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Phylogeny, Species Delimitation and Revision of Pleioluma (Sapotaceae) in New Caledonia, a Frequently Gynodioecious Genus

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Phylogeny, Species Delimitation and Revision of Pleioluma (Sapotaceae) in New Caledonia, a Frequently Gynodioecious Genus CSIRO PUBLISHING Australian Systematic Botany, 2018, 31, 120–165 https://doi.org/10.1071/SB17040 Phylogeny, species delimitation and revision of Pleioluma (Sapotaceae) in New Caledonia, a frequently gynodioecious genus Ulf Swenson A,D, Johan A. A. Nylander B and Jérôme Munzinger C ADepartment of Botany, Swedish Museum of Natural History, PO Box 50007, SE-104 05 Stockholm, Sweden. BNBIS/Department of Bioinformatics and Genetics, Swedish Museum of Natural History, PO Box 50007, SE-104 05 Stockholm, Sweden. CAMAP, IRD, CIRAD, CNRS, INRA, Université Montpellier, F-34000 Montpellier, France. DCorresponding author. Email: [email protected] Abstract. Pleioluma (Baill.) Baehni (Sapotaceae) circumscribes some 40 medium-sized trees and shrubs, many gynodioecious, in Australia, Malesia and New Caledonia. Systematics of the group is unclear and delimitations of species are notoriously difficult. We explore species boundaries in New Caledonia by multiple accessions of ‘species’, molecules and morphology in a Bayesian framework. The molecular phylogenetic signal is weak, but morphology provides enough information to support groups, species and recognition of one cryptic species. Pleioluma is then revised for New Caledonia, a genus distinguished by areolate higher leaf venation, sepals being pubescent on both surfaces, stamens inserted in or below the middle of the corolla tube, presence of staminodes, foliaceous cotyledons and endosperm. Seventeen endemic species are recognised with descriptions, recognition notes, distributions, etymologies and conservation assessments. Six species are described as new, of which four are assigned IUCN preliminary status as Critically Endangered and in urgent need of protection (Pleioluma acutifolia Swenson & Munzinger, P. belepensis Swenson & Munzinger, P. butinii Swenson & Munzinger and P. tchingouensis Swenson & Munzinger). The new species, P. dioica Swenson & Munzinger and P. tenuipedicellata Swenson & Munzinger are respectively assessed as Data Deficient and Vulnerable. The micro-endemic species P. vieillardii (Baill.) Swenson & Munzinger, confined to the Koniambo massif, is also critically endangered and needs urgent conservation management. Received 28 July 2017, accepted 18 January 2018, published online 1 May 2018 Introduction sepals having indument on the outer and inner surface, stamens Pleioluma (Baill.) Baehni is a genus of Sapotaceae subfamily inserted in the middle or near the base of the corolla tube, and Chrysophylloideae Luerss. (Swenson and Anderberg 2005) and presence of staminodes, which often are reduced in female it circumscribes ~40 species of medium-sized trees and shrubs. flowers. Seeds have foliaceous cotyledons, an exserted radicle The centre of diversity is in Australia, New Caledonia and below the commissure and an endosperm. Pleioluma may be New Guinea, but the genus extends through Malesia to South- confused with the related genus Pichonia Pierre, with which it east Asia. Historically, a limited number of highly variable floral shares a similar areolate leaf venation and indument on both features and the inability to identify consistent morphological surfaces of the sepals (Swenson and Munzinger 2012). characters have caused taxonomists to propose various Despite the fact that specimens can be readily placed in classification systems of Sapotaceae during the past 50 years Pleioluma, species are frequently difficult to circumscribe. (Aubréville 1964a; Baehni 1965; Pennington 1991; Swenson Wim Vink at the Leiden herbarium (L) has worked for and Anderberg 2005). Therefore, members of Pleioluma have decades to sort out problems in what he believed was Pouteria been misplaced in several genera, especially Pouteria Aubl. sensu Pennington (1991) in New Guinea (Vink 2002). In 2012, (Baehni 1942; Pennington 1991; Govaerts et al. 2001; Vink Vink showed me (US) several boxes of specimens he had 2002); however, phylogenetic analyses have demonstrated that set aside as especially problematic and tentatively calling it Pleioluma forms a strongly supported group, sister to all other ‘the firma-group’ after Pouteria firma (Miq.) Baehni. He had genera of the subfamily in Australasia (Bartish et al. 2005, 2011; unfortunately given up revising the group because he was Swenson et al. 2007a, 2008, 2013). unable to circumscribe the species. However, most, if not all, All members of the genus are easily distinguished by were easily identified as members of Pleioluma, a genus that a character combination, including areolate higher leaf venation, was resurrected 1 year later (Swenson et al. 2013). Material from Journal compilation Ó CSIRO 2018 