Artabotrys (Annonacea) in East Malesia

ARTABOTRYS (ANNONACEAE) IN EAST MALESIA

TRIASTINURMIATININGSIH

THE POST GRADUATE PROGRAM
BOGOR AGRICULTURAL UNIVERSITY
2007

LETTER OF STATEMENT

I express that thesis entitling

:

ARTABOTRYS (ANNONACEAE) IN EAST MALESIA
is true represent result of my research and have never been published before. All
information and data that used have been expressed clearly and can be checked its
Truth.

ABSTRAK

Penelitian taksonomi marga Artabotrys

di Malesia Timur dilakukan

berdasarkan pada ciri-ciri morfologi spesimen herbarium dari Herbarium
Bogoriense (BO), Herbarium Celebense (CEB), Herbarium Manokwari (MAN),
National Herbarium of Papua New Guinea (LAE) dan koleksi hidup di Kebun
Raya Bogor. Hasil penelitian menunjukkan terdapat 13 jenis, 9 jenis diantaranya
telah dikenal sebelumnya yaitu A. camptopetala Diels, A. gracilis King,
A. hexapetalus (L.f.) Bhandari, A. inodorus Zipp., A. macranthus Holthuis,
A. speciosus Kurz., A. suaveolens Blume, A. sumatranus Miq., dan A. venustus
King. Empat jenis lainnya diusulkan sebagai jenis baru yaitu A. desmidantha
Diels ex Triasti., A. longipetalus Triasti., A. palmatiflorus Triasti. dan A.
trichofolius Triasti.. Kunci identifikasi dan deskripsi dari masing- masing jenis
telah dibuat. Artabotrys suaveolens mempunyai persebaran yang luas sedangkan
A.camptopetala, A. desmidantha, A. longipetalus, A. inodorus, A. palmatiflorus
dan A. trichofolius persebarannya terbatas. New Guinea merupakan kawasan yang
paling tinggi keanekaragaman jenisnya di Malesia Timur.
Analisa hubungan kekerabatan dengan Cyathocalyx sumatranus sebagai
outgroup menghasilkan satu kladogram parsimony dengan panjang 26 langkah

dan menunjukkan 3 kelompok besar. Kelompok I adalah Cyathocalyx
sumatranus, kelompok kedua adalah Artabotrys macranthus yang paling dekat
dengan outgroupnya. Sedangkan kelompok III disatukan oleh karakter
synapomorf no 2

(panjang daun), 3(hook), 11(bentuk daun buah), 14(jumlah

bakal biji) dan 15 (letak biji).
Kata Kunci : Artabotrys, Annonaceae, Malesia Timur, Analisis filogenetik.

ABSTRACT

Studies on the taxonomy of the genus Artabotrys R. Br. ( Annonaeceae )
in East Malesia were based on morphological characters by examining a large
number of Herbarium Bogoriense (BO), Celebense (CEB), Manokwari (MAN),
Departemen of Forest Lae (LAE) and living plants of Bogor Botanical Garden.
There are eight species which have been known previously: A. camptopetala
Diels, A. gracilis King.,

A. hexapetalus (L.f.) Bhandari, A. inodorus Zipp.,

A. macranthus Holthuis, A. speciosus Kurz., A. suaveolens Blume, A. sumatranus
Miq. and A. venustus King. Four new species are proposed in this treatment : A.
desmidantha Diels ex Triasti., A. longipetalus Triasti., A. palmatiflorus Triasti.,
and A. trichofolius Triasti.. An identification key and detailed discription are
provided for taxa. Artabotrys suaveolens Blume is widely distributed. While
A. camptopetala, A. desmidantha, A. longipetalus, A. inodorus, A. palmatiflorus
and A. trichofolius have a limited distribution. New Guinea is the area with the
highest diversity of Artabotrys species in East Malesia.
A phylogenetic analysis with Cyathocalyx sumatranus as outgroup, shows
three major groups. The first group is Cyatocalyx sumatranus. The second group
is A. macranthus which has the closest relationship with the outgroup. The third
group separated from the other group by the synapomorph characters 2 (leaf
length), 3 (hook), 11 (carpel shape), 14 (number of ovule) and 15 (position of
seed).
Keyword: Artabotrys, Annonaceae, East Malesian, phylogenetic analysis

ARTABOTRYS (ANNONACEAE) IN EAST MALESIA

TRIASTINURMIATININGSIH

Thesis submitted
As partial fulfillment requireme nt for the Master Degree
In Plant Taxonomy

THE POST GRADUATE PROGRAM
BOGOR AGRICULTURAL UNIVERSITY
2007

Title

: Artabotrys (Annonacea) in East Malesia

Name

: Triastinurmiatiningsih

Reg. Number

: G351040041

Certified by
Supervisor Committee

Dr. Sri Sudarmiyati Tjitrosoedirdjo, M. Sc.

Dr. Rugayah, M. Sc.

Chairman

Member

Acknowledged by

Head of Study Program of Biology

Dr. Ir. Dedi Duryadi Solihin, DEA

Date of graduation :

Dean of Graduate School

Prof. Dr. Ir. Khairil Anwar Notodiputro, M.Sc.

Examination Date : 12 January 2007

1

CURRICULUM VITAE
The author was born in Ngawi on 22th January 1969. The third daughter
from four children of Mr. Soebari and Mrs. Pudji Asti
She passed her Elementary School (SD) in 1981, Junior High School
(SMP) in 1984 and Senior High School (SMA) in 1987, all in Ngawi. She
attended the Faculty of Biology, Gadjah Mada University, Yogyakarta and
graduated in 1992.
Since 1994 she was employed by Department of Biology, Faculty of
Mathematic and Natural Science, Pakuan

University (UNPAK), Bogor as

candidate and promoted as lecturer in 1995.
In 2004 she received Post Graduate Education Schoolarship (BPPS) from
Director of high education (DIKTI) and UNPAK, Bogor to continue her study at
the Bogor Institute of Agriculture (IPB) at the majoring on plant taxonomy.

