Recent Advances in Understanding Apiales and a Revised Classification

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Recent advances in understanding Apiales and a revised classification

GM Plunkett1*, GT Chandler1,2, PP Lowry II3, SM Pinney1 and TS Sprenkle1

1 Department of Biology, Virginia Commonwealth University, PO Box 842012, Richmond, Virginia 23284-2012, United States of America 2 Present address: Department of Biology, University of North Carolina, Wilmington, North Carolina 28403-5915, United States of America 3 Missouri Botanical Garden, PO Box 299, St Louis, Missouri 63166-0299, United States of America; Département de Systématique et Evolution, Muséum National d’Histoire Naturelle, Case Postale 39, 57 rue Cuvier, 75231 Paris CEDEX 05, France * Corresponding author, e-mail: [email protected]

Received 23 August 2003, accepted in revised form 18 November 2003

Despite the long history of recognising the angiosperm Apiales, which includes a core group of four families order Apiales as a natural alliance, the circumscription (Apiaceae, Araliaceae, Myodocarpaceae, Pittosporaceae) of the order and the relationships among its constituent to which three small families are also added groups have been troublesome. Recent studies, howev- (Griseliniaceae, Torricelliaceae and Pennantiaceae). After er, have made great progress in understanding phylo- a brief review of recent advances in each of the major genetic relationships in Apiales. Although much of this groups, a revised classification of the order is present- recent work has been based on molecular data, the ed, which includes the recognition of the new suborder results are congruent with other sources of data, includ- Apiineae (comprising the four core families) and two ing morphology and geography. A unified picture of rela- new subfamilies within Apiaceae (Azorelloideae and tionships has now emerged regarding the delimitation of Mackinlayoideae).

Introduction

Almost all authors have considered the dicot families made in the ordinal classification of Apiales (Dahlgren 1980 Apiaceae and Araliaceae closely related (e.g. Bentham and being the only notable exception). In the past ten years, Hooker 1867, Engler and Prantl 1898, Bessey 1915, however, a unified picture of relationships has rapidly Dahlgren 1980, Cronquist 1981, 1988, Takhtajan 1987, emerged regarding both the circumscription and internal Thorne 1992, but see Hutchinson 1967, 1973) and have relationships of the order. Similar progress has been made usually treated them in the same order, albeit under various in many other angiosperm orders, and several ongoing names, including Umbellales, Cornales (when associated efforts are now underway to formalise the results of these with Cornaceae), Araliales, and Apiales (the name we shall advances (APG 1998, 2003, Stevens 2003). Most authors use hereafter). The near-ubiquity of this interpretation stands working on Apiales have hesitated to provide a formal recir- in stark contrast to the diverse treatments both above and cumscription of the order during this ‘period of discovery’. below the ordinal level, such as the placement of Apiales The recent publication of a new apialean classification by an among the other orders of dicots, the inclusion of additional author with little or no expertise in the group (Doweld 2001), families within the order (Cornaceae, Torricelliaceae, including the description of two new families based on our Helwingiaceae, Griseliniaceae, etc.), and the many inter- own work (viz. Plunkett and Lowry 2001), has prompted us and infrafamilial treatments of Apiaceae and Araliaceae to provide both a formal classification of Apiales together themselves. As with many higher taxonomic groups, the dif- with a review of the relevant literature upon which our deci- ficulties in sorting out relationships in Apiales presumably sions are based. We hope this effort will also provide a fitting stem from repeated cycles of divergence and migration, fol- framework from which the other contributions to this sympo- lowed by convergence and parallelism. sium volume can be better understood. In the decades immediately preceding the development of Several publications already provide comprehensive objective approaches to phylogenetic analysis (e.g. parsi- reviews of the taxonomic history of Apiales and/or their con- mony, phenetic, and likelihood methods) and the use of stituent groups (e.g. Constance 1971, Heywood 1978, molecular sources of data, few substantial advances were Plunkett et al. 1996a, 1996b, 1997, Downie et al. 2001, 372 Plunkett, Chandler, Lowry, Pinney and Sprenkle

