Lumut Hati Di Gunung Sibayak Sumatra Utara

THE LIVERWORTS (

MARCHANTIOPHYTA

)

OF MOUNT SIBAYAK NORTH SUMATRA

ETTI SARTINA SIREGAR

THE GRADUATE SCHOOL

BOGOR AGRICULTURAL UNIVERSITY BOGOR

STATEMENT OF DISSERTATION AND SOURCES OF

INFORMATION AND COPYRIGHT DEVOLUTION *

This is to verify that my dissertation entitled: The Liverworts (Marchantiophyta) of Mount Sibayak North Sumatra is my own work and never

been submitted to any institution before. All of the incorporated data and information are valid and stated clearly in the text, and listed in the references.

Bogor, August 2015 Etti Sartina Siregar NIM G363100011

RINGKASAN

ETTI SARTINA SIREGAR. Lumut hati (Marchantiophyta) di Gunung Sibayak Sumatra Utara. Dibimbing oleh SRI SUDARMIYATI TJITROSOEDIRDJO, NUNIK SRI ARIYANTI dan MIEN A. RIFAI.

Penelitian mengenai lumut hati di Sumatra masih sedikit dibandingkan dengan Jawa dan daerah Malesia lainnya. Beberapa penelitian floristik lumut hati sudah dilakukan di Sumatra Barat dan Jambi, sedangkan di Sumatra Utara masih terabaikan. Penelitian ini mencakup 5 topik yaitu: 1) keanekaragaman dan persebaran jenis, dan taksonomi beberapa takson terpilih: 2) genus Marchantia (Marchantiaceae), 3) anak suku Ptychanthoideae (Lejeuneaceae), 4) Plagiochila, dan 5) Radula.

Spesimen yang diperiksa pada penelitian ini dikoleksi dari 7 lokasi di Gunung Sibayak, Sumatra Utara (perkemahan Sibolangit, Jagawana, Pasir Putih, air terjun dua warna, Panatapan, Lau Debuk-debuk, dan Brastagi. Spesimen disimpan di Herbarium Bogoriense (BO), Herbarium Departemen Biologi Universitas Sumatra Utara, dan Herbarium SEAMEO BIOTROP (BIOT). Spesimen diidentifikasi dengan menggunakan kunci identifikasi lumut hati Gradstein (2011), dan kunci identifikasi pada publikasi studi taksonomi lumut hati lainnya di Malesia, dan Asia Tropik. Hasil identifikasi disusun dalam bentuk tabel jenis dan distribusinya berdasarkan lokasi, ketinggian dan pola distribusi geografis. Pola distribusi geografi mengikuti Hyvonen (1989), berdasarkan data distribusi yang diperoleh dari literatur. Studi taksonomi dari taksa terpilih, dilakukan untuk menyediakan data deskripsi, nomenklatur, dan kunci identifikasi jenis yang terdapat di Gunung Sibayak.

Beberapa kebaruan pada penelitian ini adalah: 1) daftar jenis lumut hati di Gunung Sibayak, 2) Rekaman baru untuk Sumatra dan Indonesia, 3) menambahkan variasi baru pada deskripsi beberapa jenis, 4) menyediakan kunci identifikasi jenis Marchantia di Sumatra, kunci identifikasi jenis Ptychanthoideae, Plagiochila, dan Radula di Gunung Sibayak.

Topik 1. Keanekaragaman dan distribusi lumut hati di Gunung Sibayak Sumatra Utara. Diperoleh sebanyak 163 jenis lumut hati di Gunung Sibayak Sumatra Utara yang termasuk ke dalam 53 marga dan 22 suku. Dua puluh dua jenis merupakan rekaman baru untuk Sumatra. Suku terbesar yang diperoleh adalah Lejeuneaceae (18 marga dan 49 jenis), meliputi 30% dari jumlah total jenis yang ditemukan. Suku kedua terbesar adalah Lepidoziaceae (26 jenis).

Lumut hati di Gunung Sibayak ditemukan pada berbagai substrat. Jenis yang paling banyak ditemukan adalah epifit (127 jenis), tumbuh pada batang atau cabang pohon dan perdu, delapan jenis sebagai epilitik (tumbuh pada batu), tujuh jenis tumbuh di tanah, enam jenis tumbuh pada kayu lapuk, dua jenis epifil (tumbuh pada daun hidup), dan satu jenis tumbuh di air. Beberapa jenis memiliki banyak pilihan substrat (mampu hidup pada lebih dari satu substrat). Sebagian jenis memiliki sedikit pilihan substrat atau hanya hidup pada satu jenis substrat. Berdasarkan keberadaan jenis pada masing-masing lokasi penelitian, Jagawana memiliki jenis yang paling tinggi.

Sebagian besar lumut hati di Gunung Sibayak (79 jenis) memiliki kisaran persebaran yang luas berdasarkan ketinggian, yaitu dari sub pegunungan hingga pegunungan bawah. Sebanyak 67 jenis terbatas persebarannya pada hutan dataran rendah, dan 17 jenis terbatas persebarannya pada pegunungan bawah. Diperoleh 10 pola persebaran lumut hati Gunung Sibayak secara geografis yaitu: kosmopolit (1 jenis), pantropikal (13 jenis), paleotropikal (14 jenis), Asia-Australia (2 jenis), Asian-Oseanik-Australia (17 jenis), Asia-Oseanik (25 jenis), Asia Tenggara (55 jenis), Malesia (30 jenis), endemik (1 jenis), dan misellanous (4 jenis).

Topik 2. Genus Marchantia (Marchantiaceae) di Gunung Sibayak. Ditemukan sebanyak tujuh jenis Marchantia di Gunung Sibayak. Marchantia polymorpha merupakan catatan baru untuk Sumatra. Variasi ciri baru ditemukan pada jenis Marchantia emarginata. Pada publikasi sebelumnya, identifikasi jenis ini didasarkan pada ciri tonjolan berbentuk bulat pada bagian tengah permukaan dorsal reseptakel betina. Pada studi ini ditemukan spesimen tanpa tonjolan hingga tonjolan yang jelas pada bagian tengah permukaan dorsal reseptakel betina.

Topik 3. Anak suku Ptychanthoideae (Lejeuneaceae) di Gunung Sibayak. Ditemukan sebanyak 16 jenis anak suku Ptychanthoideae di Gunung Sibayak, yang termasuk ke dalam 8 marga: Acrolejeunea: (1 jenis), Caudalejeunea (1 jenis), Lopholejeunea (7 jenis), Mastigolejeunea (1 jenis), Ptychanthus (1 jenis), Schiffneriolejeunea (1 jenis), Spruceanthus (1 jenis), dan Thysananthus (3 jenis). Tiga jenis (Mastigolejeunea virens, Schiffneriolejeunea tumida dan Thysananthus retusus) merupakan catatan baru untuk Sumatra.

Topik 4. Plagiochila di Gunung Sibayak. Ditemukan sebanyak 18 jenis Plagiochila di Gunung Sibayak, yaitu sekitar 60% dari jumlah total jenis yang sebelumnya dilaporkan ada di Sumatra. Dua jenis (P. gracilis dan P. laxissima). merupakan catatan baru untuk Sumatra. Plagiochila junghuhniana dan P. dendroides merupakan jenis yang paling umum di Gunung Sibayak. Plagiochila gracilis, P. korthalsiana, P. laxissima, P. obtusa, P. salacensis, P. sumatrana dan P. singularis merupakan jenis-jenis yang tidak umum di Gunung Sibayak.

Topik 5. Radula di Gunung Sibayak. Ditemukan sebanyak 14 jenis Radula di Gunung Sibayak. Jumlah jenis yang ditemukan di Gunung Sibayak ini sekitar 60% dari jumlah jenis yang pernah dilaporkan sebelumnya ada di Sumatra. Tiga jenis (R. lingulata, R. loriana dan R. reflexa) merupakan catatan baru untuk Sumatra. Ditemukan ciri baru berupa gemma pada tepi daun Radula sumatrana. Sebelumnya jenis ini dilaporkan tidak memiliki gemma pada tepi daunnya.

Tingginya jumlah catatan baru untuk Sumatra membuktikan bahwa koleksi lumut dari Sumatra masih sedikit. Oleh karena itu dibutuhkan penelitian yang lebih komprehensif terhadap lumut di Sumatra. Koleksi spesimen harus dilakukan secara intensif dengan waktu pengkoleksian yang memadai dan jumlah tim kolektor yang cukup, disertai oleh ahli sewaktu mengkoleksi.

Kata kunci: Gunung Sibayak, keanekaragaman, lumut hati, Marchantiophyta, Sumatra Utara, studi floristik

SUMMARY

ETTI SARTINA SIREGAR. The Liverworts (Marchantiophyta) of Mount Sibayak North Sumatra. Supervised by SRI SUDARMIYATI TJITROSOEDIRDJO, NUNIK SRI ARIYANTI and MIEN A. RIFAI.

The liverworts of Sumatra are poorly known compared to the liverworts flora of Java and other Malesian regions. Floristic studies of liverworts have been done in West Sumatra and Jambi, while the liverworts of North Sumatra are still neglected. There are five topics in this study on the liverworts of Mount Sibayak, Nort Sumatra. 1) the diversity and distribution of species, and the taxonomy of selected taxa: 2) the genus Marchantia (Marchantiaceae), 3) subfamily Ptychanthoideae (Lejeuneaceae), 4) Plagiochila, and 5) Radula.

Specimens examined in the study were collected from seven localities at Mount Sibayak, North Sumatra (Sibolangit campground, Jagawana, Pasir Putih, Dwiwarna waterfall, Panatapan, Lau Debuk-debuk, and Brastagi). The specimens were deposited at Herbarium Bogoriense (BO), Herbarium of Biology Department, University of Sumatra Utara, and Herbarium SEAMEO BIOTROP (BIOT). The specimens were identified using identification key of liverworts provided by Gradstein (2011), and the others published key of Malesian and Tropical Asian liverworts. The results were compiled in a table showing the species and their local and altitudinal distribution, and pattern of geographical distribution. The geographical distribution patterns determined following Hyvonen (1989), based on the distribution data compiled from literatures. The taxonomy of selected taxa were studied to provide description, nomenclature, and identification key for the species occuring at the Mount Sibayak.