2

ACKNOWLEDGEMENT

The author realizes that this thesis will never be completed without
assistance of many colleagues and friends who have contributed in various ways.
I would like thank to Dr. Sri Sudarmiyati Tjitrosoedirdjo and Dr. Rugayah

for

their valuable advices and guidance in completing the thesis. I am grateful to
DIKTI and UNPAK Bo gor for the financial support for a master degree at the
graduate school IPB.
I would like to express my gratitude to Dr. Eko Baroto Waluyo Head of
the Herbarium Bogoriense (BO) and to other Herbaria: National Herbarium of

Papua New Guinea (LAE), Herbarium Celebense (CEB) and Herbarium
Manokwari (MAN) for grating me to examine their specimens for studies. In
particulary I am grateful to Prof. Dr. Soedodo Hardjoamidjojo Head of UNPAK
Bogor; Dr. Khairil Anwar Notodiputro Director of Graduate School Bogor
Agricultural university; Dr. Dedi Duryadi Program coordinator of the biology
program studies, Prof. Dr. Mien A. Rifai Program coordinator taxonomy sub
program studies.
I am also very grateful to Nunik Sri Ariyanti M.Si. for her interest ,
discussions and valuable comments on the manuscript. Bilal, Nida and Asti for
helping me in the fields. I would like to thanks Mr. Soebari and Mr. Affandi for
his excellent drawing; Miss. Rina, Mr. Sutijono and all of the librarian staff of the
Herbarium Bogoriense, for provid ing me with the pertinent literature. My special
thank go to my husband, my children, my parents, my brother ,my sister and all
my family for their spirit, patience and moral support during the conduct of my
studies.

ix

TABLE OF CONTENTS
LIST OF TABLES ........................................................................................... x

LIST OF FIGURE............................................................................................ xi
INTRODUCTION ............................................................................................ 1
MATERIAL AND METHODS ........................................................................ 3
Exploration............................................................................................ 3
Morphology........................................................................................... 3
Revision ................................................................................................ 3
Phylogenetic analysis ............................................................................ 3
RESULT AND DISCUSSION ......................................................................... 4
Morphology .......................................................................................... 4
Distribution .......................................................................................... 7
Phylogenetic analysis ............................................................................ 9
Taxonomy ........................................................................................... 12
Generic description................................................................. 12
Key to the Species................................................................... 13
Species description.................................................................. 14
1. A. camptopetala Diels ....................................................... 14
2. A. desmidantha Diels ex Triasti. ...................................... 15
3. A. gracilis King ................................................................ 16
4. A. hexapetalus (L.f.) Bhandari ......................................... 17
5. A. inodorus Zipp. ............................................................ 17

6. A. longipetalus Triasti. ..................................................... 18
7. A. macranthus Holthuis ................................................... 19
8. A. palmatiflorus Triasti. .................................................... 28
9. A. speciosus Kurz.............................................................. 28
10. A. suaveolens Blume ......................................................... 29
11. A. sumatranus Miq............................................................ 30
12. A. trichofolius Triasti. ....................................................... 31
13. A. venustus King ............................................................... 32
CONCLUSION............................................................................................... 40
REFERENCES ............................................................................................... 41

x

LIST OF TABLE

Table

Page

1. Distribution of Artabotrys in East Malesia and the other place in

Malesia ......................................................................................................8
2. Morphological characters and character states used in phylogenetic
Analysis.....................................................................................................9
3. Matrix of morphological characters at the taxa ......................................10

ARTABOTRYS (ANNONACEAE) IN EAST MALESIA

TRIASTINURMIATININGSIH

THE POST GRADUATE PROGRAM
BOGOR AGRICULTURAL UNIVERSITY
2007

LETTER OF STATEMENT

I express that thesis entitling

:

ARTABOTRYS (ANNONACEAE) IN EAST MALESIA
is true represent result of my research and have never been published before. All
information and data that used have been expressed clearly and can be checked its
Truth.

ABSTRAK

Penelitian taksonomi marga Artabotrys

di Malesia Timur dilakukan

berdasarkan pada ciri-ciri morfologi spesimen herbarium dari Herbarium
Bogoriense (BO), Herbarium Celebense (CEB), Herbarium Manokwari (MAN),
National Herbarium of Papua New Guinea (LAE) dan koleksi hidup di Kebun
Raya Bogor. Hasil penelitian menunjukkan terdapat 13 jenis, 9 jenis diantaranya
telah dikenal sebelumnya yaitu A. camptopetala Diels, A. gracilis King,
A. hexapetalus (L.f.) Bhandari, A. inodorus Zipp., A. macranthus Holthuis,
A. speciosus Kurz., A. suaveolens Blume, A. sumatranus Miq., dan A. venustus
King. Empat jenis lainnya diusulkan sebagai jenis baru yaitu A. desmidantha
Diels ex Triasti., A. longipetalus Triasti., A. palmatiflorus Triasti. dan A.
trichofolius Triasti.. Kunci identifikasi dan deskripsi dari masing- masing jenis
telah dibuat. Artabotrys suaveolens mempunyai persebaran yang luas sedangkan
A.camptopetala, A. desmidantha, A. longipetalus, A. inodorus, A. palmatiflorus
dan A. trichofolius persebarannya terbatas. New Guinea merupakan kawasan yang
paling tinggi keanekaragaman jenisnya di Malesia Timur.
Analisa hubungan kekerabatan dengan Cyathocalyx sumatranus sebagai
outgroup menghasilkan satu kladogram parsimony dengan panjang 26 langkah
dan menunjukkan 3 kelompok besar. Kelompok I adalah Cyathocalyx
sumatranus, kelompok kedua adalah Artabotrys macranthus yang paling dekat
dengan outgroupnya. Sedangkan kelompok III disatukan oleh karakter
synapomorf no 2

(panjang daun), 3(hook), 11(bentuk daun buah), 14(jumlah

bakal biji) dan 15 (letak biji).
Kata Kunci : Artabotrys, Annonaceae, Malesia Timur, Analisis filogenetik.

