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THE GARDENS’ BULLETIN

SINGAPORE

TROPICAL BOTANY

Essays presented to

E. J. H. Corner

for his seventieth birthday, 1976

Compiled and edited by

D. J. MABBERLEY and CHANG KIAW LAN

Published by Authority

Issued by the Commissioner, Parks and Recreation Department

Printed by the Singapore National Printers (Pte) Ltd

1977

To be purchased at the Botanic Gardens, Singapore

Price: $$30.00

CONTENTS

H. M. BurxILu: Introduction - - - . : :

D. J. MaBBERLEY: E. J. H. Corner’s Botany - - ‘ :

William T. STEARN: The of gis gaia’, imme With Sa a:

Vegetation

P. S. AsHTon: Ecology and the Durian Theory — - ‘ E

E. SoepapMo & B. K. Eow: hai Roa Per ~—

zibethinus Murr. -

Frances M. JARRETT: The ne of Artocarpus — a unique binloniels

phenomenon - - - a a : F

D. J. MABBERLEY: The Origin . the fap abies ai Flora and

its Implications - . M ‘

Frank WHITE: The fintier ida Forests of Africa: A preliminary

review - - - - - - - -

B. L. Burtr: Notes on Rain-Forest Herbs sz : if 7

E. F. Bkunic & H. KLINGE: Comparison of the Phytomass Structure

of Equatorial ‘‘Rain-Forest” in Central Amazonas, Brazil, and in

Sarawak, Borneo - - - - - -

C.G.G.J. VAN STEENIS: Autonomous Evolution in Plants: differences

in plant and animal evolution - i A :

Andrey A. FEporov: On Speciation in the Humid Tropics: some

new data - - - - - - - -

Benjamin C. STONE: The Morphology and SS i ni of Pandanus

Today (Pandanaceae) - - - -

Hsuan KENG: Ternstroemia corneri (Theaceae) - - - :

R. E. HoLtruM: Thelypteridaceae Allied to Phegopteris in Malaya -

A. Davip & M. JAQUENOUD: Tremellales with Tubular Hymenophores

Found in Singapore - : . . : : ‘

Jacqueline PERREAU & RoGeR HeEIM: Sur Un Nouveau Bolet Tropical

a Spores Ornées~ - - - ‘ i . :

A. FAHN & D. M. JoEL: Development of Primary Secretory Ducts in

the Stem of Mangifera indica L. (Anacardiaceae) - - -

Kenneth R. SporNe: Girdling Vascular Bundles in Dicotyledon

Flowers - - . _ ; z P ;

F. HALLE & D. J. MABBERLEY: Corner’s Architectural Model - -

Robert F. THORNE: Where and When Might ¥e Trop Ansa

mous Flora Have Originated? . -

J. GALIL, M. STEIN & A. Horovitz: On the en of the SCORES

Fig (Ficus sycomorus L.) in the Middle East - -

J. T. Wiepes: A Short History of Fig Wasp Research - - :

V. H. Heywoop: The Taxonomist’s Dilemma - : : .

D. G. FRoDIN: On the Style of Floras: some general considerations —-

Edwin A. MENNINGER: This World We Live in Will Be Only as

Beautiful as You and I Make It - - - : -

Index - - - .

Errata - . , “ ;

PAGE

12

s-11

13-18

19-23

25-33

35-39

41-55 —

57-71

73-80

81-101

103-126

127-136

137-142

143-144

145-150

151-153

155-160

161-164

165-173

175-181

183-189

191-205

207-232

233-237

239-250

251-253

255-266

266

THE

GARDENS BULLETIN

SINGAPORE

Vol. XXIX 31st August, 1977

Introduction

H. M. BurKILL

Royal Botanic Gardens, Kew

(Botanic Gardens, Singapore, 1954-1969)

Corner’s septuagenary fell on 12 January, 1976, It was the intention of a number of

his research students and friends to develop an idea mooted by David Frodin into a little

book to mark the occasion. However.

‘The best-laid schemes o’ mice an’ men

Gang aft a-gley,

And lea’e us nought but grief an’ pain

For promised joy.’

(Robert Burns: To a mouse, 1785.)

Very considerable difficulties have arisen over the preparation and publication, so that

only now, by the courtesy of the Editor of the Gardens’ Bulletin, Singapore, does it appear

— in retrospect, but, nevertheless, in a token of our esteem.

It was but inevitable that with such innate stimulating enthusiasm for botany, Corner

should find the opportunity during his service in Singapore to give free rein to it. The

‘Durian Theory’ of evolution is here discussed, as along with the tropical rain-forest which

Corner demonstrated in his later years as Professor of Tropical Botany at Cambridge ought

to form the central pillar of any basis for teaching botany. Universities in tropical regions

in centres of floral evolution with the plant materials on their door-step should be mindful

of establishing leading research schools instead of letting the world rely on botanists tutored

on temperate botany. Long before announcing his Durian Theory but with perhaps the seeds

of the idea quietly growing in his mind, Corner began teaching, amongst his other duties

in the Botanic Gardens, students in the Raffles College and in the King Edward VII

College of Medicine in Singapore. These are now integral parts of the University of

Singapore, and many of the older collegiates recall his lectures with interest and pleasure.

In 1937 while on expedition in N.E. Malaya he brought a young berok monkey (Macaca

nemestrina). This is the species that is trained to pick ripe coconuts, and Corner saw the

possibility of training one to pick plant specimens from high forest trees at a height of

perhaps 50-60 m from the ground. The berok had its début on a trip to Fraser’s Hill and

proved to be so successful that two more were acquired, and later a fourth. Words of a

command had to be taught to guide the monkey to what was wanted visible to the operator

lying on the ground scanning the tree-canopy through binoculars. Infinite patience was

necessary, and both he and his assistant, Ngadiman bin Haji Ismail, often suffered painful

monkey-bites. Closer to Singapore, the Mawai-Sungei Sedili swamp-forest, accessible on

single-day forays, was an area of much interest to Corner, and the monkeys were often used

there. To ‘those-in-the-know’, this area is called Corner’s Corner, and it was here that

he contracted a disease akin to black-water fever that very nearly killed him, an end

frustrated by skilled and devoted nursing in the Singapore General Hospital, At that time

the only access to Kuala Sedili was by river from Mawai. Now the time-conscious and

hurry-mad swoosh down to the river-mouth by highway and agricultural settlement has

pushed back very large tracts of the drier forest, and has chased out the elephants, tigers

and wild-life that I have been fortunate enough to see there. But the actual swamp-forest,

by virtue of its wetness, still has a life-expectancy (who knows?) for many years till

l

2 Gardens’ Bulletin, Singapore — X XIX (1977)

‘development’ demands further rapine. So it is good to learn that Corner has written

an account of the Southern Malayan swamp forests that he knows so well and that his

account is soon to appear as a supplement to the Gardens’ Bulletin, Singapore.

Under a growing conciousness for conservation of biological resources, nature reserves

were created in Singapore in 1937 and were put under the Gardens control. Ngadiman

was Head Ranger and the team of monkeys were daily exercised there when they were not

out on expedition. Thus Corner had constant interest in the reserves, especially the Bukit

Timah Reserve where the use of the monkeys added to our knowledge of the tree flora.

The mangrove reserve at Pandan was patrolled by an honorary warden, the late Towkay

Chua Ho Ann, who was allowed to take a limited amount of timber for charcoal burning

as guid pro quo for replanting and his wardenship. During the Japanese occupation Chua

had a big charcoal contract with the Japanese Navy and consequently was ‘in the money.’

Both Holtum and Corner were retained by the Japanese in an advisory capacity in the

Gardens, and Chua was able to pass not inconsiderable sums of money over to Corner

which he used for the benefit of Gardens staff on the black market. During the latter part

of this time, he and Holttum lived in a single room in the Botanic Gardens Director’s

house which was my study while I lived there. Corner, it seems, liked to ‘live dangerously.’

Contact with outside persons was not allowed and the receipt of money, had it been dis-

covered, would have had the most serious consequences. Furthermore, Japanese Military

Officers lived upstairs and their radio had its attractions and risks.

When Singapore surrendered to General Yamashita in 1942, the arrival of Professor

Hidezo Tanakadate rescued the Botanic Gardens from military occupation. Sir Shenton

Thomas, as former Governor of the Straits Settlements, had written a letter requesting the

Japanese authorities to respect libraries, scientific collections, and places of historic interest.

This letter Corner gave to Tanakadate who, with his own high influence and a long friend-

ship with the General from student days, combined the Botanic Gardens and Raffles Museum

into a unit of conservation. Presidency of this unit was accepted by Marquis Tokugawa,

Supreme Consulting Adviser to the Nippon Military Administration, and this organisation

received the personal approval of Count Terauchi, Supreme Commander of S.E, Asia. On

the return of Tanakadate to Tokyo, Professor Kwan Koriba took charge of the Botanic

Gardens, He was assisted by K. Watanabe who, in Singapore and Penang, assembled a

remarkable collection of drawings of economic plants. In 1945 the drawings were deposited

for safety in the Singapore herbarium. In 1960 Watanabe asked if they might be returned

to him for publication, but they could not be found. Then blew an ill wind. In 1963 the old

herbarium was in danger of collapse; its contents were hurriedly removed, and the drawings

came to light. There followed an encyclopaedic work of reference prepared jointly by

Corner and Watanabe: Illustrated Guide to Tropical Plants (1969).

Of the early days, Dr. Furtado, of the Gardens Staff, recalls a matter of interest and

importance that is worth recording. Corner foresaw looting and persuaded the authorities to

have officially signed notices of prohibited entry to the Raffles Library, the Raffles College

and the building of the offices of the law firm Donaldson and Burkinshaw in which lay the

largest private collection of lawbooks. Corner personally drove Tanakadate in the Gardens

lorry to fix up these decrees. Equipment and the books of these buildings were thus saved

from looting and damage. Count Terauchi also directed the valuable books from the

Government House Library to be stored in the Tanglin Barracks. Corner was also able

to salvage parts of the library of the Colonial Secretariat in Empress Place which had been

thrown out of the building. At the end of the war when the Allied Forces entered Singapore

Corner was again instrumental in obtaining similar protection from the British Military

Administration, and though the Garden became a tented campsite no unauthorised entry

was made into the buildings.

During these difficult years both Corner and Holttum, free from administrative duties,

were able to devote much time to research. Corner worked on the larger fungi; and the

development of flowers and fruits of various families of trees, The monograph on Clavaria,

as indeed also, the Durian Theory began to take shape at this time, and in the post war

years we have seen with admiration a succession of major works that must have had their

origins in adversity. But this period had made a mark: he was invalided out of service in

1947, though happily he was soon to regain good health, and we have been delighted to

see him return again and again to Singapore, and as leader of the Royal Society’s expedi-

tions of 1961 and 1964 to Kinabalu in Sabah and of 1965 to the Solomon Islands.

This note started as a brief introduction to the articles that follow. Write something

about Corner’s Singapore days, said the Editors of this Festschrift. There is much, but

let this suffice.

Salam masera! Lanjutkan usia!

(All hail! Long Life!)

Thus we hope it will be with him and with his charming wife, Helga.

. 7

—

E. J. H. Corner’s Botany

by

D. J. MABBERLEY

Botany School, Oxford

The spirit of our little book is one of progress; although nodding to the past.

we are looking ahead. Here then, is not the place to list the events of Professor

Corner’s life, his appointments, wanderings and honours: it has been done before*.

What has not been written is that courses of Tropical Botany at Cambridge begun

by Professor Corner and now, alas, discontinued, were an inspiration to generations

of undergraduates and research students. Further, those beginning in less favourable

surroundings and hearing Professor Corner as a visiting lecturer, have been led to

see through the blinkers of that botany which is orientated to the plants of the

temperate zone and peddled by the pusillanimous, These are the blinkers which

have dragged the study of the whole plant down to the popular image of “‘pressing

flowers’, and driven many to the narrow reaches of the esoteric in pursuit of

academic respectability. Of those fortunate to have been able to shake off such

tyranny, and of the few who were able to do so at the Botany School in Cambridge

under Professor Corner’s supervision, J am privileged to say that I was one,

though the last.

How did it begin? A new schoolmaster fresk from Cambridge went to Rugby:

in the sixth form was John Corner. The schoolmaster had read the writings of

A. H. Church, a remarkable philosopher of botany, then working in the Botany

School at Oxford. Corner read Church’s unassuming, unillustrated and rather slim

Oxford Botanical Memoir entitled Thalassiophyta. Despite the tightly argued and

rather heavy prose, much of which was not understandable to a schoolboy, the

blinkers fell away. Much of the botany taught at Cambridge, whither he went from

Rugby, was, in consequence, dull and uninteresting. He cut lectures. He read. In

1928 he presented a paper (still preserved at the Botany School) on Thalassio-

phyta to the Botany Club. A friend introduced him to Church, and, whilst still a

research student in mycology at Cambridge, he travelled to Oxford to see Church

and became his disciple. Church’s works and teaching, unfashionable at the time,

reflected an astounding vision and an unparalleled grasp of the fundamental

problems of botany. He, who had never ventured beyond Plymouth, could

discourse on the floras of the world. When Corner set out for the forests of

Malaya, Church advised him, “‘Note everything! Draw everything! Photograph

everything!”’, advice passed through Corner to his pupils, and now to Church’s

“great-grand-pupils”’.