Some novelties of this study are: 1) a list of the liverwort species of Mount Sibayak, 2) new records of species for Sumatra and Indonesia, 3) adding new variations to the description of some species, 4) provide the key to species of Marchantia of Sumatra, the key to species of Ptychanthoideae, Plagiochila, and Radula of Mount Sibayak.

Topic 1. The diversity and distribution of liverworts of Mount Sibayak, North Sumatra. A total of 163 species are recorded from Mount Sibayak, they belong to 53 genera and 22 families. Twenty two species are new records for Sumatra. The largest family was Lejeuneaceae (18 genera and 49 species), contributed 30% to the total species. The second largest family was Lepidoziaceae (26 species).

The liverworts of Mount Sibayak were found on various substrates. The species are mostly epiphytes (127 species); they grow on bark or branch of trees and shrubs, eight species are epilith (grow on rocks), eight species grow on soil, six species grow on rotten logs, two species are epiphyll (grow on living leaves), and one species is aqutic. Some species have broad substrate preferences (occured on more than one substrate types). The others have narrow preferences, they occured on one substrate type. Based on the species occured in the study sites, Jagawana has the highest species richness.

Most of the liverwort species (79 species) have a wide altitudinal distribution, ranged from lowland to lower montane forest. Sixty seven species are

restricted to lowland forest, and 17 species are restricted to lower montane forest. Ten geographical distribution patterns were recognized : cosmopolite (1 species), pantropical (13 species), paleotropical (14 species), Asian-Australian (2 species), Asian-Oceanian-Australian (17 species), Asian-Oceanian (25 species), South East Asiatic (55 species), Malesian (30 species), endemic (1 species), and miscellaneous (4 species).

Topic 2. The genus Marchantia (Marchantiaceae). There are seven species of Marchantia at Mount Sibayak. Marchantia polymorpha is a new record for Sumatra. New variation was found in Marchantia emarginata. The species was previously identified based on the distinct rounded median projection on dorsal side of the female receptacles. In this study, specimens examined of the species have indistinct to distinct median pojection on the dorsal surface of female receptacles.

Topic 3. Subfamily Ptychanthoideae (Lejeuneaceae). There are 16 species of subfamily Ptychanthoideae at Mount Sibayak, they belong to eight genera: Acrolejeunea (1 species), Caudalejeunea (1 species), Lopholejeunea (7 species), Mastigolejeunea (1 species), Ptychanthus (1 species), Schiffneriolejeunea (1 species), Spruceanthus (1 species), and Thysananthus (3 species). Three species (Mastigolejeunea virens, Schiffneriolejeunea tumida and Thysananthus retusus) are new records for Sumatra.

Topic 4. Plagiochila of Mount Sibayak. There are 18 species of Plagiochila at Mount Sibayak, this number is about 60% of the total species previously reported from Sumatra. Two species (P. gracilis and P. laxissima) are new records for Sumatra. Plagiochila junghuhniana and P. dendroides were the most common species at Mount Sibayak. Plagiochila gracilis, P. korthalsiana, P. laxissima, P. obtusa, P. salacensis, P. sumatrana and P. singularis were uncommon at Mount Sibayak.

Topic 5. Radula of Mount Sibayak. Fourteen species of Radula are recorded from Mount Sibayak. The species recorded in this study represent about 60% of the species previously recorded from Sumatra. Three species (R. lingulata, R. loriana and R. reflexa) are new records for Sumatra. Marginal gemmae were found on leaf-lobes of Radula sumatrana. The presence of marginal gemmae was a new character for describing the species since the species was previously reported that they did not have marginal gemmae on leaf-lobes.

The high number of new records for Sumatra support the notation that bryophytes of Sumatra were undercollected. Therefor, more comprehensive studies of liverworts in Sumatra are needed. Specimens collection should be done intensively with adequate collecting time and sufficient number of collector teams, as well as the presence of specialist when collecting.

Key words: Diversity, floristic study, liverwort, Marchantiophyta, Mount Sibayak, North Sumatra

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Dissertation

Submitted to fulfill one of the requirements for the Doctor Degree at the Study Program of Biology

THE LIVERWORTS (

MARCHANTIOPHYTA

)

OF MOUNT SIBAYAK NORTH SUMATRA

THE GRADUATE SCHOOL

BOGOR AGRICULTURAL UNIVERSITY BOGOR

2015

Examiners of Closed Examination: 1 Dr Ir Titien Ng. Praptosuwiryo, MSi 2 Dr Ir Sulistijorini, MSi

Examiners of Opened Examination: 1 Dr Rugayah, MSc 2 Dr Ir Sulistijorini, MSi

FOREWORD

In the Name of Allah, the Most Gracious and Most Merciful

This study emphasizes five different topics namely diversity and distribution, the genus Marchantia (Marchantiaceae), subfamily Ptychanthoideae (Lejeuneaceae), Plagiochila, and Radula. The second topic “The liverwort genus Marchantia (Marchantiaceae) of Mount Sibayak North Sumatra, Indonesia” was published in Biotropia, 2013, 20(2):73-80. The third topic was published in Floribunda, 2014, 4 (8):218-225. The fifth topic “Radula of Mount Sibayak North

Sumatra, Indonesia” was presented in Ninth International Flora Malesiana

Symposium, August 27-31, 2013, in Bogor Indonesia.

I understand that this dissertation will never be completed without assistance of many colleagues and friends who have contributed in various ways. I greatly appreciate to the advisory committees for their advice, wise guidance, attention, patience and valuable discussion during the conduct of the studies and reading critically the manuscript, Dr. Sri S. Tjitrosoedirdjo MSc., Dr. Nunik Sri Ariyanti and Prof. Mien A. Rifai. Appreciation also to Dr. Narin Printarakul and Dr. Hiroyuki for some literatures and discussions. My gratitude and appreciation to the Rector of the University of Sumatra Utara through dean of the Faculty of Mathematics and Sciences, head of Biology Department for allowing me to pursue the doctorate program.

I gratefully acknowledges the financial support for this work from Directorate General of Higher Education (DIKTI), DIPA Project SEAMEO BIOTROP 2012/2013 (Research fellowship for PhD student), and University of Sumatra Utara. I would like to thank to BKSDA SUMUT for permitting the research in Mount Sibayak. Thank to the head of Herbarium Bogoriense (BO) for giving an opportunity to study some specimens of liverworts from North Sumatra. Thanks are also due to the head and technician of Plant Taxonomy Laboratory in Biology Departement IPB for some facilities during my research. Many thanks are also to my field assistants in Mount Sibayak for helping the specimen collection, to Dr. Bejo Slamet for making the map of the study sites, and my friends at Program Study of Plant Biology for their friendship.

I am indebted to my large family for continuing support during my study. My deep gratitude to my husband Drs. Suprin Hasibuan, and my lovely daughters Febri Maulida Sari Hasibuan, Mufida Rahmadhani Hasibuan, Lainatus Syifa Hasibuan and Hafizah Hani Majidah Hasibuan for their prayer, spirit, patience, and support during my study.

Bogor, August 2015 Etti Sartina Siregar

TABLE OF CONTENTS

LIST OF TABLES vi

LIST OF FIGURES vi

LIST OF APPENDIX vi

1 INTRODUCTION 1

1.1 Background 1

1.2 Objectives of Study 3

1.3 Benefit of Study 3

2 LITERATURE REVIEW 4

2.1 Morphology of Liverworts 4

2.1.1 Thalloid liverworts 4

2.1.2 Leafy liverworts 5

2.2 The Ecological and Economic Importance of Bryophytes 5 2.2.1 Bioindicators 5

2.2.2 Pioneer plants and erosion control 6

2.2.3 Habitat for other organisms 6

2.2.4 Horticultural uses 6

2.2.5 Medicine 6

2.2.6 Household uses 7

2.3 Distribution of liverworts 7 3 METHODS 9 3.1 Study Sites 9 3.2 Sampling Method 10 3.3 Identification 11 3.4 Data Analysis 12 3.4.1 Diversity and distribution of species 12

3.4.2 Taxonomic studies of particular taxa 12

4 RESULTS 13 4.1 Diversity and Distribution of Liverworts of Mount Sibayak 13 4.1.1 Local distribution 14

4.1.2 Substrates 14

4.1.3 Altitudinal and geographical distribution 15

4.2 The Genus Marchantia (Marchantiaceae) of Mount Sibayak 16 4.2.1 Key to species of Marchantia of Mount Sibayak and the species recorded from Sumatra 16

4.2.2 Species description 17

4.3 Subfamily Ptychanthoideae (Lejeuneaceae) of Mount Sibayak 23 4.3.1 Key to species of Ptychanthoideae of Mount Sibayak 23

4.3.2 Species description 24

4.4 Plagiochila (Plagiochilaceae) of Mount Sibayak 32 4.4.1 Key to species of Plagiochila of Mount Sibayak 32

4.4.2 Species description 33 4.5 The genus Radula (Radulaceae) of Mount Sibayak 45

4.5.1 Key to species of Radula of Mount Sibayak 45

5.5.2 Species description 46

5 DISCUSSION 55

5.1 Species Diversity and Distribution of Liverworts of Mount Sibayak 55

5.2 Taxonomy of Particular Taxa 58

6 CONCLUSIONS AND RECOMMENDATIONS 61

6.1 Conclusions 61

6.2 Recommendations 61

REFERENCES 63

APPENDIX 72

LIST OF TABLE

1 The number of families, genera, species, and new record species of liverworts in Mount Sibayak included in this study

13 2 Number of species based on location of liverworts at Mount

Sibayak North Sumatra

14 3 Number of liverworts species based on geographical and altitudinal

distribution type at Mount Sibayak

LIST OF FIGURE

1 Map of study sites at Mount Sibayak 9

2 Method of measurement in Thysananthus 11

3 Variations of female receptacle of Marchantia emarginata 19

LIST OF APPENDIX

1 Locations, substrates, altitudinal and geographical distribution of the liverwort from Mount Sibayak

72 2 The new records species of liverworts for Sumatra and the

previously known distribution

82

3 Glossary 86

1 INTRODUCTION

1.1 Background

Bryophytes are non-vascular land plants, small size, characterized by a life-cycle of alternating haploid and diploid generation with a dominant gametophyte. Bryophytes are an important element of tropical ecosystems, and they occure at lowland to high mountains. Bryophytes play an important role in forest ecosystem, they serve as water storage, and maintain humidity. They may serve as substrate for establishment of vascular epiphytes and offer shelter for some small animals (Bishler-Causse 1989; Gradstein 2011; Ho 2013). Bryophytes are pioneer on bare soil, their ability to withstand high rainfall could reduce erosion (Glime 2007b). The others importance of bryophytes are: bioindicators (Govindapyari et al. 2010; Dymytrova 2009), medicine (Ludwiczuk et al. 2011; Shen et al. 2010; Dey and De 2012), and inhibiting the growth of fungal pathogens on vegetables (Xie and Lou 2009).