ABSTRACT

Studies on the taxonomy of the genus Artabotrys R. Br. ( Annonaeceae )
in East Malesia were based on morphological characters by examining a large
number of Herbarium Bogoriense (BO), Celebense (CEB), Manokwari (MAN),
Departemen of Forest Lae (LAE) and living plants of Bogor Botanical Garden.
There are eight species which have been known previously: A. camptopetala
Diels, A. gracilis King.,

A. hexapetalus (L.f.) Bhandari, A. inodorus Zipp.,

A. macranthus Holthuis, A. speciosus Kurz., A. suaveolens Blume, A. sumatranus
Miq. and A. venustus King. Four new species are proposed in this treatment : A.
desmidantha Diels ex Triasti., A. longipetalus Triasti., A. palmatiflorus Triasti.,
and A. trichofolius Triasti.. An identification key and detailed discription are
provided for taxa. Artabotrys suaveolens Blume is widely distributed. While
A. camptopetala, A. desmidantha, A. longipetalus, A. inodorus, A. palmatiflorus
and A. trichofolius have a limited distribution. New Guinea is the area with the
highest diversity of Artabotrys species in East Malesia.
A phylogenetic analysis with Cyathocalyx sumatranus as outgroup, shows
three major groups. The first group is Cyatocalyx sumatranus. The second group
is A. macranthus which has the closest relationship with the outgroup. The third
group separated from the other group by the synapomorph characters 2 (leaf
length), 3 (hook), 11 (carpel shape), 14 (number of ovule) and 15 (position of
seed).
Keyword: Artabotrys, Annonaceae, East Malesian, phylogenetic analysis

ARTABOTRYS (ANNONACEAE) IN EAST MALESIA

TRIASTINURMIATININGSIH

Thesis submitted
As partial fulfillment requireme nt for the Master Degree
In Plant Taxonomy

THE POST GRADUATE PROGRAM
BOGOR AGRICULTURAL UNIVERSITY
2007

Title

: Artabotrys (Annonacea) in East Malesia

Name

: Triastinurmiatiningsih

Reg. Number

: G351040041

Certified by
Supervisor Committee

Dr. Sri Sudarmiyati Tjitrosoedirdjo, M. Sc.

Dr. Rugayah, M. Sc.

Chairman

Member

Acknowledged by

Head of Study Program of Biology

Dr. Ir. Dedi Duryadi Solihin, DEA

Date of graduation :

Dean of Graduate School

Prof. Dr. Ir. Khairil Anwar Notodiputro, M.Sc.

Examination Date : 12 January 2007

1

CURRICULUM VITAE
The author was born in Ngawi on 22th January 1969. The third daughter
from four children of Mr. Soebari and Mrs. Pudji Asti
She passed her Elementary School (SD) in 1981, Junior High School
(SMP) in 1984 and Senior High School (SMA) in 1987, all in Ngawi. She
attended the Faculty of Biology, Gadjah Mada University, Yogyakarta and
graduated in 1992.
Since 1994 she was employed by Department of Biology, Faculty of
Mathematic and Natural Science, Pakuan

University (UNPAK), Bogor as

candidate and promoted as lecturer in 1995.
In 2004 she received Post Graduate Education Schoolarship (BPPS) from
Director of high education (DIKTI) and UNPAK, Bogor to continue her study at
the Bogor Institute of Agriculture (IPB) at the majoring on plant taxonomy.

2

ACKNOWLEDGEMENT

The author realizes that this thesis will never be completed without
assistance of many colleagues and friends who have contributed in various ways.
I would like thank to Dr. Sri Sudarmiyati Tjitrosoedirdjo and Dr. Rugayah

for

their valuable advices and guidance in completing the thesis. I am grateful to
DIKTI and UNPAK Bo gor for the financial support for a master degree at the
graduate school IPB.
I would like to express my gratitude to Dr. Eko Baroto Waluyo Head of
the Herbarium Bogoriense (BO) and to other Herbaria: National Herbarium of
Papua New Guinea (LAE), Herbarium Celebense (CEB) and Herbarium
Manokwari (MAN) for grating me to examine their specimens for studies. In
particulary I am grateful to Prof. Dr. Soedodo Hardjoamidjojo Head of UNPAK
Bogor; Dr. Khairil Anwar Notodiputro Director of Graduate School Bogor
Agricultural university; Dr. Dedi Duryadi Program coordinator of the biology
program studies, Prof. Dr. Mien A. Rifai Program coordinator taxonomy sub
program studies.
I am also very grateful to Nunik Sri Ariyanti M.Si. for her interest ,
discussions and valuable comments on the manuscript. Bilal, Nida and Asti for
helping me in the fields. I would like to thanks Mr. Soebari and Mr. Affandi for
his excellent drawing; Miss. Rina, Mr. Sutijono and all of the librarian staff of the
Herbarium Bogoriense, for provid ing me with the pertinent literature. My special
thank go to my husband, my children, my parents, my brother ,my sister and all
my family for their spirit, patience and moral support during the conduct of my
studies.

ix

TABLE OF CONTENTS
LIST OF TABLES ........................................................................................... x
LIST OF FIGURE............................................................................................ xi
INTRODUCTION ............................................................................................ 1
MATERIAL AND METHODS ........................................................................ 3
Exploration............................................................................................ 3
Morphology........................................................................................... 3
Revision ................................................................................................ 3
Phylogenetic analysis ............................................................................ 3
RESULT AND DISCUSSION ......................................................................... 4
Morphology .......................................................................................... 4
Distribution .......................................................................................... 7
Phylogenetic analysis ............................................................................ 9
Taxonomy ........................................................................................... 12
Generic description................................................................. 12
Key to the Species................................................................... 13
Species description.................................................................. 14
1. A. camptopetala Diels ....................................................... 14
2. A. desmidantha Diels ex Triasti. ...................................... 15
3. A. gracilis King ................................................................ 16
4. A. hexapetalus (L.f.) Bhandari ......................................... 17
5. A. inodorus Zipp. ............................................................ 17
6. A. longipetalus Triasti. ..................................................... 18
7. A. macranthus Holthuis ................................................... 19
8. A. palmatiflorus Triasti. .................................................... 28
9. A. speciosus Kurz.............................................................. 28
10. A. suaveolens Blume ......................................................... 29
11. A. sumatranus Miq............................................................ 30
12. A. trichofolius Triasti. ....................................................... 31
13. A. venustus King ............................................................... 32
CONCLUSION............................................................................................... 40
REFERENCES ............................................................................................... 41

x

LIST OF TABLE

Table

Page

1. Distribution of Artabotrys in East Malesia and the other place in
Malesia ......................................................................................................8
2. Morphological characters and character states used in phylogenetic
Analysis.....................................................................................................9
3. Matrix of morphological characters at the taxa ......................................10