Plunkett and Lowry 2001, Plunkett 2001), and therefore this step that we now take with the description of Azorelloideae information is not repeated herein. Instead, we focus on as a new subfamily of Apiaceae in Table 1. reviewing (or in some cases previewing) results from recent A third group of ‘hydrocotyloids’ forms a clade together studies (or unpublished work) completed since the publica- with two genera traditionally referred to Araliaceae, tion of the preceding Apiales Special Issue of the Edinburgh Mackinlaya and Apiopetalum. This clade is currently recog- Journal of Botany (2001, Volume 58, no. 2). Following this, nised either as a tribe (Mackinlayeae, e.g. in Plunkett and we provide a formal recircumscription and interfamilial clas- Lowry 2001), a family (Mackinlayaceae, Doweld 2001), or sification of the order. simply as the ‘Mackinlaya group’ (Chandler and Plunkett 2004). In addition to Mackinlaya and Apiopetalum, it Apiaceae includes the ‘hydrocotyloid’ genera Centella, Micropleura, Actinotus, Platysace, Xanthosia and possibly other, as yet In their contributions to the last symposium volume, both unsampled, genera (see Plunkett et al. 1997, Downie et al. Plunkett (2001) and Downie et al. (2001) explored relation- 2000, Plunkett and Lowry 2001, Chandler and Plunkett ships within Apiaceae using ‘supertree’ and ‘consensus’ 2004). In the study of Chandler and Plunkett (2004), a approaches, respectively (Downie et al. 2001 also examined Bayesian inference tree based on combined 26S rDNA, relationships within subfamily Apioideae using a ‘combined rbcL, and matK data place the Mackinlaya group as sister to data’ approach). With the exception of Chandler and core Apiaceae (Figure 1), in agreement with an earlier study Plunkett (2004), most recent studies of Apiaceae have using matK and ITS rDNA data (Plunkett and Lowry 2001). focused on relationships within subfamilies and/or among These results are supported by several morphological char- genera (e.g. Lee et al. 2001, Spalik et al. 2001a, 2001b, acters that serve to link the Mackinlaya group to Apiaceae, Valiejo-Roman et al. 2002, Liu et al. 2003), and relatively few such as laterally-compressed bicarpellate fruits, valvate developments have been made in the familial and subfamil- petals that are both clawed and inflexed, and sheathing peti- ial classification of Apiaceae during the past two years. ole bases. For this reason, we recognise the Mackinlaya Unfortunately, several different definitions of Apiaceae are group as a distinct subfamily of Apiaceae, which is likewise currently in use, including the traditional circumscription formally published as Mackinlayoideae in Table 1. (Drude 1898 as updated by Pimenov and Leonov 1993), a Great progress has recently been made in re-circumscrib- much more expansive circumscription that includes both ing subfamily Saniculoideae. In their study of fruit structure, Apiaceae (sensu Drude) and Araliaceae (e.g. Judd et al. Liu et al. (2003) refined the list of carpological features that 2002), and a narrower concept generally referred to as ‘core characterise Saniculoideae, which now includes (with some Apiaceae’ (originally coined by Plunkett et al. 1997). Core exceptions) the presence of non-lignified endocarps, meri- Apiaceae are in large part consistent with Drude’s familial carp outgrowths, and prominent intrajugal secretory ducts and subfamilial concepts, but not his tribes, which rarely cor- (also called ‘companion canals’ by Tseng 1967), plus the respond to monophyletic groups (see Downie and Katz- lack of true vittae in the commissures. On the basis of these Downie 1996, Downie et al. 1996, 2000, 2001, Plunkett et al. findings, several taxa can now be added to or removed from 1996b, Plunkett and Downie 1999). the subfamily, and in most cases these transfers are con- At the subfamilial level, the greatest taxonomic impact of firmed by molecular data. For instance, both matK data recent phylogenetic studies has been the recognition that (Plunkett et al. 1996b) and ITS data (Valiejo-Roman et al. the apiaceous subfamily Hydrocotyloideae is polyphyletic, 2002) indicate that Lagoecia should be removed from with no fewer than three unrelated clades of hydrocotyloids Saniculoideae and placed in Apioideae, and this finding is spread throughout Apiales (e.g. Plunkett et al. 1997, supported by the presence of commissural vittae in Plunkett and Lowry 2001, Chandler and Plunkett 2004) Lagoecia, a feature lacking in all other saniculoids but com- (Figure 1). Of those hydrocotyloids sampled to date, a large mon among the apioids (Liu et al. 2003). Fruit anatomical clade approximates Drude’s original circumscription of this characters also suggest that Saniculoideae should be subfamily, including Azorella, Bolax, Bowlesia, broadened to include three former apioids, Lichtensteinia, Dichosciadium, Dickinsia, Diplapsis, Eremocharis, Polemanniopsis and Steganotaenia, plus the former ‘hydro- Gymnophyton, Huanaca, Mulinum, Schizeilema and cotyloid’ Arctopus, a finding that agrees with ITS sequence Spananthe, plus Stilbocarpa (which has been transferred data for Polemanniopsis and Steganotaenia (see Downie from Araliaceae; see Mitchell et al. 1999) and possibly and Katz-Downie 1999), as well as data sets based on ITS Klotzchia. This clade, however, cannot retain the name + matK (Plunkett and Lowry 2001) and 26S rDNA + rbcL+ Hydrocotyloideae because it does not contain the type matK (Chandler and Plunkett 2004) for Arctopus. genus, Hydrocotyle, which instead forms a subclade with Much work remains to be completed in subfamily Trachymene within Araliaceae (a result that is strongly sup- Apioideae, which includes about 400 genera and over 3 000 ported in all studies based on molecular data; Plunkett et al. species (Pimenov and Leonov 1993). The study of Downie et 1996a, 1997, Downie et al. 2000, Plunkett and Lowry 2001, al. (2001) remains the best overview of the status of inter- Chandler and Plunkett 2004, but see also Henwood and generic taxa among the apioids. In recognising only mono- Hart 2001). Downie et al. (2000) used the informal name phyletic groups, Downie et al. (2001) reported ten formal ‘Azorella clade’ to describe the ‘hydrocotyloids’ that remain tribes and seven informally-named groups currently accept- in Apiaceae, but refrained from recognising it formally1, a ed on the basis of recent molecular studies. However, these