Bryophytes are divided into three main groups, namely Marchantiophyta (liverworts), Bryophyta (mosses) and Anthocerotophyta (hornworts). The diversity of liverworts include about 7500 species worldwide (Konrat et al. 2010). Diversity of liverworts in tropical forests increased with the altitude. The diversity in terms of number of genera is highest at submontane, and low at montane belts, and lowest at subalpine and alpine belts. The species richness is highest at upper montane forest, and lowest at subalpine and alpine (Gradstein et al. 2001).

Bryophytes were not a concern of Indonesian botanists, due to their small size and difficulties in identification. Therefore, knowledge of bryophytes in Indonesia is still limited and far behind the flowering plants. The study on bryophytes in Indonesia is less than the other countries in Southeast Asia. The record on Malaysian liverworts and hornworts was published in 2011 (Chuah-Petiot 2011), it was supplemented by others publications of the research on the particular taxa (Lee et al. 2010; Lee and Gradstein 2013; Lee 2013; Lee et al. 2013; Yong and Furuki 2013; Pocs et al. 2014). Some floristic studies on Malaysian mosses were also recently published (Suleiman et al. 2006, 2009; Suleiman and Akiyama 2014, Akiyama and Suleiman 2015). A list of liverworts and hornwort of Thailand was prepared by Lai et al. (2008). Floristic studies and the studies on particular taxa recently added information on the bryophytes (mosses and liverworts) of Thailand (Kornochalert et al. 2010; Sukkharak et al. 2011; Kornochalert et al. 2012; He et al. 2012; Lee et al. 2014; Sukkharak 2015; Tan et al. 2006; Printarakul et al. 2009; Akiyama et al. 2011; Printarakul et al. 2012, 2013; Promma and Chantanaorrapint 2013; Printarakul et al. 2014; Pollawatn et al. 2008; Akiyama and Tsubota 2009; Tan et al. 2006; Wongkuna et al. 2009; Akiyama et al. 2010).

Studies on the mosses of Singapore were studied earlier than the liverworts. A book of mosses of Singapore and Malay Peninsular was published in 1980 (Johnson 1980). Other records on the mosses of Singapore were reported by Mohamed and Tan (1988), and Tan and Ho (2008). The liverworts of Singapore

were published after the mosses (Piippo et al. 2002); Furuki and Tan 2013; Ho 2013).

List of mosses (Bartram 1939; Tan and Iwatsuki 1991) and liverworts (Tan and Engel 1986) in the Philippines have been provided. In this region, study of mosses were more intensive than liverworts. Some floristic and ethnobotanic studies of Philippine mosses and liverworts have been recently published (Lubos 2007; Hipol et al. 2007; Azuelo et al. 2010; Linis 2010; Lubos 2010; Azuelo et al. 2011; Linis and Tan 2013; Tan and Shevock 2014).

Studies on the bryophytes of Indonesia are still limited. The bryophytes of Indonesia was mostly studied by foreigner botanists (Sande-Lacoste 1884; Herzog 1943; Gradstein et al. 2005; Schafer-Verwimp 2006; Söderström et al. 2010; Gradstein 2011). The availability of data on bryophytes are varies among the regions. Records on the bryophytes of Java are more than the other Indonesian regions. The bryophytes of Java have been studied for more than 150 years. The earlier records on the liverworts and hornworts of Java were published by Reinwardt et al. (1824) and Nees (1830), while Söderström et al. (2010) published the latest catalogue of the liverworts and hornworts of Java. A total of 465 species were compiled to the key identification of liverworts and hornworts of Java (Gradstein 2011). Floristic studies on the bryophytes of Java increased after the biennial training course on bryology and lichenology organized by SEAMEO BIOTROP in Bogor in 2001 to 2011. Some studies on species diversity, taxonomy, and ecology of the bryophytes were recently published (Haerida 2009; Haerida et al. 2010; Gradstein et al. 2010; Gradstein 2011; Haerida and Gradstein 2011; Haerida and Gradstein 2012; Damayanti 2006; Tan et al. 2006; Iskandar 2008; Windadri 2009a, 2009b; Windadri 2010; Ariyanti and Sulistijorini 2011; Haerida and Ho 2014).

The other Indonesian region which already have adequate data of bryophytes is Sulawesi. Some studies of bryophytes have been conducted in Sulawesi, either for liverworts or mosses. The earlier studies on the bryophyte of Sulawesi were published by Brotherus (1899), Brotherus (1900), and Cardot (1901). The latest study presented the first catalogue of bryophytes in Sulawesi. The catalogue was published in 2005 and consist of 340 species of mosses, 134 species of liverworts, and 2 species of hornworts (Gradstein et al. 2005). Studies on the bryophytes of Sulawesi increased due to STORMA project of University of Gottingen, Bogor University of Agriculture (IPB), and Tadulako University (UNTAD) in 2005. The studies on bryophytes of Sulawesi published in the last ten years are Ariyanti and Gradstein (2007), Windadri (2007), Ariyanti et al. (2007, 2008, 2009), Gradstein and Culmsee (2010), and Sporn et al. (2010).

Studies on the bryophyte of Sumatra are relatively scanty. Ho et al (2006) published a checklist of Sumatran Mosses in 2006. There are 490 species of mosses reported in the checklist. However, the liverwort was neglected. The first publication on the liverworts of Sumatra was written by Sande-Lacoste (1884). The other earlier records on the liverworts of Sumatra was reported based on the expedition of Indomalaya in April-September 1930 by Verdoorn (Meijer 1953). Verdoorn studied liverworts based on specimen collected in the expedition covered Java, Sumatera, and Malaya. He published studies on some important taxa: Frullaniaceae (Verdoorn 1929), Lejeuneaceae (Verdoorn 1933), and some genera of liverworts (Verdoorn 1931). After the second world war, no more

studies were conducted in these areas. Fortunately, Herzog was continuing to collect Malesian bryophytes during the second world war (Meijer 1953). After several years there was no liverworts studies in Sumatra, Herzog (1943) described 72 species of liverwort collected from Padang, West Sumatera. In 1950s, Malesian bryophytes flora was included in the Flora Malesiana project (Wijk 1951). The studies on Malesian bryophytes were done based on the specimens kept at the European herbaria. Due to lack of locality information and poor specimens, the study did not reflect ecological variability of the taxa (Meijer 1953).

The liverworts of Sumatra were not studied for some long periods until the studies on the Asian liverworts conducted in 1970s (Yamada 1979; Mizutani 1988; Inoue 1984 Bischler-Causse 1989, So 2003, Zhu and Gradstein 2005). Some specimen collected from Sumatra were included in the examined specimen in these studies. The specimens were collected from West Sumatra and Jambi. However, there was no specimen collected from North Sumatera were examined in the studies. The latest report on the liverworts of North Sumatra was published by Schafer-Verwimp (2006) based on the specimen collected from Mount Sinabung. The exploration to collect specimens of liverwort from North Sumatra and the floristic study on the liverworts of North Sumatra has not been done.

Plant taxonomists, such as Ridley (1923), Iwatsuki (1973), Siregar and Pasaribu (2008), Utami (2006), Hutasuhut (2011), and Praptosuwiryo et al. (2011), have visited Mount Sibayak for studying the spermatophytes and pteridophytes. However, the bryophytes of Mount Sibayak were not being the object of their studies.

1.2 Objectives of Study

The objectives of this study on the liverworts of Mount Sibayak is to provide a checklist of the liverworts of Mount Sibayak, to investigate diversity and distribution of the species and to study the taxonomy of the genus Marchantia (Marchantiaceae), the subfamily Ptychanthoideae (Lejeuneaceae), the genus Plagiochila, and the genus Radula.

1.3 Benefits of Study

This research provide information about the liverworts of Mount Sibayak for completing the liverworts data of Sumatra, as well as Indonesia. The specimens collected in this study are useful for studies on the taxonomy of liverworts.

2 LITERATURE REVIEW

2.1 Morphology of Liverworts

Liverworts are an ancient and belong to the oldest land plants. They existed already in the Palaeozoic period in forms which were hardly different from the extant species. They remained relatively unchanged with relatively low evolution rates, and are thus often called a “conservative“ plant group (Frahm 2003).

Liverworts are non vascular plant (without vessels), attached to the substrate by rhizoids (do not have roots), and without cuticle and stomata on their leaves. The process of transporting water and minerals in the body takes place in diffusion and assisted by the flow of cytoplasm. Due to the lack of roots, stomata and cuticle leaves, make them as typically poikylohydric plants, or easy to absorb and emit water, that is, their turgor depends on moisture in the environment. During dry periods, the plants dry up almost completely and may become dormant. When wetted, water is taken up rapidly by plants (Gradstein et al. 2001).