xi

LIST OF FIGURE

Figure

Page

1. Forms of Artabotrys leaves. shape : a. ovate, b. obovate, c. lanceolate,
d&e. oblong, f. ellipse. Apex : a. acute, b. cuspidate, c&f. long acuminate, d&e.
shortly acuminate. Base : a, d&f. cuneate, b&c. attenuate, e. rounded. .......5
2. Variation of Artabotrys stamens. 1. filament, 2. theca, 3. apical. a. oblong flat
apical prolongation, b. oblong suborbiculate apical prolongation,c. oblong
suborbiculate apical prolongation .......................................................................6
3. Variation of Artabotrys carpel. 1. stigma; 2. carpel. a. cylindrical carpel bilobed
stigma, b. cylindrical carpel clavate stigma, c. cylindrical carpel Ellipsoid
stigma, d. ellipsoid carpel, e. ovoid carpel wooly stigma, f.ovoid carpel cup
stigma, g.ovoid carpel axe stigma, h. ovoid carpel ovoid stigma ........................7
4. Cladogram of Artabotrys ...................................................................................10
5. A. desmidantha Diels ex Triasti.: a. habit, b. sepal, c. petal, d.stamen, e. carpel
and stigma (a-e: Docters van Leuween 11388) .................................................21
6. Artabotrys gracilis King, a. habit, b. calyx, c. stamen, d. carpel and
stigma (from Nurainas, 2004)...........................................................................22
7. Artabotrys hexapetalus (L.f) Bhandari. a. habit, b. calyx, c. inner petal, d.outer
petal, e. carpel and stigma, f. stamen ( from Nurainas, 2004)……….……..23
8. Artabotrys inodorus Zipp.: a. habit, b.sepal, c. outer petal, d.inner petal
e. stamen, f. carpel (a- f: J.S. Womersly 13430).................................................24
9. Artabotrys longipetalus Triasti.: a. habit, b. leaf, c. sepal, d. outer petal, e.inner
petal, f. stamen, g. carpel and stigma (a-g: M. Jacobs 9315) ...........................25
10. Artabotrys macranthus Holthuis: a. habit, b. petal, c. stamen d. carpel and
stigma ( from L. B. Holthuis, 1942) ................................................................26
11. Distribution of Artabotrys in East Malesia. A. camptopetala, A. desmidantha,
A. gracilis, A. hexapetalus, A. inodorus, A. longipetalus and A. macranthus ..
.........................................................................................................................27
12. Artabotrys palmatiflorus Triasti.: a. habit, b.sepal, c. outer petal, d. inner petal,
e. stamen, f. carpel (a- f: Ramlanto 444)..........................................................33
13. Artabotrys speciosus King : a. habit, b. sepal, c. outer petal, d. inner petal,
e . stamen, f. carpel (a- f: P. van Royen 3574) ...................................................34

xii

14. Artabotrys suaveolens Blume, a. habit, b. sepal, c.outer petal, d. inner petal,
e. stamen, f. carpel and stigma (a-c: G. Kjellberg 2752; d-f: Moh. Amir 254) ...
.........................................................................................................................35
15. Artabotrys sumatranus Miq.: a. habit, b. flower, c. outer petal, d.inner petal,
f. carpel and stigma (from Nurainas, 2004) ...................................................36
16. Artabotrys trichofolius Triasti. : a. habit, b. sepal, c. petal, e. stamen, f.carpel.
(a-f : Ramadhanil & Ch. H. Scultze 816) ........................................................37
17. Artabotrys venustus King : a. habit, b. stamen, c. carpel and stigma, d. fruit
( from Nurainas, 2002) ....................................................................................38
18. Distribution of Artabotrys in East Malesia. A. palmatiflorus, A. speciosus,
A. suaveolens, A. sumatranus, A. trichofolius and A. venustus.......................39

1

INTRODUCTION

Artabotrys is one of the large genus of Annonaceae family. The genus has
more than 100 species distributed in Tropical Africa and Eastern Asia. Several
species can be used for drugs, poison and cosmetic (Burkill, 1935). One of them
has economically important for parfume namely A. odoratissimus, known as
Ylang-ylang oil (Keßler, 1993).
The genus Artabotrys was described almost 187 years ago by Robert
Brown, based on A. odoratissimus

R. Br. Previously A. odoratissimus was

included in genus Unona, Annona, and Uvaria. However, it differs from Unona in
petal shape, seed number, seed position and peduncle characters, from Annona in
fruit, petal and peduncle characters, and from Uvaria in their peduncle shape,
petal and fruits characters (Brown, 1820). Bhandari (1964) reduced A.
odoratissimus as the synonym of A. hexapetalus.
Keßler (1993) include Artabotrys in an informal grouping of Xylopiae
together

with

Xylopia,

Anaxagorea,

Pseduo

artabotrys,

Cyathocalyx,

Drepananthus and Diclinanona based on climbers habitat, peculiar hooked
peduncle, bisexual flowers, equal depth of petal, spoon like outer petal, connivent
inner petal covering reproductive organ and berry fruits. While Sinclair (1955)
placed Artabotrys as a member of sub family Annonoideae tribe Unonae together
with Cyathocalyx, Desmos, Monocarpia, Oncodostigma, Meiogyne, Polyalthia,
Cananga, Mezzetia and Disepalum. Artabotrys included in the tribe Unoneae
based on valvate petal, flat, differentiation of blade and claw, and inner petal
covering reproductive organ.
Most studies on the taxonomy of Artabotrys was conducted in West
Malesia . Some previous authors such as Sinclair (1955) described 12 species of
Artabotrys of Malay Peninsula, Priyanti in 2002 described 5 species of Artabotrys
of East Borneo and Nurainas in 2004 described 10 species with 2 varieties of
Artabotrys of Sumatra. However in East Malesia is poorly understood and the
number of

Artabotrys species is unknown. Diels in 1915 described A.

camptopetala as new species from New Guinea. Engelman in 1918 described A.
suaveolens and A. inodorus with two varietas namely A. inodorus ß lanceolata

2

and A. inodorus ß inodorus from New Guinea. Keßler et. al (2002) said in the
checklist of plant in Sulawesi that there are Artabotrys suaveolens, Artabotrys
trichopetala and Artabotrys sp. Which have not recorded yet in Moluccas..
The limited data of Artabotrys in East Malesia is due to the lack of
intensive explorations, collections and investigations so this is the reason that
studies were worshy subject of investigations.
The purpose of this studies are to know diversity and the distribution
pattern of Artabotrys in East Malesia, to provide an identification key to the
species, and to determine the relationships among the species of Artabotrys in
East Malesia.

