A reassessment of Anthurium species with palmately divided leaves, and a reinterpretation of Anthurium section Dactylophyllium (Araceae)

Abstract A reappraisal is made of the Anthurium Schott species with palmately divided leaves with 3 or more segments free to the base (i.e. palmatisect leaves), previously recognized as section Dactylophyllium Schott (Engler), as well as those species with 5 or more segments united at the base (i.e. palmatifid leaves), formerly placed in section Schizoplacium Schott (Engler). New molecular data indicates that several species (Anthurium pedatum (Kunth) Schott, Anthurium pedatoradiatum Schott, and possibly, Anthurium podophyllum (Schltdl. & Cham.) Kunth) should be excluded from section Schizoplacium, and other species previously placed in that section cannot be separated from section Dactylophyllium. Thus, Anthurium section Schizoplacium is here synonymized within section Dactylophyllium and type species are designated for both groups. This paper also provides an updated description of section Dactylophyllium as here emended, listing the 24 accepted taxa now included (20 species and 4 varieties or subspecies), along with their geographic distributions.


Introduction
Anthurium Schott species with palmately divided leaves (as included in Madison 1978) represent a very distinct morphological group within the genus (Fig. 1). In these species, leaf segments (i.e. leafl ets) are free to the base, in palmatisect leaves, or leaf segments (i.e. lobes) are united at the base, in palmatifi d leaves (Fig. 2). Th e current sectional classifi cation of Anthurium (Croat and Sheff er 1983) separates these species into two groups, section Dactylophyllium (Schott) Engler (Engler 1879), comprising species with three or more segments (leafl ets) free to the base (Fig. 2 A-B), and section Schizoplacium (Schott) Engler (Engler 1879), including species with fi ve or more segments (lobes) united at the base (Fig. 2 C). A recent molecular phylogeny (Carlsen 2011, Carlsen and Croat in press) has shown that most of the species of Anthurium with palmately divided leaves belong to a single highly supported clade (Fig. 3, Clade 3), therefore suggesting that previous divisions of the group are unnecessary. Indeed, the newly circumscribed Clade 3 merits sectional rank. Moreover, although all members of Clade 3 share palmately divided leaves, this leaf form has evolved independently at least two more times within Anthurium, in Clades 14 and 16 (Fig. 3). Th e goal of this study is to reevaluate the limits of sections Dactylophyllium and Schizoplacium in the light of the new molecular evidence and provide an updated description of this redefi ned group of Anthurium species with palmately divided leaves (Fig. 1).

Taxonomic history
In the fi rst comprehensive revision of the genus, Schott (1860) classifi ed Anthurium species with lobed or divided leaves in three groups (Table 1): grex Semaeophyllium, comprising species with "hastate-trilobed" blades with segments united at the base; grex Schizoplacium, including species with "pedately-partite" blades with fi ve or more leaf segments united at the base (i.e. palmatifi d leaves, according to our defi nition) ( Fig. 2 C); and grex Dactylophyllium, containing species with "digitisect" leaf blades with three or more segments divided completely (i.e. free) to the base (i.e. palmatisect leaves, in our defi nition) (Fig. 2 A-B). Carlsen and Croat (2007) recently revised the 23 species included in Anthurium section Semaeophyllium (Schott) Engler (Engler 1879). Th e section comprises species with trilobed leaf blades, where leaf lobes are always united at the base, and the lobes can be directed forward (i.e. falcate) or to the sides (i.e. spreading) but never toward the back. On the basis of molecular evidence (Carlsen 2011, Carlsen and Croat in press), section Semaeophyllium appears not to be monophyletic. However, species with trilobed leaves are more closely related to other Anthurium species with cordate leaves than to the species with palmately divided leaf morphology clustered in Clade 3 (Carlsen 2011, Carlsen and Croat in press). Th erefore, this paper will only deal with the Anthurium species with palmately divided leaves (Fig. 1), those included in sections Dactylophyllium and Schizoplacium. Schott (1860) included 27 names in his grex # 28 (Table 1), Dactylophyllium, but according to the most updated species synonymy for the genus (Govaerts et al. 2012), only seven species are currently recognized: Anthurium clavigerum Poepp., A. digitatum (Jacq.) Schott, A. eminens Schott, A. kunthii Poepp., A. pentaphyllum (Aubl.) G.Don, A. sinuatum Benth, and A. triphyllum (Willd. ex Schult.) Brongn. ex Schott. On the other hand, Schott (1860) included seven names in his grex # 27 (Table 1), Schizoplacium, but only four species are now recognized, A. palmatum (L.) Schott, A. pedatoradiatum Schott, A. pedatum (Kunth) Schott, and A. podophyllum (Schltdl. & Cham.) Kunth. Engler (1879) gave formal sectional ranking to these, and others, of Schott's greges, maintaining the species circumscriptions in both groups.