This is not the only legacy as we hope this volume shows. It reflects Professor

Corner’s interests as shown by comparison with his list of publications. Some of

the papers are controversial: Professor Corner’s writings have never avoided

controversy. Obvious are the Durian Theory, the new classification of Clavaria,

as well as papers on conservation and the teaching of botany which have encouraged

and excited discussion.

* Flora Malesiana I, 1: 117-118 (1950) & I, 8: XXVI (1974); Biol J. Linn. Soc, 2: 322-324

(1970); Who’s Who: 680 (1975); Flora Malesiana Bull. (29): 2536-2538 (1976).

4 Gardens’ Bulletin, Singapore — X XIX (1977)

The Indomalayan flora and ‘“‘funguses”, figs and breadfruit, durians and

pachycauls; from trees, their form and evolution, to trees and man, to trees in

horticulture and trees in conservation — a few of his subjects. And so here is

offered Stearn’s paper on the impact of tropical rain forest on those introduced

to it for the first time; Ashton on the ecology of the Durian Theory; Soepadmo

and Eow on the reproductive biology of Durio itself; Jarrett on the construction of

the syncarp of Artocarpus; Mabberley on the afroalpine pachycaul flora; White on

the origins of African geoxylic suffrutices, the final bars of the leptocaul opera;

remarks on the evolution of rainforest herbs by Burtt. Brunig & Klinge compare

the structure of forests in Borneo and South America. Van Steenis takes up the

question of differing modes of evolution in animals and plants, while Fedorov

deals with the ‘Vavilovian’ evolution he sees in Dipterocarpaceae. Stone sets down

the infrageneric classification of Pandanus, pachycaul monocotyledons par

excellence, Of the Malayan flora so well known to Professor Corner, Hsuan Keng

describes a new species of Theaceae and Holttum monographs a group of

thelypterid ferns, whilst David and Jaquenoud describe new Tremellales from

Singapore. Perreau & Heim continue the mycological papers with a new Boletus

whilst developmental anatomy is represented by Fahn & Joel’s paper on the

secretory ducts of the mango, and Sporne presents an essay on the enigmatic

girdling bundles of dicotyledonous flowers. The construction studies pioneered by

Professor Corner are represented by the paper of Hallé and Mabberley on primitive

tree-forms while the origin of primitive flowering plants is tackled from a different

angle by Thorne. Professor Corner’s monographic work on Asian and Australian

Ficus is here complemented by a study of the origin of the sycomore in the Middle

East by Galil and co-workers, and by Wiebes’s history of fig wasp research. The

importance and limits of taxonomy are stressed by Heywood and the problems

and objectives of Flora-writing by Frodin, whilst Menninger ends the volume with

a consideration of the aesthetic importance of trees in tropical and subtropical

horticulture.

Although Professor Corner has retired, the flow of work is unabated. The

monumental Seeds of Dicotyledons which appeared in 1976, is the fruit of over

thirty years’ painstaking investigation and interpretation, whilst even now in Shelford

surrounded by his books, notes and collections in a veritable thesaurus botanicus,

enlarged to contain his fungus herbarium and other specimens, he is writing up the

flora of the Sedili River in eastern Johore!

List of Publications

(excluding reviews, letters and reports of discussion)

(To 1 January 1977)*

CORNER, E. J. H. (1927). A cytological investigation of a sport in a plant of

the garden stock. Proc. Linn. Soc. Lond. 139: 75-77.

—_—_——— (1929). A Humariaceous fungus parasitic on a liverwort. Ann. Bot.

43: 491-505.

(1929). Studies in the morphology of Discomycetes I. The marginal

growth of apothecia. Trans. Br. mycol. Soc. 14: 263-275.

(1929). Studies in the morphology of Discomycetes II. The structure

and development of the ascocarp. Trans. Br. mycol. Soc. 14: 275-291.

(1930). Studies in the morphology of the Discomycetes III, The

Clavuleae. Trans. Br. mycol. Soc. 15: 107-120.

* The compiler is indebted to Mrs. Heap of the Botany School Library, Cambridge for

assistance, particularly in tracing some of the rarer items.

E. J. H. Corner’s Botany 5

(1930). Studies in the morphology of the Discomycetes IV. The

evolution of the ascocarp. Trans. Br. mycol. Soc. 15: 121-134.

(1931). Studies in the morphology of the Discomycetes V. The

evolution of the ascocarp (continued). Trans. Br. mycol. Soc. 15: 332-350.

(1931). The identity of the fungus causing wet rot of rubber trees

in Malaya. J. Rubb. Res. Inst. Malaya 3: 120-123.

(1932). The fruit body of Polystictus xanthopus Fr. Ann. Bot.

46: 72-111.

(1932). A Fomes with two systems of hyphae. Trans. Br. mycol.

Soc. 17: 51-81.

(1932). The identity of the brown-root fungus. Gdns’ Bull. Straits

Settl. 5: 317-352.

(1933). A revision of the Malayan species of Ficus: Covellia and

Neomor phe. J. Malay. Brch R. Asiat. Soc. 11: 1-65.

(1934). An evolutionary study in Agarics: Collybia apalosarca and

the veils. Trans. Br. mycol. Soc. 19: 39-88.

(1935). The fungi of Wicken Fen, Cambridgeshire. Trans. Br. mycol.

Soc. 19: 280-287.

(1935). Observations on resistance to powdery mildews. New

Phytol. 34: 180-200.

(1935). A Nectria parasitic on a liverwort: with further notes on

Neotiella crozalsiana. Gdns’ Bull. Straits Settl. 8: 135-144.

(1935). Cassia in Malaya. Malay. Agri-hort. Ass. Mag. 5: 37.

(1935). The seasonal fruiting of agarics in Malaya. Gdns’ Bull.

Straits Settl. 9: 79-88.

(1936). Hygrophorus with dimorphous basidiospores. Trans. Br.

mycol. Soc. 20: 157-184.

(1938). Annual Report of the Director of Gardens for the year 1937.

Singapore: Govt, Printing Office.

(1938). The systematic value of the colour of withering leaves.

Chronica bot. 4: 119-121.

(1939). Notes on the systematy and distribution of Malayan

phanerogams. Part I. Gdns’ Bull. Straits Settl. 10: 1—SS.

(1939). Notes on the systematy and distribution of Malayan

phanerogams. Part II. Gdns’ Bull. Straits Settl. 10: 56-81.

(1939). A revision of Ficus, subgenus Synoecia. Gdns’ Bull. Straits

Settl. 10: 82-161.

(1939). Notes on the systematy and distribution of Malayan

phanerogams. Part III. Gdns’ Bull. Straits Settl. 10: 239-329.

———————— (1940). Botanical monkeys. Malay Agri-hort. Ass. Mag. 10:

147-149.

(1940). Wayside Trees of Malaya, Vol. 1: 770 pp; vol. II: 228 pl.

Singapore: Government Printing Office [2nd Ed. 1952].

168: 1031.

Gardens’ Bulletin, Singapore — X XIX (1977)

(1940). Note: larger fungi in the tropics. Trans. Br. mycol. Soc.

24: 357.

(1941). The flora of Singapore. Malay. Agri-hort. Ass. Mag. 11:

59-62. |

(1941). Further notes on the Moreton Bay Chestnut, (Castano-

spermum australe). Malay. Agri-hort. Ass. Mag. 11: 151-154.

(1941). A naturalist’s companion. Malay. Nat. J. 2: 11-14.

(1941). Notes on the systematy and distribution of Malayan

phanerogams IV — Ixora. Gdns’ Bull. Straits Settl. 11: 177-235.

(1946). Suggestions for botanical progress. New Phytol.45: 185-192.

(1946). Tropical biology — an international problem. Biol. &

Human Affairs. 12: 53-57.

(1946). Centrifugal stamens. J. Arnold Arbor, 27: 423-437.

(1946). The pig-tailed monkey as a plant-collector. Zoo Life

1: 89-92.

(1946). Need for the development of tropical ecological stations.

Nature 157: 377.

(1947). Variation in the size and shape of spores, basidia and

cystidia in Basidiomycetes. New Phytol. 46: 195-228.

(1948). Asterodon, a clue to the morphology of fungus fruit-bodies:

with notes on Asterostroma and Asterostromella. Trans. Br. mycol. Soc. 31:

234-245.

(1948). Studies in the basidium 1, The ampoule effect, with a note

on nomenclature. New Phytol. 47: 22-49.

(1949). The Annonaceous seed and its four integuments, New

Phytol. 48: 332-364.

(1949). The Durian Theory or the origin of the modern tree. Ann.

Bot. (N.S.) 13: 367-414: translated (1964) as ‘‘La théorie du Durian ou

Porigine de lVarbre modern. Adaptation francaise par N. & F. Hallé”

Adansonia (N.S.) 4: 156-184.

(1950). A Monograph of Clavaria and allied Genera, Ann. Bot.

Mem. 1: 740 pp. + 16 pl.

(1950). Descriptions of two luminous tropical agarics (Dictyopanus

and Mycena). Mycologia 42: 423-431.

(1950). Report on fungus-brackets from Star Carr, Seamer. Pp.

123-124 in F. G. D. Clark, Preliminary report on excavations at Star Carr,

Seamer, Yorkshire (Second season 1950). Proc. prehist. Soc. 1950 (9): 109-129.

(1951). Prof. H. Tanakadate, Nature 167: 586.

— (1951). The Leguminous seed. Phytomorphology 1: 117-150.

(1951). Lectotypes in mycology: a taxonomic proposal. Nature

(1952). Durians and dogma, /ndones. J. nat. Sci. 5-6: 141-145.

—— (1952) Generic names in Clavariaceae. Trans. Br. mycol, Soc.

35: 285-298.

E. J. H. Corner’s Botany 7

(1952). Addenda Clavariacea I. Two new Pteruloid genera and

Deflexula. Ann. Bot. (N.S.) 16: 269-291.

(1952). Addenda Clavariacea II. Pterula and Pterulicium. Ann. Bot.

(N.S.) 16: 531-569.

(1953). Addenda Clavariacea III. Ann, Bot. (N.S.) 17: 347-369.

(1953). The construction of polypores — I. Introduction: Polyporus

sulphureus, P. squamosus, P. betulinus and Polystictus microcylus. Phytomor-

phology 3: 152-167.

(1953). The Durian Theory extended — I. Phytomorphology 3:

465-476.

(1953). Proposal No. 10, principles for stability of nomenclature

(VIIIth Int. Bot. Congr. prop. 10). Taxon 2: 101.

& L. E. HAWKER (1953). Hypogeous fungi from Malaya. Trans.

Br. mycol. Soc. 36: 125-137.

(1954). The classification of higher fungi. Proc. Linn. Soc. Lond.

165: 4-6.

(1954). The Durian Theory extended — II. The arillate fruit and

the compound leaf. Phytomorphology 4: 152-165.

(1954). The Durian Theory extended — III. Pachycauly and

megaspermy — Conclusion. Phytomorphology 4: 263-274.

(1954). Evolution of tropical rainforest. Pp. 34-46 in J. Huxley,

A. C. Hardy & E. B. Ford (eds.), Evolution as a Process. London: Allen &

Unwin.

(1954). Further descriptions of luminous agarics. Trans. Br. mycol.

Soc. 37: 256-271.

(1955). Botanical coilecting with monkeys. Proc. R. Instn Gt Br.

36 (no. 162): 1-16.

———_—— (1955). Epilogia [sic] pro monographia sua. Taxon 4: 6-8.

(1956). Taxonomy and tropical plants. Proc. Linn. Soc. Lond.

168: 65-70.

(1956). A new European Clavaria: Clavulinopsis septentrionalis

sp. nov. Friesia 5: 218-220

K. S. THIND & G. P. S. ANAND (1956). The Clavariaceae of the

Mussoorie Hills (India) II. Trans. Br. mycol. Soc. 39: 475-484.

(1957). Craterellus Pers., Cantherellus Fr. and Pseudocraterellus

gen. nov. Sydowia, beih. 1, Festschr. f. Franz Petrak: 266-276.

(1957). Some Clavarias from Argentina. Darwiniana 11: 193-206.

» K. S. THIND & SUKH DEV (1957). The Clavariaceae of the

Mussoorie Hills (India) VII. Trans. Br. mycol. Soc. 40: 472-476.

-—————. (1958). The Clavariaceae of the Mussoorie Hills (India) IX. Trans

Br. mycol. Soc. 41: 203-206.

(1958) Transference of function. J. Linn. Soc. Bot, 90: 33-40: J.

