taxonomy and phylogeny of crustose brown algae (phaeophyceae)

352 Pages·2014·20.88 MB·English

TAXONOMY AND PHYLOGENY OF CRUSTOSE BROWN
ALGAE (PHAEOPHYCEAE) FROM MALAYSIA AND
LOMBOK ISLAND, INDONESIA

POONG SZE WAN

FACULTY OF SCIENCE
UNIVERSITY OF MALAYA
KUALA LUMPUR

2014
TAXONOMY AND PHYLOGENY OF CRUSTOSE BROWN
ALGAE (PHAEOPHYCEAE) FROM MALAYSIA AND
LOMBOK ISLAND, INDONESIA

POONG SZE WAN

THESIS SUBMITTED IN FULFILLMENT OF THE
REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY

INSTITUTE OF BIOLOGICAL SCIENCES
FACULTY OF SCIENCE
UNIVERSITY OF MALAYA
KUALA LUMPUR

2014
ABSTRACT

Studies on crustose brown algae are relatively few despite a long history of studies
conducted since the 1800s, with temperate species forming the bulk of these studies.
There is a need for more focus on crustose brown algae particularly in the tropics as
they are generally different from those in the temperate regions. These algae received
little attention due to their simple appearance (brownish-black spots on rocks) and lack
of apparent economic value despite some being the dominant flora of certain habitats.
Taxonomic confusion arising from morphological simplicity largely dependent on the
reproductive structures and overlap in morpho-anatomical features among species
necessitates the use of molecular approach. This study aims to enhance our
understanding of the taxonomy and phylogeny of these understudied algae in Malaysia
and Lombok Island by combining morpho-anatomical observations and molecular
sequence data [plastid rubisco large subunit (rbcL) and partial mitochondrial
cytochrome c oxidase subunit 1 (cox1-5’) gene sequences]. Key diagnostic
morphological characters for identification include relative thickness of the crust,
assembly of erect filaments, number of chloroplast(s) and most importantly the
organisation of reproductive structures. Results indicated that the common crustose
brown algae in Malaysia and Lombok Island are species of Mesospora, Diplura and
Neoralfsia expansa. Seven species of Mesospora were identified in the present study of
which three were formally described (M. schmidtii, M. negrosensis and M. elongata)
and four are putative new species to be described (Mesospora sp. C, Mesospora sp. D,
Mesospora sp. 1 and Mesospora sp. 2). Partial output from this study leads to the recent
description of Mesospora elongata Poong, Lim & Phang from Japan and Lombok
Island and a new record of M. negrosensis for Malaysia. The presence of M. elongata in
Malaysia is reported here for the first time since the initial publication of this taxon.
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Mesospora sp. C and M. schmidtii were reported earlier in Malaysia. This study also
marks the first report of Mesospora sp. D (previously reported in Japan) and four
putative species of Diplura for Malaysia and Indonesia. The taxon provisionally named
“Mesospora” sp. 3 and the closely related Mesospora sp. G are likely members of a new
genus. Other crustose brown algae examined in this study include a Ralfsia-like species
and two yet-to-be identified taxa. The crustose brown algae are polyphyletic and occur
in widely divergent clades among the brown algae with the majority placed in Ralfsiales
while the rest are closely associated with other phaeophyceaen orders such as
Sphacelariales and Ishigeales. Circumscription of Ralfsiales comprises the Ralfsiaceae,
Neoralfsiaceae, Mesosporaceae and a possible new family to accommodate
“Mesospora” sp. 3. Establishment of a new family for members of the genus Diplura is
underway pending the collection of the generitype, Diplura simulans. Molecular
analyses incorporating Hapalospongidion saxigenum indicate that Mesospora, currently
synonymised with Hapalospongidion should be retained as a separate genus. The rbcL
marker performed better in the elucidation of phylogeny at higher classification levels,
whereas cox1-5’ is more suited as a barcoding marker for species level identification of
the crustose brown algae.

