet, et souvent imperceptibles; leur face externe convexe porte sur sa partie superieure quelques petits collecteurs papilliformes, epars" (Cassini, 1819: 199). The Nassauvieae, on the other hand, included genera with long, truncate style branches, with a crown of collector hairs at the apex: "... ses deux stigmatophores d'une longueur moyenne, divergens, arquds en dehors, demi-cylindriques, tronques au sommet qui est un peu epaissi; leur face interne plane porte deux tres-petits bourrelets stigmatiques marginaux, souvent imperceptibles; leur troncature terminale est garnie d'une touffe de collecteurs piliformes" (Cassini, 1819: 198).

The Mutisioideae were first proposed by Lindley (1829) as his suborder Mutisieae with two tribes, Archetypae (containing Chaetanthera Ruiz & Pav.) and Gerbereae (with Chaptalia Vent., Gerbera L., and Perdicium L.) (Table 1). Lindley (1829) also established the Nassauvioideae as his suborder Nassauvieae, with the tribes Archetypae (including Triptilion Ruiz & Pav.) and Trixideae (including Jungia L. f. and Trixis P. Browne). Lindley's subfamily ranks were not used by further authors until Bremer in 1996.

In 1830, Don established the tribe Stifftieae characterized by bisexual florets with tubular five-lobed corollas, stamens inserted in the corolla throat, with caudate anthers and separate and recurved style branches. Don's tribe Stifftieae included the genera Stifftia J. C. Mikan, Anastraphia D. Don [= Gochnatia Kunth], and Pentaphorus D. Don [= Gochnatia].

After Cassini, Lessing (1832) made another important contribution to the tribal classification of Asteraceae. Lessing also emphasized style features and reduced the number of Cassini's tribes from 19 to eight. Two of Lessing's tribes were Mutisiaceae, divided into three subtribes (Mutisieae, Lerieae, and Facelidae), and Nassauviaceae, divided into two subtribes (Nassauvieae and Trixideae) (Table 1).

As previously pointed out, Bentham, another great contributor to the family's classification, produced in 1873 a system of 13 tribes. His tribe Mutisiaceae included the five subtribes Bamadesieae, Onoserideae, Gochnatieae, Gerberieae, and Nassauvieae, which were reduced to three by Hoffmann in 1894 (Gochnatinae, Mutisinae [Gerberinae in the key] and Nassauvinae) (Table 1). Bentham used a wider spectrum of different morphological characters than did previous authors. He emphasized types of capitula in his classification and included in the Mutisieae genera with other types of corolla than the bilabiate, such as ligulate and tubular corollas.

In the twentieth century, Jeffrey (1967) revised African Mutisieae and established 12 informal series mainly based on style morphology. Some of Jeffrey's series, such as the Dicoma Cass., Pertya Sch. Bip., and Pleiotaxis Steetz series, were the basis, with much re-arrangement, of some generic groups that would be recognized by future authors (e.g., Hansen 1991a; Bremer, 1994). On the other hand, the Stifftia series, defined by rounded, glabrous, and short style branches and glabrous corollas, has been substantially modified from Jeffrey's concept. The genera included by Jeffrey in the Stifftia series were Achnopogon Maguire, Steyenn. & Wurdack, Cnicothamnus Griseb., Duidaea S. F. Blake, Gochnatia, Glossarion Maguire & Wurdack, Gongylolepis R. H. Schomb., Nouelia Franch., Oldenburgia Less., Quelchia N. E. Br., Stifftia, Stomatochaeta (S. F. Blake) Maguire & Wurdack, and Wunderlichia Riedel ex Benth. Some of these genera were later studied in more detail (e.g., Pruski, 1997; Ortiz, 2000; Freire et al., 2002) and shown to have papillose styles and/or pubescent corollas instead of glabrous as treated by Jeffrey.

Crisci (1974a, 1980) treated the subtribe Nassauviinae, performing detailed morphological and palynological studies and establishing its monophyly and the relationships among its genera.

Cabrera's paper on Mutisieae (1977), first presented at the International Symposium on the Biology and Chemistry of Asteraceae in 1975, can be viewed as the first, modern systematic review of the tribe Mutisieae. Cabrera divided Mutisieae into four subtribes: Barnadesiinae, Gochnatiinae, Mutisiinae, and Nassauviinae, following his previous classification (Cabrera, 1961). In the subtribe Barnadesiinae, he included several genera from Hoffmann's subtribes Gochnatiinae and Mutisiinae. Of the four subtribes, he considered the Nassauviinae as the most natural in the tribe, morphologically homogeneous and geographically well-defined. Cabrera defined the Mutisieae as having bilabiate corollas, caudate anthers, and characteristic style shape. He pointed out, however, that several genera of Mutisieae differ in having actinomorphic or ligulate corollas and ecaudate anthers (the last feature in some genera of Barnadesiinae). Cabrera concluded that "... there is no doubt that certain genera must be excluded from the tribe or transferred to other subtribes; perhaps genera of other tribes should be included in the Mutisieae" (Cabrera, 1977: 1041). As circumscribed by Cabrera (1977), the Mutisieae included 83 genera (Table 2) and about 950 mainly American species, with some representatives in southern Asia and Africa and one species in Australia. The four subtribes were mainly distinguished as follows: central florets actinomorphic in Barnadesiinae and Gochnatiinae versus bilabiate in Mutisiinae and Nassauviinae; corollas villous and axillary spines in Barnadesiinae versus non villous and absence of axillary spines in Gochnatiinae; style branches rounded at the apex without collector hairs in Mutisiinae versus truncate with a crown of collector hairs in Nassauviinae. Cabrera distinguished papillae (very short, conical to rounded hairs, spread on the outer side of the style branches) from collector hairs (longer, cylindrical, obtuse at the apex hairs, that form a truncate brush terminally at the style branches), restricting the use of the term collector hairs to Nassauviinae.

Jansen and Palmer (1987) found that a large chloroplast DNA inversion present in Asteraceae is absent in some genera of the subtribe Barnadesiinae, which were then put in their own subfamily (Bremer & Jansen, 1992). With this change, the Asteraceae were divided into three subfamilies: Barnadesioideae with one tribe, Cichorioideae with six tribes (one the Mutisieae), and Asteroideae with ten tribes. At this point, Mutisieae began to attract the attention of many workers because of its still unresolved taxonomy and its ancestral position, highlighting its importance for understanding the classification and evolution of the whole family.

Also in 1987, Bremer presented the first cladistic analysis of Asteraceae involving 81 characters of morphology, anatomy, chromosomes, chemistry, and the chloroplast DNA inversion. This study showed the Mutisieae as a paraphyletic grade at the base of the family. One year later, Jansen and Palmer (1988) obtained phylogenies of Mutisieae based on chloroplast DNA restriction site mapping. In this second study, the Barnadesiinae were basal, the Nassauviinae monophyletic, and the Mutisiinae and Gochnatiinae were either monophyletic (using ten restriction enzymes) or paraphyletic (using nine additional restriction enzymes).

Hansen (1991a), considered the tribe Mutisieae as monophyletic on the basis of petal "mutisioid" epidermal pattern (tabular cells with crested outer cell walls) if the Barnadesiinae and several Old World genera of Gochnatiinae (sensu Cabrera, 1977) were excluded from the tribe. Hansen proposed to exclude from Mutisieae the genera Dicoma, Erythrocephalum Benth., Gladiopappus Humbert, Pasaccardoa Kuntze, and Pleiotaxis (and their current synonyms), later called the Dicoma group by Bremer (1994). Hansen also suggested the genera Adenocaulon Hook., Brachylaena R. Br., Tarchonanthus L., and Warionia Benth. & Coss. to be excluded from Mutisieae. Mutisioid ray corolla epidermal cells appear to be not exclusive of Mutisieae, they also occur in the Barnadesiinae and in some Arctoteae (Bremer, 1994).

Robinson (1991) and formally Bremer (1994) abolished the limits between the Mutisiinae and the Gochnatiinae. Thus, the Mutisieae included only two subtribes: the Mutisiinae s.l. (Mutisiinae s. str. plus Gochnatiinae) and the Nassauviinae. The artificial taxonomic separation of the Mutisiinae and the Gochnatiinae was also confirmed by palynological evidence (Telleria et al., 2003).

Karis et al. (1992) performed a morphology-based cladistic analysis of the family Asteraceae with emphasis on Cichorioideae on the basis of 53 taxa of Asteraceae and 72 characters, using the Barnadesiinae as outgroup. Their tree supported the placement of a paraphyletic tribe Mutisieae as a basal assemblage to the rest of Asteraceae. Genera of the Mutisieae (Stenopadus S. F. Blake, Hesperomannia A. Gray, Wunderlichia, Ainsliaea DC., and Gochnatia) appeared as isolated clades at the base of one of the two equally parsimonious final trees, other genera (Actinoseris (Endl.) Cabrera, Cnicothamnus, and Brachylaena) were sister to most Mutisieae, and others (Stifftia, Gongylolepis, Hyaloseris Griseb., and Pertya) were clades basal to the rest of Cichorioideae and Asteroideae.

In Bremer's (1994) treatment of the family Asteraceae, Mutisieae included 76 genera and ca. 970 species (Table 2). This treatment represented, after Cabrera (1977), a second, modern systematic review of the tribe. Bremer included in Mutisieae the subtribes Mutisiinae s.l. and Nassauviinae. Within Mutisiinae, he presented a tentative arrangement of generic groups, some already suggested by previous authors: the Stenopadus group (Achnopogon, Chimantaea Maguire, Steyerm. & Wurdack, Duidaea, Glossarion, Gongylolepis, Neblinaea Maguire & Wurdack, Stenopadus, Stomatochaeta); Gochnatia and related genera (Actinoseris, Chucoa Cabrera, Cyclolepis D. Don, Gochnatia, Hyalis D. Don ex Hook. & Am., Nouelia); the Ainsliaea group (Ainsliaea, Macroclinidium Maxim., Myripnois Bunge, Pertya); Brachylaena and Tarchonanthus; the Plazia group (Aphyllocladus Wedd., Gypothamnium Phil., Plazia Ruiz & Pav.); the Dicoma group (Achyrothalamus O. Hoffm., Dicoma, Erythrocephalum, Gladiopappus, Pasaccardoa, Pleiotaxis); Onoseris Willd. and Urmenetea Phil.; Mutisia L. f. and Hyaloseris; the Chaetanthera group (Brachyclados D. Don, Chaetanthera, Pachylaena D. Don ex Hook. & Arn.); the Gerbera group (Chaptalia, Gerbera, Leibnitzia Cass., Perdicium, Trichocline Cass., Uechtritzia Freyn). Further, Bremer's Nassauviinae included 24 genera with ca. 320 species. The genera Catamixis Thomson, Cnicothamnus, Hecastocleis A. Gray, Hesperomannia, Lulia Zardini, Lycoseris Cass., Oldenburgia, Stifftia, and Wunderlichia were regarded as isolated in the tribe Mutisieae. Again, the monophyly of Nassauviinae and the paraphyly of Mutisiinae s. 1. were recognized. Bremer (1996) later modified the traditional scheme of the subfamily Cichorioideae, which, until then, was constituted by the tribes Arctoteae, Cardueae, Lactuceae [= Cichorieae], Liabeae, Mutisieae, and Vernonieae. He treated the subfamily Cichorioideae as only containing Arctoteae, Lactuceae, Liabeae, and Vernonieae, with the tribe Cardueae the sole member of the subfamily Carduoideae. Although implicit in the cladogram, the Mutisieae were not raised to subfamilial level: it remained as an unresolved grade awaiting their reclassification, at the base of the family tree above the Barnadesioideae. Molecular phylogenies based on ndhF sequences (Jansen & Kim, 1996) mostly supported Bremer's scheme but with a paraphyletic Cardueae.

Pruski (2004) and Jeffrey (2004; for Stifftieae) resurrected the tribes Stifftieae and Nassauvieae. Pruski and Sancho (2004), following Bremer's (1996) scheme, recognized the subfamily Mutisioideae as one of the five subfamilies of Asteraceae: Barnadesiinae, Mutisioideae, Carduoideae, Cichorioideae, and Asteroideae. In this contribution, morphologically based, we follow this scheme and consider the subfamily Mutisioideae to be comprised of three tribes: Mutisieae, Nassauvieae, and Stifftieae.

Two molecular phylogenetic studies (Kim et al., 2002; Panero & Funk, 2002) investigated the circumscription of Mutisieae. Kim et al. (2002) used DNA sequences of the chloroplast gene ndhF from 31 genera and obtained an unsolved strict consensus tree showing that the Mutisieae are polyphyletic and that the genera Tarchonanthus, Brachylaena, Dicoma, Pasaccardoa, Ainsliaea, Pertya, and Myripnois are related to the Cardueae. Results of Panero and Funk (2002), using several chloroplast genes and molecular markers (ndhF, trnL-trnF, matK, ndhD, rbcL, rpoB, rpoC1, exonl, 23S-trnI, and ndhI), supported the establishment of the new subfamilies Gochnatioideae (Cnicothamnus, Cyclolepis, Gochnatia, Rickterago Kuntze, possibly Chucoa), Hecastocleidoideae (Hecastocleis), and Pertyoideae (Ainsliaea, Diaspananthus Miq. [= Ainsliaea; Freire, 2007], Macroclinidium, Myripnois, Pertya). The tribes Dicomeae (Dicoma, Erythrocephalum, Gladiopappus, Macledium Cass., Cloiselia S. Moore, Pasaccardoa, Pleiotaxis), and Tarchonantheae (Brachylaena, Tarchonanthus), containing members of the Mutisieae s. 1., were included in Carduoideae. Remaining Mutisieae were recognized as the Stifftia group and a basal, unresolved clade referred to as the Mutisioideae. No tribes, subtribes, or constituting genera were indicated by Panero and Funk within the Stifftia group and the Mutisioideae. Further, more defined molecular phylogenies of the family Asteraceae (Funk et al., 2005; Panero & Funk, 2008) showed approximately the same branching sequence of Panero and Funk's (2002), with a Mutisieae clade containing three clades: the Onoseris clade, the Mutisia clade, and the Nassauvia clade. Based on these results, Panero & Funk (2007) established the following new taxa: the subfamily Stifftioideae (with Dinoseris, Duidaea, Eurydochus, Glossarion, Gongylolepis, Hyaloseris, Neblinaea, Quelchia, and Stifftia), the subfamily Wunderlichioideae with the tribes Wunderlichieae (Chimantaea, Stenopadus, Stomatochaeta, and Wunderlichia) and Hyalideae (Ianthopappus, Hyalis, Leucomeris, and Nouelia), and the tribe Onoserideae of Mutisioideae (with the genera Aphyllocladus, Gypothamnium, Lycoseris, Plazia, Onoseris, and Urmenetea).

The systematic treatment by Hind (2007) regarded a tribe Mutisieae s. 1., which was divided into five subtribes (Nassauviinae, Mutisiinae, Gerberinae, Gochnatiinae, and Tarchonanthinae) and seven groups (Catamixis, Dicoma, Hecastocleis, Nouelia, Pertya, Stenopadus, and Stifftia groups) and recognized two genera, Adenocaulon and Eriachaenium, as having a problematic placement.