1 Downie et al. (2000) indicated that Cerceau-Larrival (1962) invalidly and illegitimately published the name Azorelloideae. However, her use of this name was not accompanied by the designation of type nor by a Latin diagnosis; thus it was not validly published and remains available. South African Journal of Botany 2004, 70: 371–381 373

97 Aegopodium 91 Lagoecia Apiales 90 Pimpinella 100 Apium Petroselinum 100 100 Arracacia 98 100 Donnellsmithia 65 100 Angelica Endressia Apioideae 100 Coriandrum Neogoezia 100 100 Aciphylla 100 Daucus Bupleurum 100 Anginon 100 Heteromorpha 100 Eryngium Apiaceae 100 Sanicula Saniculoideae 100 Astrantia Arctopus 99 Azorella sel. 99 100 Huanaca 100 Azorella trif. 100 100 Mulinum chil. 100 Mulinumsp. Diplaspis Azorelloideae 100 Spananthe 100 Bolax 100 100 100 Dichosciadium Bowlesia Eremocharis 100 Centella 100 Micropleura 100 100 Mackinlaya conf. Mackinlaya macr. Mackinlayoideae 99 100 Apiopetalum 100 Actinotus Platysace 98 Hymenosporum 100 Pittosporum 100 Rhytidosporum Pittosporaceae 100 Marianthus 98 Sollya 100 Delarbrea 100 Pseudosciadium Myodocarpaceae Myodocarpus 100 Dendropanax 91 Fatsia 99 Trevesia 100 Hedera 99 100 86 Kalopanax 82 Eleutherococcus Polyscias 86 86 Astrotricha Osmoxylon 98 Tetrapanax Tupidanthus 100 Gastonia 100 Reynoldsia 86 100 Munroidendron 100 86 Tetraplasandra Araliaceae 99 Arthrophyllum 96 Meryta Pseudopanax 100 Aralia 100 100 98 Panax Schefflera Cheirodendron 100 Cussonia 100 Hydrocotyle mod. 100 100 Hydrocotyle vert. Hydrocotyle bowl. 100 Trachymene Griselinia Griseliniaceae 70 Melanophylla 100 96 Torricellia Torricelliaceae Aralidium Pennantia Pennantiaceae 100 100 Helianthus 100 Menyanthes Campanula 100 Dipsacus Valeriana 100 Alangium Outgroups 100 Cornus Nyssa Schizophragma

Figure 1: Phylogenetic tree showing relationships among 87 representative taxa of Apiales and outgroups based on the analysis of 5 958 characters derived from a combined data set of nuclear 26S rDNA and plastid rbcL+ matK sequences using Bayesian inference (with a GTR + I model of nucleotide substitutions). Posterior probability scores are indicated above each node. Redrawn from Chandler and Plunkett 2004 374 Plunkett, Chandler, Lowry, Pinney and Sprenkle

