SYSTEMATICS OF ELATOSTEMA (URTICACEAE)
Julisasi Tri Hadiah
A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy
University of New South Wales
July 2007
Acknowledgements
I would like to express my gratitude to my supervisors, A/Prof Paul Adam (University of New South Wales), Dr Barry Conn (NSW), and Dr Chris Quinn (NSW) for providing guidance and expert advice throughout my thesis, with a special thanks to Chris who continued supporting me even after his retirement.
I would especially like to thank Drs Dedy Darnaedi, (former Director Kebun Raya Indonesia) and Irawati (current Director) for giving me permission to study overseas and for their continuing support throughout this project. Likewise, I wish to thank Drs Tim Entwisle (Director Royal Botanic Gardens Sydney) and Brett Summerell (Director Plant Sciences and Public Programs, NSW) for generously allowing me full access to the facilities of their organisation.
I would also like to thank the staff of the Royal Botanic Gardens, Sydney and, particularly, those of the National Herbarium of New South Wales, who have provided assistance to ensure that my research on the systematics of Elatostema was successful. It has always been an enjoyable and excellent organisation in which to work. I have met many friendly people. Especially, I wish to thank Hannah McPherson, Lucy Nairn, Gillian Towler, Andrew Perkins and Nick Yee for their warm friendship, their help when moving to new homes, taking me to hospital when sick, for great weekends together, for having fun collecting orchids and learning about freshwater ecology, up to my knees in the freezing water of the Kangaroo River. They have always cheered me up when I needed it most and have helped me to feel at home in Australia.
I would like to give special thanks to Andrew Perkins and Margaret Heslewood for their introduction to molecular techniques and assistance in the laboratory. Margaret also provided additional sequences used in this project. Caroline Porter and Adam Marchant generously provided additional support in the molecular laboratory at NSW. Kathi Downs kindly inducted me into the processes and procedures of NSW. Louisa Murray assisted with the management of the loan herbarium material. Zonda Erskine kindly ensured the prompt processing of all loan material upon its arrival at NSW. I
v thank Miquel Garcia for helping me to understand the cataloguing system use in the library at NSW and for promptly obtaining important references that I was unable to locate. Thanks to Peter Hind for introducing me to the flora of the Sydney region and for making me feel welcome in Sydney. Lesley Elkan and Catherine Wardrop provided the excellent botanical illustrations and diagrams used in this thesis. Gary Chapple expertly re-formatted the various data matrices exported from PAUP* software into a more suitable format for inclusion in the Appendices.
And, to Andrew, thanks for the frequent cups of coffee; to Elizabeth and Chris, a special thanks for allowing me to take-over their computers for hours, days, in fact, for weeks at a time.
Esti Ariyanti (Kebun Raya Purwodadi), Barry Conn (NSW), Tjetjep Rayadi (Kebun Raya Bogor), Adjun, Rustandi, Nanang Suryana, (latter three Kebun Raya Cibodas) and Frank Zich (then Kebun Raya Eka Karya, Bali) provided field assistance and companionship on my various field work in Indonesia. Elizabeth Brown, Barry Conn, Andrew Perkins and David Orr and Bruce Casler (both Waimea Valley Audubon Center, Hawaii, USA) kindly provided additional collections for DNA analysis. Ruspandi (Kebun Raya Bogor) assisted with initial identification of field collections. I also thank the Cibodas staff for maintaining a living collection of wild-sourced material of Elatostema for this project and for future study. Dick Brummit, Petra Hoffman (both K), James Reveal (University of Maryland, USA), Nicholas Turland (MO), Peter Wilson (NSW) kindly provided informative comments on the nomenclature of the tribal names of the Urticaceae.
I am very grateful for the four-year funded AusAID scholarship, from 1999 until 2003. I wish to thank the staff of the Australian Development Scholarship (ADS) agency for making this possible.
I thank the Directors and staff of the following herbaria for access to their collections and/or for providing loan specimens: BO, BRI, CANB, GH, K, KRB, L, LAE, MEL, NSW and NY.
vi I am very indebted to Helen and Barry Conn for their continuous support throughout my time in Australia. They welcomed me into their home, provided mental and material support, and assisted me academically and personally during my study and especially during the writing phase of my thesis. They keep encouraging me to remain positive when it all seemed to be too hard and they helped me stay cheerful when I was feeling overwhelmed by what had to be completed. Sometimes I thought that I would not be able to put a smile on my face any more, but they always found a way to make me laugh through the hardest times. They introduced me to ‘NCIS’, ‘Life on Mars’, ‘House’, ‘Medium’, the new ‘Robin Hood’ and Rugby League. I shall never be able to repay them for everything they have done for me.
Finally, I would like to thank my beloved family, especially my husband Tansen, for their endless love and support, and for always believing in me.
vii viii ABSTRACT
Elatostema J.R.Forst. & G.Forst. (Urticaceae) is a taxonomically problematic genus of approximately 300 species that is widespread throughout the tropical, subtropical and sub-temperate regions of Africa through to SE Asia, Australasia to Polynesia. Morphological and molecular analyses were conducted to evaluate the infra-familial classification of the Urticaceae, to test the monophyly of Tribe Elatostemeae, to define generic limits of Elatostema and assess its relationship within the tribe, and to examine the current infrageneric grouping within Elatostema.
Phylogenetic analyses based on choloroplast DNA sequences of rbcL and trnL-F do not provide support for the monophyly of Urticaceae, because of the position of Poikilospermum (currently Cecropiaceae) within the tribe Urticeae. Although the status of Cecropiaceae is equivocal, there is support for the inclusion of this family in the Urticaceae, with Cecropia and Coussapoa (Cecropiaceae) having close affinities to the Boehmerieae and Parietarieae. The phylogenetic position of Myriocarpa is unresolved, but is excluded from the Boehmerieae, as currently classified. The Elatostemeae is paraphyletic with Pilea placed sister to the Urticeae.
Evaluation of the infrageneric classification of Elatostema, based on phylogenetic analyses of both morphological and molecular data (trn and ITS) does not support the current subgeneric classification as proposed by Schröter and Winkler (1935, 1936). The analyses support two main infrageneric grouping: (1) a group consisting of Elatostema subg. Pellionia and Procris, and (2) a group consisting of the remaining members of Elatostema (including E. griffithianum – subg. Pellionia).