Finally, Katinas et al. (2008a) performed a molecular phylogenetic analysis of Nassauviinae based on the nuclear ITS and plastid trnL-trnF regions, with a sampling of 46 species of Mutisieae s. 1. The study shows the monophyly of the Nassauviinae and a partial agreement with the tree of Funk et al. (2005) concerning generic relationships within the subtribe.

Despite previous phylogenetic morphological and molecular studies, consensus has not been reached for the limits of Mutisioideae. Since its establishment in 1816 by Cassini and until recent years, the broadest concept of the tribe (Mutisieae sensu lato) was the prevailing one, with little fluctuation in the number of genera and species according to the different authors. After the two central revisionary works of Cabrera (1977) and Bremer (1994), much morphological and palynological work has been done to elucidate the taxonomic limits of Mutisioideae or at least to define generic groups (e.g., Pruski, 1991; Ortiz, 2000; Sancho, 2000, 2004; Freire et al., 2002; Telleria & Katinas, 2004). Moreover, new genera have been described (e.g., Zardini, 1980; Crisci & Freire, 1986; Katinas, 1994; Ortiz, 2001; Roque & Hind, 2001; Jimenez Rodriguez et al., 2004), and generic systematic revisions have been published (e.g., Egerod & Stahl, 1991; Harling, 1995; Katinas, 1996b; Freire, 2007).

There are currently two main taxonomic concepts of the Mutisieae that are in use. One is the concept of the tribe Mutisieae sensu lato, based mainly on morphological grounds. This is the concept employed, for example, by Cabrera (1977), Bremer (1994), Jeffrey (2007, as subfamily Mutisioideae), Hind (2007), and in this contribution (as subfamily Mutisioideae) with some genera variation in each circumscription. These authors recognized groups that were proposed at various times as distinctive 'generic groups' or associations, tribes, or subfamilies based on morphological and/or molecular data. The other concept, based on phylogenies obtained with chloroplast molecular data (e.g., Panero & Funk, 2002, 2007, 2008 as subfamily Mutisioideae; Funk et al., 2005), is that of the tribe Mutisieae sensu stricto (or subfamily Mutisioideae sensu stricto).

This contribution is the result of the extensive work by the authors on the Mutisioideae, toward a comprehensive treatment of the subfamily. We refrain from prematurely creating taxonomic units within tribes. No new formal subtribes are established here, and generic groups are not given ranked status, since several lineages received taxonomic status as a result of the last molecular studies mentioned above. The objectives are (1) to describe and evaluate morphological and palynological characters of taxonomic value within the subfamily Mutisioideae and (2) to describe and illustrate the genera of Mutisioideae.

Material and Methods

Information on the morphology of each genus was obtained from the literature and from our observations of herbarium and fresh specimens. These data result from original as well as from our previous work. In all, 73 of the 74 genera of Mutisioideae (specimens of Catamixis were not seen), ca. 700 of the ca. 860 species of Mutisioideae, 12 of the 13 excluded genera (specimens of Gladiopappus were not seen), and ca. 35 of the 127 excluded species were studied. The source literature is cited below each generic description, and types and representative herbarium specimens studied are cited under the Species list and in the corresponding figure legends. In general, the terminology follows Harris and Wolf Harris (1994) and Steam (1996). Nomenclatural, taxonomic, and other observations were made only when pertinent. In general, the plant illustrations were drawn by Gisela Sancho mostly as modifications from earlier publications, although some drawings are originals; the sources of the figures that were redrawn are cited in the corresponding figure legend. A Wild MS stereomicroscope and a Leitz SM Lux microscope both with the camera lucida technique were used for drawing the details. The style of Tables 5, 6, 7, 8, 9 and 10 is that of the tables of Harold Robinson in his work on Vemonieae (Robinson, 1999). Vegetative and floral parts were dissected and observed after boiling in water and staining with 2% safranin. For the scanning electron microscopy (SEM), portions of styles of FAA-fixed samples were taken, critical-point dried in C[O.sub.2], and examined in a JEOL/EO JSM-6360 microscope at Museo de La Plata, Argentina.

Pollen grains were removed from herbarium specimens and were acetolyzed under standard methods and then chlorinated (Erdtman, 1960). For light microscopy (LM), slides were prepared by mounting the pollen in glycerol jelly and sealing with paraffin. Measurements of the polar (P) and equatorial (E) diameters of pollen grains were based on 25 grains, and measurements of the thickness of the exine were based on at least 15 grains. The P/E ratio was calculated for each specimen. Acetolyzed pollen grains were suspended in 90% ethanol, mounted on stubs for SEM, sputter-coated with gold palladium, and examined with a JEOL JSM T-100 scanning electron microscope. Palynological terminology, in general, follows Punt et al. (1994); the size classification was taken from Erdtman (1969). Pollen sources are cited in the figure legend of each genus and marked with an asterisk (*) in the Species list. Because the pollen of a broad sample of Nassauvieae was studied by Crisci (1974a), we emphasized the study of the pollen of tribes Mutisieae and Stifftieae herein. Two types of pollen descriptions are under each genus: (1) those containing measurements of the polar and equatorial diameters and exine thickness made for this study on the basis of the material marked with an asterisk (*) in the Species list, (2) those lacking measurements already published in previous papers where more detailed descriptions can be found, in which case we cite the relevant literature and important pollen features of the genus.

Morphological Characters

The subfamily Mutisioideae has been subject to previous morphological and palynological studies, among them those of Wodehouse (1929a, b), Koch (1930), Carlquist (1957b, c, 1958), Parra and Marticorena (1972), Crisci (1974a), Baagoe (1977), Cabrera (1977), Skvarla et al. (1977), Grau (1980), Hansen (1991a, b), Freire and Katinas (1995), and Freire et al. (2002).

Key characters for the classification of Mutisioideae are discussed here.

Corolla

Variation in Mutisioideae

The bilabiate corolla was generally considered the typical form in the Mutisioideae. However, as noted by Cabrera (1977), corolla shape is highly variable in the group (Table 3, Fig. 1a-k).

Four basic types of corollas are found in the group under study:

(a) Bilabiate (3+2 corolla lips): zygomorphic, with an external three-dentate lip, radiating or not, and an internal two-cleft lip (Fig. 1d,f).

(b) Tubular (0+5 corolla lobes): actinomorphic, limb five-lobed at the apex, the lobes usually deeply or very deeply incised (Fig. 1j) and less commonly shortly incised (Fig. 1k). These corollas are usually funnelform with a tube gradually expanding into a limb or less frequently sub-campanulate with the tube expanding into the limb.

(c) Ligulate (5+0 ligule lobes): zygomorphic, with a short and narrow tube expanding into a ligule five-lobed at the apex, the lobes deeply (Fig. 1c) or shallowly incised (Fig. 1b).

(d) True ray (3+0 limb lobes): zygomorphic, with a short and narrow tube expanding into a shallowly three-lobed limb (Fig. 1a).

Modifications of these four basic types occur:

(e) Tubular-bilabiate (intermediate between 3+2 corolla lips and 0+5 corolla lobes): sub-zygomorphic, transitional type where the lip-lobes are erect and short and the incisions in the corolla are unequal, resulting in a slightly bilabiate corolla (Fig. 1g,i).

(f) Sub-bilabiate (or pseudobilabiate; 4+1, 3+1 corolla lips): zygomorphic, probably derived from a bilabiate corolla with different degrees of fusion among the teeth. The most common types are corollas with an external three-dentate or four-dentate lip and one entire, untoothed, internal lip (Fig. 1e).

(g) Filiform: irregular or zygomorphic, a very narrow, reduced tubular corolla with a short apical portion irregularly cleft, approaching other types of corollas (e.g., filiform-bilabiate, filiform-tubular, filiform-true ray) (Fig. 1h).

The genera of Nassauvieae, with few exceptions (Acourtia, Lophopappus Rusby), have capitula with all bilabiate corollas. Most genera of Stifftieae have capitula with all tubular corollas; Quelchia is the only genus of the tribe that has tubular and bilabiate corollas. In Mutisieae, corolla morphology is more variable (Table 3), including genera that have capitula containing solely bilabiate corollas (e.g., Achnopogon, Pachylaena) or solely tubular corollas (e.g., Chucoa, Gochnatia). Some genera of Mutisieae are highly variable in corolla morphology (e.g., Lycoseris, Onoseris), and sometimes the variation appears within the same capitulum with transitional forms from the marginal to the central florets (e.g., Leibnitzia). Therefore, corolla morphology is not the main taxonomic character circumscribing the Mutisioideae, despite its use in previous treatments.

The combination of the different types of corollas results in some basic types of capitulum (Bremer, 1994):

(a) Discoid: with morphologically similar, non-radiating florets throughout the capitulum. The capitula may be composed by florets with all tubular (Fig. 1j) or all bilabiate (Fig. 1f) corollas.

(b) Radiate: with true ray corollas or some kind of distinctly radiating marginal florets (e.g., bilabiate, Fig. 1d). Pruski (1997) uses the term "bilabiate" for genera centered in the Guayana Highlands that have generally few-flowered capitula, with all bilabiate corollas, all of them with a large outer lip.

(c) Ligulate: with all corollas possessing a strap-shaped limb with five apical teeth (Fig. 1b) or with deeply five-lobed corollas with one deeper split (Fig. 1c), these slightly ligulate and with unilateral lobes.

(d) Disciform: with at least two morphological types of non radiating florets. Examples include: (1) marginal bilabiate and central tubular (some species of Aphyllocladus), (2) marginal bilabiate, sub-bilabiate, or true ray and central tubular-bilabiate (some species of Chaetanthera), (3) marginal sub-bilabiate, tubular four- or five-lobed and central tubular five-lobed (Adenocaulon), (4) marginal tubular four-lobed and central five-lobed (Eriachaenium Sch. Bip.). There are genera with three types of corollas in the same capitula (capitula trimorphic). For example, Chaptalia has true ray or bilabiate marginal corollas, filiform intermediate corollas, and tubular-bilabiate central corollas.

[FIGURE 1 OMITTED]

Comparison with Closer Subfamilies

Corolla morphology helps to differentiate Mutisioideae from related subfamilies only to some degree. Bilabiate-like corollas exist in other Cichorioideae (e.g., Heterolepis Cass. in Arctoteae, Dipterocypsela S. F. Blake in Vernonieae), but they are not truly mutisioid bilabiate corollas (Bremer, 1994: 220). Tubular corollas in general gradually dilate into a limb (funnelform) in Mutisioideae. In Nouelia and Wunderlichia, the corollas abruptly dilate into a limb (campanulate) as occurs in Arctoteae, most Cardueae, and some Vernonieae and Liabeae. The Barnadesioideae are the most similar subfamily to the Mutisioideae regarding corolla shape, although in the former the corollas are covered by barnadesioid hairs. For instance, the genus Dasyphyllum Kunth (Cabrera, 1959b) has tubular, sub-bilabiate, and ligulate corollas; Fulcaldea Poir., Doniophyton Wedd., and Duseniella K. Schum. have tubular, funnelform corollas; Barnadesia Mutis has sub-bilabiate (4+1 corolla lips) marginal corollas and disc corollas that show all of the transitional morphological states including tubular-funnelform five-lobed, tubular three-four-lobed, sub-bilabiate (3+1, 4+1 corolla lips), sub-ligulate (with one deeper split), and ligulate five-dentate (Urtubey, 1999). Arnaldoa Cabrera, Chuquiraga Juss., and Schlechtendalia Less. have sub-bilabiate (4+1 corolla lips) corollas.

Anthers

Variation in Mutisioideae

The anthers are typically caudate, with the pollen-bearing anther thecae extending below the attachment point of the filament (i.e., calcarate or spurred anthers; Robinson, 1983, 1999) (Fig. 1p). The anther collar was only found in Adenocaulon and Eriachaenium, and the antheropodium is common in some genera of Nassauvieae. The tails are short only in Adenocaulon and Eriachaenium (Fig. 1q). Tails are smooth (glabrous) or papillose, sometimes showing variation within the same genus (e.g., Chaptalia, Gochnatia, Onoseris, Trixis). Tails are usually free, but in some cases (e.g., Glossarion, Gongylolepis, Stenopadus) the tails of adjacent anthers are partially or completely connate. According to Karis et al. (1992), the endothecial thickening is polarized (Dormer, 1962) in Mutisioideae.

The apical appendage is also well developed. In most genera, the appendage is acute (Fig. 1m), but apiculate (e.g., Gochnatia, Cnicothamnus, Chimantaea, some species of Ainsliaea) (Fig. 1n) and truncate apices (e.g., Aphyllocladus, Macrachaenium Hook. f., Plazia) (Fig. 11) are also found. The apical appendages are neither constricted nor demarcated from the thecae, as commonly occurs in the subfamily Asteroideae, except in Adenocaulon and Eriachaenium (Fig. 1o).

Exerted anthers are typical of some Guayana Highland-centered genera and are also present, for example, in Cnicothamnus and species of Gochnatia and Mutisia. In many genera of Mutisieae the anthers are reduced to staminodes in the functionally female florets. The staminodes range from diminute and filiform to very well developed with the appearance of sterile anthers, in some cases containing few pollen grains.

We did not find important morphological differences among the anthers of Mutisieae, Stifftieae, and Nassauvieae.

Comparison with Closer Subfamilies

As occurs with the corolla, the anthers help to differentiate the Mutisioideae only to some extent. Long-caudate anthers are characteristic of Mutisioideae, most Carduoideae, some genera of Barnadesioideae, and part of tribes Lactuceae and Liabeae of Cichorioideae (vs. auriculate). In Barnadesioideae, anthers that are auriculate or decurrent with the filament, such as those of Barnadesia (Urtubey, 1999), are very common. Robinson (1999) considers stamens of most Cichorioideae s.1. (i.e., Mutisioideae, Carduoideae, and Cichorioideae s. str.) as calcarate. The polarized endothecial thickening of Mutisioideae is shared with Carduoideae and Cichorioideae, although in some tribes other types of thickening may exist (Bremer, 1994).

Style

Distinction of Tribes

Style features constitute one of the most important characters to define Mutisioideae and to circumscribe tribes within the subfamily. The subfamily Mutisioideae is characterized by its glabrous to papillose styles, with the papillae or the relatively short hairs apically rounded. The stigmatic area is continuous, covering the whole inner surface of the style branches.

In the tribe Mutisieae, the style branches are usually very short (styles bilobed, Fig. 1s, e.g., Ainsliaea, Trichocline), but there are also genera with long style branches (styles bifid, Fig. 1r, e.g., Dinoseris Griseb., Hyaloseris, Lycoseris). Variation of the style branch length, short or long, occurs also within the same genus (e.g., Chaetanthera, Chaptalia, Gochnatia). The style branch apex is rounded in most genera, rarely truncate (e.g., Eurydochus Maguire & Wurdack, Plazia) or acute (e.g., Cnicothamnus, Chucoa, Macroclinidium). Sometimes the stigmatic surface apically projects upwards, forming an edge that gives an apiculate aspect to the branches (e.g., some species of Gochnatia, Salcedoa F. Jimenez Rodr. & Katinas) (Fig. l s). Dorsally, the style branches are papillose in most genera (Fig. 77a), although smooth (e.g., Gochnatia, Hecastocleis, Gongylolepis) (Fig. 77b) or rugulose branches with swollen dorsal cells (Chimantaea) are present (Fig. 77d). The papillae or short hairs may be variable in length, but they are always rounded at the apex (Fig. 78a-c); acute hairs are completely lacking in Mutisioideae. The papillae are distributed above the style branch bifurcation point in most taxa, covering the whole branch or restricted to the terminal, apical portion of the branch (Fig. 77a). In a few cases, the papillae extend below the style branch bifurcation point (e.g., Pachylaena, Pertya).