Linn. Soc. Zool. 44: 33-40

8 Gardens’ Bulletin, Singapore — X XIX (1977)

(1958). An introduction to the distribution of Ficus. Reinwardtia

4: 15-45

CASH, E. K. & E. J. H. CORNER (1958). Malayan and Sumatran Discomycetes.

Trans. Br. mycol. Soc. 41: 273-282.

CORNER, E. J. H. (1959). Vegetation of the humid tropics. Nature 183: 795-796.

——_—_—— (1959). The importance of tropical taxonomy to modern botany.

Gdns’ Bull. Singapore 17: 209-214.

(1960). Taxonomic notes on Ficus Linn., Asia and Australasia.

I-IV. Gdns’ Bull. Singapore 17: 368-485.

(1960). The Malayan flora. Pp. 21-24 in R. D. Purchon (ed.), Proc.

Centen. & Bicenten. Cong. Biol., 1958 (Singapore).

(1960). Taxonomic notes on Ficus Linn., Asia and Australasia.

V-VI. Gdns’ Bull. Singapore 18: 1-69.

(1961). Impact of man on the vegetation of the humid tropics.

Nature 189: 24-25.

(1961). Agnes Arber. Phytomorphology 11: 197-198.

(1961). A tropical botanist’s introduction to Borneo. Sarawak

Mus. J. 10: 1-16.

(1961). Taxonomic notes on Ficus Linn., Asia and Australasia.

Addendum. Gdns’ Bull. Singapore 18: 83-97.

(1961). Introduction. Pp 1-7 in J. Wyatt-Smith & P. R. Wycherley

(eds), Nature Conservation in Western Malaysia, Kuala Lumpur: Malay.

Nat. Soc.

(1961). Evolution. Pp. 95-115 in A. M. McLeod & L. S. Cobley

(eds), Contemporary Botanical Thought. Edinburgh: Oliver & Boyd.

(1961). A note on Wiesnerina (Cyphellaceae). Trans. Br. mycol.

Soc. 44: 230-232.

CORNER, E. J. H. & K. S. THIND (1961). Dimitic species of Ramaria (Clava-

riaceae). Trans. Br. mycol. Soc. 44: 233-238.

(1962). Botany and prehistory. Pp. 38-41 in [U.N.E.S.C.0.],

Symposium on the Impact of Man on the Humid Tropics Vegetation, Goroka

1960.

(1962). The Royal Society Expedition to North Borneo, 1961.

Emp. For. Rev. 1962: 224-233.

(1962). The classification of Moraceae. Gdns’ Bull. Singapore

19: 187-252.

(1962). Taxonomic notes on Ficus L., Asia and Australasia.

Addendum II. Gdns’ Bull. Singapore 19: 385-415.

& C. BAS (1962). The genus Amanita in Singapore and Malaya.

Persoonia 2: 241-304.

(1963). The tropical botanist. Advmt Sci, Lond. 20: 328-334.

(1963). Ficus in the Pacific region. Pp. 233-249 in J. L. Gressitt

(ed), Pacific Basin Biogeography. Honolulu: Bishop Mus. Press.

E. J. H. Corner’s Botany 9

(1963). A criticism of the gonophyll theory of the flower.

Phytomorphology 13: 290-292.

(1963). A Dipterocarp clue to the biochemistry of Durianology.

Ann. Bot. (N.S.) 27: 339-341.

(1963). Studies in the flora of Thailand 16. Moraceae. Dansk Bot.

Ark. 23: 19-32.

(1936). Exploring North Borneo. New Scient. 366: 488-490.

(1963). Royal Society Expedition to North Borneo 1961: reports.

Proc. Linn. Soc. Lond. 175: 9-32 (General Report); 37-45 (Special Reports).

(1964). The Life of Plants. Pp. 315 + 41 pl. London: Weidenfeld

& Nicholson. [Also trans. Léo Dilé as La Vie des Plantes (1964), and trans.

Lucia Maldacea as La Vita delle Plante (1972), both with additional pp.

after p. 316 by P. Coursin.]

(1964). A discussion of the results of the Royal Society Expedi-

tion to North Borneo, 1961. Organized by E. J. H. Corner. Proc. R. Soc. Lond.

B161: 1-91 (Commentary on the general results: pp. 3-6; Conclusion: pp.

90-91).

(1965). Check-list of Ficus in Asia and Australasia with keys to

identification. Gdns’ Bull. Singapore 21: 1-186.

(1965). Mount Kinabalu East. Sabah Soc. J. No. 4: 170-187.

(1966). A Monograph of Cantharelloid Fungi. Ann. Bot. Mem.

2: 255 pp. + 5 pl.

(1966). The Natural History of Palms. Pp. 393 + 24 pl. London:

Weidenfeld & Nicholson.

(1966). Debunking the New Morphology. New Phytol.65: 398-404.

(1966). Species of Ramaria (Clavariaceae) without clamps. Trans.

Br. mycol. Soc. 49: 101-113.

(1966). Kinabalu. Straits Times Annual 1966: 34-37.

(1966). On Clavaria inaequalis Fr. Nova Hedwigia 12: 61-63.

(1966). The clavarioid complex of Aphelaria and Tremelloder-

dropsis. Trans. Br. mycol. Soc. 49: 205-211.

(1966). Paraphelaria, a new genus of Auriculariaceae. Persoonia

4: 345-350.

(1967). Ficus in the Solomon Islands and its bearing on the post-

Jurassic history of Melanesia. Phil. Trans. R. Soc. Lond. B253: 23-159.

(1967). On thinking big. Phytomorphology 17: 24-28.

——————— (1967). Notes on Clavaria. Trans. Br. mycol. Soc. 50: 33-44.

(1967). Clavarioid fungi of the Solomon Islands. Proc. Linn. Soc.

Lond. 178: 91-106

(1967). Biological expeditions. May & Baker Lab. Bull. 7: 90-92.

(1967). Moraceae. [Bot. Rep. Danish Noona Dan Expedition].

Dansk bot. Ark. 25: 64-67.

10 Gardens’ Bulletin, Singapore — X X1X (1977)

(1968). A monograph of Thelephora (Basidiomycetes). Beih. zur

Nova Hedwigia 27: 110 pp + 4 pl.

(1968). Mycology in the tropics— apologia pro monographia sua

secunda. New Phytol. 67: 219-228.

(1968). Conservation — future prospects. Biol. Conserv. 1: 21-26.

(1969). Notes on Cantharelloid fungi. Nova Hedwigia 18: 738-818.

(1969). A discussion of the results of the Royal Society Expedition

to the British Solomon Islands Protectorate, 1965. Organized by E. J. H.

Corner. Phil. Trans R. Soc. Lond. B255: 185-631 (Introduction: 187-188;

Ficus: 567-570; The botany of Jaagi Is., Santa Isabel: 571-573; Mountain

‘flora of Popomanusen, Guadalcanal: 575-577; Larger fungi of the Solomon

Islands: 579; Summary of the discussion: 621-623).

(1969). The complex of Ficus deltoidea; a recent invasion of the

Sunda Shelf. Phil. Trans. R. Soc. B256: 281-317.

(1969). Ficus sect. Adenosperma, Phil. Trans. R. Soc. B256:

318-355.

(1969). The conservation of scenery and wild life. Proc. Ceylon

Asst. Advmt Sci. 2: 220-231.

(1969). Ecology and natural history in the tropics. Proc. Ceylon

Asst. Advmt Sci. 2: 261-273.

WATANABE, K. & E. J. H. CORNER (1969). Illustrated Guide to Tropical

Plants. 1147 pp. Tokyo: Hirokawa.

CORNER, E. J. H. (1970). Ficus subgen. Ficus. Two rare and primitive pachycaul

spscies. Phil.’ Trans, “Ise B259: 353-381.

(1970). Ficus subgen. Pharmosycea with reference to the species of

New Caledonia. Phil. Trans. R. Soc. Lond. B259: 383-433.

(1970). New species of Streblus and Ficus (Moraceae). Blumea

18: 393-411.

(1970). Phylloporus Quél. and Paxillus Fr. in Malaya and Borneo.

Nova Hedwigia 20: 793-822.

(1970). Supplement to “‘A Monograph of Clavaria and _ allied

genera’’. Beih. zur Nova Hedwigia 33: 299 pp. + 4 pl.

(1970). 37. Ficus (Moraceae). Ident. Lists Malaysian Spec.:

537-648b. Foundation Flora Malesiana.

(1971). Merulioid fungi in Malaysia. Gdns’ Bull. Singapore 25:

355-381.

(1971). Mycological reports from New Guinea and the Solomon

Islands. 4, Enumeration of the Clavariaceae, Bull. natn Sci. Mus., Tokyo

$4: 423-427.

(1972). New taxa of Ficus (Moraceae). Blumea 20: 427-432.

(1972). Studies in the basidium — spore space and the Boletus

snore. Gdns’ Bull. Singapore 26: 159-194.

(1972). Boletus in Malaysia. 263 pp. +- 23 p. Singapore: Govt.

Printing Office.

E. J. H. Corner’s Botany 1]

(1972). 43. Ficus (Moraceae) from India, Burma, Thailand, China,

Korea, Japan, Ryu Kyu, Formosa and Hainan, Ident. Lists Malaysian Spec.:

735-784. Foundation Flora Malesiana.

(1972). Urgent exploration needs: Pacific Floras. Pac. Sci. Assoc.

Inform. Bull. 24: 17-27.

(1974). Boletus and Phylloporus in Malaysia: further notes and

descriptions. Gdns’ Bull. Singapore 27: 1-16.

(1975). New taxa of Ficus (Moraceae) 2. Blumea 22: 299-309.

(1975). Prototypic organisms XIII. Tropical trees. Theoria to

Theory 9: 33-43.

(1975). The evolution of Streblus Lour. (Moraceae): with a new

species of sect. Bleekrodea. Phytomorphology 25: 1-12.

(1975). Ficus in the New Hebrides. Phil. Trans. R. Soc. Lond.

B 272: 343-367.

(1976). The climbing species of Ficus: derivation and evolution.

Phil. Trans. R. Soc. Lond. B 273: 379-386.

(1976). The Seeds of Dicotyledons. Vol. I: 311 pp.; Vol. II:

552 pp. Cambridge: Cambridge University Press.

—— (1976). Further notes on Cantharelloid fungi and Telephora. Nova

Hedwigia 27: 325-342.

—_———_ (1976). A new species of Parartocarpus Baillon (Moraceae).

Gdns’ Bull, Singapore 28: 183-190.

(in press). The freshwater swamp-forest of south Johore and

Singapore. Gdns’ Bull. Singapore, Supp. 1.

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The Earliest European Acquaintance

with Tropical Vegetation

by

WILLIAM T. STEARN

British Museum (Natural History), London

“Das Glanzstiick der botanischen Mitteilungen tiber ost-indische Pflanzenwelt

die unter Alexander erschienen, ist die Schilderung des riesigen Feigenbaums, des

Banyan,” wrote Hugo Bretzl in his massive work on the botanical results of

Alexander the Great’s invasion of northern India in 326-325 B.C., Botanische

Forschungen des Alexanderzuges (1903). With this account of the banyan (Ficus

benghalensis L.) preserved in Theophrastus’s Enquiry into Plants ( péri phuton

historia), there began well over two thousand years ago the European investiga-

tion of the genus Ficus in tropical Asia to which Professor John Corner has made

such illuminating contributions. Theophrastus (370-c.285 B.C.) himself never went

to India; as a pupil first under Plato, then under Aristotle, whose library and

garden he inherited, and later as an academic teacher, he spent almost all his life

in Athens. His career spanned completely the life of Alexander (356-323 B.C.),

whose army undoubtedly included well-educated highly intelligent observers and

recorders, and the reports of these officers came into Theophrastus’s hands, Their

firsthand accounts disappeared long ago but parts have survived, being embedded,

like fragments of Roman masonry in medieval walls, within the writings of others,

notably Theophrastus and Arrian, and among them is the description of the banyan,

the Indian fig (suké hé indiké), praised so highly by Bretzl. This occurs in

Theophratus’s Enquiry IV. iv. 4-S.

Since so much of Professor Corner’s life, research and writing has been

devoted to the study of tropical plants, particularly those of Indo-Malaya, the

celebration of his seventieth birthday provides a fitting occasion on which to bring

to notice again these first records of the impact of tropical vegetation upon the

receptive analytic Western mind.

Even for a present-day young botanist versed firsthand only in the north

temperate flora, first acquaintance with the strange diverse vegetation of the tropics,

with plants of a luxuriance and character unknown in Europe and North America,

is a stimulating and mentally bewildering or overwhelming experience. A succession

of narratives indicate that this has always been so.