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ABSTRAK

Kajian mengenai alga perang berkerak agak terhad walaupun kajian tersebut telah
bermula sejak abad ke-19 dan kebanyakannya melibatkan spesies dari kawasan beriklim
sederhana. Tumpuan yang lebih berat perlu diberikan terhadap alga jenis tersebut,
khasnya di kawasan tropika kerana ianya adalah berbeza daripada mereka di kawasan
beriklim sederhana. Alga-alga ini kurang menerima perhatian disebabkan rupanya yang
biasa (tompok perang-kehitaman di atas batuan) dan tiadanya kepentingan ekonomi
yang ketara, meskipun sesetengahnya merupakan flora yang dominan di beberapa
habitat. Kekeliruan taksonomi berikutan morfologi yang biasa dan bergantung berat
terhadap struktur reproduktif serta pertindihan dalam ciri-ciri morfologi dan anatomi di
antara spesies memerlukan penggunaan pendekatan molekular. Kajian ini bertujuan
meningkatkan pemahaman terhadap taksonomi, filogeni dan floristik bagi alga perang
berkerak di Malaysia melalui penggabungan data molekular [jujukan gen plastid
rubisco large subunit (rbcL) dan mitochondrial cytochrome c oxidase subunit 1 (cox1)
separa] dan pemerhatian morfo-anatomi. Karakter morfologi diagnostik yang utama
untuk pengenalpastian merangkumi ketebalan kerak secara relatif, struktur bina filamen
terdiri, nombor kloroplas dan yang paling mustahak organisasi struktur reproduktif.
Keputusan menunjukkan bahawa alga perang berkerak yang biasa dijumpai di Malaysia
dan Lombok terdiri dari spesies Mesospora, Diplura dan Neoralfsia expansa. Tujuh
spesies Mesospora dikenalpasti dalam kajian ini yang mana tiga telah dihuraikan secara
formal (M. schmidtii, M. negrosensis dan M. elongata) dan empat berkemungkinan
merupakan spesies baru yang perlu dihuraikan (Mesospora sp. C, Mesospora sp. D,
Mesospora sp. 1 dan Mesospora sp. 2). Sebahagian hasil kajian ini menjurus kepada
penghuraian Mesospora elongata Poong, Lim & Phang dari Jepun dan Lombok dan
rekod baru M. negrosensis bagi Malaysia. Kehadiran M. elongata di Malaysia
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dilaporkan di sini buat julung kali sejak penerbitan pertama spesies ini. Mesospora sp. C
dan M. schmidtii telah dilaporkan di Malaysia sebelum ini. Kajian ini juga merupakan
laporan pertama Mesospora sp. D (sebelum ini dilaporkan di Jepun) dan empat spesies
Diplura bagi Malaysia dan Indonesia. Spesies yang buat sementara dinamai
“Mesospora” sp. 3 dan Mesospora sp. G yang berkait rapat dengannya berkemungkinan
besar merupakan ahli genus yang baru. Alga perang berkerak lain yang diselidik dalam
kajian ini merangkumi satu spesies seiras Ralfsia dan dua taksa yang belum
dikenalpasti. Alga perang berkerak adalah polyphyletic dan hadir dalam clades yang
amat berjauhan antara alga perang, yang mana kebanyakkannya ditempatkan dalam
Ralfsiales manakala lebihannya berkait rapat dengan order alga perang seperti
Sphacelariales dan Ishigeales. Ralfsiales kini merangkumi family-famili Ralfsiaceae,
Neoralfsiaceae, Mesosporaceae dan sebuah famili baru bagi “Mesospora” sp. 3.
Penubuhan famili baru untuk ahli-ahli genus Diplura perlu ditangguh sehingga
spesimen generitype iaitu Diplura simulans diperoleh. Analisa molekular yang
merangkumi Hapalospongidion saxigenum menunjukkan bahawa Mesospora yang kini
dianggap sebagai sinonim Hapalospongidion patut diasingkan sebagai genus berlainan.
Penanda rbcL adalah lebih sesuai bagi penghuraian filogeni pada peringkat klasifikasi
yang lebih tinggi manakala cox1-5’ lebih sesuai sebagai penanda barkod bagi
pengenalpastian alga perang berkerak di peringkat spesies.