The molecular data are regarded as a more accurate estimate of the phylogeny than provided by morphology, with molecular data having a higher Rescaled Consistency Index on the most parsimonious trees, together with a much greater level of resolution and support than that of the morphological analyses.
ix x Table of Contents
TABLE OF CONTENTS
Title Page ...... i Originality Statement ...... iii Acknowledgements ...... v Abstract ...... ix Table of Contents ...... xi List of Figures ...... xix List of Tables...... xxiii
Chapter 1 Introduction ...... 1 1.1 The family Urticaceae...... 1 1.2 Rationale for project ...... 2 1.3 Objectives of project ...... 4
Chapter 2 Taxonomic history ...... 5 2.1. Taxonomic history of Urticaceae A.L.Juss. noms. cons...... 5 2.1.1. Early taxonomic history of family...... 5 2.1.2. Circumscription of tribes of Urticaceae...... 7 2.1.3. Modern taxonomic history of Urticaceae ...... 8 2.2. Phylogeny of Urticaceae ...... 9 2.3. Nomenclature of tribe Elatostemeae/Lecantheae/Procrideae...... 10 2.3.1. Justification for recognition of tribal names proposed by Gaudichaud ...... 11 2.4. Taxonomic history of Elatostema and related genera...... 13 2.5. Conclusion ...... 20
Chapter 3 Plant materials ...... 21 3.1 Introduction...... 21 3.2 Plant materials for morphological observation ...... 23 3.3 Plant materials for molecular study ...... 32
Chapter 4 Molecular data ...... 37 4.1 Introduction...... 37 4.1.1 Chloroplast data...... 38 4.1.2 Nuclear data...... 40 4.2 Material and methods...... 42
xi Table of Contents
4.2.1 Choice of regions...... 42 4.2.2 Outgroup choice ...... 43 4.2.3 Nested sampling ...... 44 4.2.4 DNA extraction and purification of DNA products...... 45 4.2.5 Gene amplification and purification of PCR products...... 45 4.2.6 DNA sequencing...... 46 4.3 Sequence alignment and insertions/deletions ...... 48
Chapter 5 Data analyses...... 51 5.1 Introduction...... 51 5.2 Analyses of data...... 53
Chapter 6 Preliminary molecular studies...... 59 6.1 Introduction...... 59 6.2 The rbcL database...... 59 6.3 The atpß-rbcL database ...... 60 6.4 The trn database ...... 63 6.5 Discussion...... 64 6.6 Conclusion ...... 69
Chapter 7 Infra-familial phylogeny of Urticaceae using molecular data ...... 71 7.1 Introduction...... 71 7.2 The rbcL database...... 71 7.3 The trn database...... 76 7.4 Discussion...... 78 7.4.1 Status of tribes of Urticaceae...... 78 7.4.2 Status of Cecropiaceae sensu Berg (1978) ...... 78 7.5 Conclusion ...... 80
Chapter 8 Phylogeny of Elatostema using molecular data ...... 83 8.1 Introduction...... 83 8.2 The trn database ...... 83 8.3 The ITS database...... 84 8.4 Discussion...... 92 8.5 Conclusion ...... 97
xii Table of Contents
Chapter 9 Morphological data...... 99 9.1 Introduction...... 99 9.2 Morphological characters used by Robinson (1910) ...... 99 9.2.1 Inflorescence involucre – presence or absence...... 100 9.2.2 Pistillate flowers ...... 100 9.2.2.1 Perianth...... 100 9.2.2.2 Staminodes presence or absence (in pistillate flowers) ...... 102 9.2.2.3 Appendage of perianth (in pistillate flowers) ...... 102 9.3 Morphological characters used by Schröter and Winkler (1935) ...... 103 HABIT AND FORM ...... 103 9.3.1 Herbs, sub-shrubs and shrubs ...... 103 LEAF ...... 104 9.3.2 Phyllotaxy ...... 104 9.3.3 Anisophylly ...... 104 9.3.4 Leaf shape symmetry ...... 105 9.3.5 Leaf base symmetry ...... 105 9.3.6 Leaf venation ...... 105 9.3.7 Cystoliths ...... 106 9.3.8 Stipules ...... 107 INFLORESCENCE ...... 109 9.3.9 Form ...... 109 9.4 Data management ...... 112 9.5 Choice and definition of characters ...... 112 GENERAL HABIT AND FORM...... 113 9.5.1 Habit ...... 113 9.5.2 Form ...... 114 9.5.3 Epiphyte/hemi-epiphyte ...... 114 9.5.4 Sexuality ...... 115 VEGETATIVE CHARACTERS...... 115 INDUMENTUM...... 115 9.5.5 Branched hairs ...... 115 9.5.6 Stinging hairs ...... 115 LEAF CHARACTERS...... 116 9.5.7 Stipules ...... 116 9.5.8 Stipule attachment ...... 116 9.5.9 Stipule position ...... 116
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9.5.10 Leaf arrangement ...... 117 9.5.11 Leaf petiole ...... 117 9.5.12 Leaf base ...... 118 9.5.13 Leaf lobbing ...... 119 9.5.14 Leaf margin ...... 119 9.5.15 Leaf margin indumentum ...... 119 9.5.16 Leaf apex ...... 119 9.5.17 Leaf texture/configuration ...... 120 9.5.18 Venation arrangement ...... 120 9.5.19 Venation symmetry ...... 120 9.5.20 Veins – basal secondary pair origin ...... 121 9.5.21 Veins – basal secondary pair distance ...... 121 9.5.22 Veins – secondary arrangement ...... 121 9.5.23 Leaf cystolith shape ...... 121 9.5.24 Leaf abaxial cystoliths venation ...... 121 9.5.25 Leaf abaxial cystoliths interstices ...... 122 9.5.26 Leaf adaxial cystoliths venation ...... 122 9.5.27 Leaf adaxial cystoliths interstices ...... 122 9.5.28 Leaf abaxial indumentum venation ...... 122 9.5.29 Leaf abaxial indumentum interstices ...... 122 9.5.30 Leaf adaxial indumentum venation ...... 122 9.5.31 Leaf adaxial indumentum interstices ...... 122 9.5.32 Nanophylls (small leaves) [presence or absence] ...... 122 REPRODUCTIVE CHARACTERS...... 123 9.5.33 Flower sexuality ...... 123 9.5.34 Male inflorescence ...... 123 9.5.35 Male inflorescence density ...... 123 9.5.36 Male inflorescence branch ...... 123 9.5.37 Male inflorescence type ...... 124 9.5.38 Male inflorescence involucral bracts ...... 124 9.5.39 Appendages ...... 124 9.5.40 Male inflorescence bract margin ...... 124 9.5.41 Male inflorescence order ...... 124 9.5.42 Male flower symmetry ...... 125 9.5.43 Male flower tepal number ...... 126 9.5.44 Male flower tepal fusion ...... 126 9.5.45 Male flower tepal appendage ...... 126
xiv Table of Contents
9.5.46 Male flower tepal indumentum ...... 126 9.5.47 Male flower stamen number ...... 126 9.5.48 Male flower staminal inflection in bud ...... 127 9.5.49 Male flower with rudimentary ovary ...... 127 9.5.50 Female inflorescence ...... 127 9.5.51 Female inflorescence branching ...... 127 9.5.52 Female inflorescence arrangement ...... 127 9.5.53 Female inflorescence type ...... 127 9.5.54 Female inflorescence involucral bracts ...... 128 9.5.55 Female inflorescence bracts appendage ...... 128 9.5.56 Female flower bract margin ...... 128 9.5.57 Female flower symmetry ...... 128 9.5.58 Female flower tepal number ...... 128 9.5.59 Female flower tepal comparative size ...... 128 9.5.60 Female flower tepal fusion ...... 129 9.5.61 Female flower staminode presence ...... 129 9.5.62 Female flower ovary ...... 129 9.5.63 Female flower style ...... 129 9.5.64 Female flowerstigma ...... 129 FRUIT...... 129 9.5.65 Achene covered by perianth or involucre ...... 129 9.5.66 Achene surface ...... 130 Non-overlapping (qualitative) characters converted from overlapping (quantitative) characters...... 130 9.5.67 Plant height (non-overlap) ...... 132 9.5.68 Leaf petiole length (non-overlap) ...... 134 9.5.69 Leaf lamina length (non-overlap): length of lamina, from base to apex ... 135 9.5.70 Leaf lamina width (non-overlap): width at broadest part of lamina ...... 136 9.5.71 Leaf lamina length:width ratio (non-overlap) ...... 137 9.5.72 Leaf lamina symmetry:width comparison on each side of midvein or central axis of macrophylls (normal leaf) ...... 138 9.5.73 Veins number (pairs; non-overlap) ...... 139 9.5.74 Male flower tepal length (non-overlap) ...... 140