Thus Henry Walter Bates arrived with Alfred Russel Wallace at Para, Brazil,

on 28 May 1848, having left Liverpool on 26 April. They immediately walked

across the town, then small and closely encompassed by native vegetation. ““The

impressions received during this first walk,’ Bates wrote in his The Naturalist on

the River Amazons (1863) after eleven years in the Amazon valley, “can never

wholly fade from my mind ... ... so striking, in the view, was the mixture of

natural riches and human poverty ... ... But amidst all, and compensating every

defect, rose the overpowering beauty of the vegetation ... ... Strange forms of

vegetation drew our attention at every step.” Tropical fruit trees, tall palms with

smooth columnar stems, epiphytes perched amid boughs, slender woody lianes,

luxuriant creeping plants overrunning alike tree-trunks, roofs and walls, sword-

leaved bromeliads and many other plants remarkable in leaf, stem or manner of

13

14 Gardens’ Bulletin, Singapore — X XIX (1977)

growth together exemplified for them “‘the teeming profusion of Nature’, to which,

as night came on, the whirring of cicadas, the shrill stridulation of grasshoppers,

each sounding its peculiar note, the hooting of tree frogs, the croaking of toads

and frogs in pools together provided an audible expression almost deafening. This

rich diversity had earlier affected Alexander von Humboldt and Aimé Bonpland

as vividly. They arrived at Cumana, Venezuela, on 16 July 1799, having sailed

from Spain on 4 June 1799. The effect of the tropical environment upon both the

travellers led Alexander to write to his brother Wilhelm: ‘What trees! Coco-nut

trees 50-60 feet high; Poinciana pulcherrima* with a foot high bouquet of magni-

ficent bright red flowers; pisang and a host of trees with enormous leaves and

scented flowers, as big as the palm of a hand, of which we knew nothing ... ... We

rush around like the demented; in the first three days we were unable to classify

anything; we pick up one object to throw it away for the next. Bonpland keeps

telling me he will go mad if the wonders do not cease.”

Even earlier James Wallace (d. 1724), an Orkney man who had taken part

in the ill-fated Scottish attempt of 1698-1700 to found a colony at Darien, Panama,

wrote: ““This place affords legions of monstrous plants enough to confound all the

methods of Botany ever hitherto thought upon ... ... some of their leaves exceed

three ells in length and are very broad, besides these Monsters, reduceable to no

Tribe, there are here a great many of the European kindred but still something

odd about them’’. The equally remarkable tropical vegetation of Amboina in the

East Indies inspired Georg Everard Rumpf. (c. 1627-1702) to the vast task of

preparing his Herbarium Amboinense (6 vols, 1741-1750) which describes vividly

and accurately some 1200 species.

In southern India the governor of the Dutch possessions along the Malabar

coast, Hendrik Adriaan von Rheede tot Draakenstein (1637-1692), was so

impressed by the diversity of plants there, particularly by the epiphytes — ‘“‘on

one tree ten or twelve different sorts of leaves, flowers and fruits might be met

with,”’ as he said — that he set in hand the preparation of a detailed account, on

which were engaged himself, an Italian missionary, about sixteen learned Brahmins,

four artists and various native collectors. His Hortus Indicus Malabaricus (12

vols. folio, 1678-1703) was the first major work to bring a tropical flora to the

notice of stay-at-home botanists in Europe. He introduced the banyan into cultiva-

tion at Amsterdam.

These works were by-products of European conquest and dominion, above

all of the establishment of the Dutch empire in the East Indies during the 18th

century A.D., an empire reached only after a long and hazardous voyage around

Africa. The first European contact with tropical vegetation likewise resulted from

European empire-building in Asia, but was made overland in the 4th century B.C.

Having defeated Darius in 331, Alexander marched his army into Turkistan

(Bactria) and then in 327 invaded north-western India by way of the Khyber Pass

and entered the Punjab; the river Indus became the eastern boundary of his

extended Asiatic empire. Short-lived though this was, it led to a flow of Greek

ideas and art into northern India and a flow of information about the country

back to Greece. Such information must have been very extensive, since the

surviving fragments of it, preserved in the writings of Theophrastus, Plutarch,

Strabo and Pliny, for example, embrace Indian customs and geography as well as

plants. Bretzl has so exhaustively collected all which is available of a botanical

nature that were his book better known and easy to acquire — it seems to be

scarce, is accessible in few libraries and has never been translated — there would

be little justification for calling attention to this here. It deserves, however, not to

be forgotten.

* Caesalpinia pulcherrima (L.) Swartz.

Tropical vegetation, European acquaintance 15

The banyan (Ficus benghalensis L.) is an evergreen tree widespread in India

with entire leathery leaves and small red fruits, and rises to about 26 m. (85 feet) and

by pushing down, from its horizontally spreading branches, supporting prop- or

pillar-roots at intervals, spreads over so wide an area that, as Corner has said, it

“develops the biggest crown of any plant in the world’’, One individual tree can

thus make a small wood.

This habit of the banyan, sending down aerial roots from its

branches away from the main stem, caught Greek attention. It raised moreover

an interesting morphological question such as indeed could only be seen as a

question when the study of plants had passed from being purely utilitarian, as was

presumably that of unlettered herb-gatherers, the rhizotomoi (literally ‘root-cutters’),

to being scientific and philosophical as was that of Theophrastus and his associates,

namely the distinction between root and shoot. Clearly Theophrastus rejected the

common view that any underground organ of a plant is a root, in other words, that

all underground parts are homologous, by emphasizing the differences between the

tuber of arum, the bulbs of squill, garlic and onion and the roots they send out.

“His whole treatment of the subject of the roots of plants reads as if he had gone

stealthily to work,” so E. L. Greene wrote in 1909, “‘to undermine an old and

everywhere received opinion that roots are simply the underground parts of plants.”

He based his definition on natural function and not position. This means that roots

like shoots can be aerial and the banyan, though he can never have seen it himself,

had been so well described, possibly even sketched, by Greek observers in India

that it provided a most remarkable example of them. ‘“‘The character and function

of the roots of the Indian fig are peculiar, for this plant sends out roots from the

shoots until it has a hold upon the ground and roots again; and so there comes

to be a continuous circle of roots around the tree, not connected with the main

stem but at a distance from it” (Loeb Classical Library translation by A. Hort,

1: 41; 1916).

Theophrastus had indeed made a detailed study, very remarkable for his

period, of the underground parts of plants, distinguishing between rhizomes, tubers,

bulbs and roots and distinguishing within the last-named various types, a matter

discussed by Greene (1909), Str6mberg (1937) and Arber (1950).

Theophrastus’s fuller account of the banyan occurs later in his work, in a

section on trees and herbs special to Asia: “The Indian land has its so-called

fig-tree which drops its roots from its branches every year, as has been said above,

and it drops them not from the new branches, but from those of last year or even

from older ones; these take hold of the earth and make, as it were a fence about

the tree, so that it becomes like a tent, in which men sometimes even live. The

roots as easily distinguished from the branches being whiter, hairy, crooked and

leafless, The foliage above is also abundant and the whole tree round and

exceedingly large. They say that it extends its shade for as much as two furlongs;

and the thickness of the stem is in some instances more than sixty paces, while

many specimens are as much as forty paces through. The leaf is quite as large as a

shield, but the fruit is very small, only as large as a chick-pea, and it resembles a

fig. And that is why the Greeks named this tree a ‘fig-tree’. The fruit is curiously

scanty, not only relatively to the size of the tree, but absolutely. The tree also

grows near the river Akesines’’. The mixture here of plain fact and of exaggeration

Suggests strongly that it is a description made from memory, perhaps told to

Theophrastus by a soldier returned from India. Thus the leaves of the banyan,

though up to 20 cm. long and, 12 cm. broad, are much smaller than the smallest

round shield (pelté, Latin pelta) of the Ancient Greeks. Nevertheless, in addition

to the general description of habit, this account contains two very significant

remarks. The tree’s prop-roots, though aerial, woody and stem-like, are distin-

guished from stems by being leafless (aphulloi seems a more correct rendering than

the diphulldi of most codices). Moreover the fruits are compared to those of the

16 Gardens’ Bulletin, Singapore — XX1X (1976)

fig (suké, Ficus carica L.) on account of their structure, though not their size;

hence the Greeks classified the banyan as a fig, swké hé indiké; this indicates real

taxonomic insight since the banyan, except for these, is so utterly different from

the cultivated Mediterranean figs.

Theophrastus also mentions in Book IV. iv. 5 other Indian plants, e.g. a very

large tree with a large sweet fruit, presumed to be the jack-fruit (Artocarpus

heterophyllus Lam.), another with a crooked sweet fruit, presumed to be the mango,

(Mangifera indica L.), one with a fruit like the cornelian cherry (Cornus mas

L.), presumed to be the jujube (Zizyphus jujuba Mill.), and another with an oblong

leaf, like the feathers of the ostrich, 2 cubits (3 feet) long, presumed to be the

banana (Musa).

The clothes of the Greeks were made from linen, hemp and wool. In India

they found people wearing clothes that were the product of a tree with a leaf like

the mulberry but resembling the wild rose; this was cotton (Gossypium); the plants

were grown in the plains in rows, so that seen from a distance they looked like

vines.

The mangroves on the sea-coast provided another kind of tropical vegetation

wholly strange to men from the Mediterranean region, which has no counterparts

to these trees growing in tidal waters and partly submerged at high tide. In

December 325 B.C. the Cretan admiral Nearchus with a fleet built for Alexander

on the Hydaspes (now the Jhelum) river sailed into the Persian Gulf from Pattala

(now Tatta east of Karachi), then at a mouth of the Indus though now inland,

while Alexander marched his army into Gedrosia, the modern Makran region of

Baluchistan and adjacent southern Iran, evidently along the coast over part of the

way, for Arrian, quoting Aristobulus, records mangrove trees: “‘one, with a leaf

like laurel, is found growing below high-water mark on the sea-shore; this tree

is left high and dry by the ebb tide, and on the succeeding flood looks as if it were

growing in the sea. Some of them, growing in hollows which do not dry at low

tide, are never out of the water, but even so take no harm from the constant

immersion of their roots. Some trees are as much as 45 feet in height and were

in blossom when Alexander saw them; the flower is rather like the white violet

[i.e. stock, Matthiola incana (L.) R. Br.] but much more fragrant” (Arrian, Life

of Alexander the Great, transl. A. de Sélincourt, 214; 1958). This was either

Avicennia marina (Forsk.) Vierh. or Rhizophora mucronata Lam.

An essentially similar account, derived evidently from Nearchus’s voyage past

the mangrove-fringed creeks on the northern coast of the Persian Gulf, occurs in

Theophrastus’s Enquiry, IV. vii: ““There are plants in the sea which they call

‘bay’ [daphné, Laurus nobilis L.] and olive [élaia, Olea europaea L.] In foliage

the ‘bay’ is like the aria [aria, holm oak, Quercus ilex L.], the ‘olive’ like the real

Olive. The latter has a fruit like olives.”” To this Theophrastus added: “‘On the

islands which get covered by the tide they say that great trees grow, as big as

planes or the tallest poplars, and that it came to pass, that when the tide came up,

while the other things were entirely buried, the branches of the biggest trees

projected and they fastened the stern cables to them, and then, when the tide

ebbed again, fastened them to the roots. And that the tree has a leaf like that of

the bay, and a flower like gilli-flowers [i6n, Matthiola incana] in colour and smell,

and a fruit the size of that of the olive, which is also very fragrant. And it does

not shed its leaves, and that the flower and the fruit form together in autumn and

are shed in spring.” The roots to which the ships were fastened at low tide must

have the prop-roots of Rhizophora, but evidently the Greeks were not there at the

right time to observe the viviparous germination of the fruit; otherwise they would

surely have noted the long club-shaped radicle produced while the fruit still clings

to the bough.

Theophrastus also incorporated observations referring to Avicennia marina

made on the northern coast of the Persian Gulf, probably in the Strait of Hormuz

Tropical vegetation, European acquaintance 17

near Bandar-Abbas, southern Iran: “In Persia in the Carmanian district where

the tide is felt there are trees of fair size like the andrachne [andrachlé, Arbutus

andrachne L.] in shape and leaves; and they bear much fruit like in colour to

almonds on the outside but the inside is coiled up as though the kernels were all

united”. This obviously refers to the longitudinally folded cotyledons, one

enclosing the other, in the seed of Avicennia. ““These trees are all eaten away up

to the middle by the sea and are held up by their roots”.

Through an exploratory voyage by Androsthenes along the southern coast

of the Persian Gulf the Greeks also became acquainted with the island of Tylos,

a very ancient centre of trade and civilization, now known as Bahrain, and

recorded some of the plants grown there, as noted by Theophrastus. These included

cotton, date palms, an evergreen fig and vines. They also stated “‘that there is

another tree with many leaves [i.e. leaflets] like the rose and that this closes at

night but opens at sunrise and by noon is completely unfolded; and at evening

again it closes by degrees and remains shut at night, and the natives say that it goes

to sleep”. This is the first record of the sleep-movement of the tamarind (Tamar-

indus indica L.), indeed of any plant.