Liverwort life cycle have an alternation of two phases or generations, a sporophyte and a gametophyte. The dominant generation in the life cycle is the gametophyte, which originate from a spore produced by the sporophyte. Sporophyte is comparatively short lived and nutritionally depent on the free-living gametophyte. The sporophytes also completely mature in gametophytic body (Stotler and Stotler 2000; Gradstein et al. 2001).

Liverworts are small in size but they can be very conspicuous growing as extensive mats in woodland, as cushions on walls, rocks and tree trunks, and as pioneer colonists of disturbed habitats. They are very diverse in structure and often with highly variable morphology. There are two types of liverworts based on body form: thallose and leafy liverworts.

2.1.1 Thalloid liverworts

Thalloid liverworts have a dorsiventrally flattened gametophyte or thallus, ribbon-like, dichotomously branching structure (pinnate in Riccardia). They are not divided into stem and leaves and variable in its structure. Thallus surface that contact with the substrate is called the ventral surface while the other is called the dorsal part. Many rhizoids and sometimes many scales are found on the ventral surface. Tissue within the thallus can be quite differentiated or have little differentiation. There are two types of thalloid liverwort: simple thalloid and complex thalloid. The simple thalloid liverworts have undifferentiated thallus composed of one or two cell layers, all cells are green and filled with chlorophyll and oil bodies. The simple thalloid liverworts are clasified in Metzgeriales, for example: Metzgeria, Pallavicinia and Riccardia. The structure of complex thalloid are divided into ventral and dorsal side. The ventral side have colorless tissue, for saving metabolites and often contains specialized oil cells. The dorsal side have green tissue in which contain air chambers that open by pores to the upper thallus surface. The dorsal side have green tissue, contains The complex thalloid liverworts are clasified in Marchantiales: Marchantia and Dumortiera (Gradstein et al. 2001; Gradstein 2011).

The antheridia and archegonia of thalloid liverworts are produced on the dorsal of thallus surface, inside the thallus, or on swollen organ called receptacles. The stalked of female receptacle is called as archegoniophore and the stalked of male receptacle is called as antheridiophore (Gradstein 2001).

2.1.2 Leafy liverworts

The stem of liverworts are rather thin, simple or variously branched. There are two basic types of branches: intercalary and terminaly branches. In general, leafy liverworts have two or three rows of leaves, two lateral rows (lateral leaves) and one ventral row (underleaves). The lateral leaves position may be transverse, incubous, or succubous. Incubous leaves have dorsal leaf margin lies on top of the ventral margin of the younger leaves. It is just the other way around in succubous leaves. The leaves are only one cells thick, lack a midrib or costa. The leaf cells vary in shape and often have collenchymatous thickenings called trigones. The cells usually have chloroplasts and oil bodies when fresh. The characteristics of oil body such as number per cell, size, and structure are taxonomically important in identification of the majority of liverworts taxa The underleaves are usually smaller than the lateral leaves and sometimes lacking (Gradstein et al. 2001; Gradstein 2011).

2.2 The Ecological and Economic Importance of Bryophytes

The bryophytes were thought to have no use since they are inconspicuous and have small size. However, bryophytes are used for many purpuse, such as horticulture, household, medicine, and they have ecological importace.

2.2.1 Bioindicators

Liverworts and mosses have been found to be good indicators of environmental conditions. The suitability of liverworts as bioindicators is mainly due to the lack of conductive tissues and do not have a protective leaf cuticle. Consequently, gasses and solutions entrance freely to the living cells of bryophytes. The structure without cuticle could easily to intake the water and minerals including heavy metals. Their sensitivity to environmental changes and air pollution make them as a good bioindicator of environmental conditions, disturbances in ecosystem, and climatic changes. They absorp pollutants through the leaf or thallus directly from the atmosphere or water and accumulate them in large amounts (Gradstein et al. 2001).

Some bryophytes grow only in a narrow and specific pH range, therefore they could be used as an indicator of soil pH. Some aquatic species are indicator for calcium and other nutrient content in water as well as water pollution. The liverworts have also been used to monitor air pollution caused by emissions from various sources. They could absorb and retain pollutants in higher quantities than those absorbed by other plants in the same habitat (Saxena and Harinder 2004).

The role of liverworts as indicators of environmental changes have been reported in various types of landscape (Holz and Gradstein 2005; Drehwald 2005; Larsen et al. 2007). Some bryophytes are metal tolerant and able to withstand levels of heavy metals that are toxic to other species. Heavy metals are absorbed

from the atmosphere or the substrate. Marchantia polymorpha, Solenostoma crenulata, are the example of the metal tolerant populations. Scapania undulata is used to monitor water pollution (Govindapyari et al. 2010). Some other species of bryophyte have also been used as indicator of air pollution caused by people activities in residential areas, polluted by fumes or industry (Dymytrova 2009). 2.2.2 Pioneer plants and erosion control

Bryophytes have capability to rapidly colonize substrate, therefor they are pioneer plants in bare lands. Thick layer of bryophyte on soil may have ability to absorb and store a large quantities of rain water, and prevent soil erosion (Gradstein et al. 2001). The ability to reduce erosion have important role, especially on the outskirts of the newly opened road and the slope of the hill, before the larger plants are growing. Bryophytes also has potentially role in helping revegetation of degraded land, for example in the former mining areas, clearing land, and forest conversion. This capability is supported by the ability of bryophytes to form a large population or a vast expanse quickly (Glime 2007b). 2.2.3 Habitat for other organisms

Bryophytes may offer shelter to small animals. Epiphytic liverworts are widely used as habitat by insects such as ants, beetles, and mites. The insects also used the bryophytes for storing their larvae. Small animals such as lizards, snails, frogs, and arthropods are frequently found on the terrestrial liverworts mats. They used the liverworts to create moist environment, protect them from the wind, and for laying their eggs. Liverworts can accumulate organic matter and dust, making it possible to accomodate food source for the small animals. Liverworts also may serve as substrate for other plants (Glime 2007a).

2.2.4 Horticultural uses

Bryophytes have been involved in horticulture as soil additives, ground cover, greenhouse crops, ornamental of potted plants, and for seedling beds. Bryophytes are often used to conditionize and fertilize the soil. Coarse textured of bryophytes increase water-storage capacity. They may improve the nutrient condition by holding nutrients, especially those borne by dust and rainfall, and releasing the nutrients to the soil surface. Recently, one of the more important functions of the liverwort is in the study of the physiology and genetic potential in gene transplantation for traits tolerant to drought and as antiherbivora for agricultural crops (Glime 2007b). .

Many species of liverworts may contain natural pesticides, for example: the species of Plagiochila contains the sesquiterpene hemiacetyl plagiochiline A, a poison extremely potent in mice, and it inhibits the feeding of an African army worm. Extracts of Frullania brasiliensis can inhibit the growth of fungal pathogens on vegetables such as tomatoes and potatoes. (Asakawa et al. 1980). 2.2.5 Medicine

One reason in the bryophyte exploitations is the biological compounds that can be used for medicine. Liverworts are used in traditional medicine for treating some diseases such as liver, hookworm, swelling, fever, digestive and urinary problems, infections, lung, and skin diseases. The traditional use of liverworts

have also been realized in medical science (Ludwiczuk and Asakawa 2008; Harris 2008 ).

The use of bryophytes, including the liverwort in herbal medicines has been common in China, India, and among Native Americans since ancient times. The most widely known example of medicine used is Marchantia polymorpha. The species has commonly been used as a cure liver, lung disease and ulcers (Shen et al. 2010; Dey and De 2012). Marchantia are wellknown in traditional Chinese medicinal herbs extensively used to treat skin tumefaction, to protect the liver and treat hepatitis, reduce inflammation, as a diuretic, and being also used as antipyretics (Glime 2007). Himalayan Indians use M. polymorpha to treat boils, against inflammation and abscesses; Riccia species were used to against ringworms in children (Harris 2008; Shirsat 2008).

Liverworts contains a number of important medicinal compounds such as antibacterial, antioxidant, antibiotic, antifungal, cytotoxic, anticancer, antitumor, anti-venom and anti-inflammatory. Liverworts also contain oil bodies in their cells and elaborate with sesquiterpenes, diterpenes and lipophilic aromatics as their major chemical constituents. Several biological activities of liverworts are triggered by these active ingredients. Porella species contain terpenoid compounds (Fischer et al. 1995; Ludwiczuk et al. 2011). The secondary metabolic compounds produced by liverworts can resist or overcome a number of biotic and abiotic stresses such as predation, ultraviolet radiation, extreme temperatures and microbial decomposition (Xie and Lou 2009). In addition, some utilization of liverwort in modern medicine such as anti-leukemia and anti-cancer are promising outlook (Ludwiczuk and Asakawa 2008; Harris 2008). Marchantia polymorpha contains terpenoids, flavonoids, antifungal, antimicrobial, anti-inflammatory, antioxidative, marchantin A and C. Marchantin A and C have been demonstrated to exhibit multiple pharmacological activities such as antimicrobial activity against the gram positive bacterium Bacillus subtilis, as antioxidant, and induced the inhibition of cell growth in human breast cancer cells (Huang et al. 2009; Shen et al. 2010).

2.2.6 Household uses

Bryophytes are used for household such as for decorating, mattresses, pillows, dolls, packaging fruit and fragile objects for delivery, clothes decorating, buttons, fiber rugs, mats, blankets, and toilet paper (Glime 2007b). Bryophytes have been used for decorative purposes in Japan, England, France, Finland and America. The Himalayans also use bryophytes as insect repellents when storing foods. Dried mosses and liverworts were made into coarse powder and sprinkled over the grains and other things for storing in containers. Sphagnum is used for cushioning the foot and absorbing moisture and odors in hiking boots. Sphagnum is also used for sending or supplying live plants in India (Saxena and Harinder 2004).

2.3 Distribution of Liverworts

Liverworts are commonly found in moist and shaded areas, although some species are tolerant to drought. Liverworts are found in all environment except

marine ones, covering moist areas, creeks, rivers or periodically flooded areas. The majority of liverworts are terrestrial plant, the other are epiphytic and saxicolous plants (Gradstein et al. 2001).

