REVISIONARY STUDIES IN SYNOSTEMON (, )

Morphological and molecular data corroborate generic recognition of Synostemon and with increased diversity

Ian R. H. Telford Grad. Dip. Sci. (ANU), M. Sc. (UNE)

A thesis submitted towards requirements for Doctor of Philosophy in the Faculty of Arts and Sciences University of New England

March 2015

University of New England Armidale, NSW 2351, Australia I.R.H. Telford Revision of Synostemon

Declaration

I, Ian Robert Hall Telford, certify that the substance of this thesis has not been submitted for any degree for myself, and is currently not being submitted for any other degree or qualification.

I also certify that any assistance in preparing this, and all sources used, have been duly acknowledged in this thesis.

Ian R. H. Telford

i I.R.H. Telford Revision of Synostemon

Abstract Phylogenetic analysis using an expanded data set of nrDNA ITS and PHYC and cpDNA accD and trns sequence data retrieves a monophyletic Synostemon F.Muell. (Phyllanthaceae, Phyllantheae, Flueggineae), previously subsumed into Blume or L. Sauropus s. str., excluding Synostemon, is shown to be nested within J.R.Forst. & G.Forst. (Chapter 2). Morphological data clarifies infrageneric relationships within Sauropus and its species are transferred to Breynia in a new subgenus, B. subgenus Sauropus (Blume) Welzen & Pruesapan (Chapter 3).

Synostemon hamersleyensis I.Telford & Naaykens, a recently discovered new species endemic to ironstone detrital formations of the Hamersley Range in the Pilbara, central Western Australia, is named, its distribution, habitat and contentious conservation status discussed (Chapter 4).

Analysis of nrITS sequence data from all described and putative new species of Synostemon corroborates the ‘Queensland clade’ consists of the previously recognised members S. albiflorus (F.Muell. ex Müll.Arg.) Airy Shaw, S. sphenophyllus Airy Shaw (syn. Sauropus convallarioides J.T.Hunter & J.J.Bruhl), Sauropus podenzanae (S.Moore) Airy Shaw, with a new combination provided as Synostemon podenzanae (S.Moore) I.Telford & Pruesapan and the undescribed Synostemon spinosus I.Telford & J.J.Bruhl (Chapter 5).

Morphometric analyses using PATN of the widespread, mainly eremaean Synostemon ramosissimus F.Muell. and the putative new species Sauropus sp. Woolgorang (M.Officer s.n. 10/8/94) indicate clinal variation across the continent; the western populations warrant subspecific rank and are named Synostemon ramosissimus subsp. occidentalis I.Telford & J.J.Bruhl. Similarly, S. rigens F.Muell. demonstrates a longitudinal cline and the most easterly populations are named as S. rigens subsp. virgatus I.Telford & J.J.Bruhl. Phylogenetic analysis using nrITS sequence data points to the close relationship of S. ramosissimus and S. rigens and justifies the rank proposed for the new subspecies of each (Chapter 6)

Synostemon trachyspermus (F.Muell.) Airy Shaw is shown by morphological studies, corroborated by phylogenetic analysis using nrITS sequence data, to be a heterogeneous

ii I.R.H. Telford Revision of Synostemon species assemblage (Chapter 7). Included in the clade with S. trachyspermus but warranting reinstatement as species are Phyllanthus rhytidospermus F.Muell. ex Müll.Arg., with a new combination provided as Synostemon rhytidospermus (F.Muell. ex Müll.Arg.) I.Telford & Pruesapan, and Sauropus hubbardii Airy Shaw, with a new combination as Synostemon hubbardii (Airy Shaw) I.Telford & Pruesapan and Synostemon lissocarpus (S.Moore) I.Telford & Pruesapan, the new combination provided for Phyllanthus lissocarpus S.Moore. Synostemon umbrosus I.Telford & J.J.Bruhl, sister to S. trachyspermus, is named as new. Synostemon hamersleyensis I.Telford & Naaykens and Sauropus aphyllus J.T.Hunter & J.J.Bruhl are shown to be closely related and atypical members of the S. trachyspermus clade, with the new combination Synostemon aphyllus (J.T.Hunter & J.J.Bruhl) I.Telford & Pruesapan provided for the latter. Sauropus sp. A of “Flora of the Kimberley Region” shows a more distant relationship and is named as Synostemon judithae I.Telford & J.J.Bruhl.