In the tribe Stifftieae (e.g., Stenopadus, Stomatochaeta, Wunderlichia), the papillae extend below the style branch bifurcation point toward the style base (Fig. 77c-d); the only exception is the genus Quelchia, which has smooth styles.

In the tribe Nassauvieae, most of the styles have relatively long branches and papillae or collector hairs (Crisci, 1974a; Cabrera, 1977) that form a tuft restricted to the branch apex (Fig. 77e-f). Exceptions are Lophopappus and Macrachaenium, which have styles with dorsally papillose branches.

Crisci (1974a) performed a careful study in all genera of Nassauviinae and determined four style types according to differences in branch length, apex shape, and papilla length and considered the papillae in the styles of Nassauvieae as "collector hairs." The first type has truncate stylar branches (Ameghinoa Speg., Burkartia Crisci, Calopappus Meyen, Dolichlasium Lag., Holocheilus Cass., Jungia, Leucheria, Marticorenia Crisci, Moscharia Ruiz & Pav., Nassauvia, Oxyphyllum Phil., Perezia, Pleocarphus D. Don, Polyachyrus Lag., Triptilion, and Trixis). The second type has the branches less than 1 mm long, rounded at the apex, bearing long collector hairs on the distal half (Cephalopappus Nees & Mart., Lophopappus, Macrachaenium, and Proustia). The third type has the branches more than 1 mm long, rounded and slightly expanded at the apex, with long collector hairs on the distal fifth (Acourtia, Berylsimpsonia B. L. Turner, Leunisia Phil., and Perezia). The fourth type has style branches spathulate, with very long collector hairs in the distal third (Criscia Katinas).

Considering the morphology and pubescence of styles, Erbar and Leins (1995) distinguished different mechanisms of secondary pollen presentation in the Campanulales-Asterales-complex. Two different mechanisms were established for Asteraceae: the brushing and the pump mechanisms. In the brushing mechanism, the back of the style branches and the upper part of the style bear short hairs. The anthers open and pollen is partly loaded onto the hairs of the style. As the style elongates, the pollen grains are completely swept out of the anthers by the brushing hairs. In the pump mechanism, the style branches are truncate with hairs only at their tips. The growing style acts as a piston and pushes the pollen gradually out of the anther tube. Given the style morphology of the tribes, the brushing mechanism would characterize members of Mutisieae and Stifftieae, and the pump mechanism would characterize Nassauvieae.

Comparison with Other Subfamilies

Unlike the styles found in Mutisioideae, the arctotoid and the carduoid styles (Bremer, 1987, 1994) have a ring of collector or sweeping hairs on the shaft below the style branch bifurcation point. In addition, the Arctoteae and many Cardueae have apically thickened styles, whereas the style of Mutisioideae is usually uniform in width. A few genera of Cardueae, such as Amphoricarpus Spruce ex Miers, Chardinia Desf., and Tugarinovia Iljin (subtribe Carlininae), were described as having shortly bilobed and apically minutely pilose styles (Bremer, 1994), thus resembling many genera of Mutisioideae. However, close examination with the light microscope shows that the style branches of these genera of Cardueae have their subapical papillae longer than their apical ones, thus approaching the subapical tuft of hairs typical of the tribe. The tribes Lactuceae, Liabeae, and Vernonieae of Cichorioideae have vernonioid styles (Bremer, 1987), with style branches apically tapered or rounded and with acute collector hairs (in some Vernonieae, there are rounded, multicelled collector hairs; Cabrera, 1944) distributed from the apex to below the branch bifurcation point. Although a continuous stigmatic surface on the style branches is shared among Mutisioideae, Carduoideae, and Cichorioideae, differences in style shape, papillae arrangement, and especially papilla shape (i.e., rounded in Mutisioideae vs. acute in Carduoideae and Cichorioideae, Fig. 78d-f) in the external side of the branches set the subfamily Mutisioideae apart from the other two subfamilies. Styles of the members of the subfamily Asteroideae have collector hairs, with different hair arrangements. In Asteroideae, the stigmatic surface is usually restricted to two bands (Carlquist, 1976), thus strongly differing from the condition in the Mutisioideae.

However, styles of genera of Mutisioideae are more similar to those of the Barnadesioideae than to any other group of Asteraceae. For instance, smooth styles are found in Dasyphyllum, styles dorsally papillose below the branch bifurcation point such as those of tribe Stifftieae may be found in Chuquiraga, Dasyphyllum, Doniophyton, and Schlechtendalia (Cabrera, 1977), and styles papillose above the bifurcation point are found in Barnadesia (Cabrera, 1977; Urtubey, 1999). One might argue that these style characters are symplesiomorphic, however primitive and advanced states recognition for these features depends on the choice of the outgroup (Calyceraceae, Goodeniaceae, Menyanthaceae).

Pollen

Distinction of Tribes

The pollen of Mutisioideae is a useful character mainly to distinguish the subfamily from other subfamilies and to distinguish Nassauvieae from Mutisieae and Stifftieae.

The Mutisioideae would be considered an eurypalynous subfamily because of its wide range of variation in grain size, shape (P/E), aperture type, and exine sculpture and structure. This agrees with Skvarla et al. (1977) who concluded that the pollen of Mutisioideae is diverse at the exo- and endomorphic levels. It should be noted, however, that the major variation occurs in the pollen of the tribes Mutisieae and Stifftieae, whereas the pollen in the tribe Nassauvieae is more homogeneous.

The pollen of the genera of Nassauvieae is tricolporate, microechinate with few developed microspines, the exine distinctly bilayered, and both the ectosexine and the endosexine clearly columellate (Crisci, 1974a) (see 109B of Figs. 107-111 and 112B of Figs. 112-116).

The pollen of Mutisieae and Stifftieae is microechinate, echinate, or almost psilate in some members of Mutisieae; the exine is distinctly bilayered but commonly with a compact ectosexine constituted by columellae very thickly disposed and an endosexine with columellae clearly distinguishable, stout and ramified (Hansen, 1991b; Telleria et al., 2003; Telleria & Katinas, 2004; Zao et al., 2006) (see 80C of Figs. 80-85, 98A of Figs. 95-100, 118B, C of Figs. 117-118 and Fig. 119c).

Besides the characteristic exine structure, additional pollen characters reinforce the distinction of the Nassauvieae from the Mutisieae and Stifftieae: (1) the pollen of Nassauvieae and Stifftieae is always tricolporate, whereas in Mutisieae it can be tricolporate (most genera) or tricolpate (Hecastocleis and some species of Ainsliaea); (2) polar caps are more frequent in pollen of Nassauvieae (e.g., Ameghinoa, Leunisia, Trixis) than in pollen of Mutisieae and Stifftieae; (3) the spheroidal and suboblate pollen shape mainly occurs in Nassauvieae (e.g., Leucheria, Triptilion), whereas the pollen of Mutisieae and Stifftieae have generally subprolate to prolate shape; (4) in Mutisieae (e.g., Chaetanthera, Lulia, Mutisia) the mesoaperture is either clearly distinguishable or diffuse, whereas in Stifftieae it rarely occurs, and it was never reported in Nassauvieae; and (5) the pollen of Nassauvieae is generally smaller (see Material and Methods) than that of Mutisieae and Stifftieae (Parra & Marticorena, 1972; Crisci 1976b; Hansen, 1991b; Zao et al., 2006).

Exine Types

The organization of the exine consists of tectum, ectosexine, endosexine, and nexine. The ectosexine and the endosexine are columellate and they are separated by an internal tectum (clearly distinguishable or not); the nexine is usually thickened at level of aperture.

The pollen of the genera of Nassauvieae may be distinguished on the basis of the thickness of the external and internal tectum and the orientation of the internal tectum. Crisci (1974a) distinguished five exine types; all of them have a tectum surface with very few developed microspines:

(1) Oxyphyllum type: ectosexine and endosexine equally thick, separated from each other by zigzag (non-parallel to nexine) internal tectum (Leucheria, Moscharia, Nassauvia, Oxyphyllum, Polyachyrus, and Triptilion).

(2) Trixis type: ectosexine thinner than endosexine, both layers columellate (Acourtia, Ameghinoa, Berylsimpsonia, Burkartia, Criscia, Dolichlasium, Holocheilus, Jungia, Leunisia, Lophopappus, Macrachaenium, Marticorenia, Pleocarphus, Proustia, and Trixis).

(3) Proustia type: ectosexine and endosexine equally thick, both layers columellate (Lophopappus and Proustia).

(4) Calopappus type: ectosexine thinner than endosexine, both layers columellate and separated by a zigzag internal tectum (Calopappus).

(5) Cephalopappus type: ectosexine thicker than endosexine, both layers columellate and separated by an internal tectum more or less parallel to nexine (Cephalopappus).

In the genera of Mutisieae and Stifftieae, differences in exine sculpture led us to classify six types of exine (Table 4). Three of them, the Gongylolepis, Macroclinidium, and Stenopadus types, are proposed here, increasing the typification made by Stix (1960), Crisci (1974a) and Telleria et al. (2003). The exine types are as follows:

(1) Ainsliaea type (82B of Figs. 80-85) (Telleria et al., 2003; Telleria & Katinas, 2005): exine microechinate, tectum imperforate. Ectosexine and endosexine equally thick, both layers scarcely differentiated, with compact aspect or slightly columellate. Ratio ectosexine/endosexine: ca. 1:1. Exclusively present in some species of Ainsliaea of the tribe Mutisieae.

(2) Gongylolepis type (94B of Figs. 92-94) (Telleria, 2008): exine echinate, with short or long spines (until ca. 6 [micro]m length), spines with apical channel, tectum very perforate. Ectosexine thinner than endosexine, ectosexine slightly columellate, endosexine with stout and ramified columellae, both layers separated by a conspicuous internal tectum. Ratio ectosexine/endosexine among spines: 1:4; 1:5. Present in Glossarion rhodanthum Maguire & Wurdack, Gongylolepis benthamiana R. H. Schomb., G. huachamacari Maguire, and Duidaea marahuacensis Steyerm. of the tribe Mutisieae, and in Quelchia of the tribe Stifftieae.

(3) Mutisia type (98A of Figs. 95-100) (Telleria et al., 2003; Telleria & Katinas, 2004): exine scabrate, microechinate or echinate with short spines (usually less than 2 [micro]m), tectum imperforate or scarcely perforate. Broad range of exine thickness (4-18 [micro]m). Ectosexine equal, thinner or thicker than endosexine, ectosexine slightly columellate or with compact aspect, endosexine with stout and ramified columellae, both layers separated by an inconspicuous or conspicuous internal tectum. Ratio ectosexine/endosexine: 1:1; 1:2; 1:2.5; 1.5:1; 2:1; 2.5:1. The most common type in the tribe Mutisieae and also present in the tribe Stifftieae.

(4) Macroclinidium type (100B of Figs. 95-100): exine echinate, with long spines (4-5 [micro]m length), spines usually with compact tip, tectum very perforate. Ectosexine thinner than endosexine; ectosexine slightly columellate-granulate, endosexine with ramified columellae. Internal tectum conspicuous. Ratio ectosexine/endosexine among spines: ca. 1:3; 1:2. Exclusively present in Macroclinidium of the tribe Mutisieae.

(5) Stenopadus type (118B, C of Figs. 117-118) (Telleria, 2008): exine psilate (with light microscope), very perforate, with scarce and inconspicuous microspines (with SEM). Ectosexine and endosexine equally thick, ectosexine and endosexine columellate (apparently single columellae). Ratio ectosexine/ endosexine: 1:1. Exclusively present in species of Stenopadus and Stomatochaeta of the tribe Stifftieae.

(6) Wunderlichia type (121 of Figs. 120-121) (Telleria et al., 2003; Telleria, 2008): exine echinate, with short spines (less than 3 [micro]m length), spines with apical channel, tectum very perforate. Ectosexine columellate, equal to or slightly thinner than endosexine, with compact inner layer and thinner scarcely columellate outer layer. Ratio ectosexine/endosexine: 1:1; 1:1.5. The Wunderlichia exine type is very similar to the Gongylolepis type but with less developed spines. The Wunderlichia type can be viewed as transitional between the Mutisia and the Gongylolepis types. Present in the tribe Mutisieae in Eurydochus, species of Gochnatia, and in Salcedoa and in the tribe Stifftieae in Wunderlichia.

[TABLE 4 OMITTED]

Comparison with Closer Subfamilies

Despite the diversity of pollen types that occurs in Asteraceae (e.g., Wodehouse, 2008; Erdtman, 1966), and despite the fact that the Anthemoid pattern pollen is present in Mutisioideae and also in the tribes Anthemideae (subfamily Asteroideae) and Cardueae (subfamily Carduoideae) (Skvarla & Turner, 1966; Skvarla et al., 1977; Bolick, 1978), the pollen of Mutisioideae can be distinguished from the pollen of other subfamilies. In the tribe Anthemideae, Skvarla et al. (1977) recognized two basic pollen types: Anthemis L. and Artemisia L. types, distinguished by the presence or absence (or great reduction) of spines respectively (see also Vezey et al., 1994). The spines in Anthemideae, when present, are generally large in proportion to the size of the grain (Wodehouse, 1935). In contrast, in the genera of Mutisioideae with echinate pollen, the spines are short when compared with the overall size of the pollen grain. The Artemisia exine type resembles the Mutisia exine type, but the grains of Anthemideae are small and spheroidal with a thin exine, whereas those of Mutisioideae (excluding the tribe Nassauvieae) are usually large and elliptic with a thick exine. The closest genera of Mutisioideae to the Artemisia exine type are Adenocaulon and Eriachaenium, which were once considered members of the tribe Anthemideae (Stix, 1960; Leins, 1968; Skvarla et al., 1977 for Adenocaulon).

In comparison with the pollen in the tribes of Cichorioideae, pollen in the subfamily Mutisioideae is clearly different. Arctoteae, Lactuceae, Liabeae, and Vernonieae have echinate and echinolophate pollen, with caveate exine in Arctoteae and most Lactuceae, and an ecaveate exine in Liabeae and Vernonieae (Skvarla et al., 1977; Robinson & Marticorena, 1986; Robinson, 1999). Moreover, pollen of Liabeae is prominently echinate and the exine has much broader columellae than in the Anthemoid pattern (Skvarla et al., 1977), which characterizes the pollen of Mutisioideae.