17 clades represent only 171 genera (less than half the total Myodocarpaceae number) and just a small fraction of the species currently included in Apioideae. Moreover, many of these genera show Myodocarpaceae comprise three genera segregated from evidence of non-monophyly. In short, despite the many Araliaceae: Delarbrea, Myodocarpus and Pseudosciadium. advances made in recent years, Apioideae remain both the The formal recognition of this new family by Doweld (2001) largest and most vexing group in Apiales, and many years of is based largely on our molecular data (Plunkett and Lowry additional study will be needed to resolve fully relationships 2001; see also Plunkett et al. 1996a, 1997, Plunkett 2001, within and among the apioid genera. Fortunately, the Lowry et al. 2001, Chandler and Plunkett 2004), but is also progress made over the past decade should provide a frame- supported by a unique morphological character found in no work from which more detailed analyses can be undertaken. other member of Apiales (viz. specialised oil vesicles in the endocarp; see Lowry 1986a, 1986b). The recognition of very Araliaceae small families is often considered undesirable (e.g. Cronquist 1981: x–xi), and we agree that Myodocarpaceae Overall relationships in Araliaceae are reviewed by Lowry et (with only three genera and 17 species) should be accepted al. (2004), on the basis of two recent studies (Wen et al. only if our dual criteria of monophyly and morphological 2001, Plunkett et al. 2004), necessitating only a brief coherence compel their recognition. Our data strongly indi- overview here. First, all molecular studies confirm the cate that Delarbrea, Myodocarpus and Pseudosciadium fall removal of five genera from Araliaceae: Mackinlaya and outside the main ‘core Araliaceae’ clade. The only approach Apiopetalum (now placed in Apiaceae subfamily that could unite these three genera to the other araliads in a Mackinlayoideae, discussed above), plus Delarbrea, monophyletic family would also necessitate the union of Myodocarpus and Pseudosciadium (placed in the newly Araliaceae with both Apiaceae and Pittosporaceae. Given recognised family Myodocarpaceae, discussed below). After the distinctive morphologies of these families, and especial- the additional transfer of Stilbocarpa to Apiaceae (see ly of Pittosporaceae, the union of these clades would yield a Mitchell et al. 1999), the remaining araliad genera form a highly heterogeneous family. Similarly problematic would be monophyletic group, often referred to as ‘core Araliaceae’. the union of Myodocarpaceae with Pittosporaceae as a sin- This clade is the basis for our recircumscription of gle family (see Figure 1), a solution that satisfies the criteri- Araliaceae in the revised classification provided in Table 1. on of monophyly but not of morphological coherence. Thus, Among the major findings within this somewhat narrowed we contend that Delarbrea, Myodocarpus and Araliaceae are the non-monophyly of the two largest genera: Pseudosciadium are best treated as a distinct family. Schefflera, which is polyphyletic, comprising at least five Within Myodocarpaceae, phylogenetic relationships unrelated clades (confirmed by a much broader study of among the genera were first discussed by Lowry (1986a, Schefflera, Plunkett, Lowry, Frodin and Wen, in prep.), and 1986b), and later tested by Plunkett and Lowry (2001). Polyscias, which is rendered paraphyletic by the inclusion of Additional data are now available from the study of Sprenkle, Tetraplasandra, Munroidendron, Reynoldsia, Gastonia, Plunkett and Lowry (in prep., see also Sprenkle 2002), Arthrophyllum and Cuphocarpus in the broad ‘Polyscias based on both plastid and nuclear sequence data from sam- sensu lato’ clade (see also Plunkett et al. 2001). Taken as a ples of all species and subspecies in each genus (Figure 2). whole, Araliaceae comprise three major clades plus as Molecular data suggest that Myodocarpaceae comprise two many as nine much smaller clades, whose interrelationships well supported clades, Myodocarpus and Delarbrea + are poorly resolved (see figures in Lowry et al. 2004). The Pseudosciadium. These clades are also well differentiated three large clades are (1) the Asian palmate group, centered on the basis of morphology, and in particular fruit types (the in eastern and southeastern Asia but also including several fleshy or spongy drupes of Delarbrea and Pseudosciadium, Neotropical lineages, (including genera such as vs the dry, schizocarpic fruits of Myodocarpus). Eleutherococcus, Kalopanax, Brassaiopsis, Macropanax, Pseudosciadium, however, is nested within the Delarbrea Dendropanax, Fatsia, Hedera and Oplopanax, plus two clade, necessitating the taxonomic transfer of its single clades of Schefflera (Asian and Neotropical)); (2) the species into Delarbrea (Lowry, Plunkett and Sprenkle in Polyscias–Pseudopanax group, including both Polyscias prep.). sensu lato and a subclade uniting Pseudopanax (sensu In Myodocarpus, the species with simple leaves and those Mitchell and Wagstaff 1997), Meryta, and most Pacific having pinnately-compound leaves are found in distinct subspecies of Schefflera; and (3) the Aralia–Panax group, clades. Plunkett et al. (1996a) postulated that simple leaves including both of these genera and their former segregates were ancestral throughout Apiales (see also Lowry et al. (e.g. Pentapanax, Sciadodendron). Among the poorly 2001, Plunkett 2001, Chandler and Plunkett 2004), but given resolved clades forming the basal polytomy are two addi- the tree topology in Figure 2, and the fact that the species of tional clades of Schefflera (the ‘African–Malagasy’ and ‘sec- Delarbrea (including Pseudosciadium) are entirely pinnate, tion Schefflera’ clades), plus seven other clades: the ancestral state cannot be unequivocally reconstructed in Cheirodendron + Raukaua, Cussonia + Seemannaralia, Myodocarpaceae. If we interpret pinnate leaves as ancestral Harmsiopanax, Cephalaralia, Motherwellia, Osmoxylon and in Myodocarpaceae, there must have been a single gain of Astrotricha. As discussed above, Hydrocotyle and this character in the common ancestor (from the simple Trachymene form a clade sister to the large clade of arali- leaves that characterised the rest of Apiales), followed by a ads, and are herein transferred to Araliaceae (Figure 1, see reversal in the simple-leaved subclade of Myodocarpus. also Lowry et al. 2004). Alternatively, pinnate leaves may have evolved twice inde- South