Bamboos are so important in the rural economy of India and grow there to

so much greater heights than those of the two similar plants known to the Greeks,

the common reed (Phragmites australis (Cav.) Trin. ex Steud.) and the giant reed

(Arundo donax L.), that it would be strange indeed if the Greeks had failed to

mention them at all. Theophrastus’s reference to them in his Enquiry IV. xi. 13

is, however, brief: ‘““The Indian reed is very distinct and as it were of a wholly

different kind; the ‘male’ is solid and the ‘female’ hollow ... ... a number of reeds

of this kind grow from one base and they do not form a bush, the leaf is not long,

but resembles the willow leaf, these reeds are of great size and good substance, so

that they are used for javelins’. The terms ‘male’ and ‘female’ are used here

metaphorically as they were for other plants, excluding however the date-palm;

the ‘male’ has been identified as Dendrocalamus strictus (Roxb.) Nees, the ‘female’

as Bambusa arundinacea (Retz.) Willd.

Since Theophrastus, Arrian and other Ancient Greek writers only incorporated

such information about tropical plants and vegetation as was relevant to their own

work, almost indeed incidentally, it is reasonable to believe that the sources whence

this came must have contained much more which has long been lost. Theophrastus’s

task in his botanical writings — he also wrote on astronomy, education, ethics,

logic, mathematics, odours, meteorology, religion and rhetoric — was to bring

together an immense quantity of information, no small part based upon his own

observations, which he presented in a classified form, using facts not simply for

themselves but also to provide examples for general statements, giving particular

attention to differences which delimited or expressed the essential nature of subjects.

It was his intention not to list all the known individual kinds of plants but simply

those characteristic of certain features or regions. His fourth book in the Enquiry

deals with the plants special to particular districts and habitats; in the sections

relating to Asia, since he had never been there himself, he accordingly extracted

what seemed especially interesting or relevant from the writings and recollections

of his contemporaries who had accompanied Alexander on his invasion of India.

Indeed he said “‘there are also many more different from these found among the

Hellenes, but they have no names, There is nothing surprising in the fact that these

trees have so special a character; indeed, as some say, there is hardly a single tree

or shrub or herbaceous plant, except a few, like those in Hellas”’.

The task of Arrian, who lived some four hundred years later, was to write a

reliable biography of Alexander, again taking what seemed relevant from earlier

sources. The loss of these sources is not surprising. Thus the immense libraries of

Pergamon and Alexandria had virtually perished by the 5th Century A.D., their

18 Gardens’ Bulletin, Singapore — XX1X (1976)

decline hastened by fanatical Christians who regarded them as pernicious reposito-

ries of pagan literature. Because of this, the effect upon the Hellenic world of the

new knowledge stemming from Alexander’s Asiatic conquests can only be dimly

surmised. In the field of botany it enlarged European vision by bringing to notice

plant structures, such as the banyan with its prop-roots, and ways of life, such as

that of the mangroves growing as trees within the sea, as well as individual plants,

which had no counterparts in Europe. Various European plants perform nyctitropic

movements of the leaflets but none so conspicuously as does the tamarind. This

extension of biological concepts through contact with tropical vegetation is

necessary to counteract the impoverishing narrowness of outlook and experience

which afflicts botany taught from a few plants in the laboratory by teachers who

have never felt the excitement of seeing the plant world in its most complex form,

above all in tropical rain forest regions, As Professor Corner has said in the last

chapter of his The Life of Plants (1964), “‘high rainfall, sunshine and temperature

make the tropical forest the prime of plant life ... ... But the forests, which show

how trees were made, are going. They are vanishing nowhere faster than from the

alluvial plains where the vestiges of the last creative phase of plant life, that

prepared the way for the modern world, may survive’’. Because Professor Corner,

with a stimulating breadth of outlook fostered in the tropical environment of

Malaya, has striven so much to make stay-at-home European botanists aware of

the evolutionary significance of tropical plants and the urgent need to study them

before destruction of their habitats deprives humanity of many of them forever,

it has been appropriate to recall here the first chapter in the history of European

botanical contact with their challenging diversity.

Some Sources of Further Information

ARBER., A. 1950. The Natural Philosophy of Plant Form, Cambridge University

Press.

ARRIAN. 1958. The Life of Alexander the Great, Transl. by A. de Sélincourt.

London, Penguin Books.

BRETZL, H. 1903. Botanische Forschungen des Alexanderzuges. Leipzig.

GREENE, E. L. 1909, Landmarks of Botanical History, Part 1 (Prior to 1562

A.D.). Washington, D.C.

SENN, G. 1934. Die Pflanzenkunde des Theophrast von Eresos. Basel.

STEARN, W. T. 1957. Botanical exploration to the time of Linnaeus, Proc. Linn.

Soc. Lond. 169 (sess. 1956-57): 173-196.

STROMBERG, R. 1937. Theophrastea: Studien zur botanischen Begriffsbildung.

(Géteborgs Kungl. Vet. Handl. V. A. 6 no 4). Goteborg.

THEOPHRASTUS. 1916. Enquiry into Plants, Transl. by A. Hort. 2 vols. (Loeb

Classical Library). London & New York.

Ecology and the Durian Theory

by

P. S. ASHTON

Department of Botany, University of Aberdeen

The Durian Theory (Corner 1949-1964) is on a base of comparative

morphology, yet provides insight on the ecology and evolution of tropical forest.

The hypothetical angiosperm archetype that is deduced from it no longer exists;

from ecological theory though we may speculate why this is so, and may deduce

the conditions in which these plants evolved. What ecological bonuses and limita-

tions does each of the primitive characteristics impose?

Large spiny loculicidally dehiscent capsule or follicles, with large black seeds more or

less enveloped in a colourful fleshy aril and dangling on persistent funicles. A large

seed provides a large food store. essential in the perennial shade of evergreen

forest. In a windless climate fruit dispersal of forest plants is most effectively

accomplished by animals, yet the large slowly developing seed must be protected

from them until ripe. The significance of colour and movement to attract animal

vectors has been discussed at length by Corner. It is astonishing how disinterested

even monkeys are with green fruits; we have observed that the embryo and flesh

of wild rambutan (Xerospermum intermedium Radlk.) fruits matures before the

pericarp changes from green to yellow, yet the voracious monkeys always failed to

distinguish maturity before the colour change. Experience of modern trees may have

led them to fear all green fruits as unpalatable or poisonous; primitive armour,

once pierced, provides protection against no predator, but the evolution of specific

poisons reduces attacks to a few specialists. When in Sarawak I had the opportunity

to identify the food of orangutans set free in Bako National Park, I was struck by

the dexterity with which they dismembered the horrid defenses of rotan and nibong

cabbages, and wondered whether these primates might be recent immigrants,

possibly to the extending Holocene forests; otherwise such plants as the hapaxanthic

Plectocomia, a particular favourite, would have disappeared as, we can assume,

already have many other spiny but palatable organisms of former days.

Moreover, these great spiny primitive fruits are expensive and can only be

produced in small numbers at a time; they confine those plants that bear them to

stable habitats where their populations are least likely to suffer large fluctuations,

and in places where opportunities for establishment are greatest. Such is the case

in the shade of the forest canopy, but where is the pioneer with such a fruit? The

mature phase of the forest is hence the home of our large seeded tropical fruits,

and many more live there still awaiting cultivation; destroy the forest and this

bounty will be lost.

Stout, pithy-stemmed, unbranching and monocarpic trees, with a terminal inflores-

cence. Such a habit and reproductive strategy still occurs in some palms and other

monocotyledons, but is rare among dicotyledons. The polygamodioecious tree-ivy

Harmsiopanax of New Guinea is one example. It is a semigregarious treelet with

huge pinnatisect leaves, of mid-mountain glades. As a nomad, however, it

produces an abundance of flowers and small fruit as do such monocarpic palms. A

large fruited monocarpic progenitor could only maintain cross-pollination, and

hence the genetic variability for further continued evolution, by growing in

19

20 Gardens’ Bulletin, Singapore — XX1X (1976)

gregarious stands; each unbranching treelet would thus be analogous to the

monocarpic stems of the rhizomatous branching sago-palm Metroxylon. A stout

pithy stem is the perfect adaptation to the unbranched monocarpic habit; The

tube as a supporting structure is cheap and provides adequate tensile strength for

a vertical member in a windless environment; while, as every Melanau sago

farmer knows, the pithy core, which in dicotyledons expands as the apex enlarges

(eg. Mabberley, 1974b), is the bank where insoluble polysaccharides gradually

accrete until, in a flamboyant vegetable sneeze, they are converted to soluble sugars

and surge up the giant terminal inflorescence into the developing flowers and fruits.

The biochemistry of durianology demands further attention!

Large pinnate leaves borne spirally with short internodes. Givnish has elegantly

defined the adaptive significance of leaf size and shape: large entire leaves are

structurally and photosynthetically efficient individually, but carry a high heat load

and are therefore expensive on water resources. They more completely exclude light

beneath than small leaves do and thus reduce the leaf area index. Pinnate leaves

comprise small leafy organs borne on deciduous twigs; when arranged in dense

spirals they will still cast the deep shade of large entire leaves yet bear a lesser heat

load. Evergreen trees with large thin leaves, whether entire or variously divided and

in dense spirals, are confined to well-watered habitats even in the humid tropics.

Some, such as the pinnate-leaved Chisocheton and pinnatisect Heliciopsis are in

the forest understorey and bear large, usually dehiscent fruits; here, as Givnish

points out, the large thin leaf is advantageous on the ‘gamblers ruin’ principle, by

spreading a given number of chloroplasts horizontally the chance of encountering

sunflecks is increased. Others, such as the small fruited tree-ivies Harmsiopanax

and Arthrophyllum skirt the forest fringe on river banks and in gaps. Here large

rapidly transpiring leaves, which prevail among nomad trees of well-watered places,

provide the most economic means of building a photosynthesizing mantle for

rapid growth and at the same time cast deep shade, deterring competition. In a

densely spirally pinnate-leaved slow-growing tree the latter advantage is still

conferred, as anyone who has rested in the uncluttered shade of Dracontomelum

mangiferum Bl. on a Bornean river bank will remember with gratitude.

If now we add a massive inflorescence of large actinomorphic magnoliaceous

flowers, with weakly differentiated perianth and many centrifugal stamens, we

further define our plant’s ecology. Such flowers are a crude means of ensuring cross-

pollination, unless self-incompatable. They are expensive to produce, and the

greater part of the costly pollen will be wasted, unless the trees are gregarious

which, as we have already suggested, they probably were, or the flowers conspicuous

and the vectors specific and far-roaming. The simple thin-walled short-lived pollen

grain so common among still existing primitive families has, like the fruit, confined

them to habitats where the atmosphere is warm and humid at least during the

flowering season.

The stage may now be set for the reenactment of angiosperm evolution: we

can visualise hills clothed in tall Araucaria forest; ferns grow in the deep shade

beneath, while Cycadophytes and Caytoniales occupy the open fringes, along rocky

tidges and in swampy plains. The gap phase of the Araucaria forest would have

lacked the fast growing opportunists of modern rain forests. Here, on moist stable

fertile slopes, hence especially on basic volcanic soils, the protoangiosperm would

have found its niche; from a massive seed a tall shoot rapidly overtopped its

gymnosperm seedling competitors in the shafts of light penetrating the crowns of

ageing giants, allowing the building of the light-excluding schopf of densely spiral

large pinnate leaves. Only its own kind could survive beneath its shade, and thus

small, temporarily isolated but eventually expanding and coalescing, gregarious

stands would accumulate on these slopes. These short unbranched trees hence

excluded gymnosperms from the most favourable sites by depriving them of

suitable conditions for establishment. This remains the secret of angiosperm

Ecology and the Durian Theory 21

success, and even now it is the gymnosperms which, if allowed to, can finally

achieve the greater growth and stature, as the dwarfing of New Guinean angiosperm

forest by the scattered araucarias still witnesses.

Here then are the perfect conditions for further evolution and diversification:

small gregarious colonies with few flowers and free cross-pollination, temporarily

isolated along the slopes and thus allowing rapid local diversification; yet each

valley, and each mountain chain, more permanently isolated. The significance of

animal dispersal now becomes apparent.

The evolution of the enclosed seed in an eventually dehiscing fruit is seen,

then, not to be a response to increasing aridity, for which there is little evidence in

the upper Jurassic-lower Cretaceous period of continental drift, but for the need

to develop a protective covering for the enlarged endosperm until the seed is ready

to germinate.

Why should not cycads have accomplished the same? On the upper slopes of

Susungdalaga in Camarines Sur, Luzon, I have seen Cycas circinalis L. growing

in forest shade on volcanic soils. Their leaflets were sparse and their crowns

diffuse; perhaps their less evolved vascular system and physiology prevents them

from rapidly building and subsequently maintaining the dense excluding crown

of the primitive angiosperm?