However, Engler (1905) made major modifi cations in the classifi cation of Schott. He described his newly circumscribed section Semaeophyllium as comprising species with "hastate-trilobed or pedatisect or digitisect" leaf blades, and very long and relatively thin (i.e. myosuroideous) spadices. Engler (1905) included in his new version of section Semaeophyllium, along with more typical species with trilobed leaves, a pair of species from Schott's grex Dactylophyllium (namely A. sinuatum and A. clavigerum) and also A. palmatum, previously placed by Schott in grex Schizoplacium. Alternatively, Engler's amended section Schizoplacium (Engler 1905) included the remaining species of both Schott's greges Dactylophyllium and Schizoplacium, along with a few more recently described species, for a total of 17 species, of which only eight are currently accepted (Table 1). Engler's (1905) new delimitation of section Schizoplacium included species with "pedately-partite" leaf blades, with segments either united at the base or completely separated, and thick, conic spadices. He further divided this section into two informal groups, § 1. Euschizoplacium Engler, with short stems and internodes, but long peduncles, and § 2. Dactylophyllium (Schott) Engler, with scandent stems, elon-  Table 1. Anthurium species with palmately divided leaves formerly included in Dactylophyllium and Schizoplacium, a comparison of previous circumscriptions. Th is is not an exhaustive list of all species names that have been previously included in these groups, it only contains taxa that were accepted at the time of publication of each work. Names in bold denote species included in the newly redefi ned section Dactylophyllium (Schott) Engler emend. Croat & Carlsen, as proposed here. Species marked with (*) are now formally excluded from this emended section. All other species names are either synonyms or species dubia, fi de Madison (1978).

Species name
Year published Schott ( gated internodes, but peduncles often short (Engler 1905). Engler placed most of the species from Schott's grex Schizoplacium in the Euschizoplacium group and the remaining species from Schott's grex Dactylophyllium in the Dactylophyllium group (Table 1). Th e last taxonomic revision of Anthurium species with palmately divided leaves (Madison 1978) recognized 27 species and three varieties divided into seven "natural" groupings based on the author's understanding of the taxonomy, morphology and growth habit of the species (Table 1). Groups 1-3 included species with trilobed leaves with falcate lobes united at the base now placed in section Semaeophyllium (Carlsen and Croat 2007). Th e remaining groups in Madison's (1978) (Table 1; following Croat and Sheff er 1983). Group 4 contained two terrestrial Mexican species with short stems, elongated peduncles and "pedately divided" (i.e. palmatifi d) leaf blades (A. pedatoradiatum and A. podophyllum). Group 5 consisted only of the Colombian species A. pedatum, with deeply dissected leaf blades with 11-15 lobes, and a pendent infl orescence borne on an erect peduncle. Group 6 included climbers with palmately divided leaves with the lobes united at the base (i.e. palmatifi d leaves) (Fig. 2 C), and elongated spadices, which range from northern Colombia to the West Indies (A. an-gustisectum Engl., A. expansum Gleason, A. longissimum Pittier and A. palmatum). Th e species in Madison's groups 4, 5 and 6 were placed in section Schizoplacium by Croat and Sheff er (1983). His group 7 is a predominantly Amazonian group of species with "digitisect" (i.e. palmatisect) leaf blades, where the leaf segments are free to the base and have a basal pulvinus (Fig. 2 A-B), and spadices are purple to gray. Madison called this group section Schizoplacium, apparently following Engler's (1905) circumscription of that section, but it indeed includes species placed in section Dactylophyllium by both Schott (1860) and Croat and Sheff er (1983) (Table 1). Croat and Sheff er (1983) provided the previously accepted treatment of the sections of Anthurium with palmately divided leaf blades. Following Schott's (1860) original classifi cation system, they separated the species of Anthurium with lobed or divided leaf blades into three sections, Semaeophyllium, Schizoplacium and Dactylophyllium (Table 1). Th ey provided a key to the sections, descriptions, and illustrative examples of species belonging to each group.

Results and discussion
Th e current molecular phylogeny of the genus Anthurium, based on chloroplast (trnG intron, trnH-psbA and trnC-ycf6 intergenic spacers) and nuclear (fi rst intron of CHS and partial fl anking coding regions) DNA sequences (Carlsen 2011, Carlsen and Croat in press) shows that the palmately divided leaf morphology is homoplasious within the genus, having evolved at least three times independently, in Clades 3, 14 and 16 (Fig. 3).