On the other hand, the Carduoideae have pollen resembling some genera of the Mutisieae and Stifftieae (Table 4). For instance, the exine of Macroclinidium (100 of Figs. 95-100) resembles that of Carduoideae, differing only in having solid spines rather than spines with an apical channel (Skvarla et al., 1977; Tormo-Molina & Ubera-Jimenez, 1995). The Guayana Highland-centered genera of Mutisieae and Stifftieae include the major number of pollen types close to the Carduoideae types (Telleria, 2008). Four exine types in Carduoideae (Tormo-Molina & Ubera-Jimenez, 1995) resemble those in Mutisioideae. (1) The Arctium L., Cyanopsis Cass., and Onopordum L. exine type is characterized by long spines with apical channels and an intricate layer of columellae under the tectum. This type closely resembles the Gongylolepis type and the Wunderlichia exine type (see Exine types). (2) The Carlina L. and Cyanus Mill. exine type is characterized by a microechinate surface, ectosexine with compact aspect, an endosexine thicker than the ectosexine, and stout and ramified columellae. This type is similar to the Mutisia exine type. (3) The ecaveate pollen of some species of Centaurea L. (Wagenitz, 1955; Nordenstam & El-Ghazaly, 1977; Pehlivan, 1995) is also very similar to the Mutisia exine type. (4) The particular Echinops L. pollen type, with its very thick exine (Dimon, 1971; Gamatje & Martin, 2007), resembles the pollen of some species of Chaetanthera (type II; Telleria & Katinas, 2004). These observations reinforce Wodehouse's (1929b) suggestion of a possible relationship between genera of Mutisioideae and Carduoideae.

The pollen of Barnadesioideae strongly differs from that of Mutisioideae. In Barnadesioideae, three main pollen types occur (Urtubey & Telleria, 1998): two of them are lophate or with a variable number of intercolpal depressions, both generally caveate; the third lacks the intercolpal depressions, the exine columellate-granulate or with compact aspect. All of these features are absent in Mutisioideae.

Summary of the Morphological Observations

We conclude the following: (1) Style features (smooth, rugulose to papillose styles, the papillae being relatively short and rounded) constitute the main characters delimiting the subfamily Mutisioideae. (2) Pollen morphology (i.e., pollen surface psilate, microechinate or echinate with a densely columellate exine) is secondarily helpful for delimitating the subfamily. (3) The presence and distribution of style papillae differentiate the three tribes: (a) those genera with smooth or with dorsally papillose styles with the papillae distributed above the branch bifurcation point belong to the tribe Mutisieae (43 genera, ca. 500 species); (b) those with styles rugulose or papillose, both above and below the bifurcation point (almost reaching the base), belong to the tribe Stifftieae (six genera, 48 species); and (c) those with the papillae clustered in an apical tuft belong to the tribe Nassauvieae (25 genera, ca. 320 species). (4) The pollen of genera of Nassauvieae can be clearly differentiated from that of Mutisieae and Stifftieae, being microechinate, with few developed microspines, having a distinctly bilayered exine, and having both the ectosexine and the endosexine clearly columellate. The pollen of Mutisieae and Stifftieae is psilate, microechinate, or echinate, with a compact ectosexine constituted by very thickly disposed columellae and a clearly columellate endosexine. (5) The overall morphology of tribes Nassauvieae and Stifftieae is homogeneous, whereas tribe Mutisieae is heterogeneous for most of its morphological features (e.g., corolla shape, pollen morphology). (6) Morphological data support the molecular studies that exclude certain genera (see Excluded taxa) and disagree with the exclusion of other genera, for example Hecastocleis, and the members of the Gochnatia complex and the Ainsliaea group (see Circumscription of the tribes of Mutisioideae). (7) The morphologically closest subfamilies to Mutisioideae are Barnadesioideae in corolla shape (both have the same range of corolla types except that true ray and filiform corollas are present only in Mutisioideae) and style features (smooth, rugulose to papillose styles, the papillae being relatively short and rounded), and Carduoideae in pollen features (both have the Anthemoid exine pattern as well as some genera with echinate and highly perforate surfaces).

Taxonomic Circumscription

Circumscription of the Subfamily Mutisioideae

The subfamily Mutisioideae can be morphologically defined (Fig. 2) to include genera characterized by (1) frequent presence of bilabiate florets and tubular florets that are funnelform to sub-campanulate (vs. truly campanulate as in most Arctoteae, Cardueae, Liabeae, and Vernonieae); (2) styles with the same width from base to tip (vs. apically widened in Arctoteae and some genera of Cardueae); (3) styles smooth, rugulose, or with short and rounded papillae, the papillae distributed uniformly either only above or both above and below the branch bifurcation point, or constituting a tuft restricted to the branch apex (vs. vernonioid, carduoid, or arctotoid styles); (4) the anthers caudate with long tails, except for Adenocaulon and Eriachaenium (vs. shortly caudate or ecaudate in Arctoteae, Vernonieae, and certain genera of Liabeae and Barnadesioideae); (5) lack of barnadesioid hairs (Bremer & Jansen, 1992) which are restricted to Barnadesioideae; (6) pollen ecaveate (vs. caveate in Lactuceae, Arctoteae, and some genera of Cardueae and Barnadesioideae); (7) pollen surface almost psilate, microechinate or echinate (vs. lophate in some Arctoteae, Barnadesioideae, Lactuceae, and Vernonieae); and (8) exine structure always densely columellate with stout columellae (vs. with sparse and broad columellae in Liabeae and Vernonieae, never with the sponge-like complex of freely branching and anastomosing columellae structure as in the lophate type of Lactuceae and some Barnadesioideae).

[FIGURE 2 OMITTED]

The style of Mutisioideae is obviously different from the carduoid, arctotoid, and vernonioid styles (Bremer, 1987) that characterize the subfamilies Carduoideae and Cichorioideae. However, styles of Mutisioideae and those of the subfamily Barnadesioideae are similar. Despite this resemblance, the subfamily Barnadesioideae is distinguished from Mutisioideae by a combination of two other morphological characters: exclusive presence of barnadesioid hairs and a pollen morphology very different from that of the Mutisioideae. The resemblance in style features between Mutisioideae and Barnadesioideae supports Cabrera's (1961, 1977) inclusion of the Barnadesioideae as a subtribe of the tribe Mutisieae (= Mutisioideae).

Circumscription of the Tribes of Mutisioideae

Three tribes are distinguished within Mutisioideae: tribe Mutisieae, tribe Nassauvieae, and tribe Stifftieae (Fig. 2).

Tribe Mutisieae

The tribe Mutisieae is much more heterogeneous when compared with Nassauvieae and Stifftieae. A central core (Fig. 2, Tables 5 and 6) of genera have mostly bilabiate corollas, generally combined with other types of corolla, and dorsally papillose style branches with the papillae uniformly distributed above the branch bifurcation point (Fig. 77a). Around these genera, a number of "satellite" genera exist, most of them defined as generic groups by Bremer (1994). Although with some distinguishing features, all of these groups have morphological characters that link them to Mutisioideae. Some of these groups of genera have been recently excluded from Mutisioideae on the basis of molecular phylogenetic analyses (Panero & Funk, 2002, 2008; Funk et al., 2005). A discussion of those generic groups follows:

Gochnatia complex. The Gochnatia complex (Freire et al., 2008) comprises the genera Actinoseris, Cnicothamnus, Cyclolepis, Gochnatia, Hyalis, Ianthopappus Roque & D. J. N. Hind, and Nouelia and is defined by the combination of apiculate anther appendages and smooth style branches (Fig. 77b; Table 7). Hansen (1991a) and then Bremer (1994) treated some of these genera as the Gochnatia group. Cabrera (1971a) related Pleiotaxis and Chucoa to Actinoseris, Cyclolepis, and Gochnatia. Pleiotaxis and Chucoa, however, lack the characters typical of the Gochnatia complex, such as apiculate anther appendages (acute in Chucoa) and smooth styles (papillose in Chucoa and Pleiotaxis) (Freire et al., 2002; Sancho et al., 2005). Phylogenetic molecular data supported relationships between Gochnatia and Cnicothamnus (Kim et al., 2002). Panero and Funk (2002) created the subfamily Gochnatioideae, based also on molecular data, that includes Cnicothamnus, Cyclolepis, Gochnatia, Richterago (= Gochnatia sect. Discoseris (Endl.) Cabrera and Actinoseris pro parte), and possibly Chucoa. Nouelia and Gochnatia sect. Leucomeris (D. Don) Cabrera (sensu Cabrera, 1971a) were not included in the subfamily Gochnatioideae. Panero and Funk (2007) established the tribes Wunderlichieae and Hyalideae of the subfamily Wunderlichioideae, the latter including genera of the Gochnatia complex, i.e., Ianthopappus, Hyalis, Leucomeris (= Gochnatia sect. Leucomeris), and Nouelia. From a morphological point of view, the relationships between Hyalideae and Wunderlichieae are not strongly supported. There are other genera of the tribe Mutisieae s. l. with glabrous styles (e.g., Hecastocleis) or apiculate anthers (e.g., Ainsliaea, Wunderlichia), but they do not have both features together. On the other hand, some genera of the Guayanas (e.g., Gongylolepis, Quelchia) have smooth style branches and acuminate anthers, providing a link between the two generic groups. The genera of the Gochnatia complex in general share the Mutisia exine type, supporting their placement in Mutisioideae, tribe Mutisieae. However, some species of Gochnatia (e.g., G. amplexifolia (Gardner) Cabrera, G. buchii (Urb.) J. Jimenez Alm., G. glutinosa (D. Don) D. Don ex Hook. & Am., G. magna M. C. Johnst. ex Cabrera, G. shaferi (Britton) Jervis & Alain) show a close palynological relationship with some Guayana Highland-centered genera because both have the Wunderlichia exine type (Table 4).

[TABLE 5 OMITTED]

[TABLE 6 OMITTED]

Guayana Highland-Centered Genera. Members of this group have been generally viewed as natural by some authors (Maguire, 1956; Carlquist, 1958; Pruski, 1991), with Pruski (1989a, b, 1991) circumscribing the group as comprising Achnopogon, Chimantaea, Duidaea, Eurydochus, Glossarion, Gongylolepis, Neblinaea, Quelchia, Stenopadus, Stifftia, Stomatochaeta, and Wunderlichia. The group, also known as the Stenopadus group (Bremer, 1994), is mainly centered in the Guayana Highlands of northern South America, with representatives in eastern Brazil and the Andes. Because of their high degree of endemism and biogeographic isolation, the Guayana Highland-centered genera have generated considerable interest. Recently, the genus Salcedoa from the Dominican Republic has been linked to some of the genera centered in the Guayana-Highland by Jimenez Rodriguez et al. (2004). Despite the fact that some authors regarded the Guayana-Highland centered genera as a group, some others (e.g., Maguire et al., 1957a, b; Cabrera, 1977) placed the genera of this complex in different subtribes. From a morphological point of view, two main groups are distinguished within the Guayana-Highland centered genera and relatives: (1) the zygomorphic-flowered genera with epaleate, homogamous capitula of all bilabiate corollas (rarely ligulate by abortion of the inner two corolla lips) and smooth style branches (Table 8), and (2) the actinomorphic-flowered genera with epaleate to paleate, homogamous capitula of all tubular corollas and rugulose to papillose styles beyond the branches bifurcation point. The genera with bilabiate corollas were included in the subtribe Mutisiinae and those with tubular corollas in the subtribe Gochnatiinae (Maguire et al., 1957a, b; Cabrera, 1977). The latter group is currently treated as the tribe Stifftieae (see below). Molecular studies (Kim et al., 2002; Funk et al., 2005) have shown the two sampled Guayana Highland-centered genera Duidaea and Stifftia in separate branches. Panero and Funk (2002), in their molecular analysis based on several regions from the chloroplast genome, proposed the circumscription of the Stifftia group, which includes genera of South America and Asia. A morphology-based phylogeny of the group (Jimenez Rodriguez et al., 2004) produced clades with partially contradictory branching patterns when Gochnatia was used to root the cladogram. In the alternative minimal length trees, the genera with bilabiate florets are either monophyletic or polyphyletic, whereas the genera with tubular florets are either monophyletic or paraphyletic. The relationships of the Guayana Highland-centered genera, according to the morphology, seem to point in two different directions: (1) they resemble genera or species of the Gochnatia complex in their discoid capitula with all tubular corollas (tribe Stifftieae), acuminate to apiculate anther appendages (e.g., Chimantaea, Wunderlichia), styles with smooth branches (e.g., Achnopogon, Duidaea), and pollen morphology (see Gochnatia complex); and (2) they resemble the tribe Cardueae in the pollen morphology (e.g., Gongylolepis, Quelchia). The group is taxonomically complex and is currently under study by John Pruski. After Pruski's (2004) work, the Guayana Highland-centered genera were placed into two groups: those with bilabiate florets belonging to the tribe Mutisieae and those with tubular florets belonging to the tribe Stifftieae. In taxonomic and molecular works, Panero and Funk (2007, 2008) established the subfamilies Stifftioideae and Wunderlichioideae, both containing Guayana- and non Guayana-centered genera. There are not morphological characters that support these taxa.

[TABLE 7 OMITTED]

[TABLE 8 OMITTED]

Ainsliaea Group. The Asian genera Ainsliaea, Macroclinidium, Myripnois, and Pertya were considered as a monophyletic group within the Mutisioideae by Hansen (1991a) and Bremer (1994; Table 9). The group was principally supported by its trinerved leaves, few-flowered capitula, and style branches short and dorsally pilose. Kim et al. (2002), using a molecular approach, confirmed the monophyly of the group (adding two morphological synapomorphies: homogamous capitula arranged laterally on the branches) and suggested that the Asian clade could be recognized as a distinct tribe. Simultaneously, Panero and Funk's (2002) molecular studies produced results congruent with Kim et al.'s (2002). Panero and Funk proposed the new subfamily Pertyoideae, sister to most tribes of Asteraceae, excepting Mutisieae and its segregates and the tribe Cardueae. Morphologically, the corolla of these Asian genera deviates from the typical bilabiate or tubular corolla of Mutisioideae (Fig. 1c). Although bilabiate corollas have been mentioned as occurring in the group (Mattfeld, 1934 for Myripnois; Panero & Funk, 2002), a closer examination reveals deeply five-lobed corollas with one deeper split (6 of Figs. 3-6, 31 and 33 of Figs. 31-34, 40 of Figs. 39-42), these slightly ligulate and with unilateral lobes (Koyama, 1975; Freire, 2007). The pollen of Macroclinidium has a particular exine type, and some species of Ainsliaea have tricolpate pollen, which is unusual in Asteraceae with the Mutisia or the Ainsliaea exine type (Telleria et al., 2003; Telleria & Katinas, 2004, 2005) (82 of Figs. 80-85). The Mutisia exine type in species of Ainsliaea, Pertya, and Myripnois links the group to other members of the tribe Mutisieae. Most importantly, the style branches covered by short papillae above the branch bifurcation point (Fig. 79a) or above and somewhat below (Pertya) is the main character that supports keeping the Asian group within Mutisioideae. This generic group is unique within Mutisioideae by its particular corollas, but the complete morphology of the group is still unknown mainly because of the lack of revisionary studies in some of its genera.

Hecastocleis. The genus Hecastocleis, with its only species H. shockleyi A. Gray, is endemic to western United States in the states of California and Nevada (Hickman, 1993; Table 10). It has a distinctive and peculiar morphology when compared with other genera of Mutisieae, with its single-flowered capitula aggregated into compound heads and with each aggregation of one-five heads surrounded by spiny, ovate bracts. In the most recent molecular phylogenetic studies (Panero & Funk, 2002, 2008; Funk et al., 2005), Hecastocleis appears as an independent clade separated (subfamily Hecastocleidoideae) from the rest of Mutisioideae. The unique occurrence of tricolpate pollen in Hecastocleis (and some species of Ainsliaea) would provide additional evidence to support that this genus stands apart from other genera of Mutisioideae (95 of Figs. 95-100). But the Mutisia exine type of the pollen of Hecastocleis, together with its smooth style branches (Fig. 79b), does not suggest a complete independence of this genus from the subfamily (Telleria & Katinas, 2005).