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ACKNOWLEDGEMENTS

I would like to begin by thanking both my supervisors, Dr Lim Phaik Eem and
Professor Dr Phang Siew Moi for their valued guidance, advice and relentless support
throughout the course of this study. I thank my past and present colleagues (Poh Kheng,
Chew Hock, Tan Ji, Yoon Yen, Sze Looi, Fiona, Pei San, Hui Yin, Sim, Jelveh,
Victoria, Pui Ling, Jeannette and others) for their support and extensive help in the
laboratory and for a joyful research journey.
I am grateful to Drs Hiroshi Kawai, Wendy A. Nelson, John A. West and
Stefano G.A. Draisma for providing specimens for my research and to Dr. Willem F.
Prud’homme van Reine for his assistance in obtaining the lectotype from the Nationaal
Herbarium of Nederland. My sincere gratitude to Drs Kazuhiro Kogame and Akira F.
Peters for supply of literature, and to Professor Sunarpi for assistance in sample
collection. Joseph Buchanan is thanked for providing the rbcL sequence of Mesospora
negrosensis. My appreciation to Poh-Kheng Ng for providing photographs of collection
sites and to Yoon-Yen Yow for sample collection from Pulau Sayak, Kedah. I also
thank Matrix Optics (M) Sdn. Bhd. for providing me a copy of the analysis getIT and
measureIT softwares for morphological analysis work.
The Malaysia Toray Science Foundation (MTSF), University of Malaya
Postgraduate Research Fund (PPP) and High Impact Research (HIR) grants supported
this work with research funding. I also thanked University of Malaya for providing me
a scholarship (SBUM) during the course of this study. Finally, I would like to express
my utmost gratitude to my beloved parents for their unwavering moral support, patience
and encouragement throughout the years.

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TABLE OF CONTENTS
Page
ABSTRACT …………………………………………………………………………..iii

ABSTRAK ……………………………………………………………………............v

ACKNOWLEDGEMENTS ……………………………………………………….....vii

TABLE OF CONTENTS…………………………………………………………….viii

LIST OF FIGURES…………………………………………………………………..xvi

LIST OF TABLES……………………………………………………………………xxi

LIST OF SYMBOLS AND ABBREVIATIONS……………………………………xxii

LIST OF APPENDICES…………………………………………………………….xxiii

CHAPTER 1: INTRODUCTION

1.1 Current scenario of taxonomy studies with emphasis on algal taxonomic
effort……………………………………………………………………………….1

1.2 Importance of phylogenetic studies……………………………………………….5

1.3 The crustose brown algae………………………………………………………….7

1.4 Research Question………………………………………………………...……….9

1.5 Research Objectives……………………………………………………………….9

1.6 Research Hypotheses……………………………………………………………..10

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CHAPTER 2: LITERATURE REVIEW

2.1 The Phaeophyceae ………………………………………………………………..11

2.2 Classification of the brown algae ………………………………………………...15

2.2.1 Historical account on the classification of brown algae ………………..15

2.2.2 Types of early development of the thallus as a taxonomic criterion…18

2.2.3 Resolution of brown algal evolutionary relationships through
molecular phylogeny………………………………………………….19

2.3 Crustose brown algae and the controversies concerning their systematic
treatment at the ordinal and familial levels………………………………………25

2.4 Ralfsiales Nakamura ex Lim & Kawai …………………………………………..27

2.4.1 Ralfsiaceae Farlow ……………………………………………………..35

2.4.1.1 Ralfsia Berkeley in Smith & Sowerby ………………………36

2.4.2 Lithodermataceae Kjellman ………………………………………….46

2.4.2.1 Lithoderma Areschoug …………………………………….47

2.4.2.2 Pseudolithoderma Svedelius …………………………………51

2.4.3 Nemodermataceae Kuckuck ex Feldmann …………………………...58

2.4.3.1 Nemoderma Schousboe ex Bornet ………………………....58

2.4.4 Mesosporaceae Tanaka & Chihara ………………………………….....60

2.4.4.1 Hapalospongidion Saunders ………………………………....60

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2.4.4.2 Mesospora Weber-van Bosse ………………………………..63

2.4.4.3 Basispora John & Lawson ………………………………..65

2.4.4.4 Synonymisation of Hapalospongidion, Mesospora and
Basispora …………………………………………………..66

2.4.5 Neoralfsiaceae Lim & Kawai ………………………………………..67

2.4.5.1 Neoralfsia Lim & Kawai ………………………………….68

2.4.6 Other crustose brown algal genera associated with the Ralfsiaceae
and/or Lithodermataceae ……………………………………………..71

2.4.6.1 Diplura Hollenberg …………………………………………..71

2.4.6.2 Endoplura Hollenberg …………………………...............73

2.4.6.3 Zeacarpa Anderson, Simons & Bolton …………………..75

2.4.6.4 Petroderma Kuckuck …………………………................76

2.4.6.5 Porterinema Waern …………………………..................80

2.4.6.6 Sorapion Kuckuck …………………………...................83

2.4.6.7 Symphyocarpus Rosenvinge ………………………….......85

2.4.6.8 Acrospongium Schiffner …………………………………..88

2.4.6.9 Heribaudiella Gomont ……...................……………….90

2.4.6.10 Analipus Kjellman ………………………….................93

2.4.6.11 Heteroralfsia Kawai…………………………................96

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