African Journal of Botany 2004, 70: 371–381 375 pendently, once in the Delarbrea + Pseudosciadium clade, trnL-trnF data (Chandler, Pinney, Cayzer and Plunkett, in and a second time in the pinnately-compound subclade of prep.; see also Pinney 2002) is presented in Figure 3. This Myodocarpus. Because both scenarios require a minimum tree confirms the inclusion of Sollya within Billardiera. of two steps, they are equally parsimonious. Studies of leaf Moreover, Pittosporum is monophyletic only if the species development may offer some clues as to the evolution of this previously placed in Citriobatus are included and those of character. Auranticarpa are excluded. In fact, the species of Biogeographically, Myodocarpaceae are clearly centred Auranticarpa are not closely related to Pittosporum, but on New Caledonia, where all but two of the taxa are endem- rather form a clade sister to Bursaria + Rhytidosporum. ic (Lowry 1986a, 1986b). Delarbrea paradoxa subsp. para- Molecular data indicate that Marianthus may be paraphylet- doxa is more widely distributed across the south-western ic (Figure 3), and the nature of this paraphyly may necessi- Pacific, and D. michieana is endemic to Queensland, tate the union of all species assigned to Marianthus, Australia. The placement of D. paradoxa subsp. paradoxa in Bentleya, and Billardiera (+ Sollya) into a single genus. the cladogram (nested within an entirely New Caledonian Pittosporum is the largest of the nine genera (~140 clade) suggests a case of dispersal, but the position of D. species), accounting for nearly half of the species in the fam- michieana as the first-diverging lineage in the Delarbrea + ily. It is also the only genus with members found outside Pseudosciadium clade could indicate a more ancient vicari- Australia (except the monotypic Hymenosporum, which ance event associated with the separation of New Caledonia occurs in both Australia and nearby New Guinea). To from Australia (c. 55MY; see Lowry 1998 and references explore biogeographic relationships in the family, we exam- therein). ined trees resulting from two analyses, one based on ITS + trnL-trnF data (Figure 3), and another based on an expand- Pittosporaceae ed ITS data set that included sequences from the published study of Gemmill et al. (2002) (tree not shown). In agree- Evidence of a close relationship of Pittosporaceae to Apiales ment with Crisp et al. (1989), our preliminary results suggest has been available for over a century, and includes data that the family was probably not widely distributed across from stem structure (particularly the presence of schizoge- eastern Gondwanaland before its breakup, but rather was nous secretory canals, Van Tieghem 1884), ovular structure limited to Australia. Of the major clades in Pittosporaceae, and development (Jurica 1922), cytology (Jay 1969), and only the Pittosporum clade has non-Australian species. phytochemistry (Hegnauer 1971, 1982, Dahlgren 1980, Moreover, taxa from both the Pacific and Indian Ocean Jensen 1992). Choosing to dismiss these characters, some basins are nested within clades apparently originating in authors stressed the difference in ovary position (and to a Australia, suggesting more recent dispersal events to rela- lesser degree leaf shape) in separating Pittosporaceae from tively young island groups. Due to limited sample size (espe- Apiales (e.g. Cronquist 1981, Eyde and Tseng 1971). cially from the Indian Ocean basin) and the lack of strong However, the studies of Erbar and Leins (1995, 1996) have support for many clades, these results are tentative and demonstrated developmental homology among the ovary speculative, but they do suggest that Pittosporaceae may be positions of Pittosporaceae, Araliaceae and Apiaceae (see a rich source for detailed biogeographic studies. also Leins and Erbar 2004). These data, together with a growing body of molecular evidence (e.g. Plunkett et al. Griselinia, Aralidium, Torricellia, Melanophylla and 1996a, Plunkett 2001, Chandler and Plunkett 2004, Kårehed Pennantia 2003), unequivocally place Pittosporaceae within Apiales. However, the relationship of this family to the other clades in Evidence for placing Araliaceae, Apiaceae, Pittosporaceae the order remains largely unresolved. The study of Chandler and Myodocarpaceae in a single order is now overwhelming, and Plunkett (2004) suggests a relationship of and includes information from morphological, anatomical, Pittosporaceae to Myodocarpaceae, which in turn may be developmental, cytological, phytochemical, and molecular sister to Apiaceae (Figure 1). data (discussed above). Although relationships among these Within Pittosporaceae, Cayzer et al. (1999a, 1999b, four families are not yet fully resolved, all phylogenetic stud- 2000a, 2000b, 2004, see also Cayzer 1998, Cayzer and ies unite these lineages into a single clade. Molecular data Crisp 2004) have undertaken phylogenetic analyses based provide further evidence for expanding Apiales to include on morphological characters, resulting in several taxonomic five additional genera: Griselinia, Aralidium, Torricellia, changes. For example, all species of Sollya are now treated Melanophylla and Pennantia. The morphological support for under Billardiera (Cayzer et al. 2004) and the species of their inclusion, however, is less straightforward (reviewed in Citriobatus are included within Pittosporum (Cayzer et al. Plunkett 2001, Chandler and Plunkett 2004, Kårehed 2003). 2000a). In addition, the new genus Auranticarpa has been For example, none of these taxa possesses the schizoge- erected for a clade of species formerly included within nous secretory canals that so strikingly characterise the Pittosporum (Cayzer et al. 2000b). Altogether, Cayzer and wood (and often other plant parts) of the four core families in her co-workers currently recognise nine genera in the fami- Apiales. The basic chromosome number inferred for Apiales ly: Pittosporum, Billardiera, Bursaria, Marianthus, (x = 6 or 12; see Yi et al. in press) is shared by Torricellia and Auranticarpa, Rhytidosporum, Cheiranthera, Bentleya and possibly Pennantia (n = 25, which may represent an aneu- Hymenosporum. ploid increase from n = 24, and thus x = 12), but not with Molecular data provide independent confirmation of Griselinia (x = 9) or Aralidium (x = 10) (this character Cayzer’s findings. A preliminary cladogram based on ITS + remains unknown for Melanophylla) (reviewed in Plunkett 376 Plunkett, Chandler, Lowry, Pinney and Sprenkle