Thus the first flowering plants, not gymnosperms, would have provided the

environment in which their further evolution could occur. Only angiosperms could

survive beneath their own shade and hence only angiosperms could eventually

overtop them. The Durian Theory provides a morphological means by which this

could be accomplished. This increase in diversity of tree habit would initially have

been the main source of increased species diversity in the forest, which in itself

necessitated greater subsequent fruit production to overcome declining opportunities

for establishment as interspecific competition increased, and led to the extinction

of the large-fruited monocarpic ancestors. The evolution within the rain forest of

more flexibly arranged, smaller, leaves would also allow a further spread of

angiosperm hegemony into the domain of gymnosperms. Yet the sparsely branching

protoangiospermous habit and spiral divided leaves still retain their advantage in

the forest shade and many modern leptocauls, including a Philippine Knema

(Myristicaceae) and a New Guinea Sloanea (Elaeocarpaceae) with durian-like

fruit, retain this habit as saplings, as Corner has noted in other forest trees.

The evolutionary sequence of early angiospermous forest is partly reenacted

in modern seral succession on moist hillsides. The seeds of modern forest nomads

are small, with little food-store, and germinate in response to light but, once

germinated the saplings rapidly build a tortoise-shell of large overlapping leaves,

expanded by the early formation of ascending pithy shoots; among them are

microsperm pachycauls such as Senecio mannii Hook. f. (illustrated by Mabberley

(1974a) ). This at first, if complete, can effectively deter competition but after a

few years the stems and branches begin to open under their own weight, providing

the setting for the next stage, which will involve the first true leptocauls. Among

them though, and particularly on these well watered sites, the pagoda tree (Corner,

1940) comes to predominate, an ingenious compromise between pachycaul and

leptocaul and probably ancient. This, by intermittent rapid extension of a stout

pithy leader grows first into a tall unbranched sapling with spiral or whorled

leaves; but then, after a period of dormancy, it sprouts a whorl or pseudowhorl of

more or less horizontal branches around the apex, bearing dense ascending

rosettes, typically of obovate leaves by Terminalia branching (Corner, 1940). Thus

an aerial blanket of leaves, often large and presumably rapidly metabolizing is

early formed which overtops and suppresses its many-stemmed predecessors and,

by successive bold extensions, apical dominance is maintained until the final forest

canopy is reached. Only then does apical dominance give way to allow the expansion

of a dome-shaped sympodial crown, often associated with a decline in the size

22 Gardens’ Bulletin, Singapore — X XIX (1976)

and density of the leaves and twigs. The ascending spires of Alstonia, Terminalia,

Bombax, Endospermum, Tetrameles and Octomeles proclaim such a stage in the

forest cycle. Meanwhile other truly leptocaul species are establishing beneath to

fill in the forest frame.

It can be seen then that, first, the complexity of mature phase forest structure

must have been formed; this also by its nature provided obstacles to cross-pollina-

tion, and thus initiated the evolutionary sequence of floral specialization and

diversification by which our modern families are distinguished.

Meanwhile also, microsperm pachycauls evolved into the gap phase of the

forest and the alpine forest fringe, and the differing conditions for reproduction

there led to the origin of such other taxa as Senecio and Lobelia (Mabberley,

1973, 1974c) and eventually herbaceous forms.

It is now apparent why the Myristicaceae, primitive in so many respects and

with primitive arillate fruit, have nevertheless developed the leptocaul habit with

small leaves and plagiotropic branching, and flowers which are small, much reduced

and borne on dioecious trees. Here is a family that has evolved with the forest

from earliest times: first the fruit, then further evolution of the habit, and sub-

sequently the flower while the earlier evolved fruit and habit continue to retain

their adaptive advantage in the shade of the storied modern forest. But the

Myristicaceae, as Corner points out, are tied to the rainforest by their fruit; fell

the forest and they do not return.

As the origin of the primitive angiospermous fruit must be interdependent

with the early evolution of vertebrate vectors, birds and mammals, so the evolution

of the structure of the angiospermous rain forest-not by coevolution this time but

in response to previous vegetational change-provided the means for their rapid

diversification. Animal diversity, once thus initiated, in turn enhanced the coevolu-

tion of flowers and their pollen vectors, of plant hosts and their predators, which

still continues and defines the modern complexity, long after the possibilities of

structure, habit and leaf design had been exhausted and retained or repeated by

many families.

In geological time the disposition of land masses has changed, and the area

occupied by different climates, but the range of climates and soils can rarely have

changed. Life itself provides the changing scene. Evolution of species and phyla

proceeds from what has already evolved before; similarly it is in those habitats

where biotic change has been greatest that we should expect major paths of further

evolution to originate, not in the deserts or the mountains but in the lowland forests

especially those of the humid tropics.

Why, then, do we find monocarpic pachycauls prevailing in the paramo, and

the massive primitive flower more often in the mountains than the lowlands?

Evolution has proceeded outwards from the lowland forests where only the ancient

fruit and pinnate leaves have sometimes survived the palimpsest of subsequent

biotic change in the understorey. But the paramo retains the moist open conditions

of the primitive angiosperm forest while the pachycaul stem is preadapted to

year-round frost (Mabberley 1973, 1974a) and the structural simplicity of the

montane forest, though derived and leptocaul, allows the survival of clumsy

pollination systems. 7

It is therefore naive to conjecture the centre of angiosperm origin from

modern distributions. Besides, great changes in the distribution of climates have

occurred since the Jurassic, necessitating massive migration if not always extinction;

even in South-East Asia Muller has shown that temperate species prevailed,

presumably on long-vanished mountains, during the Miocene.

Similarly, plants only fossilize under restricted conditions. The most primitive

pollen types appear not to fossilize well and it is likely anyway that plant, and

possibly also fruit, form diversified both within the rainforest and into other

Ecology and the Durian Theory 23

environments largely before flower and pollen diversification. Recent fossil evidence

is therefore likely to be misleading. Using the Durian Theory as a basis for predic-

tion we should pursue a different approach and should consciously search out

volcanic ash deposits rather than riverine, swamp or aquatic, from the western

tropical margins of the great late Jurassic oceans. If they do not exist, or bear no

fossils, the origin of the angiosperms will remain enigmatic.

REFERENCES

CORNER, E. J. H. 1940. Wayside Trees of Malaya. Vol. I: 770 pp; vol. II:

228 pl. Government Printing Office, Singapore.

1949. The Durian Theory or the origin of the modern tree. Ann. Bot.

(N.S.) 13: 367-414.

1953. The Durian Theory extended — I. Phytomorphology 3:

465-476.

1954a, The Durian Theory extended — II. The arillate fruit and the

compound leaf. Phytomorphology 4: 152-165.

1954b. The Durian Theory extended — III. Pachycauly and

megaspermy — Conclusion. Phytomorphology 4: 263-274.

1964. The Life of Plants. Pp. 315 + 41 pl. Weidenfeld & Nicholson,

London.

GIVNISH, T. J. 1975. Ecological aspects of plant morphology. Unpublished MS

of paper delivered at XII International Botanical Congress, Leningrad

(Abstract in [A. Takhtajan], Abstracts of the papers presented at the XII

International Botanical Congress, July 3-10, 1975, 1: 214).

MABBERLEY, D. J. 1973. Evolution in the Giant Groundsels. Kew Bull. 28:

61-96.

1974a. Branching in pachycaul Senecios: the Durian Theory and the

evolution of angiospermous trees and herbs. New Phytol. 73: 967-975.

1974b. Pachycauly, vessel-elements, islands and the evolution of

arborescence in ‘herbaceous’ families. New Phytol. 73: 977-984.

1974c. The pachycaul Lobelias of Africa and St. Helena. Kew Bull.

29: 535-584.

MULLER, J. 1966. Montane pollen from the Tertiary of N. W. Borneo. Blumea

14: 231-235.

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The Reproductive Biology of Durio zibethinus Murr.

by

E. SOEPADMO & B. K. EOW

Department of Botany, University of Malaya

Kuala Lumpur

SUMMARY

Durio zibethinus Murr. or the common durian is a fruit-tree species widely cultivated

in villages or orchards or a semi-wild plant found growing around aborigines’ settlements

in Peninsular Malaysia. The species is generally considered by botanists as a native tree in

Borneo and Sumatra, though currently it is commonly planted throughout South East Asia,

extending from the south-eastern parts of India to New Guinea.

In Peninsular Malaysia the flowering is seasonal and normally falls during the months

of March-April and September-October, though accessory flowering may take place in between.

Development of flowers takes about five to seven weeks and the flowering lasts for about

three weeks. Floral parts develop acropetally and the epicalyx, calyx, corolla and stamens

fall off soon after anthesis. Floral anthesis is initiated at about 16.00 hrs. and completed by

about 20.00 hrs. Pollination is carried out by nectarivorous bats (Eonycteris spelaea) and by

an unidentified noctuid moth, and takes place between 20.00 and 01.00 hrs. Pollen grains

are more or less spherical, 80-150 , in diameter, 3-4- or rarely 6-porate, with a smooth but

sticky exine; kept under room temperature they remain viable for about 48 hrs. The flower

is self-compatible, though the percentage of successful fertilisation and production of fruit

reaching maturity increase if the flowers are crossed.

The anthers though initially tetrasporangiate become bisporangiate at maturity. Wall

development conforms with the basic type. Before anthesis the epidermis is made up of more

or less rectangular and isodiametric cells, but towards anthesis these cells become papillate

and filled with tannin, and eventually shed off from the anther wall. The endothecial cells

become fibrous and both the middle layers and the tapetal layer are crushed and disappear,

leaving the endothecium the only wall enclosing the pollen grains. Cytokinesis of microspore

mother cells is simultaneous and gives rise to tetrahedral tetrads. Anther dehiscense is

through a longitudinal slit caused by the breakdown of the wall at the meeting point of the

anther-lobes. Pollen grains are binucleate at the time of shedding.

__ The ovule is anatropous, bitegmic and crassinucellate. The micropyle is formed by both

anal at Embryo-sac development conforms with the Polygonum-type. Antipodal cells are

ephemera

The seed is arillate and its mode of germination is epigeal and takes place within three

days after sowing in garden soil. Seed viability can be prolonged up to 32 days (90%

oo if the seeds are surface-sterilised, kept in an air-tight container and placed under

°C.

INTRODUCTION

Previous works on Durio (Wyatt-Smith, 1953; Kostermans, 1958; Reksodi-

hardjo, 1962 and Kochummen, 1972) indicate that there are at least 28 species in

the genus, distributed throughout Burma, Thailand, Peninsular Malaysia, Singapore.

Sumatra, Borneo and Palawan Island. Though considered by botanists as a tree

native to Sumatra and Borneo, Durio zibethinus or the common durian is now

widely cultivated as a fruit-tree in the South Asia region, covering the south-eastern

parts of India, Ceylon, Burma, Thailand, Indo-china, Malaysia, Singapore.

Indonesia, the Philippines and New Guinea.

Species of Durio are found growing naturally in lowland and hill primary

forests (up to 1000 m altitude) usually not more than 3 to 4 trees per hectare.

Apart from Durio zibethinus there are five other species which produce edible

25

26 Gardens’ Bulletin, Singapore —- X XIX (1976)

fruits (Reksodihardjo, 1962). These are D. dulcis Becc. (found in Sabah and

Indonesian Borneo), D. grandiflorus (Mast.)Kost. (Sabah, Sarawak and the Indo-

nesian Borneo), D. graveolens Becc. (Peninsular Malaysia, throughout Borneo and

Sumatra), D. kutejensis (Hassk.) Becc. (throughout Borneo), and D. oxleyanus

Griff. (Peninsular Malaysia, throughout Borneo and Sumatra). All five are culti-

vated in Brunei and some to a limited extent elsewhere in Malaysian Borneo. The

other species of the genus, though not producing edible fruits, possess several

desirable features for breeding and bud-grafting purposes. These features are:

disease and pest resistance (most wild species), more regular flowering (D. acuti-

folius (Mast.) Kost. & D. griffithii (Mast.) Bakh.), flowers and fruits borne on the

lower parts of the stem (D. beccarianus Kost. & Soeg., pinangianus (Becc.) Ridl.

and testudinarum Becc.), or on the stem as well as on the lower branches (D.

malaccensis Mast.). Though this does not necessarily mean that all species are

easily hybridised, it does imply that, since the specific delimitation of the genus is

mainly based on morphological attributes and since there are several species which

are closely related to each other (e.g. D. zibethinus, malaccensis and wyatt-smithii

Kost.), and, there seem to be many intermediate forms among natural populations

of and between species, there is a possibility to improve the quality as well as the

productivity of the existing edible-fruit producing species, at least by bud-grafting.

In spite of the fact that durian fruit is of high economic importance to local

inhabitants (Lai, 1974), as far as we know there is no large scale plantation or

estate in the region, nor is there a well documented and systematic breeding and

selection programme, This lack of interest may partly be due to the fact that very

little is known about the autecology, flowering biology, cytology and breeding

system of the species. The only paper dealing with some aspects of reproductive

biology of Durio species so far published is that by Valvayor, Coronel & Ramirez

in 1965.

It is therefore the aim of the present study to gather more information about

D. zibethinus and its related species so that their economic potential and contribu-

tion to “durianology” in general is not completely forgotten.