Adenocaulon and Eriachaenium (Table 10). These two genera are problematic because their tribal and subfamilial placement in Asteraceae is uncertain. Both genera are in many respects so different from other genera of Asteraceae that they have been described and tentatively placed in several tribes both in the subfamily Cichorioideae and subfamily Asteroideae (Katinas, 2000). Some characters link them to Cichorioideae (e.g., deeply lobed central corollas, ecaveate pollen), whereas other characters are typical of Asteroideae (e.g., anther appendage basally constricted, short anther tails). The peculiarity of both genera led Rydberg (1917) to create the tribe Adenocauleae (for Adenocaulon), which was tentatively accepted by some authors (Robinson, 1994; Pruski, 1997; Katinas, 2000). Previous cladistic analyses based on molecular data undertaken to analyze relationships within Asteraceae place Adenocaulon in the tribe Mutisieae (Jansen & Kim, 1996; Kim et al., 2002). A cladistic analysis based on morphological data (Katinas, 2000) shows that Adenocaulon and Eriachaenium are sister taxa and constitute an isolated clade nested within Cichorioideae s.l. Adenocaulon and Eriachaenium are the genera of Mutisioideae that have the most number of uncommon characters for the tribe, i.e., tubular four-lobed corollas, very short anther tails, anther collar, anther appendages constricted and demarcated from the thecae, and spheroidal, small pollen grains. On the other hand, their papillose, mutisioid styles (Fig. 79c) and the Mutisia exine type of their pollen grains would suggest a link with the tribe Mutisieae of Mutisioideae.

Therefore, from the informal generic groups and isolated taxa of Mutisioideae pointed out by Bremer (1994), we recognize the seven above-mentioned as sharply distinctive taxa. The other groups of Bremer, the Chaetanthera group (Brachyclados, Chaetanthera, and Pachylaena), the Gerbera group (Chaptalia, Gerbera, Leibnitzia, Perdicium, Trichocline, and Uechtritzia), the pair Mutisia-Hyaloseris, the pair Onoseris--Urmenetea, and the Plazia group (Aphyllocladus, Gypothamnium, and Plazia), all share bilabiate florets and papillose style branches, and therefore we place them in the central core of Mutisioideae (Fig. 2, Table 5).

Tribe Nassauvieae

Genera of Nassauvieae (Table 6) are an important component of the Andean flora of South America. It is a well defined tribe that constitutes a natural group defined by capitula with all the florets bilabiate and by style branches truncate at the apex, glabrous on the outer surface, and apically crowned by elongate papillae or collector hairs (Figs. 77e, f and 78c). The pollen grains have the exine distinctly bilayered, with both ectosexine and endosexine clearly columellate, a pattern that is consistent throughout the tribe (Crisci, 1974a; Cabrera, 1977; Telleria et al., 2003) (112B of Figs. 112-116). A few genera display some features that deviate from this traditional concept of Nassauvieae: Lophopappus, Macrachaenium, and Proustia have rounded style branch apices that are dorsally papillose, and some species of Acourtia and Lophopappus have capitula with tubular florets. However, the exine stratification, typical of pollen grains of Nassauvieae (Crisci, 1974a; Telleria et al., 2003), confirms the position of these genera in the tribe.

Tribe Stifftieae

Stifftieae (Table 11), a small tribe of six genera (Chimantaea, Quelchia, Stenopadus, Stifftia, Stomatochaeta, and Wunderlichia) and 48 species, was established by David Don in 1830 and then resurrected by Pruski (2004) and Jeffrey (2004) to include genera with strictly discoid capitula and dorsally rugulose to papillose styles. The genera of Stifftieae have a unique type of style, dorsally covered by papillae that extend almost to the base of the style (Figs. 77c and 78b). In Stifftia, the papillae are restricted to the apex, and the surface below consists of swollen cells that give a rugulose aspect to the style (Fig. 77d). Quelchia is the only genus of the tribe with a smooth style, but because it has mostly tubular florets it was included in Stifftieae by Pruski (2004). The genera of this tribe show relationships with the bilabiate Guayana Highland-centered genera of tribe Mutisieae and with genera of Cardueae in their pollen.

[TABLE 9 OMITTED]

The Mutisioideae as a Primitive Subfamily

One of the recent, most important discoveries in the systematics of Asteraceae is the lack of the 22 kb inversion in the chloroplast genome of three species of some South American genera (Jansen & Palmer, 1987). These genera now belong to the subfamily Barnadesioideae, previously known as subtribe Barnadesiinae of the tribe Mutisieae (Cabrera, 1977). The findings of Jansen and Palmer (1987) reinforced an already growing body of evidence for primitiveness of the tribe Mutisieae, as suggested for example by Carlquist (1961), Poljakov (1967), Skvarla et al. (1977), and Jeffrey (1977).

Because Barnadesioideae are believed to be sister to the rest of Asteraceae, the subfamily has been a focus of attention and a model to understand the origins and evolution of the whole family. Although Barnadesioideae are considered the sister to the rest of Asteraceae, the subfamily seems most closely related to Mutisioideae, as traditionally viewed by Cabrera (1977) and as is corroborated in this contribution. Both taxa share some morphological and chemical characters in their styles, corollas, and flavonoids (Stuessy et al., 1996). According to Robinson (1987), it seems unlikely that the Barnadesioideae are so remote from Mutisieae that the remainder of the Asteraceae could evolve from within this gap. Robinson suggests that the more immediate descendents of the earliest Asteraceae with the inverted chloroplast DNA carried the two forms (with and without the chloroplast DNA inversion) mixed in their populations through many generations, and that mixture characterized much of the initial diversity of the family. It was from these mixed ancestral populations that the modern taxa of Asteraceae were derived, but the older form of DNA was retained in only one group, the Barnadesioideae.

It has been suggested (Pruski, 1991; Bremer, 1994) that the basal group of the tribe Mutisieae could be among the Guayana Highland-centered genera (e.g., Stenopadus). The assemblages of largely Guayana Highland-centered genera could be modern representatives of an ancient lineage of long extinct progenitors, with some extant taxa themselves bordering on the edge of extinction. Most genera and species that occur on mid- to high-elevation, nutrient-poor, sandstone tepuis that are actively eroding away are known only by few individuals in small populations. According to Bremer (1993), among the archaic, relict genera of the basal complex of Asteraceae are Stenopadus and its immediate relatives from the Guayana Highland in Venezuela, Hesperomannia (currently placed in Vernonieae; Kim et al., 1998) from the Hawaiian Islands, Wunderlichia from Brazil, Ainsliaea from eastern Asia, and Gochnatia from throughout America and part of southeast Asia. Bremer (1994) provided a hypothesized "Stenopadus like" ancestral morphology for the Asteraceae. This hypothesis suggests that the ancestor was a woody plant with alternate leaves, large and discoid capitula, actinomorphic deeply five-lobed corollas, caudate and calcarate anthers with sterile apical appendages, shortly bilobed styles glabrous or papillose with continuous stigmatic areas, and a pappus of scabrid bristles. These are the characteristics of the members of the tribe Stifftieae. Stuessy et al. (1996) and Urtubey and Stuessy (2001) in general suggested similar characteristics for the ancestor, except that it would have been a perennial herb similar to Schlechtendalia (Barnadesioideae) and members of Calyceraceae and would have a scaly pappus.

Until recently, the oldest known fossil record in the family corresponded to pollen of Mutisioideae type from the Eocene to middle Oligocene (to possibly Miocene) strata from the province of Malleco in Chile and Patagonia in Argentina, and from the late Oligocene of Louisiana, Texas, California, and Alaska (Barreda, 1993; Graham, 1996). This led some modern authors to propose South America as the likely place of origin for the family.

Bremer (1992) applied the ancestral areas method, an approach of historical biogeography, to a cladogram of Asteraceae to determine a probable place of origin for the family. The results indicated that Brazil south of the Amazon Basin was most probably part of the ancestral area of Asteraceae. Bremer concluded that the ancestral area was part of a Pacific distribution pattern including South America and excluding Africa and most of Eurasia. Stuessy et al. (1996) presented a detailed scenario based on a morphological cladogram of Barnadesioideae. These authors postulated that the Asteraceae and Calyceraceae, the sister family of Asteraceae, may have diverged as separate families in a southern South American (Argentina and Chile) transitional area of tropical and temperate forests in the early Oligocene. During the Miocene, the initial differentiation of Barnadesioideae began, which then gave rise to other groups of Asteraceae. According to Stuessy et al. (1996), the best candidate for this early lineage would be found in Mutisioideae, tribe Mutisieae, due to its similarity with Barnadesioideae. The results of Gustafsson et al. (2001), on the basis of a molecular cladogram of Barnadesioideae, support Stuessy et al.'s (1996) idea of a southern South American origin for the subfamily. Bremer and Gustafsson (1997) proposed a Cretaceous origin for the sunflower alliance--the monophyletic group made up by Asteraceae, Campanulaceae, and ten smaller families--with the ancestor occurring in East Gondwana, i.e., western Antarctica, Africa, and South America before the breakup of this supercontinent. The Australasian-South American connection displayed by the Goodeniaceae and the Calyceraceae and Asteraceae is, according to Bremer and Gustafsson (1997), a reflection of the early distribution of the alliance in both East and West Gondwana. In their cladogram, inferred by parsimony analysis of 35 rbcL sequences from all of the families of the alliance, the age of the Asteraceae is estimated to be at least 38 Myr.

[TABLE 10 OMITTED]

The occurrence of two asteraceous pollen types with wall structure types like those in the Mutisieae has been reported from the Upper Paleocene-Eocene of South Africa (Zavada & de Villiers, 2000; Scott et al., 2006). Interestingly, this pollen was recovered from offshore and onshore localities of southern Africa. According to Zavada and de Villiers (2000), an African origin of Asteraceae is more likely, with subsequent dispersal to southern South America, where the earliest occurrence of Asteraceae pollen is in the Oligocene (Barreda, 1993). However, these Eocene pollen records need taxonomic and/or stratigraphic confirmation (Scott et al., 2006). Those reported as Mutisiapollis spp. from the Late Eocene of the Gulf coast of Mexico (Elsik & Yancey, 2000) might be the oldest ones, but neither description nor illustration was provided to date (T. E. Yancey, personal communication) to confirm their identification.

A second, smaller chloroplast DNA inversion occurring at one end of the larger inversion was found in Asteraceae, excepting Barnadesioideae (Kim et al., 2005). Two clock calibrations from Poaceae and Oleaceae were employed to calibrate the Asteraceae molecular clock, resulting in a mid-Eocene (42-48 Myr) origin of the family. The two chloroplast genome inversions occurred, according to this study, in the Late Eocene/Early Oligocene (38-42 Myr) when the Barnadesioideae diverged from the rest of the Asteraceae. Funk et al. (2005) proposed that the origin of the extant members of Asteraceae was in southern South America and a subsequent radiation in Africa gave rise to most of the tribes we know today.

New fossil pollen discoveries of Mutisieae s. 1. and Barnadesioideae were reported from marine deposits of Patagonia, in southern Argentina (Katinas et al., 2007; Barreda et al., 2008). A minimum age of 28-23 Myr (Late Oligocene, Chattian) for fossil pollen related to the extant genera of the Gochnatia complex, and 23-20 Myr (Early Miocene, Aquitanian) for fossil pollen of the Nassauvieae and Barnadesioideae were reported (Katinas et al., 2007). Fossil pollen records of the Late Miocene (11-9 Myr) in Patagonia show high abundance and diversity of Nassauvieae associated with pollen of Astereae and Barnadesioideae. It is interesting to note that the chronological order of appearance of these groups in Patagonia, first Mutisieae s. 1. and second Barnadesioideae, differs from the branching order of the current accepted phylogenies, i.e., first Barnadesioideae and second Mutisieae s. 1. Many molecular biologists have used and are using fossils in their analyses as a way of providing a calibration point for evolutionary models used to approximate ages for the nodes of the phylogenetic trees. Opinion remains divided as to how best to use temporal (stratigraphic) data in phylogenetic reconstruction (see the online debate from 1998 at http://www.nature.com/nature/debates/fossil/). Some authors think that the order of stratigraphic appearance of taxa in the fossil record should play a role in phylogenetic tree-building. In such cases stratigraphic order is used from the outset to influence and direct branching relationships by maximizing the congruence between the age of a taxa's first occurrence in the fossil record and how early it branches from a phylogenetic tree. Others see stratigraphy as irrelevant to phylogeny, and dismiss mismatches between the fossil record and phylogenetic hierarchy as a result of an inadequate fossil record. The role of stratigraphy is then restricted to post hoc dating of branching events. If we see the last pollen findings (e. g., Katinas et al., 2007) through the former position (despite the fact that the age of fossils is considered minimum age), they contradict the branching pattern of the current hypotheses on the evolution of Asteraceae. If we see these findings through the latter position, hopefully, they will help to calibrate more precisely the phylogenetic trees involving Asteraceae.

[TABLE 11 OMITTED]

Distributional Patterns

Genera of Mutisioideae are found on all continents except Europe and Antarctica, with its major concentration in South America. The tribe Stifftieae, with its low number of genera, is very restricted in distribution compared to the tribes Nassauvieae and Mutisieae. The Nassauvieae and Mutisieae, themselves, have very different distributional patterns.

The tribe Nassauvieae is exclusively Neotropical, with mostly monotypic, endemic, Andean, Chilean, and Patagonian genera, only a few being widespread. Largely Andean-Patagonian-centered genera are Dolichlasium (one species), Leucheria (46 species), Lophopappus (6 species), Nassauvia (38 species), and Perezia (31 species). Exclusively Patagonian genera are Ameghinoa (one species), Burkartia (one species), and Macrachaenium (one species), the last from the Nothofagus Blume forest. Central and northern Chile, a hot spot in South America, hosts many endemic genera such as Calopappus (one species), Leunisia (one species), Marticorenia (one species), Moscharia (two species), Oxyphyllum (one species), Pleocarphus (one species), Polyachyrus (seven species), and six of the seven species of Triptilion. Only Jungia (27 species) and Trixis (39 species) are widespread genera ranging from North and Central America to southern Argentina. On the other hand, Acourtia and Berylsimpsonia are not South American, occurring in North and Central America and in the West Indies, respectively.