www.publish.csiro.au/journals/asb Pleioluma (Sapotaceae) in New Caledonia Australian Systematic Botany 121 New Guinea and elsewhere in Malesia is very different from Sideroxylon and one from Sapota Mill., to Planchonella Pierre, species in New Caledonia, but their species boundaries may never whereas the other remained in Beccariella. Baehni (1942) took a be solved because many forests throughout this area have been more simplistic approach and placed them all in Pouteria, a genus logged and are now gone forever. Furthermore, much existing that at the time became very heterogenous and pantropical with herbarium material has been treated with mercury and is not 318 species. Van Royen (1957), opposed to Baehni’s treatment, useful for molecular studies. removed all of the present Pleioluma species and again placed Aubréville (1967) recognised 11 Pleioluma species (placed them in Planchonella, which after that comprised a total of 99 in Beccariella Pierre at the time) in his flora of New Caledonia. species. Without justification, Herrmann-Erlee and van Royen Some of those were poorly known or believed to be merely (1957) retained several Australasian species in Pouteria, which ecological forms restricted to particular soil types. Through at the time represented a highly heterogeneous group, the species our own fieldwork in New Caledonia and herbarium studies in of which are, today, distributed in Pichonia, Planchonella, Paris, new entities have been recognised; however, taxon Pycnandra Benth., Sersalisia R.Br. and Van-royena Aubrév. boundaries, just like in New Guinea, are frequently difficult. (Swenson et al. 2013). Possible reasons for poorly resolved phylogenies and unclear In 1964, Aubréville proposed his classification of Sapotaceae species limits are the low molecular variation in the group and and recognised the tribe Planchonelleae in which he distinguished rather recent, Upper Miocene and Pliocene, divergence dates Planchonella and Beccariella, the former with ~80 species (Swenson et al. 2013, 2014). and the latter with 14 species in Australasia (Aubréville New Caledonia is an archipelago ~1500 km east of 1964a, 1964b). He used the number of seeds in each fruit to Queensland (Australia) in the south-western Pacific Ocean. distinguish between the two, one seed in Beccariella and usually The land area occupies some 19 060 km2, with Grande Terre two or more seeds in Planchonella, a character that is still rather being the largest island covering some 16 595 km2 (Neall and useful for identification purposes in New Caledonia (but it Trewick 2008). Grande Terre is a fragment of continental crust is wise to open several fruit because of variability). Aubréville that was overlain by an ophiolite nappe of ultramafic substrates in (1967) accepted 11 species in New Caledonia, of which the Eocene (Aitchison et al. 1995; Pelletier 2007; Maurizot and B. crebrifolia (Baill.) Aubrév. was suspected to be an ecological Vendé-Leclerc 2012). Today, a third of Grande Terre is covered form of B. balansana (Pierre ex Baill.) Aubrév. by this nappe and the remainder consists of schist and other In 1991, Pennington proposed a classification of Sapotaceae metamorphic rocks, with only smaller outcrops or islands of solely on the basis of morphology, and he reduced Aubréville’s calcareous rocks. All this has formed a mosaic of soil types to 122 genera to 53. Both Planchonella and Beccariella were which many species are restricted, usually to non-ultramaficor united in Pouteria section Oligotheca (A.DC.) Baehni, a section ultramafic substrates (Ibanez et al. 2014; Isnard et al. 2016). This recognised by foliaceous cotyledons, a radicle extending below is certainly true for Sapotaceae in this territory (Swenson and the cotyledon commissure, and endosperm (Seed type 1, sensu Munzinger 2016). Faria et al. 2017). The seed characters that readily distinguish The main purpose of the present paper is to present a revision section Oligotheca from the core members of Pouteria, viz. of New Caledonian Pleioluma. We begin with a historic plano-convex cotyledons, an included radicle, and absence of review, followed by assessing phylogenetic relationships of endosperm (Seed type 2), were believed to be of little importance. the entire genus. Multiple accessions of some taxa are In retrospect, section Oligotheca became a blend of several included if we consider them as problematic. Our primary goal evolutionary lineages including Beccariella (Seed type 1), is to circumscribe recognisable species, which has been Planchonella (Seed type 1), Sersalisia (Seed type 2) and Van- proven difficult in this genus (Swenson et al. 2013, 2014). The royena (Seed type 2), four genera resurrected by Swenson et al. phylogenetic results were useful for circumscribing the (2007a). Another misconception of lineages was formed when species. Seventeen species are accepted for New Caledonia, Pennington (1991) described Pouteria section
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