Myodocarpaceae 61 Myodocarpus nervatus Myodocarpus touretteorum

99 Myodocarpus simplicifolius Myodocarpus simplicifolius Myodocarpus crassifolius 50 Myodocarpus gracilis Myodocarpus involucratus 92 Myodocarpus lanceolatus simple leaves Myodocarpus simplicifolius Myodocarpus Myodocarpus vieillardii Myodocarpus vieillardii 100 70 Myodocarpus fraxinifolius 97 Myodocarpus fraxinifolius 71 Myodocarpus fraxinifolius

98 99 Myodocarpus pinnatus Myodocarpus pinnatus

Myodocarpus fraxinifolius compound leaves 100 99 Delarbrea collina 98 Delarbrea collina Pseudosciadium balansae

100 85 Delarbrea paradoxa ssp. depauperata Delarbrea paradoxa ssp. depauperata Delarbrea + 82 100 Delarbrea paradoxa ssp. paradoxa Pseudosciadium 100 Delarbrea paradoxa ssp. paradoxa 100 Delarbrea harmsii Delarbrea michieana

100 Astrotricha sp. Osmoxylon geelvinkianum Apiopetalum velutinum

Figure 2: Strict consensus of 17 most parsimonious trees based on a combined data set of nuclear rDNA spacers (ITS and partial ETS) and plastid trnL-trnF sequences from 29 taxa of Myodocarpaceae and outgroups. The total data set included 1 804 characters, of which 336 were potentially informative. The shortest trees were 569 steps long, with a consistency index of 0.815 and a retention index of 0.930. Bootstrap percentages are indicated at each node. Redrawn from Sprenkle, Plunkett and Lowry, in prep.

2001, Kårehed 2003). Similarly, both phytochemistry and 2003). In Torricellia and Melanophylla, all three carpels per- wood anatomy provide conflicting evidence for the inclusion sist, yielding three locules (reports of ‘(2–)3’ or ‘3(–4)’ appear of these five genera in Apiales (reviewed in Plunkett 2001, to be due to irregularly-shaped locules that may be either Kårehed 2003). Plunkett et al. (1996a) originally hypothe- overlooked or counted twice, respectively (GM Plunkett, sised that bicarpelly was ancestral in Apiales, a result con- pers. obs.)). In Griselinia, only a single locule is discernable, firmed for the core families (e.g. Lowry et al. 2001, Plunkett and in both Aralidium and Pennantia, two abortive locules 2001, Plunkett and Lowry 2001, Chandler and Plunkett are located adjacent to the single, fully developed one. 2004, Kårehed 2003), but not for Griselinia, Aralidium, Thus, it appears that tricarpelly was ancestral in Apiales, fol- Torricellia, Melanophylla and Pennantia. In these genera, lowed by a single reduction to two carpels only after the the number of locules is variable, but the ovaries are clearly divergence of these five genera (see also Chandler and derived from three carpels, and in all cases, only a single Plunkett 2004, Kårehed 2003). functional ovule is produced (see Watson and Dallwitz 1992, Dillon and Muñoz-Schick 1993, Plunkett 2001, Kårehed South African Journal of Botany 2004, 70: 371–381 377

Pittosporaceae 69 Billardiera cymosa Billardiera lehmanniana 62 99 Billardiera (= Sollya) heterophylla Billardiera Billardiera (= Sollya) fusiformis (incl. Sollya) Billardiera longifolia Billardiera fraseria 60 Marianthus ringens Marianthus 93 Marianthus bicolor Bentlya spinescens Bentleya Cheiranthera linearis Cheiranthera Hymenosporum flavum Hymenosporum Bursaria incana 80 Bursaria Bursaria spinosa Rhytidosporum alpinum Rhytidosporum 72 100 Auranticarpa papyracea 56 Auranticarpa edentata Auranticarpa 100 Auranticarpa ilicifolia 60 Pittosporum oreillyanum 93 Pittosporum (=Citriobatus) lancifolium Pittosporum (=Citriobatus) spinescens Pittosporum (=Citriobatus) multiflorum 98 Pittosporum trilobium Pittosporum rubignosum 85 Pittosporum suberosum Pittosporum Pittosporum moluccanum 83 (incl. Citriobatus) 80 Pittosporum venulosum Pittosporum ferrigineum 100 Pittosporum angustifolium Pittosporum ligustrifolium Pittosporum wingii Pittosporum eugenioides Pittosporum crassifolium 100 Myodocarpus fraxinifolius Delarbrea collina Outgroups Schefflera baillonii