3

MATERIAL AND METHODS

Explorations
Exploration was conducted at Celebes and Moluccas for addition of the
collected specimens due to the scarse of the previous collections. Exploration and
specimen collection were based on Balgooy method (1987)

Morphology
Morphology and distribution of the species were based on dried specimens
and spirit- preserved materials which were deposited at LAE, CEB, BO, MAN
and the collected specimens in 2006.
Measurement and observation were recorded: locality; general habitat;
stem (surface, indument, colour); branches (straight or curved); leaves (shapes,
base, apex, midrib, number of nervus lateralis, leaf length, petiole length, surface);
inflorescense (shapes, induments, branche, number of flowers); flowers (colour,
sepal surface, sepal shape, petal surface, petal shape, length pedicel, shape and
number stamen, shape and number carpells), fruitlets shape were observed from
the specimens. Terminology used in this studies following Stearn (1988) and
Harris & Harris (1994)

Revision
Revision was made using standard preparation guide-lines proposed by
Rifai (1976), Vogel (1987), and Maxted ( 1992).

Phylogenetic Analysis
A phylogenetic analysis were based on fourteen morphological characters
and analyzed using the Hennig 86 program.

4

RESULT AND DISCUSSION

MORPHOLOGY
Habit
The habit of Artabotrys are climbers. This is one of an important character
to distinguishis from other genus in Annonaceae .

Indumentum
Type of indumentum in the genus are puberulous, pubescent, tomentose
and villose. Types of indumentum on young twigs, petiols, and midrib are
pubescent or sparsely pubescent, on blade is sparsely pubescent. Indumentum in
peduncle is sparsely pubescent, while in flowers are puberulous, pubescent,
tomentose and villose.

Branches
Generally their young branches are hairy but A. suaveolens and A. gracilis
are glabrous. Most of the Artabotrys species have straight branches such as A.
desmidantha, A. gracilis, A. longipetalus, A.palmatiflorus, A. suaveolens, A.
sumatranus, A. hexapetalus, A. inodorus, A. longipetalus, A. speciosus, A.
venustus, A. venustus. Whereas A. trichofolius and A. macranthus have curved
branches.

Leaves
The leaves of the genus have various shape (Fig.1). The shape of blade
were elliptic to oblong, oblong, elliptic, ovate, obovate and lanceolate. Most
species of Artabotrys have elliptic to oblong leaves but obovate leaves found in A.
sumatranus and A. macranthus,

lanceolate or ovate in

A. palmatiflorus,

lanceolate or obovate in A. inodorus. Exception is found in A. speciosus and A.
trichofolius which only have oblong leaves. Petioles of Artabotrys are usually
short but A. palmatiflorus has longer than other species.
Most species of Artabotrys have cuneate leaves base, attenuate found in
A. sumatranus and A. palmatiflorus, while A. speciosus has rounded base.

5

Generally the leaves apex in Artabotrys are short acuminate , but A. inodorus and
A. hexapetalus have rather lengthened acuminate apex, while A.suaveolens has
acuminate to cuspidate, and A. palmatiflorus has acute apex.

3cm

a

b

c

3cm

d

e

f

Fig. 1. Forms of Artabotrys leaves. Shape : a. ovate, b. obovate, c. lanceolate,
d & e.oblong, f. elliptic. Apex : a. acute, b. cuspidate, c & f. long acuminate,
d & e. shortly acuminate. Base : a, d & f. cuneate, b & c. attenuate, e. rounded
Some species of Artabotrys have shinning upper leaf surface such as
A. camptopetala, A. suaveolens, A. venustus and A. gracilis. Generally both of leaf
surfaces are glabrous, except in midrib beneath, but A. trichofolius has hairy at
lower surface. The midrib of Artabotrys raised at lower surface, but some species
Artabotrys have midrib raised at both surface such as A. sumatranus, A. venustus,
A. macranthus and A. palmatiflorus.

6

Flowers
The flowers

are bisexual in solitary or fasicle. Peduncles are extra

axillary, opposite the leaves, reflexed, hooked, flatten or terete. Calyx consists of
3 sepal valvate, sometimes connate at base with erected or deflected in ovate,
deltoid or triangular shape. Corolla consists of 6 petals, valvate in two whorls. It
has 3 outer petal, free, fleshy, concave at base with oblong, lanceolate or linear
shape. Outer petal longer and broader than inner petals, sometimes different
shape. A. sumatranus, A. gracilis,

A. speciosus and A. longipetalus have outer

petal different from inner petal shape.
The shape of stamen was oblong with the apical prolongation flat, acute
or concave. Most of species Artabotrys have stamen oblong with apical
prolongation flat but A. sumatranus and A. trichofolius have stamen oblong with
apical prolongation acute, while A. speciosus and A. longipetalus have stamen
oblong with apical prolongation suborbiculate. They consists of three parts:
filament, theca and apical prolongation (Fig. 2).
The carpels have three shapes: ovoid for most species, cylindrical for
A. macranthus, A. hexapetalus and A. longipetalus, while ellipsoid found in
A. trichofolius and A. speciosus. Most species have 2-5 carpels, but A macranthus
has 8-13 carpels.

1
1mm

2
3

a

b

c

Fig 2. variation of Artabotrys stamens. 1. filament; 2. theca; 3. apical; a. oblong
flat apical prolongation; b. oblong acute apical prolongation; c. oblong
suborbiculate apical prolongation
The shape of stigma various for all species. A. gracilis cup shape stigma,
A. hexapetalus clavate shape, cylindrical bilobed

in A. macranthus, ellipsoid

7

villose in A. desmidantha, ellipsoid in A. longipetalus, ovoid in A. sumatranus
and axe shape in A. venustus .

1
1mm

2

a

b

c

d
d

1mm

e

f

g

h

Fig 3. Variation of Artabotrys carpel. 1. stigma; 2. carpel; a. cylindrical carpel
bilobed stigma, b. cylindrical carpel clavate stigma, c. cylindrical carpel ellipsoid
stigma, d. ellipsoid carpel, e. ovoid carpel villose stigma, f.ovoid carpel cup
stigma, g.ovoid carpel axe stigma, h. ovoid carpel ovoid stigma.

Fruits
The fruits of Artabotrys are berry, with various shape: ellipsoid with
acute or blunt apex, oblong with blunt apex, and obovoid with acute or blunt
apex. Artabotrys hexapetalus has ellipsoid fruit with acute apex. A. suaveolens
and A. sumatranus have ellipsoid fruit with blunt apex, while A. inodorus has
obovoid fruit with acute apex and A macranthus has oblong fruit with blunt
apex.