Chapter 10 Phylogeny of Elatostema using morphological data ...... 141 10.1 Introduction...... 141 10.2 Results...... 141
xv Table of Contents
10.3 Discussion...... 151 10.3.1 Overview...... 151 10.3.2 Evaluation of infrageneric groupings...... 151 10.3.2.1 Subgeneric classification of Schröter and Winkler ...... 151 10.4 Conclusion ...... 152
Chapter 11 Phylogeny of Elatostema using combined morphological and molecular data...... 157 11.1 Introduction...... 157 11.2 Narrow analysis with no missing data ...... 158 11.3 Broader analysis with missing data ...... 161
Chapter 12 Conclusion ...... 177 12.1 Summary...... 177 12.2 Future work...... 178 12.2.1 Increased infrageneric sampling ...... 178 12.2.2 Phylogenetic position of Pilea ...... 179 12.2.3 Evaluation of morphological characters...... 179 12.2.3.1 Morphological variation...... 179 12.2.3.2 Continued assessment of morphology...... 180 12.2.4 Increased tribal sampling ...... 180
References ...... 183
Appendices:...... 209 1. Protocols for DNA extraction ...... 210 2. Protocols for DNA purification (Gilmour et al. 1993)...... 212 3. Protocols for PCR ...... 214 4. Protocols for PCR products purification using CONCERTTM Rapid PCR Purification System ...... 215 5. rbcL database ...... 216 6. atpß-rbcL database...... 250 7. trn database ...... 259 8. ITS database ...... 329 9. Morphological characters used in the project ...... 357 10. Morphological database ...... 361 11. Combined morphological and molecular database: Narrow analysis ...... 365
xvi Table of Contents
12. Combined morphological and molecular database: Broader analysis ...... 377 13. Species descriptions of Elatostema and Procris, including illustrations and photographs...... 421 14. Reprint of Telopea 10(1): 235–246 ...... 461
xvii List of Figures
LIST OF FIGURES
Figure 1.1 Generalised distribution map of the Urticaceae ...... 1
Figure 1.2 Generalised distribution map of Elatostema ...... 4
Figure 4.1 A schematic diagram of the rbcL gene of cpDNA showing the
approximate position and direction of primers used in this study...... 39
Figure 4.2 A schematic diagram of the atpß and rbcL genes with the intergenic
spacer in between...... 39
Figure 4.3 A schematic diagram of the non-coding trnL-F region of the cpDNA. .40
Figure 4.4 A schematic diagram of a nuclear 18-26S ribosomal DNA repeat,
showing the position of the Internal Transcribed Spacers (ITS)...... 42
Figure 6.1 Strict consensus of two equally parsimonious trees of 374 steps
found from heuristic search of the rbcL data...... 62
Figure 6.2 Strict consensus of the 10 equally parsimonious trees of 191 steps
found from 100 replicates of heuristic search of the atpß-rbcL spacer
data set ...... 63
Figure 6.3 Strict consensus of two equally parsimonious trees of 663 steps
found from 100 replicates of heuristic search of the trn data set with
random taxon addition...... 66
Figure 7.1 Strict consensus of four equally parsimonious trees of 469 steps
found from heuristic search of the rbcL data...... 74
Figure 7.2 Majority rule tree generated from heuristic search of the rbcL data...... 75
Figure 7.3 Strict consensus tree of the trn data generated from heuristic search ....77
Figure 8.1 Strict consensus tree of the trn data generated from heuristic search ....86
Figure 8.2 Majority rule tree generated from heuristic search of the trn data ...... 87
xix List of Tables
LIST OF TABLES
Table 2.1 Summary of morphological characters used by Schröter and Winkler (1936, pp. 1 and 2) to distinguish subgenera of genus Elatostema ...... 18 Table 2.2 Summary of morphological characters used by Wang (in Wang and Chen 1979; Wang 1980a) to distinguish sections within the genus Elatostema ...... 19 Table 3.1 List of voucher specimens used in this study ...... 24 Table 3.2 List of voucher specimens used for DNA extracts and GenBank numbers for sequences...... 33 Table 4.1 List of primers used in this project for PCR (P, 20 μM) and sequencing (S, 0.8 μM) ...... 47 Table 9.1 Summary of taxonomically useful inflorescence characters based on usage by Schröter and Winkler ...... 111
xxiii List of Tables
xxiv Chapter 1. INTRODUCTION 1.1. The family Urticaceae Urticaceae is a medium-sized family consisting of about 45 genera and 1,000 species (Friis 1993). The family is widely distributed throughout the world, from the tropics to temperate regions with the centre of generic diversity being in tropical Asia (Friis 1993) (Figure 1.1). This family includes stinging trees (Dendrocnide), stinging shrubs (Laportea) and stinging nettles (Urtica). However, contrary to popular belief, the majority of species in other genera are not stinging (a few examples include: Boehmeria, Elatostema, Oreocnide, Parietaria, Pilea and Procris). Several species are used as sources of food, for example, Urtica (Pieroni 2001) and Pilea (P. microphylla (L.) Liebm. in Cuba, refer Wezel and Bender 2003). Pilea melastomoides Wedd. is a common aromatic vegetable eaten in West Java (pers. obs).
Fibres from species of Boehmeria, Debregeasia, Urtica and Girardinia have been used for textiles and string. The main fibre in economic use is extracted from Boehmeria nivea Gaudich. (Baillon 1874; Carter 1910; Friis 1993; Heywood 1993), which is widely cultivated in SE Asia, China, Bangladesh, India, Pakistan, Mexico and other tropical countries (Carter 1910). This species is also grown as a source of nutritious green feed for animals (cattle, pigs and poultry) (FAO 2006).
Figure 1.1. Generalised distribution map of the Urticaceae (coloured dark blue).
1 Chapter 1. Introduction
Several species are cultivated as ornamentals, particularly in SE Asia (Boehmeria, Elatostema, Pilea and Soleirolia; Gilman 1999a, 1999b) often for their variegated foliage (Friis 1993).