The Sauropus elachophyllus (F.Muell. ex Benth.) Airy Shaw and S. rigidulus (F.Muell. ex Müll.Arg.) Airy Shaw heterogeneous species assemblages are revised using morphological and nrITS sequence data (Chapter 8). Sauropus decrescentifolius J.T.Hunter & J.J.Bruhl and S. elachophyllus are conspecific. The ‘Top End clade’ comprises 14 species, four of which are named as new: Synostemon cowiei I.Telford & J.J.Bruhl, S. inaequisepalus I.Telford & J.J.Bruhl, S. kakadu I.Telford & J.J.Bruhl and S. nitmiluk I.Telford & J.J.Bruhl. New combinations under Synostemon are provided for S. crassifolius (Müll.Arg.) I.Telford & Pruesapan, S. ditassoides (Müll.Arg.) I.Telford & Pruesapan, S. dunlopii (J.T.Hunter & J.J.Bruhl) I.Telford & Pruesapan, S. filicinus (J.T.Hunter & J.J.Bruhl) I.Telford & Pruesapan, S. gracilis (J.T.Hunter & J.J.Bruhl) I.Telford & Pruesapan, S. rigidulus (F.Muell. ex Müll.Arg.) I.Telford & Pruesapan, S. stenocladus (S.Moore) I.Telford & Pruesapan and S. pinifolius (J.T.Hunter & J.J.Bruhl) I.Telford & Pruesapan.

A synopsis of Synostemon F.Muell. (Chapter 9) presents protologues, typification, synonyms and distributional data for all species. Synostemon angustus I.Telford & J.J.Bruhl and S. decumbens I.Telford & J.J.Bruhl are described as new and new combinations are provided for Synostemon anemoniflorus (J.T.Hunter & J.J.Bruhl) I.Telford & Pruesapan, S. arenosus (J.T.Hunter & J.J.Bruhl) I.Telford & Pruesapan, S. huntii (Ewart & O.B.Davies) I.Telford & Pruesapan and S. paucifolius (J.T.Hunter & J.J.Bruhl) I.Telford & Pruesapan.

iii I.R.H. Telford Revision of Synostemon

Prologue Format The main layout of the thesis follows the Style Guide of the University of New England (http://www.une.edu.au/tlc/styleguide).

The bibliographic style was formatted using Endnote 9 software. Formatting of the papers which constitute the major part of the thesis follows the editorial style of the relevant journal. For other chapters, the format follows that of Australian Systematic Botany.

Nomenclature The unpublished new names and combinations contained in this thesis are not to be considered validly published following Article 30.8 of the international code of nomenclature for algae, fungi and (Melbourne Code) .

Thesis layout The main body of the thesis is made up of a series of related papers, the current status of each presented below in the table of contents, together with my % contribution. Each published paper is presented as a printed pdf carrying the original pagination from the journal. Papers submitted and unpublished or those yet to be submitted are presented in the style required by each relevant journal and with the tables and figures at the end. The proposed position of these tables and figures are indicated within the text by the inserted caption. This renders redundant a separate ‘List of Tables’ and ‘List of Figures’ for the thesis as a whole. Similarly, references for each manuscript are included in their respective chapter and a combined bibliography is therefore not presented. The general introduction and aims (Chapter 1) sets out the aims of the project and shows the links between the papers, and the general conclusions (Chapter 10) tie the research project together. The Appendix presents a precursor paper to this study and a biogeographic spin-off.

History of the project This research project had its origin in the on-going treatment for the Flora of Australia project of several genera previously included in the Euphorbiaceae. The Australian Biological Resources Study provided funding for a revisionary treatment of Sauropus

iv I.R.H. Telford Revision of Synostemon

(together with Phyllanthus and the other genera of Phyllanthaceae tribe Phyllantheae ) to Jeremy Bruhl, who employed John Hunter to undertake the study through 1994–95. Although several papers were published on the and nomenclature of Sauropus (then including Synostemon) and Phyllanthus, the research was not completed. The huge amount of herbarium material on loan from Australia and overseas, including many type specimens, remained at the N.C.W. Beadle Herbarium.

Meanwhile Kanchana Pruesapan had begun her PhD research project at the University of Leiden with Professor Peter van Welzen as principal supervisor. A major aim of Kanchana’s research was the clarification of generic boundaries in Sauropus. The N.C.W. Beadle Herbarium contributed leaf samples of several Australian species for Kanchana’s DNA dataset and Jeremy Bruhl and I collaborated with them on the research. The preliminary phylogenetic analysis indicated a monophyletic Synostemon, the major Australian component of Sauropus sens. lat., worthy of reinstatement to generic rank.

Professor Jeremy Bruhl considered that a combined morphological and phylogenetic approach should be used to strengthen our Flora treatment and considered a revision of Synostemon would provide a suitable research project for me towards a PhD.

v I.R.H. Telford Revision of Synostemon

Acknowledgements

I gratefully acknowledge the support and encouragement from my principal supervisor, Professor Jeremy Bruhl, who first persuaded me to complete a Masters, and then suggested this PhD project.

To Professor Peter van Welzen, I must give sincere thanks for the invitation to collaborate on Kanchana’s research project and for then agreeing to co-supervise my studies.