DIVERSITY
Twelve taxa of Artabotrys are recognized in this study. There are nine
species which have been known previously : A. camptopetala, A. gracilis King.
A. hexapetalus (L.f.) Bhandari, A. inodorus Zipp., A. macranthus Holthuis, A.
speciosus Kurz, A. suaveolens Blume, A. sumatranus Miq. and A. venustus King.
Four species are proposed in this treatment: A. desmidantha Diels ex Triasti., A.
longipetalus Triasti., A. palmatiflorus Triasti., and A. trichofolius Triasti..

8

DISTRIBUTION
Artabotrys is found in all over East Malesian area. Artabotrys suaveolens
Blume is widespread in East Malesia and also other places. It has been recorded
from

Celebes, Moluccas, New Guinea and also in Malay Peninsula, Sumatra,

Java, Borneo, Philippines. In East Malesia some of species have limited
distribution such as A. trichofolius which only occurs in Celebes, A. palmatiflorus
only found in Moluccas, while A camptopetala, A. longipetalus, A. desmidantha
and A. inodorus are found in New Guinea.
The region with the highest species diversity in Malesia is New Guinea.
There are 9 species in New Guinea (Table 1.). Species of Artabotrys in East
Malesia are more diverse than West Malesia and Java. There are 13 species in
East Malesia, while in West Malesia has 7 species and 3 species in Java.

Table 1. Distribution of Artabotrys in East Malesia and the other place in Malesia
(from several references and own observation of the East Malesian specimens)
Species

East Malesia
A

Other places in Malesia

A. camptopetala
A. desmidantha

-

B
-

A. gracilis
A. hexapetalus
A. inodorus
A. longipetalus
A. macranthus
A. palmatiflorus
A. speciosus
A. suaveolens
A. sumatranus
A. trichofolius
A. venustus

+
+
+
+
-

+
+
+
+
+
-

+
+
+
+
+
+
+

+
+
+
-

+
+
+
+
+

+
+
+
+
+
-

+
+
+
+
+
+

+
+
+
-

Total

4

5

9

2

5

5

6

3

Note:
A. Celebes
B. Moluccas
C. New Guinea
D. Philippines (Merril, 1923)

C
+
+

D
-

E
-

F
-

G
-

H
-

E. Malay Peninsula (Sinclair, 1955)
F. Borneo (Priyanti, 2002)
G. Sumatra (Nurainas, 2004)
H. Java (Backer & Bakhüizen van den
Brink, 1963)

9

PHYLOGENETIC ANALYSIS OF ARTABOTRYS

A phylogenetic analysis of Artabotrys was carried out based on
morphological characters, using Cyathocalix sumatranus as the outgroup. The
phylogenetic analysis used 16 morphological characters (Table 2.), which all of
them are scored with the primitive state based on the state of the outgroup. Data
matrix of those characters which has been used for the analysis shown in Table 3.
The analysis result three parsimonious trees with 26 steps length, Consistency
index (CI) of 0,65 and Retention index (RI) of 0.70. A single tree, which was
selected from three fundamental tree is shown in Figures 4. From 16 characters
analysed, 8 of them are apomorph (5 synapomorph, 3 autapomorph). Other
characters with Consistency Index lower than 1.00 showed parallel ( characters 6,
7, 8, 9, 10, 13) and reversal (character 0 &11).

Table 2. Morphological characters and character states used in phylogenetic
analysis
No
Characters
Character states
0
Branches indument
0= present
1= absent
1
Lower surface leaf
0= glabrous
1= hairy
2
Leaf length
0= 14-28 cm
1= 8-13 cm
3
Hook
0= absent
1= present
4
Number of flowers
0= 1 - 7
1= 20-40
5
Outer petal
0= flat
1= terete
6
Inner petal
0= flat
1=terete
7
Petal shape
0= oblong
1= lanceolate
2= linear
8
Number of stamen
0= = 20
1= > 20
9
Stamen apex
0= flat
1= suborbiculate
2=acute
10 Number of carpel
0= =5
1= > 5
11 Carpel shape
0= ellipsoid
1= cylindrical
2= ovoid
12 Stigma
0= glabrous
1= hairy
13 Torus
0= flat
1= concave
14 Number of ovule
0= 23
1= 2
15 Position of seed
0= collateral 1= arrange of two rows
The cladogram divided the taxa into three groups which consists of group
I : Cyathocalyx sumatranus as the outgroup; group II: A. macranthus and group
III: A. camptopetala, A. desmidantha, A. gracilis, A. hexapetalus, A. inodorus,
A. longipetalus, A. speciosus,, A. palmatiflorus, A. suaveolens, A. sumatranus,

10

A. trichopetalus, A. venustus. A. macranthus is close related with the outgroup
might be the most primitive and separated from the ingroup because of character
13 (torus concave).

0-2

Fig. 4. Cladogram of Artabotrys in East Malesia

11

Table 3. Matrix of morphological characters at the taxa
No
1
2
2
3
4
5
6
7
8
9
10
11
12
13

Species
C. sumatranus
A. camptopetala
A. desmidantha
A. gracilis
A. hexapetalus
A. inodorus
A. longipetalus
A. macranthus
A. palmatiflorus
A. speciosus
A. suaveolens
A. sumatranus
A. trichofolius
A. venustus

0
0
0
0
1
0
0
0
0
1
0
1
0
0
0

1
0
0
0
0
0
0
0
0
0
0
0
0
1
0

2
0
1
1
1
1
1
1
0
1
0
1
1
1
1

3
0
1
1
1
1
1
1
1
1
1
1
1
1
1

4
0
0
0
0
0
0
0
0
1
0
0
0
0
0

5
0
1
0
0
0
1
0
0
1
0
1
0
0
0

6
0
1
0
1
0
1
1
0
1
1
1
1
0
0

characters
7 8 9
0 ? 0
2 ? 0
0 0 0
0 0 0
0 1 0
2 0 0
2 0 0
0 0 0
2 1 1
2 0 1
2 1 0
1 1 2
0 1 2
0 1 0