Based on this molecular phylogeny (Carlsen 2011, Carlsen and Croat in press) (Fig. 3), some of the Anthurium species with palmately divided leaves previously recognized as section Schizoplacium (Schott 1860, Engler 1879, Engler 1905, Croat and Sheff er 1983, do not form a monophyletic group and are not even closely related to other palmately divided species. For example, A. pedatum, a high elevation Colombian species with a highly divided palmatifi d leaf blade, consistently clustered in the moderately supported Clade 14 (Fig. 3), along with A. furcatum Sodiro, with trilobed leaves, and A. tremulum Sodiro and A. macleanii Schott, both with cordate leaves. Clade 14 is not easily characterized morphologically, although most of its species have hooded spathes and pendent spadices (Carlsen and Croat in press). Madison (1978) had pointed out the possible segregation of A. pedatum from all other palmately divided Anthurium species by placing it alone in Group 5 of his revised classifi cation. Molecular data now suggests that indeed A. pedatum is not closely related to other palmately divided Anthurium species and therefore does not belong to section Dactylophyllium as currently defi ned here.
Anthurium pedatoradiatum, a Mexican species with palmatifi d leaves and a member of section Schizoplacium (fi de Schott 1860, Engler 1879, Engler 1905, Croat and Sheff er 1983, should also be removed from this group. Results of molecular analyses (Carlsen 2011, Carlsen and Croat in press) strongly suggest that it is more closely related to other northern Central American species (Clade 16) than to the clade of Anthurium species with palmately divided leaves (Clade 3) (Fig. 3). Th e strongly supported Clade 16, although quite variable in terms of leaf morphology, presents very uniform reproductive features, including only species that possess bright orange berries with a mealy mesocarp, characteristics also found in A. pedatoradiatum. Madison (1978) previously separated A. pedatoradiatum from the rest of palmately divided Anthurium species, and grouped it along with the other Mexican species with palmatifi d leaves, A. podophyllum, in his Group 4. Th e latter species have not been sampled for the current molecular phylogeny of Anthurium (Carlsen 2011, Carlsen and Croat in press). However, geographical affi nities and similarities in fruit characteristics with other species of Clade 16 (Fig. 3) have made us consider that A. podophyllum is also a member of this clade, and as such, it should be excluded from section Dactylophyllium as delimited here.
Th ere are only four currently recognized species names included in the original description of Schott's grex Schizoplacium (Schott 1860), all of which match well the protologue of the section. However, according to molecular studies (Carlsen 2011, Carlsen and Croat in press) (Fig. 3), A. pedatum, A. pedatoradiatum, and very likely A. podophyllum, do not belong to the same clade and are not closely related to other palmately divided Anthurium species. Th erefore, these three species are also excluded from section Dactylophyllium according to the circumscription presented here. Th us, of the initial group, only A. palmatum remains. Th is climbing plant with elongated internodes and palmatifi d leaves (Fig. 2 C), restricted to the Lesser Antilles, is therefore here selected as the lectotype species for section Schizoplacium. Two other Anthurium species with palmatifi d leaves (A. expansum and A. longissimum) (Fig. 1 B) also belong to this section under its traditional circumscription (Table 1). Anthurium palmatum was not sampled in the current molecular phylogeny of the genus (Carlsen 2011, Carlsen and Croat in press) (Fig. 3), but the closely related A. longissimum, with which it shares climbing habit, palmatifi d leaf morphology, peduncle shorter than the petiole, green spathe, grayish purple spadix and reddish-purple berries, was used as a representative of this group of palmatifi d species.
Th e molecular phylogeny of Anthurium (Carlsen 2011, Carlsen and Croat in press) clearly shows that most of the palmately divided species sampled in the study (except for A. pedatum and A. pedatoradiatum), belong in a single clade, Clade 3 (Fig. 3). Th ese species were previously included in either section Schizoplacium (e.g. A. longissimum, a representative of the group with palmatifi d leaves) or section Dactylophyllium by Croat and Sheff er (1983). Th e fi ndings of molecular analyses indicate that the group of species with palmatifi d leaf morphology (i.e. A. longissimum, A. palmatum and A. expansum) (Figs 1 B, 2 C), all sharing similar vegetative and reproductive characters, is not distinct from other species with palmately divided leaves. Th us, these two sections are here combined, and the morphological limits of this emended, more inclusive, group are redefi ned.
In terms of nomenclatural choice, since both names, Schizoplacium and Dactylophyllium, were published, albeit without a formal rank (i.e. as grex names), at the same time in Schott's (1860) revision of the genus Anthurium, and were later simul-taneously formalized as sections by Engler (1879), none of them has priority over the other. Th erefore, in this study, section Schizoplacium, the smaller (probably containing only three currently accepted species names) and geographically more isolated group (mainly occurring in the Lesser Antilles and Cordillera de la Costa in Venezuela) has been placed into synonymy with the larger (probably including a total of 21 species, some undescribed) and more widespread group, section Dactylophyllium.