To Dr Kanchana Pruesapan I express my gratitude for allowing me to collaborate in her research and for her continuing provision of DNA data after the completion of her own PhD research project.

The Directors of herbaria A, BM, BRI, CANB, DAV, DNA, MEL, NSW and PERTH are acknowledged for the loan of specimens and for allowing their Phyllanthaceae material to be held at NE for so long. Particular thanks to the Director, BRI, for assistance during visits, and the Chief Botanist, DNA, for chasing additional collections.

Receipt of an Australian Postgraduate Award, a UNE Botany Top-up Scholarship and research support from the School of Environmental and Rural Science are gratefully acknowledged.

The Australian Biological Resources Study is thanked for partial funding for field work and laboratory costs for this study through the Bush Blitz program.

This thesis is dedicated to my partner of 42 years, Douglas Hunter Moffatt (1943–2013). Doug unselfishly insisted I continue with this project after his being diagnosed with an aggressive, terminal cancer when I should have been his full-time carer at home during his last months.

vi I.R.H. Telford Revision of Synostemon

Table of Contents

Declaration...... i

Abstract ...... ii

Prologue ...... ii

Format...... iii Thesis layout ...... iii History of project ...... iii Acknowledgements ...... vi

Chapter 1: General Introduction and Aims...... 1

Chapter 2 (paper 1): Kanchana Pruesapan, Ian R.H. Telford, Jeremy J. Bruhl and Peter C. van Welzen (2012) Phylogeny and proposed circumscription of Breynia, Sauropus and Synostemon (Phyllanthaceae), based on chloroplast and nuclear DNA sequences, Australian Systematic Botany 25, 313–330 ...... 13

Chapter 3 (paper 2): Peter C. van Welzen, Kanchana Pruesapan, Ian R. H. Telford, Hans- Joachim Esser and Jeremy J. Bruhl (2014) Phylogenetic reconstruction prompts taxonomic changes in Sauropus, Synostemon and Breynia (Phyllanthaceae, Phyllantheae). Blumea 59, 77–94...... 34

Chapter 4 (paper 3): Ian R. H. Telford and Jeremy Naaykens (2015) Synostemon hamersleyensis (Phyllanthaceae), a new species endemic to the Pilbara, Western Australia. Nuytsia 25, 3137...... 55

Chapter 5 (paper 4): Ian R. H. Telford, Kanchana Pruesapan, Peter C. van Welzen and Jeremy J. Bruhl (accepted Nov. 2014) Molecular data consistently recover a “Queensland clade” of Synostemon (Phyllanthaceae, Phyllantheae) with distinctive floral morphology. Australian Systematic Botany ...... 66

vii I.R.H. Telford Revision of Synostemon

Chapter 6 (paper 5): Ian R. H. Telford, Peter C. van Welzen and Jeremy J. Bruhl. Clinal variation across Australia in two eremaean species of Synostemon (Phyllanthaceae, Phyllantheae) demonstrated using morphological and molecular data. (to be submitted to Australian Systematic Botany) ...... 92

Chapter 7 (paper 6): Ian R. H. Telford, Kanchana Pruesapan, Peter C. van Welzen and Jeremy J. Bruhl. Morphological and molecular data show Sauropus trachyspermus to be a heterogeneous species assemblage in Synostemon (Phyllanthaceae, Phyllantheae). (to be submitted to Australian Systematic Botany) ...... 133

Chapter 8 (paper 7): Ian R. H. Telford, Kanchana Pruesapan, Peter C. van Welzen and Jeremy J. Bruhl. Morphological and molecular data corroborate an enlarged crown radiation in Synostemon (Phyllanthaceae, Phyllantheae) in tropical Australia concealed by heteromorphic species concepts. (to be submitted to Australian Systematic Botany) ...... 176

Chapter 9 (paper 8): Ian. R. H. Telford, Peter C. van Welzen and Jeremy J. Bruhl. Synopsis of Synostemon (Phyllanthaceae, Phyllantheae, Flueggiinae) including the description of two new species, four new combinations and emended descriptions (to be submitted to Phytokeys) ...... 240

Chapter 10: General Conclusions ...... 275

Appendix 1: Kanchana Pruesapan, Ian R. H. Telford, Jeremy J. Bruhl, Stephan G. A. Draisma, Peter C. van Welzen (2008). Delimitation of Sauropus (Phyllanthaceae) based on plastid matK and nuclear ribosomal ITS DNA sequence data. Annals of Botany 102, 1007–1018...... 282

Appendix 2: Peter C. van Welzen, Kanchana Pruesapan, Ian R. H. Telford, Jeremy J. Bruhl. Historical Biogeography of Breynia (Phyllanthaceae): What caused speciation? (accepted by Journal of Biogeography, Mar. 2015) ...... 291

viii