10
0
0
0
0
0
0
0
1
0
0
0
0
0
1

11
0
2
2
2
1
1
1
0
0
0
2
2
0
0

12
?
0
1
0
0
0
0
0
0
0
0
0
0
0

13
0
0
1
0
1
0
0
1
0
0
0
0
0
0

14
0
1
1
1
1
1
1
1
1
1
1
1
1
1

15
0
1
1
1
1
1
1
1
1
1
1
1
1
1

Group III was separated from other group because of characters 2 (leaf
length), 3 (hook), 11 (carpel shape), 14 (number of ovule) and 15 (position of
seed). This group is separated into two main groups. The first main group concist
of A. venustus as the sisters group A. sumatranus, A. trichofolius and they closely
related because of character 8 (number of stamen > 20). The second main group
is separated with the first group becaus e of character 10 ( number of carpel >7). A.
desmidantha closely related with A. hexapetalus because of character 13 (torus
concave). A. gracilis is sister group of A. longipetalus, A. speciosus, A. inodorus,
A. palmatiflorus, A. suaveolens, and A. camptopetala because of characters 6
(inner petal terete). A. palmatiflorus is sister group of A. suaveolens and A.
camptopetala because of characters 0 (branche glabrous) and 8 (number stamen >
20).

12

TAXONOMY

Generic Description
Artabotrys R. Brown

Artabotrys R. Br. Bot. Reg. 5: 423. 1819; Blume, Fl. Java. 2: 58. 1828; Miquel,
Fl. Ned. Ind. 38. 1860; Hooker, Fl . Brit. India 1 : 53. 1875; King, Jour. As. Soc.
Beng. 61: 30. 1893; Ridley, Fl. Mal. Pen. 1: 38. 1922; Sinclair, Gard. Bull. Sing.
14(2) : 146.1955; Backer and Bakhuizen van den Brink Jr., Fl. Java. 1 : 113. 1963.
-Type species: Artabotrys hexapetalus (L.f.) Bhandari, Koenig, s. n., India,
Madras (Holo: LINN).

Climbers. Lateral branches lenticellate, glabrous to hairy. Leaves:
alternate, simple; margin entire; midrib raised or flat at upper surface; lateral
nerves pinnate, flat or raised on the lower surface, anastomosing near to the
margin; veins scalariform. Inflorescence: peduncle extra – axillary, opposite the
leaves, reflexed, hooked, flattened or terete; bract small; often caducous. Flowers :
hermaphrodite, fleshy, solitary or fascicle; sepal valvate, 3, erect or deflexed,
connate at base; petal 6 in two series, valvate, the blade terete or flat, oblong,
lanceolate or linear; outer petal 3, spoon – like at base, free, longer and broader
than the inner ones; inner petal 3 remaining attached at their bases when they fall,
claws the blade joins it connivent, close to the sexual organs. Torus flat to
concave, pillose. Stamen hypogynous, numerous tongue shaped, apex flat, acute
or convex. Carpel free, few to many, glabrous or hairy; stigma persistent; ovule 2.
Fruit berried, glabrous, puncticulate. Seed 2, erect, collateral , dorsiventral,
ventral side flat and dorsal side convex.
Note: Thirteen species of Artabotrys were recognized in East Malesian,
show that New Guinea has the highest number of species. There were nine species
in New Guinea, whereas Moluccas have five species and Celebes four species.

13

Key to the Species
1.a Lateral branches curved..................................................................................2
b. Lateral branches straight .................................................................................3
2.a. Young twig with long reddish hairs; leaves 17.5-20 x 7-8 cm, lower surface
glabrous; outer petal oblong, tomentose; carpels 8-12, cylindrical bilobed ...
................................................................................................... A. macranthus
b. Young twig with short white ha irs; leaves 4-8.5 x 2.5-3.5 cm, lower surface
sparsely pubescent; outer petal ovate, puberulous; carpels 5, ellipsoid
bilobed ......................................................................................A. trichofolius
3.a. Outer petal terete, inner petal terete ...............................................................4
b. Outer petal flat, inner petal terete or flat ........................................................6
4.a. Petiole 2-4 mm long, sparsely pubescent; number of flower 3-5; pedicel 2-6
mm long, apical prolongation flat .................................................................5
b. Petiole 6-10 mm long, glabrous; number of flower 20-40; pedicel 15-20 mm
long, apical prolongation suborbiculate ...................................A. palmatiflorus
5.a. Sepal ovate or broadly ovate; petal 6-15 x 1-1.5 mm, apex recurved,
pubescent or sparsely pubescent .....................................................................7
b. Sepal lanceolate; petal 16-20 x 1.5-2 mm, apex erected, puberulous ...............
........................................................................................................ A. inodorus
6.a. Blade coriaceous; sepal ovate, pubescent; outer petal 8-15 mm long,
pubescent; stigma cup shape .......................................................A. suaveolens
b. Blade chartaceous; sepal broadly ovate, sparsely pubescent; outer petal 15-20
mm long, puberulous; stigma ovoid shape.............................A. camptopetala
7.a. Inner petal terete, linear; top of apical prolongation acute or suborbiculate ....
.........................................................................................................................8
b. Inner petal flat, lanceolate or ligulate; top of apical prolongation flat ..........9
8.a. Blade thinly coriaceous, elliptic to oblong or obovate, base cuneate; flowers
3-4; top of apical prolongation acute; carpels 5 .......................A. sumatranus
b. Blade coriaceous, oblong, base rounded; 5-6 flowers; top of apical
prolongation sub orbiculate; carpels 3 ....................................... A. speciosus
9. a. Sepal ovate to broadly ovate, apex acute to acuminate; outer petal lanceolate
or linear, 0.5-3 cm long..............................................................................10

14

b.Sepal suborbiculate, apex cuspidate; outer petal ligulate, 5.5-7 cm long .....
................................................................................................A. longipetalus
10. a. Bract elliptic; pedicel 2-3 mm; torus flat ..................................................11
b. Bract elliptic to oblong; pedicel 15-25 mm; torus convex........................12
11.a. Pedicel villose; sepal ovate, 5 x 3 mm; outer petal lanceolate, 15 x 4 mm,
villose;

carpels broadly cylindrical; stigma ellipsoid, villose .....................