Many urticaceous species are used in traditional medicine because of the various important chemical constituents. For example, Urtica dioica L. is traditionally used for the treatment of cancer in Turkey (Akbay et al. 2003) and for treatment of hypertensive cardiovascular problems in oriental Morocco, of which the direct cardiovascular action was evaluated by Tesai et al. (2002). The reported properties and traditional uses of Urtica pilulifera L. in Palestine include: aphrodisiac; diuretic; with fresh young leaves eaten to treat kidney stones and infections; rheumatism; and treatment of female sterility and bleeding (Abu- Rabia 2005). In Polynesia, an extract from the leaves of Laportea interrupta (L.) Chew is used to ameliorate the pain from stonefish spine poisoning (McClathey 2002). Anti- inflammatory and analgesic dose-related activities have been observed for Urera baccifera (L.) Gaudich. (Badilla et al. 1999); antioxidant activity has been discovered in selected traditionally used Iranian medicinal plant species including Urtica dioica (Pourmorad et al. 2006). Laportea aestuans (L.) Chew is recorded as an ethnoveterinary species that is used for urinary problems of ruminants in Trinidad and Tobago (Lans 2001). Species of Elatostema and Procris are used as a shampoo in Java and Bali (Indonesia) (pers. obs.). Several urticaceous species are also used in traditional Chinese medicine (Chen et al. 2003), for example, Boehmeria cylindrica (L.) Sw. extract is used to promote hair growth (NuLivScience 2006); Elatostema repens (Lour.) Hallier f. & H.Schroet. and Pilea plataniflora C.H.Wright have liver protection properties (Jiangsu New Medical College, without date); Urtica dioica seed and Parietaria judaica L. herb are used to relieve chronic renal failure (Yarnell and Abascal 2007).
1.2. Rationale for Project Since the family Urticaceae is one of the prioritised taxa for the current Flora Malesiana project, there is an urgent requirement to document the taxa of this family for the region. This research project is a part of an international multidisciplinary research project studying the systematics of the Urticaceae for the botanical region known as Malesia. This region includes the countries of the Philippines, Malaysia, Indonesia, Brunei Darussalam, and Papua New Guinea. One of the genera identified as requiring urgent taxonomic
2 Chapter 1. Introduction investigation is Elatostema, even though the taxonomy of many other Urticaceae genera are also inadequately known.
Elatostema is a very large genus that is considered to consist of approximately 300 herbaceous and sub-shrubby species (Friis 1993) that are characterised by having female flowers arranged on a flattened discoid or lobed receptacle. However, the International Plant Names Index (IPNI 2004+) lists 755 names for the genus, including 23 sectional and serial names (sensu Wang 1980a), as well as 58 varieties. The taxonomic status of many of these names is uncertain, largely because many of the significant herbarium collections, such as type material, were destroyed by allied bombing during the Second World War and the various early taxonomic concepts were based on few collections. Therefore, the systematics of the genus is very confusing, such that it is not possible to identify many species with confidence. Furthermore, the inadequacy of the many of the species concepts applied to this genus means that the systematics of Elatostema is very poorly known. Since the circumscription of many species is problematic, little is known about the distribution, and hence, biogeography of this genus.
Since it was first described by Forster and Forster (1776), the taxonomic circumscription of the genus and infrageneric taxa has been problematic. Furthermore, the taxonomic distinctness of the related taxa, Elatostematoides, Pellionia and Procris has continued to be problematic. There are 17 published names of Elatostematoides, 163 of Pellionia (including three sections and six series sensu Wang 1980b) and 131 of Procris (IPNI 2004+). The status of many of the names, hence taxon concepts, in all of these taxa, including Elatostema, requires thorough re-assessment.
The first and most complete account of the taxonomy of Elatostema was provided by Schröter and Winkler (1935, 1936). They included species of the genus that were classified in the subgenera Elatostematoides, Pellionia and Weddellia. Unfortunately, they did not publish a taxonomic account of subgenus Elatostema. The lack of an account of the latter subgenus, together with the loss of much of the authenticated herbarium material that they examined, has made it difficult to evaluate the taxonomic concepts applied by them and other researchers. Furthermore, there has been no further general treatment on this genus, only some works of local or restricted geographic coverage, for example, Elatostema in
3 Chapter 1. Introduction
China (Wang 1980a), Elatostema of Taiwan (Yang et al. 1995), and Elatostema of Mt. Kinabalu (Beaman 2000).
Elatostema is widely distributed throughout the tropical, subtropical and sub-temperate regions from the west to east coast of Africa, Madagascar and Mascarene Islands, through Sri Lanka, southern India, tropical Himalaya, Bangladesh, Myanmar to South-East Asia, Micronesia, then throughout Papuasia, to eastern Australia, New Caledonia, northern New Zealand, and Polynesia. It also occurs in subtropical and sub-temperate regions of China, Taiwan and Japan (Figure 1.2).
Figure 1.2. Generalised distribution map of Elatostema (coloured dark blue)
1.3. Objectives of project Within an overall Malesian framework, the objectives of this research project are: 1. To evaluate the infra-familial classification of the Urticaceae; 2. To test the monophyly of Tribe Elatostemeae, in which the genus Elatostema belongs; 3. To define the generic limits of Elatostema and assess its relationship within the tribe; 4. To examine the current infra-generic grouping within Elatostema.
4 Chapter 2. TAXONOMIC HISTORY
2.1. Taxonomic history of Urticaceae A.L.Juss. nom. cons. 2.1.1. Early Taxonomic History of Family Antoine Laurent de Jussieu was a distinguished botanist who proposed a natural classification of flowering plants, based on multiple characters to define groups, in his publication, Genera plantarum, secundum ordines naturales disposita, juxta methodum in Horto regio parisiensi … (Jussieu 1789). He was professor of botany at the Jardin des Plantes from 1770 until 1826 (Stafleu and Cowan 1979) and his herbarium (P-JU) is held at Muséum National d'Histoire Naturelle, in Paris (France) (Holmgren and Holmgren 1998+). He grouped Elatostema J.R.Forst. and G.Forst., Boehmeria Jacq., Procris Commers., Urtica L., Forsskaolea L. (as ‘Forskalea’1), and Parietaria L., together with Cannabis L., Cecropia L., Artocarpus J.R.Forst. and G.Forst., Morus L., Pteranthus Forsk., Humulus L., and Theligonum L. under the family name Urticaceae (as ‘Ordo III. [group] II. Urticæ’) (Jussieu 1789). According to the ‘International Code of Botanical Nomenclature,’ the family name Urticaceae is attributed to Jussieu (ICBN 2006). He circumscribed this group as having flowers arranged on separate, commonly many-flowered receptacles, or arranged in a capitate involucre of bracts (hence, flowers crowded), or flowers distinct and scattered. Gaudichaud (1830) revised the family (as ‘La famille des urticées’, ibid. p. 491) and classified the genera into five infrafamilial tribes or subfamilies (as ‘tribus ou sous-families’, loc. cit.). He defined the Urticaceae sensu stricto (as ‘Urticées vraies’, loc. cit.) as characterised by rectified ovules, initially attached at both ends, and with reversed and straight embryos. Within his ‘Urticées vraies’ grouping, he classified the genera into the following ‘subdivisions’: Boehmériées, Élatostémées, Forskaliées, Pariétariées, Urérées and Cécropiées (loc. cit.). In this paper, he later referred to these subdivisions using the currently accepted format for tribal names (namely, with the ‘-eae’ suffix) and provided descriptions of each subdivision and each genus within the Boehmerieæ,
1 Many orthographic variants of this genus name (namely, Forsskaolea) and the tribal name Forsskaoleeae occur in the literature, refer Friis and Wilmot-Dear (1988) and Friis (1993). However, both of these publications misspell the tribal name as ‘Forsskaoleae’ with an additional orthographic variant in Friis (1993, p. 628), namely ‘Forsskaolea.’