MATERIALS & METHODS

Field work to determine the distribution and frequency and to observe the

phenology, floral anthesis and pollination processes of D. zibethinus and its related

species was carried out in the University of Malaya campus, Damansara village,

Ulu Gombak, Mantin and Kuala Selangor (all in Selangor State), Kuala Pilah and

Pasoh Forest Reserve (in Negri Sembilan), Krau Game Reserve, Taman Negara

and Tioman Island (Pahang). For detailed studies on the floral anthesis and for

pollination experiments, a tree growing in the compound of the Faculty of Agri-

culture, University of Malaya was used.

Flowers of different developmental stages were collected regularly during the

flowering periods, fixed in 50% F.A.A. solution and then sectioned and stained

according to normal schedules. Guano samples were collected weekly from Cavern

C of the Batu Caves Limestone Hill from February 1974 to January 1975, Pollen

content was extracted from these samples and acetolysed and then stained with

safranin.

OBSERVATIONS & RESULTS

Phenology. Depending on the clones, soil and climatic condition in which the

durian tree is planted, it starts to bear flowers and fruits at the age of 5 to 12

years, In Peninsular Malaysia there seem to be two main flowering seasons,

normally falling in the period of March-April and September-October. However,

it should be noted that minor or accessory flowering may occur in between, The

flowers are born in fascicles of 3-30 on the older branches, Flowers of the same

Durio Zibethinus, Reproductive Biology 27

inflorescence usually mature more or less at the same time and open one after

another within a few days. Since during the flowering each individual tree produces

hundreds of flowers, and the maturation of the flowers of different inflorescences

is not necessarily synchronised, the flowering period of a particular season usually

lasts for about two or three weeks. It was also observed that normally the first

flowering of a particular year is heavier than the second. What causes this remains

to be investigated. The fruit set is usually very low since many of the ovaries will

drop after anthesis, either because their ovules are not fertilised or have been

disturbed or destroyed by the pollinators. Fruits take approximately three months

to reach maturity.

Floral morphology and development. At its early stage of development, each

individual flower-bud is a globose structure made up of a mass of homogeneous

cells surrounded and enclosed by bracts and epicalyx. The sepaline, petaline,

staminal and carpellary primordia develop acropetally at more or less the same

rate. The anthers develop from the distal cells of the phalanges as globular pro-

tuberances, Each protuberance is composed of a homogeneous mass of meristematic

cells surrounded by an epidermis. As the phalanges elongate and differentiate into

distinct filaments the developing young anthers assume their 4-lobed appearance.

Just before anthesis the buds attain a size of about 2 cm in diameter. Both the

epicalyx and calyx are externally densely covered with brownish peltate fimbriate

scales, and the petals are yellowish-white and sparsely hairy outside. The scales

are multicellular and originate from the epidermal cells. The nectary is located at

the inner basal part of the calyx-cup. At anthesis the flower reaches about 5-6 cm

long and 2-3 cm in diameter and emits a strong odour reminiscent of sour milk but

somewhat fragrant. The carpels develop and originate from a common primordium

situated at the centre of the flower-bud. This primordium is made

up of homogeneous and more or lesss isodiametric cells. These cells divide and

differentiate into five carpels which fuse at their marginal and central parts to

form a 5-loculate ovary with a central placental column. The style is formed by

vertical growth of the five carpels and is topped by a capitate stigma. The stigmatic

surface is uneven in outline with deep depressions or notches here and there

(Plate 4a). By the time the megaspore mother cell is formed, the spine-primordia

of the ovary wall start to develop. These primordia originate from the hypodermal

layer and appear as conical protuberances each of which is topped by a multi-

cellular, peltate and fimbriate scale similar to those of epicalyx and calyx. As the

flower develops fully, cells in the tissues of the epicalyx, calyx and petals contain

tannin and become mucilaginous.

Development of anther-wall. In each of the anther lobes and just below the

epidermis, a row of hypodermal cells increase in size and contain more conspicuous

nuclei and denser cytoplasm. These cells form the archesporial tissue. Each

archesporial cell divides periclinally into a primary parietal cell and a primary

sporogenous cell (Pl. la). The primary parietal cell further divides periclinally

into two secondary parietal cells. The outer secondary parietal cell divides once

again to give rise to an endothecial cell and outer middle-layer cell. The inner

secondary parietal cell also divides further and produces the inner middle-layer

cell and the tapetal cell. Thus the anther-wall formation conforms well with the

basic type. By the time the sporogenous cell divides and produces numerous

microspore mother cells, the anther wall is greatly stretched and the middle layers

as well as the tapetum are crushed and their cells become flattened. Meanwhile

through the disintegration of the septa separating the four original anther cavities,

the anther becomes two-loculate. Towards the end of meiosis the epidermal cells

become papillate and filled with tannin, and just before the anther dehisces they

are shed off leaving the endothecial cells as the only surviving wall enclosing the

pollen grains. At this stage the wall of the endothecial cells becomes fibrous and

the wall thickening appears as radially oriented bar-like structures.

28 Gardens’ Bulletin, Singapore — XX1X (1976)

Microsporogenesis. By the time the anther wall attains its 4-cells thickness,

the primary sporogenous cell divides into two daughter cells (Plate 1b). These cells

divide both periclinally and anticlinally to form numerous microspore mother

cells (Plate 1c & d). Meiotic division starts from those microspore mother cells

situated at the centre of the anther cavity and progresses outwards (Plate le & f).

Many of the peripheral microspore mother cells fail to complete the division and

become abortive and assume a flat outline. The first division of the microspore

mother cell is not immediately followed by wall formation (Plate le). The

resulting four microspores are formed simultaneously and clustered in a tetrahedral

arrangement (Plate 1f). At the time of shedding most of the pollen grains are

binucleate. It may be noted that development as well as formation of microspores

are not synchronised in all anthers of the same flower.

Pollen morphology. Mature pollen grains are more or less spherical, 3-4 rarely

6-porate, and measuring 80-150 » in diameter (Plate 2a). The exine is very much

thicker than the intine, smooth but covered with sticky substances, and thicker

around the pores. At anthesis they are released singly or in clumps (Plate 2b).

Pollen germination, Pollen grains collected from the anthers at the beginning

of floral anthesis do not show any sign of germination, but those collected from

the fallen phalanges on the following morning start to germinate. Two hundred of

these pollen grains were kept under room temperature, and after 40 hours from

23.5 to 80% of the pollen grains germinated. This seems to indicate that stigmatic

exudate is not the sole prerequisite of germination and that kept under room

temperature the pollen remain viable for at least 48 hours. Germination experiment

using sucrose solution of various concentrations shows that after culturing the pollen

for 12 hours, the optimal percentage of germination (c. 77%) takes place in

6% solution, In this experiment it was also observed that the higher the concentra-

tion of the sucrose, the longer the pollen-tube is.

Development of ovule. In each of the carpellary cavities two alternate rows

of 5-7 ovular primordia appear from the central placental column as minute and

somewhat conical protuberances (Plate 2c). Each primordium is at first composed

of homogeneous, thin-walled and more or less isodiametric cells, but later one of

the hypodermal cells becomes larger in size than the surrounding cells and contains

dense cytoplasm and a more conspicuous nucleus (Plate 2c). This cell develops

into the archesporial cell and divides periclinally into a primary parietal cell and

sporogenous cell (Plate 2c). The primary parietal cell divides periclinally and

anticlinally to form the 5-6 cells thick nucellus. Soon after the division of arches-

porial cells is completed, the integument primordia develop more or less simul-

taneously on both sides of the nucellus (Plate 2d). However, the outer integument

grows faster and eventually overtops the inner one. The micropyle is formed by

both the inner and outer integuments. At the formation of the megaspore mother

cell the integuments are 2-3 cells thick, and later more cells are laid down. Several

cells of the outer integument are eventually filled with tannin. It may be noted here

that on two occasions binucellate ovules were observed. The two nucelli are

enclosed by a common outer integument but each has its own inner integument.

Megasporogenesis. The sporogenous cell enlarges and functions as the megas-

pore mother cell (Plate 2d). This cell divides into two (not seen) and eventually

into four daughter cells arranged in a linear tetrad (Plate 2e). Three of these

daughter cells degenerate, leaving the cell at the chalazal end to develop further.

This functional megaspore undergoes vacuolation and forms an _ elongated

uninucleate embryo-sac. Subsequently it passes through two-, four-— and eight-

nucleate stages before cytokinesis commences (Plate 3a, b & c). One of the four

micropylar daughter nuclei moves towards the centre of the embryo-sac, and the

other three form the egg apparatus and two synergids. Similarly, one of the

chalazal nuclei also moves to the centre of the embryo-sac while the other three

form the ephemeral antipodals (Plate 3c & d). The two polar nuclei then fuse

Durio Zibethinus, Reproductive Biology 29

with one another to form the secondary polar nucleus (Plates 4c & 5a). The

development of the eight-nucleate embryo-sac, therefore, conforms well with the

Polygonum-type.

Pollination, Opening of the flower usually takes place according to the following

sequence: epicalyx splits into 2-3 ovate-concave lobes about 12-24 hours before

anthesis; the calyx then splits open at its tip into 5—6 acute lobes about 8-10 hours

before anthesis; for the next two hours or so the petals, styles and stamens which

initially take an incurved position within the calyx become fully exerted and soon

after dark the petal-lobes become recurved outwards exposing both stamens and

styles; meanwhile some of the anthers may start to dehisce but the majority do

not do so before c. 19.30 hrs; the stigmatic surface becomes receptive at about

20.00 hrs. The flower remains at this stage until about 01.00 hrs., and then the

calyx, petals and stamens begin to drop off, leaving the lone ovary remains

attached to the branch. Though initially many of these ovaries remain attached

to the branch following pollination, within a few days most of them drop off and

leave only 1-2 per inflorescence.

During the late afternoon, the flowers are visited by various insects as they

open. Among these are honey bees, house-flies, lady-bird beetles, scarab beetles,

and lacewings. Pollen grains were found on the legs and bodies of these insects but

not in their guts. Since these insects visit the flowers before the latter reach full

anthesis, they cannot be considered as pollinators. In the evening, namely between

20.00 and 01.00 hrs, the flowers are visited by three different species of bats. These

are the nectarivorous bat (Eonycteris spelaea) and the frugivorous bats Cynop-

terus brachyotis and Pteropus vampyrus. Occasionally nocturnal moths also visit

the flowers during this period. Among the bats, only Eonycteris spelaea could be

considered as the genuine pollinator, since the other two directly feed on and chew

up the flowers (Start, 1974). Our observation suggests that Eonycteris spelaea feeds

on nectar as well as on pollen grains, and it does not chew the flower. The bats

also visit the flowers regularly during the flowering season; they land on and

clutch the flowers with the frontal parts of their body facing the open flowers.

Analysis of guano samples also confirms that pollen grain of Durio zibethinus

constitutes a significant part of the bat’s diet during durian flowering season and

that the highest number of grains in the samples coincides well with the flowering

season of the trees. Other important pollen grains found constantly in the guano

samples are those of Parkia, Ceiba pentandra (L.) Gaertn., Bombax valetonii

Hochr., Oroxylon indicum Vent., Duabanga grandiflora (Roxb. ex DC.) Walp.,

Artocarpus spp. (Plate 6a-d). This suggests that the bats feed on nectar or pollen,

or both, of different species of plants which flower at different times of the year,

and pollinate the flowers.

Pollination experiments. To test the compatibility of the flowers, a series of

preliminary experiments were carried out during the flowering seasons in 1974. In

each experiment a set of 20 flowers having a similar stage of development were

selected and tagged. These flowers were then given the following treatments: (1)

all anthers were removed at anthesis and the stigmas were exposed to natural

pollinators, (2) the flowers were bagged before anthesis, (3) the stigmas were

applied with Cutex nail varnish to prevent pollination, (4) the flowers were self-

pollinated by hand and bagged, and (5) the anthers were removed and the stigmas

were cross-pollinated by hand with pollen of other flowers of the same tree, and

then bagged. At the beginning of these experiments the ovaries of all flowers used

were between 0.35 and 0.4 cm in diameter and light-brown in colour, After 5 days

all tagged flowers were re-examined and the following results were obtained: in

treatment no. 1, 45% of the ovaries remained attached to the branch and showed

further development, i.e. increase in diameter (0.50.6 cm) and change in colour

to olive green; in experiment no. 2, only 15% of the ovaries showed further sign

of development and the others either shrivelled or fell off; in the 3rd treatment

30 Gardens’ Bulletin, Singapore — X X1X (1976)

none of the ovaries underwent further development and shrivelled or dropped

off: in the 4th, 50% of the ovaries exhibited further development and remained

attached to the branch; and in the Sth 65% of the ovaries underwent further

development and remained attached to the branch. At the end of the flowering

season only 5% of the successfully pollinated ovaries developed into mature fruits.