Liverworts have wide distribution area (cosmopolitan) and abundant in the area of tropical rain forest. The abundance and diversity of liverworts increased with elevation. Diversity of liverworts in term of number of genera is highest in the submontane and lower montane forest. The species richness is highest in the upper montane forest (Gradstein et al. 2001).

The number of liverwort species also increase with addition of habitat number (especially epiphytic). Approximately 20% Marchantiophyta are as shaded epiphytes on primary forest and disappear on secondary forest or plantations and may be lost if the forest is opened (Gradstein et al. 2001).

Liverworts have a very wide distribution, due to their dispersal by spores that are easily blown by wind from low to high elevation and from one region to others. The spread of spores that can reach long distances, very important to make a new population in more distant places. Therefore, endemic species of liverwort is rare and lower than the seed plants. Liverworts have much larger geographical ranges than flowering plants (Korpelainen et al. 2005).

Liverworts are distributed throughout the world. The main distribution pattern in bryophyte followed Hyvonen (1989) are: 1) New Guinea or Western Melanesia: the whole island of New Guinea: west Sepik, East Sepik, Madang, Morobe, Enga, Western Highlands, Simbu, Eastern Highlands, Sothern Highlands, Gulf, Milne Bay, Papuan Islands, New Britain, New Ireland, Manus, and Bougenville; 2) Malesian Region: Indonesia, Malaysia, Singapore, Brunei, Sabah, Papua New Guinea (the Solomon Islands excluded), and Philippines. Papua New Guinea, and Philippines; 3) South East Asian: ranging from Asia 2 (China, Japan, Korea), Asia 3 (Bangladesh, Bhutan, Burma, Cambodia, India, Laos, Nepal, Pakistan, Sikkim, Thailand, Vietnam) to Asia 4 (Indonesia, Malaysia, Singapore, Brunei and Sabah, Papua New Guinea, and Philippines); 4) Asian-Oceanian-Australian: including Asian, Oceanian and Australian. This distribution tipe can be divided into 3 subgroups (Oceanian, Asian-Oceanian-Australian and Asian-Australian); 5) Transpacific: including area between America and Eastern Asia; 6) Paleotropical: widespread in all other tropical areas except America. This region includes tropical Africa, tropical Asia and the tropical Pasific region except for the Galapagos Islands and Cocos Island; 7) Pantropical: throughout the tropics and subtropics, from the southeastern USA to northern Argentina, futhermore in Africa, Macaronesia and along the coast of West Europe, and in Asia to Australia, New Zealand and Oceania; 8) southern hemisphere: the area restricted to the Southern Hemisphere, contains all or parts of five continents (Antarctica, Australia, apart of South America, the southern third of Africa, and some southern islands in Asia); 9) northern hemisphere: the northern hemisphere is the northern half of the earth, consists of all of Europe, North America and Asia, a portion of South America, two-thirds of the African continent and a very small portion of the Australian continent with islands in New Guinea; 10) miscellaneous: the species that cannot be included in any of geographical group mentioned are listed here; 11) widely distributed (cosmopolite): the distribution type is used for extremely widely distributed species.

3 METHODS

3.1 Study Sites

The study was conducted in the Mount Sibayak District Deli Serdang and Karo North Sumatra, approximately 52 to 65 km from Medan City. The area is located at 03°13'–03°18'20" N and 98°28'–98°37'20" E latitude, 870–2050 m altitude. Mount Sibayak is covered by tropical forest (13.680 ha). The common vegetation at mount Sibayak are Fagaceae, Lauraceae, Moraceae, Myrtaceae and Rubiaceae. Mount Sibayak has important functions as regulating the climate and hydrology of the area, cotourism, camping ground, research and environmental education. The maximum temperature in the afternoon is approximately 25°C, the minimum temperature at night is 13°C to 14°C, annual rainfall is 2400–2800 mm/year, and relative humidity is 80–90 %.

Topography of Mount Sibayak is commonly wavy to steep, and some areas are flat. The liverwort specimens were collected at seven study sites (Figure 1): 1) Sibolangit campground: ca. 870 m, a recreation area and for camping ground with open vegetation; 2) Jagawana: 880-980 m, has a primary forest and river, 3) Pasir Putih: ca. 856-935 m, has river, primary and secondary forest, and some area has been open; 4) Dwiwarna waterfall: ca.1027-1152 m, with primary forest; 5) Panatapan: ca.1250-1300 m, secondary forest; 6) Lau Debuk-debuk: ca. 1421-1572 m, has secondary forest, and planted areas; 7) Brastagi to the summit of Mount Sibayak: ca. 1421-2000 m, with primary forest and some open areas.

3. 2 Sampling Method

The exploration for collecting liverwort specimens was carried out in November 2011, April 2012, September 2012, October 2012, and June 2013. Survey explorations were carried out along the tracks in each study sites (one track for each location).

On each track, samples were taken at 10 m to the left and 10 m to the right of track. Sample collections were also carried along the river bank and around the waterfalls. Samples were collected used sharp knife from many substrats such as soils, tree trunks, rocks, rotten logs, and living leaves. For ephyphytes, samples were collected from the base to 2 meters of tree trunk height. The specimen collected were packed separately as much as possible, either in the field or directly after returning from the field when the specimens are still fresh – unless the species are too small to allow separation in the field.

Morphological characters in the field were observed used handlens 10-20 x magnification. Samples collected were put into paper envelopes, or small plastic bags. Each specimens received a collection number. All information gathered on the specimens were written in the field notebook. Characteristics of the living liverworts such as color, growth form were noted. The data recorded from habitat were: the kind of substrat, localities and altitudinal (measured using altimetre). GPS (Global Positioning System) was used for recording the coordinates of the collecting sites.

Specimens were cleaned as well as possible. In order to dry the samples, the envelopes containing leafy liverwort sample were opened and placed on a table or floor in a dry place without strong air currents. The envelope may also be packed in a broad weave sack or bag and hung in a well-ventilated area. Thalloid liverworts were pressed and the paper replaced daily. Some living samples were kept for studying the oil bodies, or to facilitate the observation of several characteristics, especially in Marchantia. For this purpose, a small portion of the sample were kept in plastic and kept cool (but not frozen) and examined under the microscope as soon as possible within a few days. Dried samples were placed into clean paper envelopes. Very small samples were placed in tiny paper envelopes and then placed into standard size herbarium envelopes to avoid loss of material (Gradstein 2011). The survey yielded about 900 specimens of liverworts, from 870 to 2000 m elevation. The specimens were deposited at Herbarium Bogoriense (BO), Herbarium of Biology Department University of Sumatra

Utara, herbarium of Biology Department Bogor Agricultural University, and Herbarium SEAMEO BIOTROP (BIOT).

3.3 Identification

Specimens collected were identified using both keys and descriptions from available taxonomic literatures, mainly Gradstein (2011), and other publications of Malesian and Tropical Asian liverworts, such as Mizutani (1961), Yamada (1979), Inoue (1984), Bishler-Causse (1989), Gradstein et al. (2002), Zhu and Gradstein (2005). Identification was done based on morphological characters using microscope in the laboratory of Plant Taxonomy, Biology Departement, Bogor Agricultural University. Specimens were observed, measured and used a camera for documentation of species.

Some important morphological characters were used in identification of liverworts were:

Thalloid liverworts:

1 Thallus: width, margin (colour, structure), median band.

2 Scales: appendage of median scales (length, width, structure of margin and apex, colour, marginal cells).

3 Cupules: ciliate lobes or ciliate (length of cilia, width of cilia basally).

4 Archegonium: archegoniophore (stalk length, colour of scales); receptacle (diameter, lobes shape apically, structure of dorsal surface, median projection, involucres position and colour).

Leafy liverworts:

1 Shoots: width, length. Shoot width is the width between opposite leaf apices. 2 Leaf lobes: arrangement, size, shape, base, margin, apex, trigones. Leaf length

is measured as the distance from the basal insertion of the leaf on the stem to the apex of the leaf lobe. Leaf width is measured parallel to the stem and is the distance from the apical insertion of the free margin of the lobule on the ventral lobe margin to the dorsal margin of the lobe.

Figure 2 Method of measurement in Thysananthus (Sukkharak 2015). A. Leaf, ventral view; d = dorsal leaf margin, f = lobule free margin, k = keel, l = leaf length, lb = lobule length, t1,2 = lobule teeth, u = auricle, v = ventral leaf margin, w = leaf width, wb = lobule width. B. Underleaf, ventral view; l = underleaf length, w = underleaf width. C. Perianth, ventral view; b = beak, l = perianth length, w = perianth width.

3 Leaf lobules: arrangement, size (wide, long), shape, base, margin, apex, keel, and teeth. Lobule length is the distance from the basal insertion of leaf on the stem to the apex of lobule. Lobule width is the widest distance from keel to free margin measured parallel to the stem (Fig. 2A).

4 Underleaves: size, margin, apex. Underleaf length is the distance from the mid-basal insertion of underleaf to the middle of apex. The width is arbitrarily chosen as the widest dimension of the underleaves (Fig. 2B).

5 Androecia: position on the shoots, bracts number

6 Archegonia: position on the shoots, bracts (number, size), perianth (size, shape, margin, apex). Female bracts were measured as leaves while bracteoles were measured as underleaves. Perianth length is the distance from the mid-basal insertion of perianth at the innovation to the base of the beak. Perianth width is arbitratily chosen as the widest distance of the perianth (Fig. 2C). Botanical terms used for liverworts in the study are in glossary.

3.4 Data Analysis 3.4.1 Diversity and distribution of species

1 Checklist of the species was conducted based on recently collected specimens of liverworts from Mount Sibayak and four addition specimens deposited in BO (collected from North Sumatra).

2 Distribution of species on substrate: all substrate of liverworts found were reported.

3 Local distribution: the occurence of species in the study site, the species diversity of study site were composed base on the number of species.