5 Chapter 2. Taxonomic History
Elatostemeæ, Forsskaoleeae (as ‘Forskalieæ’), Parietarieæ, Urticeae2 (as ‘Urereæ’), and Cecropiaeæ (ibid., pp. 493–506). The Elatostemeae sensu Gaudichaud consists of five genera: Elatostema, Sciophila3 (= Procris; refer Endlicher 1836), Pellionia, Langeveldia4 (listed as = Elatostema acuminata Brongn.) (IPNI 2004+), and Dubrueilia (listed as = Pilea) (IPNI 2004+); Urereæ: Urtica, Urera, Fleurya, Laportea and Girardinia; Boehmerieæ: Boehmeria, Procris5 and Neraudia; Parietarieæ: Parietaria, Gesnouinia, Freirea, Thaumuria, Pouzolzia, Rousselia and Soleirolia; Forsskaoleeae: Forsskaolea, Droguetia and Australina; and Cecropieæ: Cecropia and Coussapoa. Gaudichaud’s remaining un-named four ‘tribes or subfamilies’ are now regarded as belonging to plant families other than the Urticaceae.
The next major contribution to our understanding of the taxonomy of the Urticaceae was made by Weddell (1854, 1856, 1857, 1869). He followed the then new nomenclatural convention of referring to families using the ‘–aceæ’ suffix, for groupings that had previously been referred to as tribes (with the ‘-eæ’ suffix), following Endlicher (1833, 1837) who was the first author to apply the name ‘Urticaceae’ to the family. However, although he used the ‘-aceae’ suffix and was referring to what we would now regard as the family Urticaceae, he included it under his Order 94 (as ‘Ordo XCIV’). As mentioned above, in accordance with the first grouping of urticaceous genera, the concept of the name ‘Urticaceae’ is based on Jussieu’s (1789) concept, as a conserved name, with Urtica L. as the type (Greuter et al. 2000). Weddell (1854) recognised five tribes, namely, Boehmerieæ, Forsskaoleeae (as ‘Forskahleæ’), Elatostemeae (as ‘Lecantheæ’), Parietarieæ and Urticeae (as ‘Urereæ’). He excluded Cecropieæ from this family, without indicating the taxonomic status of this group. Much later, Berg (1978) raised the taxonomic status of this group to that of family, namely, Cecropiaceae.
2 Urereae corrected to Urticeae according to article 19.4 of the International Code of Botanical Nomenclature (ICBN 2006) because the genus Urtica was first published by Linnaeus (1753, 1754), whereas Urera was published later by Gaudichaud (1830), giving the tribal name Urticeae priority over Urereae (refer Friis 1989). 3 Sciophila is a later homonym of Sciophila Wibel (Liliaceae). 4 Gaudichaud (1830, pp. 494 and 495) described the new monotypic genus Langeveldia based on Procris acuminata Poiret, which had already been transferred to Elatostema acuminatum by other authors. However, the currently accepted authority for this latter species name is A.T. Brongniart. Therefore, the nomenclatural and taxonomic status of the combination from P. acuminata Poiret to Elatostema is unclear. 5 Although Gaudichaud (1830, p. 499) recognised Procris as a taxonomic entity, he did not formally recognise it at generic rank, but rather, he included it as a subdivision of Boehmeria.
6 Chapter 2. Taxonomic History
Baillon (1874) was the first to circumscribe the family Urticaceae in the narrower sense that is currently applied. He characterised it as having simple stipulate leaves; usually unisexual flowers arranged in definite cymes, with perianth reduced; male flowers with androecia of equal length (‘isostemonous’) or unequal length (‘meiostemonous’), with a rudimentary pistil; female flowers having a unicarpellary gynoecium; ovule solitary, ascending or suberect, orthotropus or suborthotropus; and fruit indehiscent.
2.1.2. Circumscription of Tribes of Urticaceae Weddell (1854, 1856, 1869) was the first to circumscribe the tribes of the family using the ‘-eae’ suffix for the tribal names, even though Gaudichaud (1830) first recognised these groupings (as ‘subdivisions’). Weddell characterised these tribes as follows (mostly based on Weddell 1854):
Boehmerieae monoecious or dioecious; having sub-opposite leaves, rarely in threes; stinging hairs absent; male flowers 4- or 5-partite; female flowers with perianth tubular and therefore fused, but then very short to indistinct, or free, 2–4- dentate or not toothed; with ovary adnate or coherent with perianth; stigma varying from filiform, spathulate to discoid-subpeltate, rarely capitate-penicillate.
Elatostemeae (initially as ‘Lecantheæ,’ later as ‘Procrideæ’ – refer Section 2.3 for further discussion of the tribal name) monoecious or dioecious; leaves opposite, rarely in fours, or alternate (by abortion of one leaf of the pair); stinging hairs absent; male flowers 4- or 5-partite; female flower with perianth free, usually 3–5- partite, with each perianth parts equal or unequal, rarely almost absent; ovary free; stigma mostly penicillate.
Forsskaoleeae (as ‘Forskahleae’) monoecious or polygamous; leaves sub-opposite; hairs sometimes hardened and spine-like, but are not stinging; flowers reduced often involucral-like; female flower with perianth tubular or often absent; ovary free or adnate to perianth; stigma filiform or sub-capitate.
7 Chapter 2. Taxonomic History
Parietarieae monoecious or polygamous; leaves always alternate and leaf margin entire; stinging hairs absent; inflorescences (at least the female inflorescences) with two to many herbaceous bracts that form an involucre; male flowers 4-partite; female flowers with perianth tubular or free, and 2–4-dentate or 4-partite; ovary free; stigma capitate-penicillate or filiform.
Urticeae (as ‘Urereæ’) monoecious or dioecious; leaves alternate or opposite; stinging hairs present; male flowers 4–5-partite; female flowers with perianth free, rarely tubular, mostly 4-partite or 4-lobed, rarely 2-lobed to 2-partite; ovary free; stigma mostly penicillate.
Baillon (1874) recognised five series within the family which appear to resemble the tribes of Weddell (1869) but at the lower rank of series. However, he renamed Urereae to Urticeae (the currently accepted name for this tribe, refer Friis 1993).