Figure 3: Strict consensus of 116 most parsimonious trees based on a combined data set of ITS nuclear rDNA and plastid trnL-trnF sequences from 35 taxa of Pittosporaceae and outgroups. The total data set included 1 705 characters, of which 299 were potentially informative. The shortest trees were 737 steps long, with a consistency index of 0.581 and a retention index of 0.719. Bootstrap percentages are indicated above each node. Redrawn from Chandler, Pinney, Cayzer and Plunkett, in prep. 378 Plunkett, Chandler, Lowry, Pinney and Sprenkle

Revised Classification of the Order Apiales logical heterogeneity, making it difficult to characterise or recognise. Thus, both Pittosporaceae and the small (but well The manner of translating phylogenetic studies into formal supported and morphologically coherent) Myodocarpaceae systems of classification is currently a subject of great are recognised as distinct families. debate (e.g. De Queiroz and Gauthier 1994, Nixon and Perhaps the most difficult issue to resolve in the classifi- Carpenter 2000, Langer 2001, Sennblad and Bremer 2002), cation of Apiales is also the most fundamental: how broadly but systematists appear to be united in espousing the prin- to define the order. The four ‘core’ families described ciple of stability. In Apiales, many of the traditional taxonom- above (Apiaceae, Araliaceae, Pittosporaceae and ic groups are now known to be non-monophyletic and are Myodocarpaceae) represent a monophyletic group that widely acknowledged to be in need of substantial realign- shares many features (e.g. anatomy, cytology, phytochem- ment. However, given the size of the order (representing istry). Molecular data agree in placing Griselinia, Aralidium, over 5 000 species), most students of Apiales have been Torricellia, Melanophylla and Pennantia as successively sis- reluctant to make formal taxonomic changes based on the ter to the four-family clade, but these five genera lack many sampling of relatively few taxa, especially when the compo- of the distinctive features uniting the four core families. Each sition of some clades appeared to be unstable from study to of these five genera has been recognised as its own order, study. Nonetheless, there is an obvious need to name but we believe that monogeneric (and in the case of clades for the purpose of discussion and as a framework for Aralidium, monotypic) orders are redundant and offer no further investigations. In the past, we have advocated the additional taxonomic information. Thus, we concur with ear- use of informal clade names (e.g. ‘core Apiaceae’, the ‘Asian lier proposals (e.g. APG 1998, 2003, Plunkett 2001, palmate clade’, the ‘apioid superclade’, the ‘Mackinlaya Chandler and Plunkett 2004, Kårehed 2003) that include group’, etc.) until a unified picture of phylogenetic relation- Griselinia, Aralidium, Torricellia, Melanophylla and ships has emerged. To a large degree, such stability in our Pennantia within Apiales, placed in three families: understanding of Apiales has now been achieved at the Pennantiaceae (monogeneric), Griseliniaceae (monogener- interfamilial level. Moreover, the multiplication of informal ic), and Torricelliaceae (broadened to include Torricellia, names (often with similar wording, but defining slightly dif- Aralidium and Melanophylla). However, because the ferent and overlapping groups) has reached the point where ‘four-family clade’ (comprising Apiaceae, Araliaceae, it is hindering rather than helping communication. For Pittosporaceae and Myodocarpaceae) is well supported, example, there are at least three informal definitions of morphologically coherent, and the focus of most of the Apiaceae in current usage (viz. the ‘traditional Apiaceae’ research being conducted within the order, we contend that (sensu Drude), ‘Apiaceae sensu lato’ (including Araliaceae), it should be recognised formally. The application of an infor- and ‘core Apiaceae’ (excluding many ‘hydrocotyloids’)), as mal name (such as ‘core Apiales’) might appeal to some, but well as a number of competing notions of both Araliaceae recent experience (at least in Apiales) suggests that the def- and the entire order. Several authors have provided formal initions and circumscriptions of such names are often unsta- names or recircumscriptions affecting Apiales either at high- ble and can lead to considerable confusion. We therefore er levels of classification (e.g. the ordinal system of the APG provide a formal name (with an explicit circumscription) in 1998, 2003) or at the intergeneric level (e.g. Downie et al. recognising a new suborder, Apiineae. Despite suggestions 2000 for core Apiaceae), but the time is now ripe to offer an to the contrary, the principle of exhaustive subsidiary taxa is interfamilial classification of Apiales as a whole. not a requirement of the ICBN (Greuter et al. 2000), and thus In the system that follows, we recognise groups on the subordinal names are neither required nor provided for the basis of two criteria, monophyly (usually determined by phy- other three families in the order. A synopsis of the revised logenetic studies based on molecular data) and morpholog- classification is presented in Table 1. ical coherence. Using these two criteria, we translate the current concept of ‘core Araliaceae’ into a formal recircum- Acknowledgements — The authors gratefully acknowledge Prof. scription of that family, which now excludes six former arali- Ben-Erik van Wyk and Dr Patricia Tilney for organising the 4th ad genera (Myodocarpus, Delarbrea, Pseudosciadium, International Apiales Symposium (Pretoria) and this proceedings Apiopetalum, Mackinlaya and Stilbocarpa) and includes two volume, and for kindly inviting our contributions to both; thanks are also extended to Dr Gordon McPherson for proofreading the Latin former ‘hydrocotyloid’ genera (Hydrocotyle and diagnoses of the new taxa. Support was provided by grants from the Trachymene, leaving open the potential to add additional National Science Foundation (DEB-9981641) and the National hydrocotyloids as more taxa are sampled). In a similar fash- Geographic Society (5793-96) to GMP and PPL. ion, we treat the three major clades of ‘core Apiaceae’ (the apioids, the saniculoids and the ‘Azorella clade’) plus one References additional clade (the ‘Mackinlaya group’) as four distinct subfamilies in a recircumscribed Apiaceae. Some authors have APG (Angiosperm Phylogeny Group) (1998) An ordinal classifica- chosen to unite Apiaceae and Araliaceae into a single fami- tion for families of flowering plants. Annals of the Missouri ly (e.g. Judd et al. 2002), but our data indicate that this can- Botanical Garden 85: 531–553 not be done without also including Pittosporaceae (which is APG (Angiosperm Phylogeny Group) (2003) An update of the placed as sister either to Apiaceae or Araliaceae; see Angiosperm Phylogeny Group classification for the orders and Plunkett and Lowry 2001, Chandler and Plunkett 2004). We families of flowering plants: APG II. Botanical Journal of the believe the union of these taxa into a single, broadly defined Linnean Society 141: 399–436 Bentham G, Hooker JD (1867) Genera Plantarum. A Black, W family yields a group with an inordinate amount of morpho- Pamplin, Lovell Reeve and Co., London South African Journal of Botany 2004, 70: 371–381 379