4 Altitudinal distribution: the altitudinal range based on Whitten et al. (1984): lowland forest (0–1200 m), lower montane forest (1200–2100 m), upper montane forest (2100–3000m), and sub alpine forest (more than 3000 m). 5 Geographical distribution: the distribution data of species were collected from

distribution note of the species in revision and floristic publications, such as Ariyanti and Gradstein (2007), Piippo (1994), Gradstein et al. (2002), Haerida et al. (2010), Inoue (1984), Kitagawa (1977), Kitagawa (1979), Lee (2013), Mizutani (1961), So (2001), So and Grolle (2000), Yamada (1979), Zhu and So (2001), Zhu and Gradstein (2005). The data were used to clarify species to the geographical distribution type prepared by Hyvonen (1989).

3.4.2 Taxonomic studies of particular taxa

The study were based on the recently collected specimens of particular taxa (Marchantia, subfamily Ptychanthoideae, Plagiochila and Radula) collected from Mount Sibayak and specimens collected from North Sumatra deposited in BO (Siregar et al. 2013, 2014). Descriptions, nomenclatures, and identification keys for each species of particular taxa occuring at the Mount Sibayak were provided. Descriptions were based on the morphological characters observed. Description and identification key of Marchantia modified from Bischler-Causse (1989); subfamily Ptychanthoideae followed Gradstein et al. (2002), Zhu and Gradstein (2005), Haerida et al. (2010), and Sukkharak (2015); Plagiochila followed Inoue (1984); Radula followed Yamada (1979).

4 RESULTS

4.1 Species Diversity and Distribution of Liverworts of Mount Sibayak There are 163 species of liverworts recorded from Mount Sibayak North Sumatra, belonging to 53 genera in 22 families. Twenty two species (13.5%) are new records for Sumatra (appendix 2). The largest family is Lejeuneaceae (49 species, 18 genera), followed by family Lepidoziaceae (26 species, 6 genera). The third largest family is Plagiochilaceae (21 species, 3 genera), followed by Radulaceae (14 species, 1 genus), Lophocoleaceae (12 species, 3 genera). The other families having less than 10 species (Table 1). The genera with the largest number of species were Plagiochila (18), followed by Bazzania (14), Radula (14), and Lejeunea (11). The genera with the smallest number of species wich has only having one species were Isotachis, Calypogaea, Cyathodium, Mastigophora, Pallavicinia, and Trichocolea (appendix 1).

Table 1 The number of families, genera, species, and new record species of liverworts in Mount Sibayak included in this study

The family with the greatest number of species at Mount Sibayak is Lejeuneaceae, similar to those reported from other mountains in Indonesia (Tan et al. 2006; Ariyanti and Gradstein 2007; Sporn et al. 2010; Gradstein and Culmsee

Families Number of genera

Number of species

Number of new record

Adelanthaceae 3 3 -

Aneuraceae 1 2 -

Balantiopsidaceae 1 1 -

Calypogeiaceae 1 1 -

Cephaloziaceae 2 2 -

Cyathodiaceae 1 1 -

Frullaniaceae 1 5 1

Geocalycaceae 2 3 -

Lejeuneaceae 18 49 8

Lepicoleaceae 1 2 1

Lepidoziaceae 6 26 5

Lophocoleaceae 3 12 1

Marchantiaceae 2 8 1

Mastigophoraceae 1 1 -

Metzgeriaceae 1 2 -

Pallaviciniaceae 1 1 -

Plagiochilaceae 3 21 2

Radulaceae 1 14 3

Scapaniaceae 1 2 -

Schistochilaceae 1 2 -

Solenostomataceae 1 4 -

Trichocoleaceae 1 1 -

2010; Gradstein et al. 2010; Haerida and Gradstein 2011). This apparently due to the large number of taxa in the family. Lejeuneaceae is the largest family of liverworts, containing about 1700 species in 81 genera (He and Zhu 2011). Futhermore, the family prefer the moist and semi shaded to shaded places, and also lives on various substrates (oligophotic habitats) as small trees and shurbs, living leaves, decaying wood and the ground surface (Gradstein and Pocs 1989). The habitat preferred of the family are also at Mount Sibayak, and it is supporting the presence of Lejeuneaceae in the region.

4.1.1 Local distribution

The number of liverworts at each location of Mount Sibayak is shown in Table 2. Jagawana has the richest species (109 species), and followed by Pasir Putih (74 species). The third richest location is Brastagi (70 species). The area was at lower montane zone, and generally have natural vegetation. The open area is only at the summit track. The location with the smallest number of species is Lau Debuk-debuk (6 species). This location is mostly under cultivation and most forests have been opened. Marchantia polymorpha as one of new record species was only found on rocks of creek wall at this location.

4.1.2 Substrates

The liverworts at Mount Sibayak grow on various substrates (appendix 1). Most of the species (127 species) are epiphytes (grow on bark or branch of trees and shrubs), 8 species are epilith (grow on rocks), 8 species are terrestrial (grow on soil), 6 species are on rotten logs, 2 species are epiphyll (grow on living leaves), and only one is aqutic (appendix 1). Some of epiphytic species can grow on other substrates such as living leaves, rotten logs, soil or rock. They are Bazzania densa (on bark and rotten logs), Chiloscyphus kurzii (bark and soil), Cololejeunea haskarliana (on bark and living leaves), and Kurzia gonyotricha (on bark and rock). Some species were found as epiphyllous and also grow as epiphytic, such as Cheilolejeunea ceylanica, Ch. longiloba, Co. haskarliana, and Lejeunea patersonii.

Some species have broad substrate preferences, such as Heteroscyphus coalitus (barks, rotten logs, rocks, and soils), H. argutus (barks, rotten logs, and Tabel 2 Number of species based on location of liverworts at Mount Sibayak

North Sumatra

Locations Number of species

Altitudes (m asl) Habitat types

Jagawana 109 880-980 primary forest

Pasir putih 74 856-935 primary,

secondary & open

Brastagi 70 1421-2000 primary & open

Panatapan 52 1250-1300 secondary forest

Dwiwarna waterfall 42 1027-1152 primary forest

Sibolangit campground

33 870-890 open habitat

soils), Calypogaea arguta (barks, rocks and soils), Cheilolejeunea ceylanica (bark, living leaves, and rotten logs). The others species have narrower preferences and occured on one substrate type, for example: Drepanolejeunea levicornua and D. thwaitesiana were occuring only as epiphyllous. Chiloscyphus propagulifer, H. wettsteini, Riccardia subexalata, Schiffneria hyalina, Solenostoma ariadne, and S. haskarlianum were occuring only on soil. Solenostoma tetragonum was found on soil and also grew in the water. Solenostoma tetragonum was the only species occuring in the water at Dwiwarna waterfall. Some species were found only on rock: Conoscyphus trapezioides, Lepicolea javanica, Marchantia polymorpha, Scapania javanica, Sc. rigida, Ra. lingulata, Ri. crenulata, and Ra. amoena. Some species of Lejeuneaceae at Mount Sibayak are epiphytes, sometimes grow on rotten log, Caudalejeunea reniloba, Ceratolejeunea belangeriana, Cheilolejeunea meyeniana, Colura acroloba, Diplasiolejeunea cavifolia, Lejeunea exilis, and Lepidolejeunea bidentula.

4.1.3 Altitudinal and geographical distribution

Based on altitudinal distribution, most of the species of Mount Sibayak (79 species) have a wide altitudinal range, from lowland forest (0–1200 m) to lower montane forest (1200–2100 m). Sixty seven species are restricted to lowland forest and 17 species are restricted to lower montane forest (Table 3).

Table 3 Number of liverworts species based on geographical and altitudinal distribution type at Mount Sibayak. L: lowland forest, LM: lower montane forest

Based on the geographical distribution type of liverworts followed Hyvonen (1989), the liverworts of Mount Sibayak can be divided into ten distribution group (Table 3): cosmopolite (widely distributed), pantropical (throughout the tropics), paleotropical (tropical area, except America), Asian-Oceanian (ranging from Asian to Ocean), Asian-Oceanian-Australian (ranging from Asia to Ocean to Australia), Asian-Australian, (ranging from Asia to Australia), South East Asia (ranging from Asia 2 to Asia 4), malesian (corresponding to Asia 4), endemic

Distribution type

No. of species

Percentage (%)

No. of species based on altitude

L LM L & LM

Southeast Asia 55 34.16 22 9 24

Malesian 30 18.63 16 2 12

Asian-Oceanian 25 15.53 8 2 15

Asian-Oceanian-Australian

17 9.94 9 1 7

Paleotropical 14 8.70 4 2 8

Pantropical 13 8.07 3 0 10

Miscellaneous 4 2.48 1 1 2

Asian-Australian

2 1.24 2 0 0

Endemic 1 0.62 0 0 1

Cosmopolite 1 0.62 1 0 0

(Sumatra only), and miscellaneous (cannot be included in any of geographical group mentioned). Asia 2: China, Japan and Korea; Asia 3: Bangladesh, Bhutan, Burma, Cambodia, India, Laos, Nepal, Pakistan, Sikkim, Thailand, Vietnam; Asia 4: Indonesia, Malaysia, Singapore, Brunei, Sabah, Papua New Guinea and Philippines.

4.2 The genus Marchantia (Marchantiaceae) of Mount Sibayak

There are seven species of Marchantia found in Mount Sibayak, North Sumatra, namely M. acaulis, M. emarginata, M. geminata, M. paleacea, M.

polymorpha, M. treubii and Marchantia sp. Marchantia polymorpha is new

record for Sumatra. Marchantia acaulis and M. geminata are common species at Mount Sibayak.