2.1.3. Modern taxonomic history of Urticaceae The taxa circumscribed in the Urticaceae, Moraceae and Cecropiaceae have been commonly regarded as very closely related to each other and have been united into one group by various authors, from Gaudichaud (1830) until Bentham and Hooker (1883). However, Weddell (1854, 1856, 1869), Engler (1894) and all recent taxonomists have recognised these three groups as distinct families. Weddell’s final treatment (Weddell 1869) has remained remarkably unchallenged, being widely followed and supported by later researchers (for example, Berg 1977, 1989; Friis 1989, 1993). Berg (1977, 1989) provides an over-view of the macro-morphological characters that are useful for distinguishing the families with the Order Urticales. Based on these data, he developed several tentative phylogenetic hypotheses for and within the Order. Although his focus was at the ordinal level, Berg provided important clarification of several morphological features (for example, inflorescence structures, perianth, androecium, gynoecium and fruits) that are relevant for understanding relationships within the family Urticaceae. Friis (1989, 1993) provided the most recent detailed comparison of morphological features of the Urticaceae at the familial, infrafamilial, and generic levels. He briefly discussed ordinal relationships based on previous classical taxonomic approaches. His work
8 Chapter 2. Taxonomic History
provided broad support for and acceptance of Weddell’s classification of the family and tribes; however, without explanation, he re-applied the name ‘Lecantheae’ for the tribe Elatostemeae, rather than Procrideae (as proposed by Weddell 1869).
Friis (1989) characterised the family as having flowers with a basal ovary and stamens that are elastically and simultaneously reflexing. He circumscribed the tribes as follows:
Elatostemeae (as ‘Lecantheae’) as having staminodes that eject the mature achenes; opposite leaves that are anisophyllous or one leaf of the pair (the nanophyll) being strongly reduced or absent; stipules intrapetiolar and fused; and with cystoliths uniformly linear.
Urticeae was characterised by the presence of stinging hairs.
However, he questioned the distinctiveness of the other three tribes (namely, Boehmerieae, Parietarieae and Forsskaoleeae), and suggested further work may lead to a taxonomic rearrangement at the tribal level (Friis 1989). Friis (1989, 1993) rejected the subtribal groupings within the Boehmerieæ that were proposed by Weddell (1854, 1856, 1869). He concluded that these subtribes were taxonomically not useful. Friis (1989) maintained the familial distinctness of the Cecropiaceae as proposed by Berg (1978; also refer Kubitzki 1993), with the following genera included in this latter family: Cecropia, Coussapoa, Musanga, Myrianthus, Poikilospermum and Pourouma.
2.2. Phylogeny of Urticaceae Recent phylogenetic studies involving the Urticaceae have concentrated on ordinal relationships. The circumscription of the Urticales has been relatively stable since the mid 1800s when Weddell (1856) included Artocarpeæ, Cannabineæ, Moreæ, Ulmaceæ and Urticaceæ in the order. This classification was used by Dahlgren (1989), Thorne (1992) and Takhtajan (1997). Cronquist (1968, 1981) united Urticaceae with Moraceae, Cannabaceae, Ulmaceae and Barbeyaceae largely based on the single ovule, stipules
9 Chapter 2. Taxonomic History
usually present, nodes tri- or multilacunar, flowers clustered and perianth usually much reduced in size.
The recent reconstructed higher-level phylogenies of Chase et al. (1993), using the DNA sequences of the chloroplast gene rbcL, support the monophyly of the Urticales with Cannabaceae, Moraceae, Ulmaceae and Urticaceae included. However, subsequent analyses including additional loci (Angiosperm Phylogeny Group 1998; Soltis et al. 2000; Savolainen et al. 2000; Stevens 2001+) and non-molecular data (Judd et al. 1999) have shown this group to be nested with the Rosales. All of these modern authors, using morphological and molecular characters, consider Cannabaceae (including Celtidaceae; Stevens 2001+), Cecropiaceae, Moraceae and Ulmaceae to be the closest families to Urticaceae.
Sytsma et al. (2002) provided information on the family concepts and inter- and intrafamilial relationships within the Urticales based on chloroplast DNA sequences, namely, rbcL, trnL-F, and ndhF. Their work supported the monophyly of Moraceae, Urticaceae (including Cecropiaceae), and Cannabaceae (including Celtidaceae; Stevens 2001+); although support for the latter family is not as strong as support for the former two families. In their work, the Ulmaceae was sister to the above Urticalean families. Hadiah et al. (2003) also supported the monophyly of the Urticaceae based on chloroplast DNA. This latter paper is discussed further (refer Chapter 6).
Phylogenetic reconstruction of the Urticaceae using morphological data (Beaman 2000, Fig. 3-3), as part of a study of Elatostema from Mt Kinabalu (Malaysia), provided support for the monophyly of Elatostemeae (as ‘Lecantheae’) and Urticeae, but suggested that the Boehmerieae is polyphyletic.
2.3. Nomenclature of Tribe Elatostemeae/Lecantheae/ Procrideae Weddell (1854, 1856, 1869) consistently circumscribed the tribes within the Urticaceae. He raised the ‘subdivisions’ of Gaudichaud (1830), while maintaining the same names as used by the latter author, to the rank of tribe for the following: Urticeae (as ‘Urereæ’), Boehmerieæ, Parietarieæ and Forsskaoleeae (as ‘Forskahleæ,’ rather than
10 Chapter 2. Taxonomic History
‘Forskalieæ’ as used by Gaudichaud 1830, p. 504). However, it is unclear why he created the tribal name Lecantheæ for the ‘subdivision’ Elatostemeae as first used by Gaudichaud (ibid. p. 493). This change in the tribal name occurred when he published the newly described genus Lecanthus (Weddell 1854). Furthermore, he provided no explanation when he changed the tribal name Lecantheæ to Procrideæ (Weddell 1856). In this latter publication, Weddell added the following three genera: Procris A.L.Juss., Achudemia Blume, and Nanocnide Blume, and transferred Touchardia to Boehmerieae. Whether the addition of the genus Procris to this tribe influenced Weddell to give preference to the name Procrideae is unclear. Furthermore, it is unclear why Weddell did not adopt Gaudichaud’s usage of the name Elatostemeae (Gaudichaud 1830). Later publications accepted Weddell’s proposal to use the tribal name Procrideae (for example, Richardson 1978). Weddell’s final taxonomic concept of the family was that it consisted of the tribes: Boehmerieae, Elatostemeae (as ‘Procrideae’), Forsskaoleeae, Parietarieae and Urticeae (as ‘Urereae’) (Weddell 1869).
Friis (1993) referred to the Elatostemeae as ‘Lecantheae,’ as originally proposed by Weddell (1854), and included the following seven genera; namely, Sarcopilea, Meniscogyne, Elatostema, Procris, Petelotiella, Pilea and Lecanthus.