The genera of Mutisieae are mainly South American but they are also represented in Asia, Africa, and Australia by only one species (Trichocline spathulata (A. Cunn. ex DC.) J. H. Willis). The genera are in general not centered in one particular area, but there are some generic groups concentrated in several different restricted areas. For instance, the Guayana Highland-centered genera belonging to tribes Mutisieae and Stifftieae inhabit the Guayana Highlands of northern Brazil, Colombia, Guyana, and Venezuela, but also extend to the Andes of Colombia, Ecuador, and Peru, Dominican Republic, and eastern Brazil. Unlike the Nassauvieae, there are few monotypic genera or genera with few species endemic to restricted areas: Gypothamnium (one species) from northern Chile, Hecastocleis (one species) from western United States, Perdicium (two species) from southern Africa, and Lulia (one species) from southern Brazil. There are many widespread genera, for instance Chaptalia in America, from southern United States to central Argentina; Gerbera in Africa, southern Asia, and America; Gochnatia, with two Asian species, from Mexico to Argentina; and Mutisia from the Andes of Colombia to southern Argentina and Chile, and in southern Brazil and adjacent regions. Some genera well represented in the Andean mountain ranges are Aphyllocladus, Chaetanthera, Chucoa, Onoseris, Pachylaena, and Plazia. Finally, the Asian Ainsliaea group ranges from Afghanistan to Japan and southeastern Asia.

The genera of Stifftieae have their major diversity in the Guayana Highlands. Chimantaea is endemic to the eastern Venezuelan Guayana Highland. All species of Quelchia are endemic to the Guayana Highland in southern Venezuela. Stenopadus is a genus of 15 species, 14 of which are found in the sandstone areas of the Guayana Highland in Colombia, Venezuela, Guyana, Brazil, with one species in the Andes of Ecuador and Peru. All species of Stomatochaeta are endemic to the Guayana Highland of southern Venezuela, Guyana, and northern Brazil. Stifftia occurs in Brazil and French Guiana and is the only genus of the tribe occurring both north and south of the Amazon River. Wunderlichia does not inhabit the Guayana Highlands; it occurs in eastern Brazil.

In general, the genera of Mutisioideae have their highest concentration in the Andes and Patagonia (25 genera), with other important centers in the Guayana shield (11 genera), northern and central Chile (seven genera), and southeastern Asia (four genera).

Taxonomy

Subfamily Mutisioideae (Cass.) Lindl.

Lindley in Loudon, Encycl. pl.: 1074. 1829, based on the tribe Mutisieae Cass., J. Phys. Chim. Hist. Nat. Arts 88: 199. 1819.

Herbs, shrubs, subshrubs, vines, or trees; monoecious, dioecious, or gynodioecious. Leaves alternate, rarely opposite, spreading along the stem or clustered in a basal rosette, in the median part of the stem, or at the stem apex; sessile, clasping, decurrent to petiolate, occasionally with stipules; blades simple, rarely compound, entire to divided, unarmed to spiny, predominantly pinnately veined, less commonly three-veined, palmately veined, or parallel-veined, glabrous to pubescent. Capitulescences monocephalous or few at the end of the branches, or laxly to densely corymbose, racemose to paniculate, rarely glomerulose or pseudocephalia. Capitula homogamous or heterogamous; discoid, radiate, ligulate, or disciform; receptacle epaleate, less frequently paleate, glabrous to pubescent, alveolate, ciliate, setose to fimbriate; involucre uniseriate to multiseriate. Florets one to more than 100; corollas isomorphic, dimorphic, sub-dimorphic, or rarely trimorphic, white, yellow, cream, pink, purple, blue, orange, or red; marginal florets functionally female, neuter, or bisexual; corollas bilabiate, sub-bilabiate, true ray, ligulate, or tubular and sub-zigomorphic, rarely tubular four-lobed; in trimorphic capitula, internal marginal florets female, with or without staminodes, corollas filiform to bilabiate; central florets bisexual, functionally female, or male, corollas tubular-funnelform to rarely sub-campanulate, deeply to very deeply-lobed, bilabiate, ligulate, rarely sub-bilabiate; anthers calcarate, caudate, with long, rarely short tails and thus anthers auriculate, smooth to papillose; connectival or anther appendage ovate to lanceolate, acute, truncate to apiculate, not constricted or demarcated from the thecae, rarely demarcated; style shortly bilobed to bifid and cleft into two long branches, rounded to truncate at the apex, smooth throughout, or dorsally papillose only above the style branch bifurcation to papillose both above and below the bifurcation, papillae rounded, never acute, or with an apical crown of short collector hairs, inner surface of the branches completely covered by stigmatic papillae. Cypselae oblong, ellipsoid, ovoid, obovoid to turbinate, truncate, attenuate to rostrate at the apex, smooth to ribbed; glabrous to pubescent, with typical or modified twin hairs, glandular hairs and leaf-like hairs (e.g., two-armed, flagellate); pappus of one to more series of bristles, equal to unequal in length, scabrid to plumose, capillary to somewhat rigid and paleaceous, reduced to a crown of fringed scales, or absent. Pollen tricolporate or rarely tricolpate, suboblate to prolate, usually of medium to large size (25-100 [micro]m); exine almost psilate, microechinate to echinate, exine structure with Anthemoid pattern, x=9.

Characters that define the subfamily are in italics.

TYPE: Mutisieae Cass.

The Mutisioideae occur mainly in the New World, with the major concentration of genera in the mountains and arid regions of South America, and some genera distributed in Central America, Mexico, and southern United States, southern and eastern Asia, Africa (including Madagascar), Arabia, and Australia. It comprises 74 genera and ca. 865 species.
Key to Tribes of Mutisioideae

1a. Style branches smooth or with papillae sparsely distributed,
 never clustered at the branch apices. Pollen microechinate or
echinate, the ectosexine with columellae very thickly
disposed (compact aspect), and the endosexine clearly columellate.

2a. Capitula isomorphic, dimorphic, or trimorphic. Style branches
dorsally smooth or with papillae completely covering the
branches or only the branch apex, very rarely extending
below the branch bifurcation point
 Tribe Mutisieae

2b. Capitula isomorphic with all tubular corollas (bilabiate in
Quelchia bracteata). Style branches rugulose with swollen cells
or papillose, exceptionally smooth (Quelchia); the swollen cells
or the papillae covering the branches and also extending much
below the branch bifurcation point (ca. 3/4 of the style)
 Tribe Stifftieae

1b. Style branches apically crowned by a tuft of papillae
(collector hairs). Pollen microechinate, both ectosexine and
endosexine clearly columellate Tribe Nassauvieae


Tribe Mutisieae Cass.

H. Cassini, J. Phys. Chim. Hist. Nat. Arts 88: 199. 1819. Mutisiinae Dumort., Anal. fam. pl.: 31. 1829; Less., Linnaea 5: 241. 1830. Mutisiaceae Burnett, Outlines Bot.: 934. 1835. TYPE: Mutisia L. f.

Onoserideae Kunth, in Humb., Bonpl. & Kunth, Nov. gen. sp. 4 (folio ed.): 4. 1818, as "Onoseridae." Onoseridinae Benth., in Benth. & Hook. f., Gen. pl. 2: 215. 1873, as "Onoserideae." Onoserideae (Benth.) Panero & V. A. Funk, Phytologia 89: 359. 2007. TYPE: Onoseris Willd.

Chaetantherae Dumort., Anal. faro. pl.: 31. 1829. TYPE: Chaetanthera Ruiz & Pav.

Gerbereae Lindl. in Loudon, Encycl. pl.: 1074. 1829, as "Gerberieae." Gerberinae Benth., in Benth. & Hook. f., Gen. pl. 2: 217. 1873, as "Gerbereae." TYPE: Gerbera L.

Perdiciaceae Link, Handbuch 1: 728. 1829. Perdicieae D. Don, Trans. Linn. Soc. London 16: 239. 1830, as "Perdiceae." TYPE: Perdicium L.

Adenocauleae Rydb., F1. Rocky Mts.: 833. 1917. Adenocaulinae A. Gray, Syn. ft. N. Amer. 1: 59. 1884. TYPE: Adenocaulon Hook.

Gochnatiinae Benth., in Benth. & Hook. f., Gen. pl. 2: 216. 1873, as "Gochnatieae." Gochnatioideae (Benth. & Hook. f.) Panero & V. A. Funk, Proc. Biol. Soc. Wash. 115: 913. 2002. Gochnatieae (Benth. & Hook. f.) Panero & V. A. Funk, Proc. Biol. Soc. Wash. 115: 913. 2002. TYPE: Gochnatia Kunth.

Hecastocleidoideae Panero & V. A. Funk, Proc. Biol. Soc. Wash. 115: 914. 2002, as "Hecastocleioideae." Hecastocleideae Panero & V. A. Funk, Proc. Biol. Soc. Wash. 115: 914. 2002. TYPE: Hecastocleis A. Gray.

Pertyoideae Panero & V. A. Funk, Proc. Biol. Soc. Wash. 115: 915. 2002. Pertyeae Panero & V. A. Funk, Proc. Biol. Soc. Wash. 115: 915. 2002. TYPE: Pertya Sch. Bip.

Hyalideae Panero, Phytologia 89: 358. 2007. TYPE: Hyalis D. Don ex Hook. & Am.

Subshrubs, shrubs, perennial herbs, vines or small trees, monoecious, dioecious, or gynodioecious. Leaves alternate to rarely opposite, rosulate, clustered at the branch apices to clustered in the axils of the old leaves; petiolate, sessile to sheathing at the base; blades entire, lyrate, pinnatisect to pinnately compound, unarmed to spiny, pinnately, palmately to three-veined, rarely parallel-veined, glabrous to pubescent. Capitulescences monocephalous, two- to three-headed at the end of the branches, laxly to densely corymbose, racemose, paniculate to glomerulose or pseudocephalia. Capitula homogamous or heterogamous, discoid, disciform, ligulate, or radiate, isomorphic or heteromorphic with dimorphic, sub-dimorphic, or rarely with trimorphic florets, with one to numerous florets; receptacle epaleate to paleate, glabrous, pilose, setose to fimbriate; involucre uniseriate to multiseriate. Isomorphic capitula with all the florets bisexual or rarely functionally female, corolla ligulate, shallowly to deeply five-dentate, sub-bilabiate to tubular-funnelform, and deeply five-lobed. Heteromorphic capitula with marginal florets bisexual, female, or neuter, corolla bilabiate, sub-bilabiate (3+1 corolla lips), true ray to tubular four- to five-lobed; intermediate florets in the trimorphic capitula female, corolla filiform to bilabiate, with or without staminodes; central florets bisexual, functionally female or male, corolla bilabiate, sub-bilabiate, tubular-bilabiate, tubular-funnelform to sub-campanulate, and five-lobed; anthers with apical appendage lanceolate, rounded, acute, truncate to apiculate, rarely basally constricted and demarcated from the thecae, tails long, rarely short, smooth to papillose, adjacent tails free to connate; style cleft into two short or bilobed to long or bifid branches, branches dorsally glabrous to papillose, with the papillae covering the branches above the branch bifurcation point, occasionally extending somewhat below, papillae short and rounded at the apex. Cypselae oblong to sub-obovate, truncate, attenuate to rostrate at the apex, glabrous to pubescent, sometimes dimorphic with the marginal cypselae conspicuously larger than the central ones; pappus of scabrid to plumose bristles, capillary to narrowly paleaceous, often plumose only at the apex, equal to different in length, less commonly reduced to a crown of fringed scales, or pappus absent. Pollen tricolporate, rarely tricolpate, microechinate with small puncta to echinate, ectosexine very compact, endosexine with stout and ramified columellae.

Characters that define the tribe are in italics.

Mutisieae include 43 genera and ca. 500 species principally South American with a concentration in the Andes and some endemics of the Guayana Highland. Five genera occur in North America, eleven genera in Asia, and three in Africa; one species of Trichocline occurs in Australia.

Genera: Achnopogon Maguire, Steyerm. & Wurdack, Actinoseris (Endl.) Cabrera, Adenocaulon Hook., Ainsliaea DC., Aphyllocladus Wedd., Brachyclados D. Don, Catamixis Thomson, Chaetanthera Ruiz &Pav., Chaptalia Vent., Chucoa Cabrera, Cnicothamnus Griseb., Cyclolepis D. Don, Dinoseris Griseb., Duidaea S. F. Blake, Eriachaenium Sch. Bip., Eurydochus Maguire & Wurdack, Gerbera L., Glossarion Maguire & Wurdack, Gochnatia Kunth, Gongylolepis R. H. Schomb., Gypotham- nium Phil., Hecastocleis A. Gray, Hyalis D. Don ex Hook. & Am., Hyaloseris Griseb., Ianthopappus Roque & D. J. N. Hind, Leibnitzia Cass., Lulia Zardini, Lycoseris Cass., Macroclinidium Maxim., Mutisia L. f., Myripnois Bunge, Neblinaea Maguire & Wurdack, Nouelia Franch., Oldenburgia Less., Onoseris Willd., Pachylaena D. Don ex Hook. & Am., Perdicium L., Pertya Sch. Bip., Plazia Ruiz & Pay., Salcedoa F. Jimenez Rodr. & Katinas, Trichocline Cass., Uechtritzia Freyn, Urmenetea Phil.
Key to Genera

1a Style branches dorsally smooth.

2a Capitula with all bilabiate or rarely ligulate corollas.

3a Leaves one-veined; capitula pendulous; phyllaries reddish Duidaea

3b Leaf venation pinnate or less commonly sub-palmate; capitula not
obviously pendulous, commonly erect; phyllaries not brightly colored.

4a Leaves tomentose abaxially; corollas bilabiate or ligulate.

5a Capitulescence monocephalous; corollas ligulate and/or bilabiate;
cypselae glabrous to scarcely glandular Glossarion

5b Capitulescence corymbose; corollas bilabiate; cypselae villose
 Salcedoa

4b Leaves frequently glabrous, less commonly slightly pubescent
beneath; corollas bilabiate.

6a Capitulescence terminal to subterminal; capitula commonly large,
> (6)10 mm wide, six- to many-flowered; involucre hemispherical.

7a Phyllaries subequal, decurrent onto peduncle; cypselae puberulent;
pappus bristles fragile, sometimes individually deciduous Eurydochus

7b Phyllaries graduated, peduncles sometimes bracteate, but the bracts
leaf-like and not resembling the phyllaries; cypselae glabrous;
pappus bristles persistent Gongylolepis

6b Capitulescence lateral, three- to nine-headed; capitula commonly
small, < 6 mm wide, two- to six-flowered; involucre cylindrical.

8a Leaves densely spirally arranged, except sometimes on
capitulescence; capitula subsessile; phyllaries woolly;
corolla tube puberulent
 Achnopogon

8b Leaves alternate, mostly at stem apex; capitula pedunculate;
phyllaries glabrous; corollas glabrous Neblinaea

2b Capitula with all or some of the corollas tubular.

9a Capitula with only tubular corollas.

10a Capitulescences with spiny bracts enclosing several, cylindrical,
oneflowered capitula Hecastocleis

10b Capitulescences without spiny bracts enclosing the many-flowered
capitula.

11a Branches unarmed; plants monoecious, gynodioecious, or polygamous;
when gynodioecious corolla tubes in female florets short (1/3 of
corolla length) Gochnatia

11b Branches modified in thorns; plants gynodioecious, corolla tubes
of female florets long and narrow (up to 2/3 of corolla length)
 Cyclolepis

9b Capitula with marginal florets bilabiate to sub-bilabiate and
central florets tubular.

12a. Leaves three-veined.

13a. Central florets numerous; pappus purplish Ianthopappus

13b. Central floret 1; pappus pale Hyalis

12b. Leaves pinnately veined.

14a. Perennial herbs Actinoseris

14b. Shrubs or small trees.