................................................................................................A. desmidantha
b. Pedicel glabrous; sepal broadly ovate, 2 x 2 mm; outer petal linear 3-5 x
1mm, pubescent; carpels broadly ovoid; stigma cup shape, glabrous .............
........................................................................................................... A. gracilis
12. a. Leave shining at upper surface, lateral nerves raised on both surface; outer
petal oblong 6-10 x 3-5 mm, stigma axe shape ........................... A. venustus
b. Leave dull at upper surface, lateral nerves flat on both surface; outer petal
lanceolate 20-30 x 5-10 mm, stigma clavate shape ................A. hexapetalus

Species description
1. A. camptopetala Diels, Engl. Jahrb. 3: 179. 1915.
-Type: Ledermann n. 8676

Lateral branches straight, lenticelled, black when dry. Young twigs
pubescent. Leaves: petiole 2 – 4 mm long, sparsely pubescent; blade chartaceous,
shining at upper surface, glabrous in lower surface, pale brown when dry; ovate or
elliptic, 3-8 – cm x 2 – 4 cm; base cuneate; apex short acuminate; midrib flat at
upper, raised at lower surface and sparsely pubescent; lateral nerves 6 – 8 pairs,
anastomosing 3–4 mm to the margin. Inflorescence: peduncle terete, three
branches, sparsely pubescent, with 3 – 5 flowers; bract not seen; flower bud not
seen, sparsely pubescent. Flowers : pedicel 2 – 3 mm long, sparsely pubescent;
sepal valvate, fleshy, erect, broadly ovate, 3-5 x 3 mm, sparsely pubescent, apex
acute; outer petals terete, fleshy, lingulate, 6-7 mm x 1-1.5 mm, sparsely
pubescent, apex obtuse, recurved; inner petals narrower, 5-6 mm x 1-1.5 mm,
sparsely pubescent; torus flat; stamen not seen; carpels 3, broadly ovoid, 2 x 1.5
mm; stigma ovoid; Fruit ellipsoid, glabrous, 3-3.5 x 1.6 x 2 cm. Seed not seen.

15

Distribution : New Guinea
Habitat and Ecology : primary forest at 5400 feet alt
Specimen examined: New Guinea. Oksapmin, Telefomin subdistrict, West Sepik
District, 17-10-1968, E.E. Henty, R. Isgar & M. Galore 41608 (LAE!); Ambunti
subdistrict, Waskuk hills, around Langu and Garuka villages, West Sepik District,
29-6-1995, J. Regalado & W. Takeuchi 1441 (LAE!).
2. A. desmidantha Diels ex Triasti., spec.nov. ( Fig. 5)
Folia sub coriacea, glabra, elliptica, 8-12 cm longa, 3.5-6 cm lata, nervus
lateribus 6-8 paribus, apica breviter acuminata, basi cuneata. Petioli 2-4 mm
longa, sparsissima pubescent. Pedunculi trifidi 2-3 flori; pedicelli villose, 2-3 mm
longa, sepal lato-ovata, 5 mm lata, apice acuminata, villose; petala externa
lanceolata, 15 mm longa, 4 mm lata, apice acute, utrinque villose; interna angustilanceolata. Stamen angusti-oblonga, apical prolongation plana. Carpels 5, latocylindrica; stigma ellipsoidea, villose. -Typus : Docters van Leeuwen 1138,
Memberamo, New Guinea ( Holo: BO!)
Lateral branches straight, lenticelled, black when dry. Young twigs
pubescent. Leaves: petiole 2 – 4 mm long, pubescent; blade thinly coriaceous,
glabrous in both surface, pale brown at upper surface, dark brown at lower surface
when dry, elliptic to oblong, 8 – 12 (-13) cm x 3.5 – 6 cm; base cuneate; apex
short acuminate; midrib flat at upper, raised at lower surface and sparsely
pubescent, lateral nerves 6 – 8 pairs, anastomosing 3–6 mm to the margin.
Inflorescence: peduncle terete, three branches, sparsely pubescent, with 3 – 5
flowers; bract elliptic, 2 x 1.5 mm, flower bud ovoid, 4 x 3 mm, villose. Flowers :
pedicel 2 – 3 mm long, villose; sepal valvate, fleshy, erect, ovate, 3 x 2.5 mm,
villose, apex acuminate; outer petals flat, fleshy, lanceolate, 15 x 4 mm, both
surface villose, apex acute; inner petals flat, narrower, 13 x 3.5 mm, villose; torus
flat; stamen c. 14, oblong, top of apical prolongation flat; carpels 5, broadly
cylindrical, 1.5 x 0.5 mm; stigma ellipsoid 1 x 1 mm, villose. Fruit and seed not
seen.
Distribution: New Guinea
Habitat and Ecology: primary forest at 60 m alt.
Notes: A. desmidantha is similar to A. hexapetalus in lanceolate petal, but differs
in leaf, peduncle, torus, stamen, stigma and flower indumentum. A. hexapetalus
has elliptic to oblong or lanceolate, flat peduncle with two branches, concave
torus, top of apical prolongation acute, stamen 29 and clavate stigma. Whereas A.

16

desmidantha has elliptic to oblong leaf only, terete peduncle with three branches,
flat torus, top of apical prolongation flat, stamen 14 and stigma ellipsoid stigma.
The indumen of pedicel, sepal, petal and stigma are the most important character
for this species. Diels (1932) described Leeuwen specimen as A. desmidantha but
it has not published yet. Therefore, this study propose this as a new species.
Specimen examined: New Guinea : Memberamo, November 1926, Docters van
Leeuwen 11388 (BO!)
3. Artabotrys gracilis King (Fig. 6)
A. gracilis King, Jour. As. Soc. Beng. 16(2): 35. 1893; Ridley, Fl. Mal. Pen. 1: 44.
1922; Ridley, Sarawak Mus. Journ. 1(3): 77. 1913; Sinclair, Gard. Bull. Sing.
2(14): 258. 1955. - Type: G. King 4987, Malay Peninsula, Perak (Holo: L,
Isotype: BO!)
Lateral branches straight, lenticelled, glabrous, dark colour when dry.
Young twigs glabrous. Leaves: petiole 2-4 mm long, pubescent; blade thinly
coriaceous, both surface glabrous, shining at upper surface, brown when dry;
elliptic to oblong, 6-12 x 5-7 cm; base cuneate; apex acuminate; midrib flat at
upper, raised at lower surface, sparsely pubescent; lateral nerves 7-9 pairs,
anastomosing 4-6 mm to the margin, flat on both surface. Inflorescence: peduncle
terete, sparsely pubescent, three branches; 5-7 flowers; bract elliptic, 5-7 x 1-2
mm, persistent, pubescent; flower bud broadly ovoid, 1.5 x 2 mm, pubescent.
Flowers : pedicel 2-2.5 mm long, glabrous; s