2.3.1. Justification for recognition of tribal names proposed by Gaudichaud Gaudichaud (1830) specifically stated that he subdivided the Urticaceae into ‘tribes or subfamilies’ (ibid., p. 491). However, his ‘five’ higher level subdivisions were published without a clear indication of rank (referred to as ‘tribes or subfamilies’); they are here regarded as probably referable to the modern taxonomic concept of subfamily. It could be concluded that names proposed by Gaudichaud at both ranks (tribes or subfamilies) are validly published according to article 34.2 of the International Code of Botanical Nomenclature (ICBN 2006). Both ranks may be validly published by a single description or diagnosis, thus dealing with Gaudichaud’s apparent ‘indecision.’ However, since Gaudichaud did not provide names for higher level ‘subdivisions,’ here presumed as subfamilies, they are not validly published. Gaudichaud’s next level of ‘subdivision’ is here regarded as representing tribes. Although the French suffix (namely, ‘-ées’) often infers tribal
11 Chapter 2. Taxonomic History rank, it has frequently been used to represent other ranks. Irrespective of this, these names have no legal status because names that are published with a non-Latin termination are not validly published, according to articles 6 and 12.1 of the International Code of Botanical Nomenclature (ICBN 2006). However, in the third paragraph of the footnote ‘I’ (Gaudichaud 1830, p. 495), he states, in reference to presence of cystoliths, ‘On les retrouve dans presque toutes les autres tribus’ (line 1) and ‘plante anomale de la tribu des pariétariées’ (line 4). Therefore, I believe that this is a clear indication that all 15 subdivisions within Gaudichaud’s five higher level subdivisions, and specifically, the six subdivisions within his ‘Urticées vraies’ grouping, are tribes. Gaudichaud clearly regarded these taxa as tribes because he later formally described them using names with the ‘-eae’ suffix, according to article 19.3 (ICBN 2006). Furthermore, Weddell (1856, p. 170) clearly recognised all of these ‘Urticées vraies’ taxa (sensu Gaudichaud) as tribes because he accepted all of the ‘tribal’ names, except for Elatostemeae. Although the first line of the following quote is unclear, Weddell (loc. cit.) definitely recognised Gaudichaud’s ‘Elatostemeae’ and his ‘Lecantheae’ as having equivalent rank when he reduced them to the synonymy of ‘Trib. II Procrideæ’: ‘Urticæ, Procridis et Parietariæ spec. Auct. Elatostemeæ Gaudich., Bot Voy. Uran, 496 [1830, p. 493] Lecantheæ Wedd., in Ann. Sc. Nat., sér. 4, I, 174 [1854]’ Since article 11.3 of the International Code of Botanical Nomenclature (ICBN 2006) recommends ‘For any taxon from family to genus inclusive, the correct name is the earliest legitimate one with the same rank …’ this would support the acceptance of the name ‘Elatostemeae’ in preference to any of the later tribal names applied to this taxon.
‘Index Nominum Supragenericorum Plantarum Vascularium’ (Reveal 2003) attributes the authorship of Boehmerieae, Elatostemeae, Forsskaoleeae, Parietarieae and Urereae to Gaudichaud.
It is here proposed that the 15 subdivisions of Gaudichaud (1830), within his five higher level subdivisions should be regarded as validly published tribes. With respect to the Urticaceae (‘Urticées vraies’ grouping sensu Gaudichaud), the six tribes described by Gaudichaud should be recognised as the correct names for these
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Urticaceous tribes with him as the author. With respect to the correct name of the tribe previously referred to as Elatostemeae, Lecantheae or Procrideae, it is here proposed that the correct name for this tribe should be Elatostemeae as first recognised by Gaudichaud (1830). The taxa included in his tribe Cecropieæ are currently regarded as belonging to the separate family Cecropiaceae (Berg 1978, Kubitzki 1993), but Sytsma et al. (2002) suggest that these taxa should be included in the Urticaceae.
2.4. Taxonomic history of Elatostema and related genera The discussion of the taxonomic history provided here is arranged in themes and within each theme is discussed in chronological order.
Elatostema was first described by J.R. Forster and G. Forster (1776). However, their generic description includes features of what is now regarded as the separate genus Procris. In the protologue of Elatostema, the species Elatostema pedunculatum J.R.Forst. & G.Forst. and E. sessile J.R.Forst. & G.Forst. were described. Elatostema pedunculatum was circumscribed as having flowers with 5 stamens (‘pentandrum’), whereas the flowers of E. sessile have 4-stamens (‘tetrandrum’). The former species was later transferred to the genus Procris (Weddell 1856; Robinson 1910) based on the 5-staminate flowers, whereas the latter remained in Elatostema, here based on the condition of four stamens per flower. Robinson (1910) suggested that the generic name Procris should be synonymised with Elatostema, which had nomenclatural priority. However, Robinson (op. cit.) and Schröter and Winkler (1935) concluded that this would cause serious nomenclatural confusion so they retained Procris as a separate genus.
Weddell (1854, 1856) recognised 60 species of Elatostema and eight species of Pellionia most of which were newly described. Hallier (1896) described a further seven new species of Elatostema, and recognised the first subgeneric classification within the genus, namely, subgenus Elatostema (as ‘Euelatostema’), subg. Pellionia and subg. Procris (hence, reducing the latter two genera to infrageneric status).
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Robinson researched the systematics of the Urticaceae of the Philippines (Robinson, 1910, 1911a-c). He re-instated Pellionia and Procris to generic level, concluding that Hallier (1896) had confused two different problems, namely, “whether there are three such genera [Elatostema, Pellionia and Procris] with well defined limits, and whether the limits assigned to them by Weddell and others are correct” (Robinson 1910, pp. 497, 498). He concluded that “these three genera are unusually distinct for the family and readily recognizable almost at a glance” (ibid. p. 498) and he recognised and published the additional new genus Elatostematoides (Robinson 1910). This new genus was typified by Elatostematoides manillense (Wedd) C.B.Rob. (basionym: Elatostema manillense Wedd.). Robinson (loc. cit.) recognised five species of Elatostematoides as occurring in the Philippines, of which two were described as new. He also transferred a further eight non-Filipino species of Elatostema to Elatostematoides.
Robinson (1911c) concluded that flower merosity was a reliable character for distinguishing species of Elatostema. He described an additional new species of Elatostematoides and recognised 20 species of Elatostema (of which five were new) from the Philippines. Ridley (1916) recognised 10 species of Elatostema from Indonesian Papua (then Dutch New Guinea), including five new species, and three species of Pellionia, two of which were new. Neither of these two workers recognised any subgeneric divisions within Elatostema.
Winkler (1922) followed Hallier’s subgeneric division of the genus (Hallier 1896) into three subgenera, namely subgenus Elatostema, subg. Pellionia and subg. Procris, when he published his work on the Urticaceae of Papuasia6. He recognised 57 species of Elatostema, 38 of which were new.
Schröter and Winkler (1935, 1936) published the first attempt at a complete account of Elatostema. They modified the subgeneric division of previous workers (Hallier 1896; Winkler 1922) and proposed four subgenera, namely, subg. Pellionia, subg. Elatostematoides, subg. Weddellia and subg. Elatostema (as ‘Euelatostema’) (refer Table 2.1). This division was primarily based on the nature of the leaves, stipules, inflorescence and the presence and form of the receptacle. They recognised Procris as a
6 The region of Papuasia includes Indonesian Papua, Papua New Guinea and Solomon Islands (excluding Santa Cruz) (Womersley 1978)
14 Chapter 2. Taxonomic History
separate genus based on distinct morphological differences. However, they did not provide further details.
Schröter (1938) regarded Procris as distinct from Elatostema by having male (staminate) flowers always arranged in glomerules that are cymosely arranged, and female (pistillate) flowers that are inserted on a fleshy receptacle but not enclosed in an involucre of bracts, or at most, with a shortly projecting rim of bracts, whereas Elatostema has both male and female flowers enclosed in an involucre of bracts and the receptacle of female flowers is not fleshy.