15a. Marginal florets with corollas sub-bilabiate (3+1 corolla lips)
 Cnicothamnus

15b. Marginal florets with corollas bilabiate (3+2 corolla lips)
 Nouelia

1b. Style branches papillose.

16a. Anthers auriculate at the base, with tails very short
and inconspicuous.

17a. Leaves alternate, distributed more or less evenly along stem;
capitulescence monocephalous Eriachaenium

17b. Leaves rosulate to sub-rosulate; capitulescences
of few capitula Adenocaulon

16b. Anthers caudate at the base, with tails long and conspicuous.

18a. Capitula usually with all florets homomorphic.

19a. All florets usually with tubular corollas.

20a. Leaves reduced, linear-oblong to linear-lanceolate, caducous
 Aphyllocladus

20b. Leaves well developed, lanceolate to obovate, persistent
 Chucoa

19b. All florets with ligulate, bilabiate, or sub-bilabiate corollas.

21a. Corollas ligulate.

22a. Corollas ligulate, deeply five-lobed limb, with one deeper
split; style bilobed.

23a. Pappus bristles plumose Ainsliaea

23b. Pappus bristles scabrid.

24a. Dioecious shrubs; phyllaries ca. 5 Myripnois

24b. Monoecious perennial herbs, vines, subshrubs, or
shrubs; phyllaries six to more.

25a. Herbs; leaves clustered at the median part of the stem
 Macroclinidium

25b. Shrubs; leaves alternate, more or less evenly
distributed along the stem or clustered on
brachyblasts (short shoots) Pertya

22b. Corollas ligulate with a five-dentate limb (occasionally some
corollas are sub-bilabiate); style bifid.

26a. Stems with brachyblasts (short shoots) and macroblasts
(long shoots) Hyaloseris

26b. Stems without brachyblasts.

27a. Leaves alternate Catamixis

27b. Leaves opposite Dinoseris

21b. All corollas bilabiate to sub-bilabiate (except Mutisia
linifolia with ligulate corollas), rarely marginal
true ray corollas.

28a. Herbs (except Chaetanthera glandulosa); pappus bristles
simple, scabrid to barbellate Chaetanthera

28b. Stout to trailing shrubs or subshrubs; pappus bristles
plumose Mutisia

18b. Capitula with heteromorphic florets.

29a. Central corollas tubular or tubular-bilabiate.

30a. Plants dioecious Lycoseris

30b. Plants monoecious.

31a. Anther apical appendages acute to long-apiculate.

32a. Anther apical appendages long-apiculate; involucre
globose-urceolate to cyathiform; central corollas deeply
five-lobed Oldenburgia

32b. Anther apical appendages acute to subapiculate;
involucre cylindrical to campanulate; central corollas
shallowly five-lobed.

33a. Leaves rugose Urmenetea

33b. Leaves smooth Onoseris

31b. Anther apical appendages truncate.

34a. Leaves reduced, caducous Aphyllocladus

34b. Leaves well developed, persistent.

35a. Leaves obovate-oblong; cypselae glabrous Plazia

35b. Leaves linear; cypselae villose Gypothamnium

29b. Central corollas bilabiate to tubular-bilabiate.

36a. Herbs usually scapose.

37a. Pappus bristles connate at the base Perdicium

37b. Pappus bristles free.

38a. Plants dimorphic: a vernal stage with reduced or no
leaves and chasmogamous capitula, and an autumnal
stage with fully developed leaves and cleistogamous
capitula Leibnitzia

38b. Plants not dimorphic.

39a. Cypselae truncate at the apex.

40a. Cypselae villose with long, shaggy hairs Uechtritzia

40b. Cypselae shortly pubescent Trichocline

39b. Cypselae distinctly rostrate to attenuate at the
apex.

41a. Capitula with dimorphic or trimorphic
florets; when trimorphic, the intermediate
florets with corollas bilabiate to filiformbilabiate,
as long as the styles or longer;
staminodes generally present Gerbera

41b. Capitula with trimorphic florets; the intermediate
florets with corollas very reduced,
filiform (irregularly tubular, true ray to
bilabiate), shorter than the styles; staminodes
absent Chaptalia

36b. Shrubs, vines, subshrubs or not scapose herbs.

42a. Pappus bristles scabrid to barbellate.

43a. Shrubs Brachyclados

43b. Caulescent herbs (except Chaetanthera glandulosa).

44a. Leaves linear, graminiform, parallel-veined Lulia

44b. Leaves not graminiform, reticulate-veined Chaetanthera

42b. Pappus bristles plumose.

45a. Herbs; leaves orbicular to spathulate Pachylaena

45b. Stout or trailing shrubs to subshrubs; leaves neither
spathulate nor orbicular Mutisia


Achnopogon Maguire, Steyerm. & Wurdack

Mem. New York Bot. Gard. 9: 437. 1957. TYPE: Achnopogon virgatus Maguire, Steyerm. & Wurdack. 3 of Figs. 3-6.

Etymology. From the Greek achno, hair, and pogon, beard, in reference to the lanate pubescence on young leaves.

Shrubs with stems either erect and simple or divaricately branched. Leaves apically clustered and densely spirally inserted, alternate; sessile to subsessile, petioles, when present, clasping; blades lanceolate to obovate, coriaceous, pinnately veined, margin entire, lanate when young, glabrous with age. Capitulescences monocephalous or lateral and cymose of three to seven heads; capitula short-pedunculate, homogamous, bilabiate, two- to six-flowered; receptacle epaleate; involucre multiseriate, cylindrical, phyllaries woolly. Florets isomorphic, bisexual, corolla bilabiate, outer lip expanded; anthers reddish to cream-colored, exserted, apical appendages acute, tails papillose; style bifid, red, branches dorsally smooth. Cypselae glabrous to sparsely pilose at the apex; pappus of scabrid, capillary bristles.

Pollen Description. Pollen not seen. According to Carlquist (1957b), the pollen of Achnopogon is similar to that of Gongylolepis in its sculpture and structure.

Habitat and Distribution. The genus contains two species, and is endemic to the eastern Venezuelan Guayana Highland. Both species occur only at about 2,000 m elevation, one on Auyan-Tepui and the second on the more southerly Chimanta Massif.

Species list

1. Achnopogon steyermarkii Aristeg., Acta Bot. Venez. 2: 350. 1967. TYPE: Venezuela. State Bolivar: Auyan-tepui, J. A. Steyermark 93512 (holotype, VEN not seen). Additional specimen examined: Venezuela. State Bolivar: Auyan-tepui, J. A. Steyermark 93497 (US).

2. Achnopogon virgatus Maguire, Steyerm. & Wurdack, Mem. New York Bot. Gard. 9: 438. 1957. TYPE: Venezuela. State Bolivar: Torono-tepui, Chimanta Massif, J. A. Steyermark & J. J. Wurdack 681 (isotype, NY!). Additional specimen examined: Venezuela. State Bolivar, Dist. Plat, macizo del Chimanta, O. Hubber 11508 (US).

Literature. Maguire et al. (1957a), Aristeguieta (1964), Pruski (1997).

Actinoseris (Endl.) Cabrera

Bol. Soc. Argent. Bot. 13: 46. 1970, based on Actinoseris Endl., Gen. pl.: 483. 1838, as group "a" of Seris Less. TYPE: Seris polymorpha Less. [= Actinoseris polymorpha (Less.) Cabrera]. 4 of Figs. 3-6.

Ingenhusia Vell., FI. flumin.: 351. 1829 (1825). TYPE: Ingenhusia radiata Vell. [= Actinoseris radiata (gell.) Cabrera].

Etymology. From the Greek aktinos, star like, radiating from a centre, and seris, seridos, chicory, lettuce.

Herbs perennial, scapose or caulescent, with simple to few branched stems. Leaves rosulate or alternate; sessile to petiolate; blades elliptic, obovate to linear, pinnately veined, margin entire to denticulate, glabrous, scarcely pubescent to lanate. Capitulescences monocephalous or corymbose; capitula pedunculate, homogamous or heterogamous, radiate; receptacle epaleate; involucre three- to six-seriate. Florets dimorphic; marginal florets bisexual or functionally female with staminodes, corolla bilabiate to sub-bilabiate (3+1, 4+1 corolla lips), outer lip expanded; central florets bisexual, corolla actinomorphic, tubular-funnelform to slightly campanulate, deeply five-lobed; anther apical appendages apiculate, tails papillose; style bifid to bilobed, branches dorsally smooth. Cypselae villose; pappus of scabrid, capillary bristles.

Pollen Description. Actinoseris angustifolia (Gardner) Cabrera (80 of Figs. 80-85). Pollen subprolate, elliptic or spheroidal in equatorial view, circular in polar view, medium to large size, P x E = (44 52 x 3443) [micro]m. Tricolporate, colpi long with margin and psilate or scarcely microgranulate membrane, mesoaperture diffuse? Exine Mutisia type with compact ectosexine, echinate, 8-10 [micro]m thick, spines 2.5 [micro]m length. Ratio ectosexine/endosexine: 1:1; 1.5:1. Nexine ca. 2 [micro]m thick. Note: pollen close to that of type II of Gochnatia (see also Roque & Silvestre-Capelato, 2001).

Habitat and Distribution. Genus of seven species of rocky and grassy places of Brazil.

Species list

1. Actinoseris angustifolia (Gardner) Cabrera, Bol. Soc. Argent. Bot. 13: 50. 1970. Basionym: Seris angustifolia Gardner. TYPE: Brazil. State Minas Geraes: Diamont District, G. Gardner 4955 (lectotype, designated by Roque & Pirani, 2001:1158, K not seen). Additional specimens examined: Brazil. State Minas Geraes: Jaboticatuba, G. Hatschbach 28756 (LP); Jaboticatuba, Serra do Cipo, G. Hatschbach 29986 (LP*).

2. Actinoseris arenaria (Baker) Roque, Kew Bull. 52: 199. 1997. Basionym: Trichocline arenaria Baker. TYPE: Brazil. State Minas Geraes: Itambe, G. Gardner 4956 (lectotype, designated by Roque, 1997: 199, K not seen; isotype, NY not seen, NY photo at LP!).

3. Actinoseris hatschbachii Zardini, Bol. Mus. Bot. Munic. 23: 1. 1975. TYPE: Brazil. State Minas Geraes: Santa Ana do Riacho, Serra do Cipo, G. Hatschbach 35366 (holotype, LP!).

4. Actinoseris polymorpha (Less.) Cabrera, Bol. Soc. Argent. Bot. 13: 48. 1970. Basionym: Seris polymorpha Less. TYPE: Brazil: s.d., Sello s.n. (lectotype, designated by Cabrera, 1970: 48, P not seen). Additional specimen examined: Brazil. State Minas Geraes: Serra do Cipo, A. C. Brade 2007 (LP).

5. Actinoseris polyphylla (Baker) Cabrera, Bol. Soc. Argent. Bot. 13: 50. 1970. Basionym: Seris polyphylla Baker. TYPE: Brazil. State Minas Geraes: Serra da Lapa, Riedel 1077 (lectotype, designated by Roque & Pirani, 2001:1159, P not seen). Additional specimen examined: Brazil. State Minas Geraes: Santa Ana do Riacho, G. Hatschbach 35304 (LP).

6. Actinoseris radiata (Vell.) Cabrera, Bol. Soc. Argent. Bot. 13: 50. 1970. Basionym: Ingenhusia radiata Vell. TYPE: Lectotype, designated by Cabrera, 1970: 50, the illustration in Fl. flumin. Icon. 8: tab. 93. 1831 (1827). Additional specimen examined: Brazil. State Paranfi: Campo Largo, G. Hatschbach 690 (LP).

7. Actinoseris stenophylla Cabrera, Bol. Mus. Bot. Munic. 15: 3. 1974. TYPE: Brazil. State Minas Geraes: Jaboticatubas, Serra do Cipo, G. Hatschbach 30061 (holotype, LP!).

Observations. Cabrera (1970) considered that the capitula of Actinoseris are homogamous with all the florets bisexual. However, in some species (e.g., A. arenaria, A.

hatschbachii, A. radiata) the capitula are heterogamous with the outer florets functionally female, with staminodes, and with the central florets bisexual (Freire et al., 2002).

The genus Richterago, which was regarded a synonym of Gochnatia by Cabrera (1970), was recently reinstated and recircumscribed (Roque & Pirani, 2001) to include the species of Actinoseris and the species of Gochnatia sect. Discoseris. Further, new species of Richterago were described: R. campestris Roque & J. N. Nakaj., R. petiolata Roque & J. N. Nakaj. (Roque & Nakajima, 2001), R. caulescens Roque, R. conduplicata Roque, R. elegans Roque, R. lanata Roque, R. riparia Roque (Roque, 2001 a). Recent molecular studies recovered Richterago amplexifolia (= Gochnatia amplexifolia) and Richterago angustifolia (= Actinoseris angustifolia) as sister taxa (Panero & Funk, 2008). A more detailed phylogenetic analysis including more species of Actinoseris as well as more species of Gochnatia may provide the final answers about the identity of Richterago.

Literature. Cabrera (1970, 1974), Roque (1997, 2001a), Roque and Nakajima (2001), Roque and Pirani (2001), Freire et al. (2002).

Adenocaulon Hook.

Bot. Misc. 1: 19. 1829. TYPE: Adenocaulon bicolor Hook. 5 of Figs. 3-6.

Etymology. From the Greek aden, gland, and kaulos, stalk, stem, by the stalked glandular hairs.

[FIGURES 3-6 OMITTED]

Herbs perennial, scapiform with stout rhizomes, stems simple, erect, with stipitate-glandular hairs. Leaves glabrous to subglabrous above, tomentose beneath; basal leaves rosulate to sub-rosulate; petiolate to pseudopetiolate; blades elliptic, ovate, obovate, to deltoid, margin entire to lyrate, pinnately to palmately veined; upper leaves similar to the basal ones but few and reduced. Capituleseences terminal, laxly racemose to corymbose, on long peduncles; capitula pedunculate, heterogamous, disciform; receptacle epaleate; involucre uniseriate. Florets dimorphic; marginal florets female, without staminodes, corolla sub-bilabiate (3+1 corolla lips), tubular-funnelform four- to five-lobed, rarely bilabiate; central florets male with a rudimentary ovary, corolla tubular-funnelform, deeply five-lobed; anther apical appendages rounded to acute at the apex, basally constricted and demarcated from the thecae, basally auriculate with tails very short, smooth; style bilobed, branches dorsally papillose. Cypselae truncate at the apex, pubescent (glandular multiseriate capitate hairs), dimorphic, marginal cypselae conspicuously bigger than the central ones; pappus absent.

Pollen Description. Adenoeaulon (81 of Figs. 80-85). Pollen spheroidal, circular in polar view, medium size, P x E = (26-32 x 26-30) [micro]m. Tricolporate, colpi long with thin margin and microgranulate membrane, mesoaperture diffuse. Exine Mutisia type, microechinate, 4-5 [micro]m thick, slightly slender at the poles. Ratio ectosexine/ endosexine: 1:1.5; 1:2. Nexine 1.5 [micro]m thick. SEM: tectum punctate. Note: pollen of A. bicolor is identical to that of A. chilense Less. and similar to that of Eriachaenium magellanicum Sch. Bip. (Mutisieae) and Artemisia verlotorum Lamotte (Anthemideae). Some grains of A. chilense have endosexine with compact aspect as occurs in E. magellanicum (see also Skvarla et al., 1977; Bittmann, 1990a).

