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The Wood Anatomy of the Polyphyletic Icacinaceae S.L., and Their Relationships Within Asterids

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The Wood Anatomy of the Polyphyletic Icacinaceae S.L., and Their Relationships Within Asterids TAXON 57 (2) • May 2008: 525–552 Lens & al. • Wood anatomy of Icacinaceae MORPHOLOGY The wood anatomy of the polyphyletic Icacinaceae s.l., and their relationships within asterids Frederic Lens1,2*, Jesper Kårehed3, Pieter Baas2, Steven Jansen4, David Rabaey1, Suzy Huysmans1, Thomas Hamann2 & Erik Smets1,2 1 Laboratory of Plant Systematics, Institute of Botany and Microbiology, Kasteelpark Arenberg 31, K.U. Leuven, 3001 Leuven, Belgium. *[email protected] (author for correspondence) 2 National Herbarium of the Netherlands—Leiden University Branch, P.O. Box 9514, 2300 RA Leiden, The Netherlands 3 The Bergius Foundation at the Royal Swedish Academy of Sciences and Department of Botany, Stockholm University, 106 91 Stockholm, Sweden 4 Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond, Surrey TW9 3DS, U.K. Wood samples from 53 species belonging to 41 genera of the Icacinaceae s.l. are investigated using light and scanning electron microscopy. The traditionally circumscribed Icacinaceae fall apart into four segregate fami- lies that are clearly nested within asterids, i.e., Icacinaceae s.str. (near or in Garryales), Cardiopteridaceae and Stemonuraceae (both Aquifoliales), and Pennantiaceae (Apiales). From a wood anatomical point of view, these families cannot easily be distinguished from each other. However, some features such as vessel distribution, perforation plate morphology, size and arrangement of vessel pits, fibre wall thickness, and the occurrence of cambial variants can be used to assign various species to one of the four families. The wood structure of the four segregate families is in general agreement with their suggested putative relatives, but the occurrence of lianas versus erect trees and shrubs is a confusing factor in getting clear phylogenetic signal from the wood structure. Maximum parsimony and Bayesian analyses using molecular data and combined anatomical-molecular data show that Icacinaceae s.str. are not monophyletic, and their closest relatives remain unclear. The combined analyses provide moderate support for a clade including Cassinopsis, the Apodytes-group, the Emmotum-group (all Icacinaceae s.str.), and the genus Oncotheca. This clade is situated at the base of lamiids and may be closely related to Garryales. The remaining lineage of Icacinaceae s.str., the Icacina-group represented by many climb- ing taxa exhibiting cambial variants, is strongly supported and might be sister to the rest of lamiids. KEYWORDS: cambial variants, comparative wood anatomy, Garryales, Icacinaceae, LM, Oncotheca, SEM Icacinaceae s.l. a poorly understood family of flowering INTRODUCTION plants (Howard, 1942; Sleumer, 1942a, b, 1972). Conse- The traditionally circumscribed family Icacinaceae s.l. quently, the taxonomic history shows much controversy includes about 55 genera and 400 species (Kårehed, 2001). (Table 1), and the family has been linked to various groups, Representatives are small shrubs to tall trees or lianas that including Olacaceae (De Candolle, 1824; Bentham, 1862) typically grow in humid lowland forests throughout the trop- and the families Celastraceae and Aquifoliaceae (Miers, ics. A small number of species prefer subtropical forests and 1852; Engler, 1893). Subsequent authors followed the savannas to more temperate areas of Africa, Asia, Australia Celastrales connection (Rosidae, Cronquist 1981; Car- and South America, while others sporadically occur in salt diopteris excluded), while Takhtajan (1997) recognised marshes or in high-altitude regions between 2,000–3,000 Icacinales as an order of its own in the Rosidae, includ- m (Guymer, 1984; Howard, 1942; Sleumer, 1972; Villiers, ing Aquifoliaceae, Icacinaceae (excluding Cardiopteris 1973; de Roon & Mori, 2003; de Stefano, 2004). Malesia and Metteniusa), Phellinaceae and Sphenostemonaceae. is the main centre of diversity comprising about half of the Progress in molecular systematics has revealed that the genera, followed by (sub)tropical America (20%–25% of Aquifoliaceae link is correct, but only for certain gen- the genera) and Africa (15%). Many genera are endemic to era within Icacinaceae s.l. (Kårehed, 2001). A combined major phytogeographical areas, with the pantropical genus data set of ndhF, rbcL, atpB and 18S rDNA together with Citronella being one of the few exceptions. morphology showed that the traditional Icacinaceae are Frequent mistakes in species determination, complex polyphyletic, and must be divided into four different fami- nomenclatural issues and undersampled collections make lies within asterids sensu APG II (2003): Icacinaceae s.str. 525 Lens & al. • Wood anatomy of Icacinaceae TAXON 57 (2) • May 2008: 525–552 Table 1. Taxonomic overview of the genera studied according to their family classification sensu Miers (1852), Engler (1893), Bailey & Howard (1941a), Sleumer (1942ab) and Kårehed (2001). Bailey & Sleumer Genus Miers (1852) Engler (1893) Howard (1941b) (1942a, b) Kårehed (2001) Apodytes Icacineae Icacineae Icacineae (I) Icacineae Icacinaceae s.str. (APO) Calatola – – Icacineae (I) Icacineae Icacinaceae s.str. (EMM?) Cantleya – – Icacineae (II) Icacineae Stemonuraceae +Cardioppteris+ – Cardiopterygoideae – Peripterygiaceae* Cardiopteridaceae Cassinopsis – Icacineae Icacineae (I) Icacineae Icacinaceae s.str. (CAS) +Chlamyydocaryya+ – Phytocreneae Phytocreneae (III) Phytocreneae Icacinaceae s.str. (ICA) Citronella – Icacineae Icacineae (I) Icacineae Cardiopteridaceae Codiocarpus – – – – Stemonuraceae Dendrobangia – – Icacineae (I) Icacineae Cardiopteridaceae Desmostachys Icacineae Icacineae Icacineae (III) Icacineae Icacinaceae s.str. (ICA) Discophora Sarcostigmateae – Icacineae (II) Icacineae Stemonuraceae Emmotum Emmoteae Icacineae Icacineae (I) Icacineae Icacinaceae s.str. (EMM) Gastrolepis – – Icacineae (II) Icacineae Stemonuraceae Gomphandra – – – Icacineae Stemonuraceae Gonocaryum Sarcostigmateae Icacineae Icacineae (II) Icacineae Cardiopteridaceae Hartleya – – – – Stemonuraceae +Icacina+ Icacineae Icacineae Icacineae (III) Icacineae Icacinaceae s.str. (ICA) +Iodes+ – Iodeae Iodeae (III) Iodeae Icacinaceae s.str. (ICA) Lasianthera – Icacineae Icacineae (II) Icacineae Stemonuraceae +Laviggeria+ – Icacineae Icacineae (III) Icacineae Icacinaceae s.str. (ICA) Leptaulus – Icacineae Icacineae (II) Icacineae Cardiopteridaceae +Mappppia+ Icacineae Icacineae Icacineae (III) Icacineae Icacinaceae s.str. (ICA) +Mappppianthus+ – Iodeae Iodeae (III) Iodeae Icacinaceae s.str. (ICA) Medusanthera – – Icacineae (II) Icacineae Stemonuraceae Merrilliodendron – – Icacineae (III) Icacineae Icacinaceae s.str. (ICA) Metteniusa – – – Icacineae Cardiopteridaceae? Oecopetalum – – Icacineae (I) Icacineae Icacinaceae s.str. (EMM) Ottoschulzia – – Icacineae (I) Icacineae Icacinaceae s.str. (EMM) Pennantia Sarcostigmateae Icacineae Icacineae (I) Icacineae Pennantiaceae +Phyytocrene+ – Phytocreneae Phytocreneae (III) Phytocreneae Icacinaceae s.str. (ICA) Platea – Icacineae Icacineae (I) Icacineae Icacinaceae s.str. (EMM?) +Polypyporandra+ – Iodeae Iodeae (III) Iodeae Icacinaceae s.str. (ICA) Poraqueiba Icacineae Icacineae Icacineae (I) Icacineae Icacinaceae s.str. (EMM?) Pseudobotrys – – – Icacineae Cardiopteridaceae? +Pyyrenacantha+ – Phytocreneae Phytocreneae (III) Phytocreneae Icacinaceae s.str. (ICA) +Rhapphiostyylis+ Icacineae Icacineae Icacineae (III) Icacineae Icacinaceae s.str. (APO) Rhyticaryum – Icacineae Icacineae (III) Icacineae Icacinaceae s.str. (ICA) +Sarcostiggma+ Sarcostigmateae Sarcostigmateae Sarcostigmateae (III) Sarcostigmateae Icacinaceae s.str. (ICA) Stemonurus Sarcostigmateae Icacineae Icacineae (II) Icacineae Stemonuraceae Whitmorea – – – – Stemonuraceae I, II and III refer to the groups of Bailey & Howard (1941b); APO, Apodytes group; CAS, Cassinopsis; EMM, Emmotum group; ICA = Icacina group. Names of climbing genera are marked with “+”. * Peripterygiaceae = Cardiopteridaceae. 526 TAXON 57 (2) • May 2008: 525–552 Lens & al. • Wood anatomy of Icacinaceae (near or in Garryales, lamiids [euasterids I]), Cardiopteri- terpreted with caution because of the large number of daceae and Stemonuraceae (both in Aquifoliales, cam- juvenile wood samples included. It is generally known panulids [euasterids II]), and Pennantiaceae (in Apiales, that the wood structure of juvenile twigs differs in many campanulids) (Kårehed, 2001). However, it is possible that aspects from the wood of mature branches or trunks of the present delimitation of Icacinaceae s.str., including the the same plant. Not only quantitative characters, such as Apodytes group, the Emmotum group, the Icacina group vessel diameter, vessel density, and ray width depend on and the genus Cassinopsis, does not constitute a mono- this, also qualitative characters such as the initiation of phyletic entity (Table 1). Also the position of Metteniusa specific cambial variants (amongst others successive cam- and Pseudobotrys within Cardiopteridaceae remains open bia and interxylary phloem) only develop when a stem for discussion (Kårehed, 2001). reaches a certain age (Obaton, 1960; Metcalfe & Chalk, Anatomical characters of the stem have been consid- 1983; Ursem & ter Welle, 1989; Carlquist, 2001). Next ered to represent key features for the intrafamily classifi- to the anatomical studies of Bailey & Howard, several cation. In order to define the four tribes of the subfamily other papers described the wood structure of a restricted Icacinoideae (i.e., Icacineae, Iodeae, Sarcostigmateae number of Icacinaceae s.str. (Chalk & al., 1935; Metcalfe and Phytocreneae), Engler
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