Schröter and Winkler (1935, 1936) published a taxonomic account of subgenus Pellionia, subg. Elatostematoides and subg. Weddellia. They included a brief description of each subgenus, including subg. Elatostema (as ‘Euelatostema’) and described 106 species from the first three subgenera, including 33 new species. Unfortunately, they did not publish a taxonomic account of subgenus Elatostema.
Since Schröter and Winkler (1935, 1936), there has been no further general treatment on this genus. Friis (1989, 1993) made no comment on the subgeneric classification. There have been several works of local or restricted geographic coverage; for example, Elatostema occurring in mainland China (Wang 1980a, Qi et al. 2003); in Taiwan (Yang et al. 1995); and Beaman’s study of species from Mt. Kinabalu (Beaman 2000, 2001; Beaman and Cellinese 2004). Each of these studies added several new species. Of these studies, Wang (1980a) rejected the subgeneric classification of Schröter and Winkler (loc. cit.). He proposed an infrageneric classification of Sections and Series based on morphology. At the sectional level, he recognised section Androsyce, sect. Elatostema, sect. Laevisperma, sect. Pellionioides and sect. Weddellia (as ‘Weddelia’)7. A summary of the morphological characters used by Wang (Wang and Chen 1979; Wang 1980a) is presented in Table 2.2 (see below). Wang and Chen (1979, p. 107) describe the receptacle of the female inflorescence of Elatostema section Elatostema as ‘Inflorescentiae feminae receptaculo paro majusculove instructae.’ The use of ‘paro’ is unclear. It could be referring to either:
7 Wang, in Wang and Chen (1979) incorrectly spelt Elatostema subgenus Weddellia H.Schroet. as Elatostema subg. Weddelia H. Schröter and so carried this error forward into his spelling of Elatostema sect. Weddelia (H. Schröter) W.T. Wang. This error should be corrected to Elatostema sect. Weddellia (H.Schroet.) W.T.Wang. This orthographic error also requires correcting in IPNI (2004+).
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(1) ‘par’ meaning equal, hence that the ‘female receptacle being equal to or slightly larger than [the male receptacle].’ However, the expected ablative form of ‘par’ would be ‘par’, ‘pari’ or ‘pare’ (Crane 2006); or (2) since the Chinese description of this Section by Wang and Chen (1979, p. 107) uses the Chinese character = small, then ‘par’ is here regarded as a typographical error for ‘parvo’ meaning smaller, hence describing the ‘female receptacle as being smaller or slightly larger than the male receptacle.
Wang (1980a) used similar morphological characters to those of Schröter and Winkler (1935, 1936) to define the sections (refer Table 2.2). However, these features have not been consistently recorded for each section. Therefore, it is difficult to compare his classification to that of Schröter and Winkler (1935, 1936). Wang used leaf venation, inflorescence and achenes characteristics, but he did not assess the presence or absence of nanophylls. He also did not evaluate other features of the stipules, nor did he consider flower merosity or perianth of female flowers in his sectional classification. All of these characters were regarded as important in Schröter and Winkler’s subgeneric classification. Wang (1980a) accepted, with some modifications, Schröter and Winkler’s circumscription of subgenus Elatostema and subg. Weddellia (as ‘Weddelia’), but classified them at sectional rank. He transferred some species from Schröter and Winkler’s subg. Elatostema into his section Weddellia (for example, Elatostema acuminatum Brongn., E. hookerianum Wedd., E. stipulosum), apparently based on a re-interpretation of the morphology of these species. As defined by Wang (1980a), Elatostema sect. Pellionioides is endemic to China and consists of nine species; section Androsyce consists of two species, namely E. brachyodontum (Hand.- Mazz.) W.T.Wang and E. ficoides Wedd., with the latter species transferred from subgenus Elatostema (sensu Schröter and Winkler 1935); and section Laevisperma (transferred from Pellionia sect. Laevisperma Hatus.) is monotypic, containing E. obtusum Wedd. only.
Wang (1980b) recognised Pellionia as a distinct genus and this taxonomic concept has been followed by later Chinese workers (for example, Qi et al. 2003). Whether or not he recognised the genus Elatostematoides is not known because he did not consider this taxon as it does not occur in China.
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Based on a subset of the same morphological characters used to characterise sections, Wang (1980a) subdivided the section Pellionioides into three series, namely Brevipedunculata, Laxicymosa and Oblongifolia; sect. Weddellia into seven series, namely Acuminata, Parva, Attenuata, Salvinioida, Stipulosa, Crenata and Involucrata; sect. Elatostema into five series, namely Cuspidata, Dissecta, Petelotiana, Nanchuaneasia and Albopilosa. However, he did not recognise series within section Laevisperma and section Androsyce. Lin and Duan (in press) proposed an additional series for section Elatostema (namely, ser. Albopilosoides) that is characterised by leaves with penninerved venation and dentate margin, plus by both male and female inflorescences being long-pedunculate. The series classification of Wang (1980a), and as expanded by Lin and Duan (in press), is not considered further in this thesis because species of Elatostema that belong to these series have not been included in this project. The recent ‘Flora of China’ account of Elatostema by Qi et al. (2003) does not follow the series classification of the genus by Wang (1980a).
Beaman (2000, 2001) carried out a cladistic analysis of species from Mt Kinabalu based on morphological characters. He found no support for the subgeneric arrangement of Schröter and Winkler (1935, 1936). He concluded that subgenus Elatostema s. str. (sensu Schröter and Winkler 1935, 1936) is a monophyletic group, but neither subgenus Pellionia nor subg. Elatostematoides (as circumscribed by previous researchers) are monophyletic, although only a few steps (that is, two and four steps, respectively) were needed to make them monophyletic on his data. He concluded that the latter two subgenera should be included within Elatostema, and should not be recognised as separate genera as proposed by Robinson (1910). Beaman did not include species from subgenus Weddellia in his study. However, the limited dataset of Beaman (2000, 2001), with only 24 taxa included, limits the usefulness of his review of the taxonomic status of the subgeneric divisions of Schröter and Winkler (1935, 1936).
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Elatostematoides Pellionia Weddellia Elatostema
Habit Always woody at base Herbaceous or woody at base Herbaceous Mostly herbaceous Leaf venation Totally semi-pinnate or pinnate at Mainly pinnate, rarely semi- or sub- Semi- or sub-pinnate Mainly sub-pinnate throughout, or sub- distal –¼ pinnate pinnate at base & pinnate at distal ½– . Rarely totally pinnate throughout Nanophylls Mostly present, often very small Mostly present, often very small (0.5- Always present Absent few mm) Stipules Both stipules of macrophyll and Both approximately equal in length, Both equal in length. Always Rarely equal in length. Macrophylls with nanophyll approximately equal in when nanophylls absent, then transparent and membranous stipules significantly smaller than length macrophylls with smaller stipules than stipules in position of absent nanophyll ones in position of absent nanophyll Inflorescence receptacle Receptacles absent Receptacles absent Receptacles present Receptacles present, broad and disk- shape Inflorescence Often ± long pedunculate, loose Mostly long pedunculate, loose cyme, Mainly sessile sessile, sometimes pedunculate (Schröter cyme, or sessile, loose capitulum rarely sessile, loose capitulum & Winkler 1935, p. 18)