Anthurium kunthii (Fig. 2 A) is here chosen as the lectotype for this emended section Dactylophyllium for several reasons. Anthurium kunthii was among the original species included in Schott's (1860) fi rst delimitation of the group and represents very well the morphological characters described in the protologue. Also, this species was sampled in the current molecular phylogeny of the genus (Carlsen 2011, Carlsen and Croat in press) (Fig. 3), and it clearly belongs to the group of species with palmately divided leaves in Clade 3. Additionally, A. kunthii is among the oldest species described within the group (in 1845) ( Table 1), but unlike A. digitatum (the oldest described species, from 1829), its taxonomic status as a species has not been previously questioned.
Th e following section provides an updated description of Anthurium section Dactylophyllium (Schott) Engler, emend. Croat & Carlsen, and lists all currently recognized species now comprising this group and their known geographic distribution.

Taxonomic treatment
Anthurium section Dactylophyllium ( Remarks. Mostly appressed-climbing or scandent plants with internodes usually longer than broad, or terrestrial short stemmed plants; roots moderately sparse at each node on climbing plants, sometimes moderately dense on terrestrial species with short internodes; cataphylls usually persisting as fi bers, sometimes deciduous, rarely persisting intact, the cataphyll fi bers typically pale, sometimes dark reddish brown; petioles typically subterete, usually at least weakly sulcate adaxially, typically drying greenish to gray-green, sometimes dark brown; blades palmately divided and deeply lobed with 5-7 lobes united at the base (i.e. palmatifi d leaves) (Figs 1 B, 2 C) (Anthurium expansum, A. longissimum, and A. palmatum) or palmatisect with segments (leafl ets) divided completely to base and free (Fig. 2 A-B), sometimes 3-sect ( Fig. 1 C) (A. arisaemoides Madison, A. thrinax Madison, A. triphyllum, and A. trisectum Sodiro), more commonly 5-11-sect ( Fig. 1 A, D) (A. brevipedunculatum Madison, A. clavigerum, A. croatii Madison, A. eminens, A. kunthii, A. pentaphyllum, A. polyschistum R.E. Schultes & Idrobo, and A. sinuatum), the petiolules of each segment short or long (Fig. 2  A-B), the segments usually entire, sometimes sinuate (A. clavigerum, A. sinuatum) or weakly to strongly pinnately lobed (A. clavigerum); the medial segment or lobe largest; side segments or lobes diminishing in size; juvenile blades simple; leaf surface usually smooth, glabrous, generally drying greenish, sometimes yellow-brown or dark brown; midrib typically raised on both surfaces; primary lateral veins typically conspicuous, usually well spaced, weakly raised or sunken above, usually narrowly rounded and prominently raised below; tertiary veins typically visible, sometimes moderately wellraised beneath. INFLORESCENCE short-(A. brevipedunculatum, A. pentaphyllum) or more commonly long-pedunculate; spathe typically green, spreading, sometimes ovate and erect (A. brevipedunculatum), usually persistent; spadix green to purplish violet, usually long-tapered, sometimes short-tapered. FRUITS purple, violet-purple or reddish-purple berries. Species of Anthurium included in section Dactylophyllium, under this revised delimitation, are mainly distributed in the Amazon lowlands, with a few widespread species ranging into Central America (A. clavigerum, A. kunthii, and A. trisectum), and into the Atlantic coast of South America to Brazil (A. pentaphyllum). Th ree taxa have disjunct distributions in the coastal mountain ranges of the Cordillera Central of Venezuela (A. digitatum and A. longissimum) and the Lesser Antilles (A. palmatum).
Presently, 24 accepted taxa (20 species and 4 varieties or subspecies) occur in section Dactylophyllium as emended here. Th ese taxa and their geographic distribution are as follow: A. polydactylum Madison (Bolivia, Peru) (Fig. 1 D) A. polyschistum R.E. Schultes & Idrobo (Brazil, Colombia, Ecuador, Peru) A. sinuatum Benth ex Schott (Brazil, French Guiana, Suriname, Venezuela) A. thrinax Madison (French Guiana, Guyana) A. triphyllum (Willd. ex Schult.) Brongn. ex Schott (Bolivia, Ecuador, Peru) A. trisectum Sodiro (Costa Rica to Ecuador) (Fig. 1 C) A. zuloagae Croat (Colombia) Th ere are also at least four more currently undescribed species in the section, and at least two more varieties that need formal recognition. A complete taxonomic revision, including identifi cation keys, species synonymy, descriptions and illustrative photographs, of all the species of Anthurium with palmately divided leaves comprising the newly amended section Dactylophyllium is indeed needed, but beyond the scope of this article.