4.2.1 Key to species of Marchantia of Mount Sibayak and the species recorded from Sumatra:

1. Thallus margin crenulate; scales over almost entire ventral surface of thallus, reaching the thallus margin, sometimes visible at the margin in dorsal view; lobes of female receptacle terete...5. M. polymorpha 1. Thallus margin entire; scales only along thallus midline of ventral surface,

invisible in dorsal view; lobes of female receptacle flat apically...2 2. Cupules with ciliate lobes and densely papillose on outer surface

...4. M. paleacea 2. Cupules ciliate, no or few papillae on outer surface... 3 3. Thallus more than 5 mm wide. Involucres ciliate ...M. miqueliana* 3. Thallus as wide as or less than 5 mm wide. Involucres not ciliate...4 4. Compact ventral tisssue of thallus with numerous mucilage cavities per section. Involuces are almost as long as or longer than lobes...5 4 Compact ventral tisssue of thallus without or with 1–3 mucilage cavities per

section. Involucres are shorter than lobes ...6 5 Appendage of median scales length: width ratio = 1.1–1.5 : 1; margins sharply toothed. Male receptacles sessile or nearly so...1. M. acaulis 5 Appendage of median scales length: width ratio = 1.5–2.4 : 1; margins nearly

entire to bluntly toothed. Male receptacle with distinctly stalked...M. wallisii* 6 Appendages of median scales acute or acuminate with row of 2–3 cells

apically...7 6 Appendages of median scales rounded or obtuse with single cell apically

...7. Marchantia sp. 7 Appendage of median scales toothed, the teeth mostly consisting of 2–3 cells and often recurved towards base of appendage. Lobe of female receptacle emarginate or truncate apically...2. M. emarginata 7 Appendage of median scales entire or toothed, the teeth mostly unicellular and

oriented obliquely towards apex of appendages. Lobes of female receptacle split apically...8 8 Appendage of median scales yellow with orange or purplish borders, ovate. Number of female lobes usually 4...3. M. geminata

8 Appendage of median scales purple, narrowly triangular. Number of female lobes variable 3–6...6. M. treubii * The species was reported from Sumatra, but it was not found and described in

this study.

4.2.2 Species description 1 Marchantia acaulis Steph.

Spec. Hepat.1: 195. 1899; Bischl. Bryophyt. Biblioth. 38: 270. 1989.

Thallus light, yellowish or bright green, with dark median band on dorsal surface, 2-4 mm wide. Margin entire, sometimes slightly crisped, hyaline or purplish, 2-3 cells wide. Epidermal pores 50-70 µm in diameter; inner opening bordered by cells with usually nearly straight (rarely convex) inner walls; mucilage cavities numerous per section, located mostly directly underneath the assimilatory layer. Ventral surface purplish, at least in median portion; scales in 4 rows extending about 30-60 % of thallus width. Median scales purplish. Appendages yellow; ovate; rounded basally; apex acute, with row of 1-2 (3) cells; margin toothed; teeth sharp, with long axis oblique to margins; marginal cells 2.5-4.5 times smaller than inner cells. Laminal scales purplish; ovate; apex obtuse or rounded; oil cells absent.

Archegoniophore at apex of main thallus. Stalk 3-8 mm long; scales reddish or purplish. Scales surrounding base of stalk similar to median scales of thallus, or with acuminate appendage. Receptacle 2-4 mm in diameter, dissected (0.4-0.6) of diameter into 4 lobes split apically to 0.2 of their length; asymmetric; dorsal surface without median projection. Involucres hyaline or purplish, entire or crenulate. Scales of receptacle purplish or reddish. Spore brown.

Antheridiophore at apex of main thallus, sometimes there are antheridium and archegonium on one thallus. Receptacles sessile or nearly so (seldom with stalk); scales purple. Scales surrounding base of stalk similar similar to median scales of thallus, or with acuminate appendage. Receptacle palmate, 4.5-7 mm in diameter, deeply dissected (0.4-0.8 of diameter) into 3-5 rays; asymmetric; dorsal surface usually with papillae. Rays with slightly crenulate margins; marginal cells small. Median scales of ventral surface of rays reddish or purplish, 3-5 cells wide with row 1-2 cells apically.

Ecology: found abundant on soil or rocks in open place or semi shaded place from 870 to 900 m altitude.

Distribution: Sumatra, Java, Borneo, Sulawesi, Malaysia, Singapore, Philippines, Sri Lanka (Burgeff, 1943; Bischler-Causse-Causse 1989; Piippo et al. 2002; Chuah-Petiot 2011).

Specimens examined: Mt. Sibayak, Etti Siregar 02, 03, 33, 102, 587, 589, 592, 594, 914, 1426, 1428; Etti Siregar & Nunik S Ariyanti 1517, 1519, 1526, 1753.

Note: Marchantia acaulis is similar to M. geminata, but the latter species has a distinctly stalked male receptacles, thallus without large cavities, and longer appendage of median scales. Marchantia acaulis is easy recognized by the male receptacle without stalk, the large and numerous mucilage cavities in compact ventral tissue in the thallus and the yellowish appendage of median scales. Thallus always with dark median band on dorsal surface, however Bischler-Causse (1989) have found some specimens without median band on dorsal surface. Antheridium

and archegonium sometimes were found on the same thallus (monoecious) but male rays are never found on the female receptacles as the description by Bischler-Causse (1989). Lobes of female receptacle sometimes curved up when mature.

2 Marchantia emarginata Reinw., Blume et Nees.

Nova Acta Phys. Med. Acad. Caes. Leop.-Carol. Nat. Cur. 12: 192. 1824. Bischl. Bryophyt. Biblioth. 38: 181.1989.

Thallus narrow, ribbon like; light, yellowish, dull or dark green, with indistinct to distinct median band on dorsal surface; 2.5-5 mm wide. Margin entire, hyaline, reddish or purplish, 2-4 cells wide; thick walled; marrginal cell smaller than inner cells. Epidermal cell without papillae. Epidermal pores not cruciate, 40-80 µm in diameter, bordered by 4-7 (8) rings of cells; inner opening bordered by cells with straight or convex inner walls; mucilage cavities absent or sometimes present in compact ventral tissue of thallus. Ventral surface purplish or brown, at least in median portion; scales in 4 rows extending about 25 to 50 % of thallus width. Median scales reddish or purplish; oil cells scattered. Appendages purplish, sometimes light red or pale brown; ovate; 5-16 (20) cells wide; apex acute or apiculate, with 1-3 cells apically; margin with sharp toothed, 1-2 (3) cells long, often curved towards base of appendage; terminal cells often lighter in colour, area (1-2.5) times smaller than that of inner cells (indistinctly smaller than inner cells). Laminal scales purplish, light red or sometimes hyaline; ovate to orbicular; apex acute or obtuse; oil cells sometimes frequent.

Cupules ciliate; cilia 1-4 cells long, 1-2 cell basally; without papillae on outer surface.

Archegoniophore at apex of main thallus. Stalk 5-14 mm long; scales purplish or light red. Scales surrounding base of stalk with appendage similar to those of median scale or with acuminate appendage. Receptacle with distinct to indistinct rounded median projection on dorsal surface; 3.5-5 mm in diameter, deeply divided (0.7-0.9) of diameter into 5-11 lobes; nearly symmetric or asymmetric; lobe convex basally, usually broadened, twice emarginate, truncate or sometimes rounded apically; the lobe opposite the basal sinus often wider than the others. Involucres hyaline, entire. Scales of receptacle purplish or somestimes light red or hyaline, lobed or toothed, seldom entire, 3-16 cells wide; apex with row of 3-7 cells. Spores light brown or brown.

Antheridiophore at apex of thallus. Stalk 5-14 mm long; scales purplish, sometimes hyaline. Scales surrounding base of stalk not differentiated, or with long acuminate appendage. Receptacle palmate, 4-7 mm in diameter, deeply dissected (0.5-0.7 of diameter) into 5-7 rays; asymmetric. Rays with entire or slightly crenulate margins; marginal cells smaller or hardly smaller tahn inner cells. Median scales of ventral surface of rays purplish, sometimes hyaline, with acute appendage, 2-6 cells wide with row of 1-3 cells apically.

Ecology: found on soils, rocks (moist, damp or wet, shaded, semi exposed places, riversides, creeks) from 870 to 1450 m altitude.

Distribution: Japan, Korea, China, India, Sri Lanka, Andaman and Nicobar Island, Thailand, Malaysia, Sumatra, Java, Borneo, Lesser Sunda Island, Bali, Moluccas, West Irian, Philippines, Marianas, Guam, New Guinea, New Britain,

Solomon Island (Bischler-Causse 1989; Bischler-Causse and Piippo 1991; Song 2006; Lai et al. 2008; Chuah-Petiot 2011; Singh and Singh 2012).

Specimens examined: Mt. Sibayak, Etti Siregar 31, 47, 70, 112, 134, 219, 367, 374, 375, 380, 460, 462, 463, 465, 467, 468, 473, 475, 476, 593, 599, 608, 757, 760, 863, 868, 1427; Etti Siregar & Nunik S Ariyanti 1445, 1447, 1520, 1524, 1794, 1826. Sibolangit-North Sumatra, Lorzing 12707 (BO).

Note: this species shows wide variations in thallus and female receptacles. Thallus can be without or with median band on dorsal side, small to medium size, margins purplish, reddish, or sometimes hyaline. Female receptacles are often curved toward stalk, sometimes straight; lobes varies from (5–13); dorsal surface flat or with indistinct to distinct rounded median projection, slightly asymetric to symmetric. Apex of receptacle lobes varies from emarginate, truncate or sometimes rounded. Female receptacles with or without a rounded median projection on dorsal side (Figure 3).

Figure 3 Variations of female receptacle in M. emarginata. A. Plant with indistinct rounded median projection on dorsal side of female receptacle; a= female receptacle, dorsal view. B. Plant with distinct rounded median projection on dorsal side of female receptacle; b= female receptacle.

3 Marchantia geminata Reinw., Blume et Nees.

Nova Acta Phys. Med. Acad. Caes. Leop. Carol. Nat. Cur. 12:194. 1824; Bischl. Bryophyt. Biblioth. 38: 261. 1989.