Table 1: Revised classification of the angiosperm order Apiales

Order: APIALES Nakai 1930 Family: TORRICELLIACEAE (Wang.) Hu 1934 (only Torricellia, Melanophylla, Aralidium) Family: GRISELINIACEAE J.R. Forst. & G. Forst. 1839 (only Griselinia) Family: PENNANTIACEAE J. Agardh 1858 (only Pennantia) Suborder: APIINEAE, Plunkett & Lowry, subord. nov. Lignum canalibus secretoriis schizogenis; gynoecium oriunum a duo carpellis. T: Apium L. Family: APIACEAE Lindl. 1836 (nom. alt., Umbelliferae Durande 1782) Subfamily: APIOIDEAE Seem. 1866 Subfamily: SANICULOIDEAE Burnett 1835 Subfamily: AZORELLOIDEAE Plunkett & Lowry, subfam. nov. Fructus teres vel a dorso compressus, sine vittis; canales intra juga praesentes; endocarpium induratum; stratum interius mesocarpii lignescens vel parenchymatum, crystallis rhombeis (sed crystallis compositis in strato exteriore Azorellae); carpella secedentes in fructu maturo.T: Azorella Lam. (also incl. Bolax, Bowlesia, Dichosciadium, Dickinsia, Diplapsis, Eremocharis, Gymnophyton, Huanaca, Mulinum, Schizeilema, Spananthe, Stilbocarpa). Syn.: Hydrocotyloideae Link 1829, pro parte, excl. Hydrocotyle Subfamily: MACKINLAYOIDEAE Plunkett & Lowry, subfam. nov. Fructus a latere compressus (vel teres in Apiopetalo), sine vittis; canales intra juga minuti vel obsoleti; endocarpium sclerescens; stratum interius mesocarpii lignescens vel parenchymatum, crystallis rhombeis; carpella non secedentes in fructu maturo. T: Mackinlaya F. Muell. (also incl. Apiopetalum, Centella, Micropleura, Actinotus, Platysace, Xanthosia). Syn.: Mackinlayeae Hook.f. 1873.; Mackinlayaceae Doweld 2001 Family: ARALIACEAE Durande 1782 (incl. Hydrocotyle, Trachymene; excl. Apiopetalum, Delarbrea, Mackinlaya, Myodocarpus, Pseudosciadium, Stilbocarpa) Family: MYODOCARPACEAE Doweld 2001 Syn: Myodocarpeae R. Vig. 1906 Family: PITTOSPORACEAE R. Br. 1814

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