Habitat and Distribution. Genus of five species with disjunct distribution in the temperate forests and Patagonia of Argentina and Chile, Guatemala and Mexico, northern United States and southern Canada, and Asia.

Species list

1. Adenocaulon bicolor Hook., Bot. Misc. 1: 19. 1830. TYPE: Canada. British Columbia: Fort Vancouver, s.d., D. Scouler s.n. (isotype, NY not seen, NY photo at LP!). Additional specimen examined: United States. California: Sierra Nevada, Placer Co., between Iowa Hill and Forest Hill, J. H. Hunziker 4943 (LP *).

2. Adenocaulon chilense Less., Linnaea 6: 107. 1831. TYPE: Chile. Antuco, s.d., E. F. Poeppig s.n. (isotype, NY not seen, NY photo at LP!). Additional specimen examined: Chile. Prov. Ayzen: Los Mallines near Balmaceda, R. M. Bruzzone 36 (LP *).

3. Adenocaulon himalaicum Edgew., Trans. Linn. Soc. London 20: 64. 1851. TYPE: Nepal. Himalaya, Nagkanda, 1844, M. P. Edgeworth s.n. (holotype, K not seen). Additional specimen examined: Japan. Hokkaido: Moiwayama region, near Sapporo, P. Dorsett & W. Morse 1179 (US).

4. Adenocaulon lyratum S. F. Blake, J. Wash. Acad. Sci. 24:435 1934. TYPE: Guatemala. Dept. Chimaltenango: Chichauac, 20 Sept 1933, A. F. Sckutch 622 (holotype, US not seen, US photo at LP!). Additional specimen examined: Mexico. State Chiapas: Mun. of San Cristobal las Casas, above Rancho Nuevo, 9 mi SE of San Cristobal las Casas, D. Breedlove 14027 (US).

5. Adenocaulon nepalense M. Bittmann, Candollea 45: 403. 1990. TYPE: Nepal. Jaljale Himal: SE of Jaljale, Farille & Lachard 847509 (holotype, GOET not seen).

[FIGURES 7-10 OMITTED]

Literature. Bittmann (1990a, b), Katinas (2000).

Liliana Katinas (1,4) John Pruski (2) Gisela Sancho (1) Maria Cristina Telleria (3)

(1) Division Plantas Vasculares, Museo de La Plata, Paseo del Bosque s/n, 1900 La Plata, Argentina

(2) Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166-0299, USA

(3) Laboratorio de Sistematica y Biologia Evolutiva (LASBE), Museo de La Plata, Paseo del Bosque s/n, 1900 La Plata, Argentina

(4) Author for Correspondence; e-mail: katinas@fcnym.unlp.edu.ar

Published online: 9 December 2008
Table 1 Main Taxonomical Changes in the Classification and
Nomenclature of the Subfamily Mutisioidcac

Lagasca de Candolle Cassini
(1811) (1812) (1819)

"Subfamily"# "Subfamily"#
Chaenanthophorae Labiatiflorae
 Tribe#
 Mutisieae

Sect. III Sect. I --
Sect. II

 Sects. II, III, IV
Sect. I Tribe#
 Nassauvieae

Cassini Lindley
(1824, 1825) (1829)

Tribe# Mutisieae "Subfamily"#
 Mutisioideae
 (as "Suborder
-- Mutisieae")
Sect. I: Archetype Tribe# Archetype

Sect. II: Gerberieae Tribe# Gerberieae
Tribe# Nassauvieae "Subfamily"#
 Nassauvioideae
 (as "Suborder
 Nassauvieae")
Sect. I: Archetype Tribe# Archetype
Sect. II: Trixideae Tribe# TrixideaeDon

Don Lessing de Candole
(1830) (1832) (1838)

"Subfamily"# "Subfamily"#
Labiatiflorae Labiatiflorae
 Tribe# Mutisiaceae Tribe#
Tribe# Barnadeseae Mutisiaceae
Tribe# Mutiseae Subtribe Mutisieae

Tribe#
 Chaetanthereae

Tribe# Stifftieae

Tribe#
 Diazeuxeae
 Subtribe
 Facelideae
Tribe# Perdiceae Subtribe Lerieae
 Tribe# Nassauviaceae Tribe#
Tribe# Polyachyreae Subtribe Nassauvieae Nassauviaceae
Tribe# Trixideae Subtribe Trixideae
Tribe# Jungeae

Bentham & Hoffman
Hooker (1873) (1894)

Tribe# Mutisiaceae Tribe# Mutisieae
Subtribe
 Barnadesieae
Subtribe Subtribe Mutisinae
 Gerbereae (in text, Gerberinae
 in key)

Subtribe
 Onoserideae
Subtribe Subtribe Gochnatinae
 Gochnatieae
Subtribe Subtribe Nassauvinae
 Nassauvieae

Cabrera Bremer & Jansen Bremer (1994)
(1961, 1977) (1992)

 Subfamily# Subfamily#
 Barnadesioideae Barnadesioideae
Subfamily# Subfamily# Subfamily#
 Cichorioideae Cichorioideae Cichorioideae
Tribe# Tribe# Mutisieae Tribe# Mutisieae
 Mutisieae
Subtribe -- (subtribal --
 Barnadesiinae categories not
 treated)
Subtribe Subtribe
 Mutisiinae Mutisiinae s.l.

Subtribe
 Gochnatiinae Subtribe
Subtribe Nassauviinae
 Nassauviinac

Panero & Funk Pruski (2004) and
(2002) present paper

Subfamily# Subfamily#
 Barnadesioideae Barnadesioideae
 Subfamily#
 Mutisioideae
Subfamily# Tribe# Mutisieae
 Mutisioideae
--

Subfamily#
 Gochnatioideae
Subfamily#
 Hecastocleidoideae Tribe# Stiffticae
 Stifftia Group

Subfamily# Tribe# Nassauvieae
 Mutisioideae

Note: Higher taxonomic categories are in bold is indicated with #.

Table 2 Comparative List of the Genera Within Mutisioideae Considered
by Cabrera (1977) and Bremer (1994) and in the Present Work

Cabrera (1977) Changes considered by Changes considered
 Bremer (1994) in this work

Subtribe
 Barnadesiinae
Arnaldoa To Bamadesioideae _ (a)
Barnadesia To Bamadesioideae _ (a)
Chuquiraga To Bamadesioideae _ (a)
Dasyphyllum To Bamadesioideae _ (a)
Doniophyton To Bamadesioideae _ (a)
Fulcaldea To Bamadesioideae _ (a)
Huarpea To Bamadesioideae _ (a)
Schlechtendahlia To Bamadesioideae _ (a)
Subtribe Subtribe Mutisiinae Tribe Mutisieae
 Gochnatiinae s. l.
Achyrothalamus Achyrothalamus (= Erythrocephalum) (a)
Actinoseris Actinoseris Actinoseris
Ainsliaea Ainsliaea Ainsliaea
Aphyllocladus Aphyllocladus Aphyllocladus
Not considered Brachylaena _ (a)
Chimantaea Chimantaeu To Stifftieae
Chucoa Chucoa Chucoa
Cnicothamnus Cnicothamnus Cnicothamnus
Cyclolepis Cyclolepis Cyclolepis
Diaspananthus = Ainsliaea = Ainsliaea
Dicoma Dicoma _ (a)
Duseniella To Barnadesioideae _ (a)
Erythrocephalum Erythrocephalum _ (a)
Gochnatia Gochnatia Gochnatia
Gypothamnium Gypothamanium Gypothamanium
Hecastocleis Hecastocleis Hecastocleis
Hesperomannia Hesperomannia _ (a)
Hochstetteria = Dicoma _ (a)
Hyalis Hyalis Hyalis
Not considered Not considered Ianthopappus
Lycoseris Lycoseris Lycoseris
Macroclinidium Macroclinidium Macroclinidium
Moquinia To Vernonieae _ (a)
Nouelia Nouelia Nouelia
Oldenburgia Oldenburgia Oldenburgia
Onoseris Onoseris Onoseris
Pasaccardoa Pasaccardoa _ (a)
Pertya Pertya Pertya
Plazia Plazia Plazia
Pleiotaxis Pleiotaxis _ (a)
Quelchia Quelchia To Stifftieae
Stenopadus Stenopadus To Stifftieae
Stifftia Stifftia To Stifftieae
Stomatochaeta Stomatochaeta To Stifftieae
Not considered Tarchonanthus _ (a)
Urmenetea Urmenetea Urmenetea
Warionia Unassigned to tribe _ (a)
Wunderlichia Wunderlichia To Stifftieae
Subtribe Mutisiinae Subtribe Mutisiinae Tribe Mutisieae
 s. s.
Achnopogon Achnopogon Achnopogon
Not considered To Nassauviinae Adenocaulon
Brachyclados Brachyclados Brachyclados
Cardonaea = Gongylolepis Gongylolepis
Catamixis Catamixis Catamixis
Chaetanthera Chaetanthera Chaetanthera
Chaptalia Chaptalia Chaptalia
Dinoseris = Hyaloseris Dinoseris
Duidaea Duidaea Duidaea
Not considered To Nassauviinae Eriachaenium
Eurydochus =Gongylolepis Eurydochus
Gerbera Gerbera Gerbera
Glossarion Glossarion Glossarion
Gongylolepis Gongylolepis Gongylolepis
Guaicaia = Glossarion Glossarion
Hyaloseris Hyaloseris Hyaloseris
Leibnitzia Leibnitzia Leibnitzia
Not considered Lulia Lulia
Mutisia Mutisia Mutisia
Myripnois Myripnois Myripnois
Neblinaea Neblinaea Neblinaea
Pachylaena Pachylaena Pachylaena
Perdicium Perdicium Perdicium
Piloselloides = sect. of Gerbera = sect. of Gerbera
Not considered Not considered Salcedoa
Trichocline Trichocline Trichocline
Uechtritzia Uechtritzia Uechtritzia
To Gochnatiinae To Mutisiinae s. 1. Chimantaea
To Gochnatiinae To Mutisiinae s. 1. Quelchia
To Gochnatiinae To Mutisiinae s. 1. Slenopadus
To Gochnatiinae To Mutisiinae s. l. Stifftia
To Gochnatiinae To Mutisiinae s. 1. Stomatochaeta
To Gochnatiinae To Mutisiinae s. I. Wunderlichia
Subtribe Subtribe Tribe Nassauvieae
 Nassauviinae Nassauviinae
Acourtia Acourtia Acourtia
Not considered Adenocaulon To Mutisieae
Ameghinoa Ameghinoa Ameghinoa
Not considered Not considered Berylsimpsonia
Not considered Burkartia Burkartia
Calopappus = Nassauvia Calopappus
Cephalopappus Cephalopappus Cephalopappus
Not considered Not considered Criscia
Dolichlasium Dolichla.sium Dolichlasium
Not considered Eriachaenium To Mutisieae
Holocheilus Holocheilus Holocheilus
Jungia Jungia Jungia
Leucheria Leucheria Leucheria
Leunisia Leunisia Leunisia
Lophopappus Lophopappus Lophopappus
Macrachaenium Macrachaenium Macrachaenium
Marticorenia Marticorenia Marticorenia
Moscharia Moscharia Moscharia
Nassauvia Nassauvia Nassauvia
Oxyphyllum Oxyphyllum Oxyphyllum
Panphalea Panphalea Panphalea
Perezia Perezia Perezia
Pleocarphus Pleocarphus Pleocarphus
Polyachyrus Polyachyrus Polyachyrus
Proustia Proustia Proustia
Triptilion Triptilion Triptilion
Trixis Trixis Trixis
Total genera: 89 76 74

(a) Excluded herein from Mutisioideae

Table 3 Corolla Types in Genera of the Subfamily Mutisioideae

Type of corolla Tribe Genera

Bilabiate Mutisieae Achnopogon, Brachyclados,
 Chaetanthera#, Duidaea,
 Eurydochus, Gerbera#,
 Glossarion#, Gongylolepis,
 Lulia, Mutisia#, Neblinaea,
 Trichocline, Uechtritzia

 Nassauvieae Acourtia#, Ameghinoa,
 Berylsimpsonia, Burkartia,
 Calopappus, Cephalopappus,
 Criscia, Dolichlasium,
 Holocheilus, Jungia,
 Leucheria, Leunisia,
 Lophopappus#,
 Macrachaenium,
 Marticorenia,
 Moscharia, Nassauvia,
 Oxyphyllum, Panphalea,
 Perezia, Pleocarphus,
 Polyachyrus, Proustia,
 Triptilion, Trixis

 Stifftieae Quelchia#

Tubular Mutisieae Chucoa, Cyclolepis,
 Gochnatia#, Hecastocleis

 Nassauvieae Acourtia#,
 Lophopappus#,

 Stifftieae Chimantaea, Quelchia#,
 Stenopadus, Stifftia,
 Stomatochaeta, Wunderlichia

Ligulate 5-deeply lobed Mutisieae Ainshaea, Macrochnidium,
 Myripnois, Pertya

Ligulate 5-shortly lobed Mutisieae Dinoseris, Glossarion,
 Mutisia, Hyaloseris

Sub-bilabiate Mutisieae Onoseris#

Tubular and bilabiate Nassauvieae Lophopappus#

Ligulate 5-shortly lobed Mutisieae Glossarion#
 and bilabiate

Sub-bilabiate to tubular Mutisieae Adenocaulon, Eriachaenium
 4-5-lobed/tubular

True ray to sub-bilabiate/ Chaetanthera#,
 bilabiate, Lycoseris#
 tubular-bilabiate

Bilabiate/bilabiate, Mutisieae Perdicium, Leibnitzia#
 tubular-bilabiate

Tubular/tubular-bilabiate Mutisieae Gochnatia#

Bilabiate/tubular to Mutisieae Aphyllocladus#,
 tubular-bilabiate Lycoseris#,
 Onoseris#, Urmenetea#

Broadly bilabiate, Mutisieae Actinoseris,
 sub-bilabiate/tubular Aphyllocladus#,
 Cnicothamnus,
 Gypothamnium, Hyalis,
 lanthopappus, Nouelia,
 Oldenburgia, Onoseris#,
 Plazia

Broadly bilabiate/ Mutisieae Chaptalia#, Gerbera#
 bilabiate/bilabiate

True ray/filiform Mutisieae Chaptalia#,
 (or absent)/ bilabiate, Leibnitzia#
 tubular-bilabiate

True ray/tubular, Mutisieae Lycoseris#
 tubular-bilabiate

Corollas separated by bars represent the different types of corolla
in the same capitulum, from the marginal to the central corollas.
In boldface are indicated with # genera that exhibit more than one
type of corolla (or corolla arrangement)
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Article Details
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Title Annotation:Part 1
Author:Katinas, Liliana; Pruski, John; Sancho, Gisela; Telleria, Maria Cristina
Publication:The Botanical Review
Article Type:Report
Geographic Code:1USA
Date:Dec 1, 2008
Words:16910
Previous Article:Molecular phylogenetic studies of Caribbean palms (arecaceae) and their relationships to biogeography and conservation.
Next Article:The subfamily Mutisioideae (Asteraceae).
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