Thallus bright green or dark green, with median distinct band on dorsal surface, 3-6 mm wide. Margin entire, reddish or purplish, sometimes hyaline, 3-4 cells wide. Epidermal pores bordered by 6-8 cells; inner opening bordered by cells with convex inner walls; mucilage cavities present in compact ventral tissue. Ventral surface purplish, at least in median portion; scales in 4 rows extending about 30-40 % of thallus width. Median scales purplish. Appendages yellow with orange or purplish borders; ovate and acuminate, sometimes acute or obtuse; rounded basally; with1 (2-3) cells in single row apically; margin irregularly crenulate or toothed, with unicellular or sometimes pluricellular, sharp teeth. Laminal scales purplish or light red; ovate; apex acute, obtuse or rounded; oil cells absent. Cupules not seen.

Specific character: leaf apex narrow

and strongly reflexed

Distribution: Java, Borneo, Sulawesi,

PNG, Solomon Is., Australia.

a=leaf-lobe

Specific

characters:

leaf-lobe

divided into 2-3 simple hairs

like-lobe without lamina.

Distribution:

Java,

Borneo,

Malaya, Philippines, China, Japan.

Kurzia lineariloba

a=leaf-lobe

Specific characters: leaf-lobes linier,

composed of 2-4 uniseriate cells.

Distribution: endemic to Borneo

K. longicaulis

Specific

character:

leaf-lobe

composed of 7-8 uniseriate cells

Distribution: endemic to New

Guinea

Lejeunea cocoes

Specific characters:leaf often caducous,

apex obtuse to rounded, underleaves

distant.

Distribution: Java, Malaysia, PNG,

China

L. obscura

Specific characters: leaves not

caducous, lobules often reduce.

Distribution: Java, China, India, Sri

Lanka, Nepal

Lepicolea rara

Specific characters: leaves of main stem

4-lobed, margin ciliate.

Lepidozia haskarliana

Specific

characters:

leaves

obliquely spreading, asymmetric

Distribution: Java, Borneo, Sulawesi,

Moluccas, Malay Peninsula, Thailand,

PNG,

Philippines,

Solomon

Is.,

Oceanic, America.

Distribution: Java, Borneo.

Lepidozia trichodes

A= leaf-lobe

Specific

characters:

leaves

subrectangular,

deeply

lobed

Distribution: Malay Peninsula, Java,

Amboina, Borneo, Philippines, Tahiti.

Marchantia polymorpha

a= female receptacle

Specific

character:

female

receptacle with 10-11 terete rays.

Distribution: Turkey, Syria, Iraq,

Iran, Lebanon, Israel, Russia,

Uzbekistan, Tadzhikistan, Pakistan,

Afghanistan, India, Sri Lanka,

Nepal, Bhutan, China, Taiwan,

Korea, Japan, Thailand, Vietnam,

Malaysia, Java, PNG, Philippines,

New Zealand, Tasmania

Mastigolejeunea virens

Specific character: apex of leaf lobule

with one long tooth consisting of 5–6

cells.

Distribution: Java, Borneo, Moluccas,

Peninsular Malaysia, Papua New

Guinea, Philippines, Thailand, Sri

Lanka, Pacific Is., Australia.

Plagiochila gracilis

Specific characters: leaf apex

rounded, with 2–4 teeth wich two

are often prominent.

Distribution: India, Buthan, Nepal,

Sri Lanka, China, Japan, Taiwan,

Thailand, Philippines, Java.

P. laxissima

Specific characters: leaves

liniear-oblong, teeth on leaves margin

restricted to the apex.

Distribution:Java, Malaysia, Philippines

Radula lingulata

a=leaf-lobe, b=lobule

Specific characters: lobules narrow

lingulate, parallel with the stem.

Distribution: Java, New Guinea,

Fiji

R. loriana

Specific characters: branched regularly

dichotomous, leaf-lobes narrow

obovate to elliptical.

Distribution: Papua New Guinea,

Solomon Islands, Queensland

R. reflexa

a=leaf-lobule

Specific character: leaf-lobules

strongly recurved from the upper

2/3 of adaxial margin to apex

Distribution:

Taiwan,

Borneo,

Ceram Island, Papua New Guinea

Schiffneriolejeunea tumida

Specific characters: margin of leaf

rolled inwards along ventral and apical

margin

Distribution:West Irian, PNG,Thailand,

Solomon Is.

Thysananthus retusus

Specific

character:

apex

of

underleaves retuse.

Distribution: Java, West Irian,

PNG,

Philippines,

Thailand,

Pacific Is., Solomon Is., Australia.

Appendix 3. Glossary

Abaxial. The side of a leaf away from the stem; the lower side of the leaf (opposite of adaxial)

Androecium (plur. androecia). Antheridia and surrounding bract; the male gametoecium Antheridiophore. Stalked, antheridia-bearing receptacle on the thallus of the Marchantiaceae.

Appressed. Lying closely together, leaves lying close or flat against the stem.

Antheridium (plur. antheridia). Male sex organ or gametangium, producing antherozoids (=spermatozoids).

Archegoniophore. Stalked, archegonia-bearing receptacle on the thallus of many complex thalloid liverworts.

Archegonium (plur. archegonia). Female sex organ or gametangium, containing an egg Androecium (plur.androecia). Antheridia and surrounding bract; the male gametoecium. Autoicous (=autoecious). With archegonia and antheridia on the same plant, but on separate shoots (when on the same shoot: paroicous).

Bracts. Specialized leaves surrounding reproductive organs. Bracteole. A modified underleaf associated with a gametangium. Caducous. Falling of.

Ciliate. With hair-like appendages

Collar. Sheath of tissue around the base of branches in leafy liverworts. Confluent. Blending of two structures into one.

Contiguous. Adjacent.

Convex. Bulging outwards (opposed to concave). Convolute. Rolled together.

Cordate. Heart-shaped.

Crenulate. With minute, rounded teeth.

Crisped (=crispate). Strongly wavy; variously curled, twisted and contorted.

Decurrent. Extending down the stem. Of leaf bases, extending downwards beyond the leaf insertion.

Dendroid. Tree-like; with erect stems that are branched only in the upper part on all

sides, the lower, unbranched part forming the “trunk”.

Disciform. Flat and circular.

Distal. Away from the base or point of attachment; toward the apex of a leaf or stem (opposite of proximal).

Dioicous (=dioecious). With archegonia and antheridia on separate plants. Dorsal. The upper surface, away from the substrate (opposed to ventral). Emarginate. Having a broad and shallow notch at the apex

Falcate. Curved like the blade of a sickle.

Frullania-type branched. Branch originating from a ventral leaf initial cell so that it replaces the ventral half of a leaf; the branch is therefore associated with a half leaf on its dorsal side.

Gemmae (sing. gemma). Small structure for vegetative reproduction, usually consisting of one or few cells only and developing on leaves or thallus.

Gemma cup. Cup-shaped, gemmae containing structure.

Gynoecium (plur. gynoecia). Archegonia and the surrounding bracts; the female gametoecium.

Imbricate. Overlapping, like shingles on a roof.

Innovation. A branch formed at the base of the perianth or inner female bract. Intercalary. Intermediate in position, somewhere below the apex.

Intercalary branch. Branch originating from the inside of stem, away from the apex, usually having a collar at the base.

Involucre. A structure, usually tubular or scale-like, surrounding the gametangia or the developing sporophyte; also, the bracts (and bracteoles) of the gynoecium.

Involute. Rolled upward (adaxially) and tightly inward. Keel. A fold.

Keeled. Folded along the middle, like the keel of a boat.

Lingulate. Tongue-shaped, oblong below, broader toward the apex. Lobe. A segment of a leaf, larger than a tooth.

Lobule. A small lobe; e.g., the smaller segment of a bilobed leaf that is positioned on top of or below the large lobe.

Merophyte. A segment cut off from the apical cell and the tissues and organs derived from it. A mature merophyte consist of one leaf and associated stem tissue.

Nodulose. With large, swollen wall thickenings. Obovate. Egg-shaped with apex broader than base.

Ocellus (plur. ocelli).A specialized cell in the leaves (and perianth) of some members of Frullania and Lejeuneaceae, having one large oil body and lacking chloroplasts.

Paraphyllia (sing. paraphyllium). Small, green outgrowths of stems, much smaller than leaves and of various shapes, i.e., filiform lanceolate etc.

Perianth. Organ of foliar origin enclosing the developing sporophyte in leafy liverworts. Receptacle. A swollen, disc-like structure bearing antheridia or archegonia in thalloid liverworts.

Recurved. Curved downward (abaxally) and inward (opposed to incurved)

Retuse. Having a narrow, shallow indentation in a broad, rounded apex (opposed to emarginate)

Rhizoid. A root like hair that functions as anchorage Shoot. General term for stem or branch.

Sinus. The depression separating two segments or lobes. Sinuate (=sinuose). wavy

Spathulate. Tapering to the base from a broad, rounded apex. Terete. Smooth-cylindrical, without keels, rounded in cross section.

Terminal branch. A branch formed at the stem apex; the branch is often associated with a half-leaf and has no collar at its base (opposed to intercalary branch).

Thallus (plur.thalli).Faflattened plant body; not differentiated into stems and leaves. Trigone. Thickening at the corners of cells.

Uniseriate. In one row

Vitta. Longitudinal band of elongate, often thicker-walled cells in leaf, resembling a nerve but only one cell layer thick.

CURRICULUM VITAE

Etti Sartina Siregar was born on 21 November 1972 in South Tapanuli

North Sumatra , as the fifth child from six children of Mr. M. Syafii Siregar and

Mrs. Kani Harahap. She graduated from Biology Department at Andalas

University in 1996. She studied plant taxonomy and obtained master degree of

Biology from the Department of Biology IPB in 2004. In 2010, she was awarded

scholarship for study at doctoral program at Plant Biology Major, Departement of

Biology, Bogor Agricultural University from Directorate General of Higher

Education, National Education Departement (BPPS DIKTI). She was employed as

a lecturer at the Department of Biology Faculty of Science and Mathematics

University of Sumatra Utara since 1998.