The above experiments seem to suggest that (i) natural pollinators contribute

at least 45% of the successful pollination, (ii) natural self-pollination can take

place and contribute to 15% successful pollination, (iii) pollination is a pre-

requisite of fruit development, (iv) up to 50% of the flowers are self-compatible, and

(v) cross-pollination between flowers of the same tree is the better means for

successful fertilisation and eventual fruit development.

However, it should be emphasised here that since the number of flowers used

in the experiments is small and the work was conducted on a single tree only, the

above mentioned results should be considered as tentative. Future experiments

using larger number of flowers and trees will either confirm or contradict the

above results.

Fertilisation. The receptive stigma is heavily papillate and has a glistening and

sticky surface. Pollen grains deposited on the stigmatic surface germinate within 3

or 4 hours. The germinating pollen grains are mostly monosiphonous, and the

tubes make their way through the stigmatic papillae into the style. The pollen tubes

grow downwards through the intercellular spaces of the vertically elongated

protoplasmic cells of the transmitting tissue (Plate 4b). The successful tube enters

the embryo-sac through the micropyle (Plate 4d). Although hundreds of slides were

examined by us, the actual process of fertilisation has not been observed in detail.

From the specimens available it seems that just before fertilisation the secondary

polar nucleus moves nearer to the egg apparatus (Plates 4e & Sa).

Endosperm. The secondary polar nucleus which is situated near to the egg

apparatus is then fertilised by one of the male gametes to form the primary

endosperm cell (Plate 5a). This cell enlarges and undergoes free nuclear division.

Most of the nuclei produced are distributed along the periphery of the embryo-sac

and aggregated mainly at the chalazal end (Plate 5b). The endosperm remains in

a free nuclear condition until a late stage of embryogeny and then becomes

cellular.

Development of embryo and seed. In the present study the embryogeny has

not been followed in detail. Sections of developing seed indicate that the endosperm

does not persist and the cotyledons occupy the greater part of the seed cavity. The

starchy food reserve is therefore stored in the cotyledons. Cells of the inner

integument are crushed and disappear, and those of the outer integument become

fibrous with the epidermal cells developing into rectangular and heavily lignified

stone cells each with a very small lumen. The aril develops from the funicular end

and eventually completely encloses the seed. This aril is very variable in thickness,

colour, taste, smell and moisture content. It may be noted here that in a few clones,

there is a high incidence of seed abortion, in which the seeds shrivel and measure

less than 4 by 1.5 cm, while fully developed and viable seeds measure up to

7 by 4 cm.

Seed germination, The first sign of germination is indicated by cracking of the

hilum at the micropylar end, and this takes place within 3 to 4 days after sowing

the seeds in suitable medium. The radicle will emerge from this crack, elongate

and grow downwards, After approximately 10 days numerous lateral roots appear

at the proximal end of the radicle and the hypocotyl elongates and straightens

up bringing the cotyledons still enclosed by the testa slightly above the soil surface.

Subsequently the petioles or stalks of the cotyledons elongate allowing the plumule

to emerge. The plumule elongates and from it the first and second leaves appear.

These leaves are much smaller than the normal leaves and are deciduous. The

cotyledons shrivel and drop off within 38 days following germination.

Plate 1: a & b developing anthers with sporogenous cell (spc); c & d dividing and developing

microspore mother cells (mc); e division of microspore mother cells; f end of

meiosis and formation of pollen tetrads (ptr).

ronennene nnn meni nay

Plate 2: a & b cross-sections of anthers just before anthesis showing fibrous endothecium and

mature pollen grains; c ovule primordium showing primary parietal cell (ppc) and :

primary sporogenous cell (psc); d ovule primordium showing developing megaspore

mother cell (mmc) and integuments; e linear tetrad and functional megaspore (fms).

Plate 3: a 2-nucleate embryo-sac; b 4-nucleate embryo-sac; c & d 8-nucleate embryo-sac;

pn = polar nuclei.

MX

Vif,

es i,

WHE,

tity,

Ye

WO

WS

SS

SSS

~

NS

Ss

SS

.

»

: @ longitudinal section of stigma (pg = pollen grain; pt = pollen tube); b pollen

tube (pt) growing downwards through the stylar tissue; ¢ migration of polar nuclei

(pn) towards micropylar end of the embryo-sac; d pollen tube (pt) entering embryo-

sac through micropyle.

‘(ou) wodsopuso

Jvojonu gq suoOHesi[sJoJ oJOJoq ysnf (oud) snojonu Ivjod Arvpuosss Jo uoeuUoy PD :¢ deg

Plate 6: a & b pollen grains extracted from guano samples (D = Durio; P = Parkia;

Db = Duabanga grandiflora; O = Oroxylon indicum); c pollen of Durio zibethinus;

d pollen of Bombax valetonit.

Durio Zibethinus, Reproductive Biology 31

Experiments show that: (i) if the aril is removed from the seedcoat, up to

95% of the seeds tested germinate 3 days after sowing in various media (saw-dust,

sands, and garden soil); (ii) if the aril is not removed, only 40% of the seeds

begin to show signs of germination 6 days after sowing, and to reach 95%

germination rate, 10 days after sowing is required; (iii) though initially there

seems to be no significant difference in percentage of germination, for further growth

of seedlings the garden soil is the best medium; (iv) the average moisture content

of a fresh seed is c. 51% (wt). Kept under room temperature (36°C) the moisture

content drops to c. 23% after 32 days of storage. If, however, the temperature is

lowered to 20°C and the seeds are stored in an air-tight container, the moisture

content can be kept at 43-45% level for the same length of storage time; (v)

surface sterilised, kept in an air-tight container and stored under 20°C the seeds

remain viable (up to 90% germination rate) for at least 32 days, but if the seeds

are stored under 36°C they lose viability after only 6 days’ storage.

DISCUSSION

From the foregoing chapters it is evident that in order to understand the

reproductive biology and the breeding system of D. zibethinus and its related

species, and to appreciate their economic potential, more detailed studies remain

to be carried out in the future. In particular, the questions — whether all existing

varieties and clones are self-compatible or require cross-pollination to produce a

good crop of fruits, and whether it is possible at all to hybridise at least the closely

related species of the genus, etc. — remain to be clarified.

Our observation on a single tree suggests that, in this particular clone at least,

there is a certain degree of self-compatibility if the flowers are cross-pollinated by

hand. This seems to disagree with the results obtained by Valmajor and his

co-workers (1965) in the Philippines, in which they observed that all trees under

their investigation were completely self-incompatible, and that the trees set fruits

only if they were reciprocally cross-pollinated. However, since in Peninsular

Malaysia alone there are at least 44 clones (Ho, 1971), differing slightly from one

another in their fruit-yield, intensity and frequency of flowering, floral and fruit

morphology, and quality of the aril, it is reasonable to assume that different clones

might have different patterns of breeding system and reproduction. This assumption

is substantiated by the fact that among the clones observed there are trees which

have the styles shorter than the stamens and exerted from the enclosing corolla

more or less at the same time with the stamens; and, there are those trees which

possess styles longer than the stamens and exerted from the enclosing corolla

before the stamens, with the stigmas thus positioned way above the anthers. Judging

from the way the bats alight on the flowers during feeding, it seems likely that in

the first category of clones both self-and cross-pollination are possible, whereas in

the second case only cross-pollination can take place. Furthermore, since in the

latter case there is a time interval intervening between the dehiscence of anthers

and the receptivity of the stigmas, under natural condition only cross-pollination

between flowers of the same or of different trees is possible. In this case any

pollinator alighting on the flowers before the stigmas become receptive will not

affect pollination, but during feeding, pollen grains of dehiscing anthers may

get attached to the mouth and frontal parts of the pollinator’s body. In moving and

alighting to another flower later in the evening the pollinator will brush pollen

grains on the now receptive stigma.

In their paper, Valmajor and his co-workers stated further that reciprocal

cross-pollination by hand of the self-incompatible trees resulted in 87.3 to 90%

fruit set. This is obviously a very high rate of fruit set by any standard, since at

least in Peninsular Malaysia, 20 to 25% fruit set is generally considered as a very

good crop already. In addition to this, our experiment also shows that up to 65%

32 Gardens’ Bulletin, Singapore — X XIX (1976)

successful pollination can be obtained if the flowers are cross-pollinated by hand

with pollen grains of other flowers of the same tree. These seem to suggest that

if a means could be found to store and keep the pollen grains viable for a longer

period than their natural viability, and a method could be devised to deposit pollen

grains on the receptive stigmas efficiently, artificial pollination may turn out to be

the best way to increase fruit production of a durian tree.

With regard to the possibility of hybridizing at least the closely related species

of the genus, Reksodihardjo (1962) stated that a natural hybrid between D.

zibethinus and D. graveolens has been discovered in the north-eastern parts of the

Indonesian Borneo. More recently, Heaslett (1972) reported that in Johore State

he found several trees of D. malaccensis with pink- or red-tinged flowers. Since

normally this species has a white or creamy flower, and moreover in Peninsular

Malaysia the only species with pink or red flowers are D. lowianus King and D.

pinangianus (Kochummen, 1972), the trees observed in the forests of Johore by

Heaslett may yet represent another natural hybrid between parents of closely

related species. If the status and origin of these “natural hybrids” could be

determined and confirmed, then there is a great possibility that through a breeding

and selection programme much improved clones could be obtained.

Finally it is re-emphasised here that the detailed processes of fertilisation and

embryogenesis, the significance of binucellate ovules and high incidence of seed

abortion, and the factors affecting the development and quality of the edible aril

also need further studies.

ACKNOWLEDGMENTS

We wish to express our sincere thanks to the Vice Chancellor of the University

of Malaya and to the Director of the Malaysian Agricultural Research and

Development Institute (MARDI) for the research grants which made the present

work possible.

We are also very grateful to Dr. N. Prakash for his kind cooperation and help

given during the execution of this work and to Dr, P. S. Ashton for his constructive

criticisms on the manuscript. For their technical assistance we are very much

obliged to Mrs. Babe Foo and Mr. Mahmud bin Sider.

Finally we would like to thank Prof, E. J. H. Corner for his continual interest

and encouragement extended to us in pursuing works on tropical plants.

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BURKILL, I. H. 1935. A Dictionary of Economic Products of the Malay Peninsula.

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CORNER, E. J. H. 1949. The Durian Theory or the origin of the modern tree.

Ann. Bot. 13: 267-414.

1952. Wayside Trees of Malaya. 2nd ed., vol. 1, 437-440. Govern-

ment Printing Office, Singapore.

—————— 1953. The durian theory extended. Phytomorphology 3: 465-476;

ibid. 1954, 4: 152-165; 263-274.

1964. The Life of Plants. Weidenfeld and Nicholson, London.

DAVIS, G. L. 1966. Systematic embryology of the Angiosperms. John Wiley &

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FAEGRI, R. & L. van der PIJL 1966, The Principles of Pollination Ecology.

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HEASLETT, E. A. 1972. Durio mualaccensis Planch. with pink-tinged flowers.

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KOCHUMMEN, K. M. 1972. Bombacaceae. In T. C. Whitmore (Ed.), Tree Flora

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KOSTERMANS, A. J. G. H. 1958. The genus Durio Adans. Reinwardtia

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LAI, ANDREW K. K. 1974. The economics of establishing a 400-acre fruit

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NG; F. ra Peay Germination of fresh seeds of Malaysian trees. Malay. Forester

: 54-65.

NG, F. S. P. & H. S. LOW, 1974. Flowering to fruiting periods of Malaysian Trees.

Malay. Forester 37: 127-132.

OCHSE, J. J. & R. C. BAKHUIZEN v.d. BRINK Sr. 1931. Fruits and fruit

cultures in the Dutch East Indies. pp. 27-30.

REKSODIHARDIJO, W. S. 1962. The species of Durio with edible fruits. Econ.

Bot. 16: 270-282.

START, A. N. 1974. The feeding biology in relation to food source of nectarivorous

bats (Chiroptera: Macroglossinae) in Malaysia. Unpublished Ph. D. Thesis,

Department of Zoology, University of Aberdeen, Scotland.

VALMAJOR, R. V., R. E. CORONEL & D. A. RAMIREZ, 1965. Studies on floral

biology, fruit set and fruit development in Durian. Philipp. Agric. 47: 355-366.

WYATT-SMITH, J. 1954. Materials for a revision of Malayan Durio with notes

on Bornean species. Kew Bull.: 513-532.

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The Syncarp of Artocarpus — a unique biological phenomenon

by

FRANCES M. JARRETT

Royal Botanic Gardens, Kew

The unique compound fruit or syncarp of Artocarpus is a fascinating object

of study, both for its basic morphology and for its structural and functional

diversity. The opportunity that was given to me as a student of Professor Corner

to continue his studies on Artocarpus and carry out a revision of the genus (Jarrett

1959a, 1959b, 1960) is one that I shall always appreciate. In honouring him in this

volume it may be of value to provide a general consideration of the syncarp,

drawing together facts that became somewhat scattered in my monograph. The

insights into both its internal structure and its biological significance originated

with Professor Corner. The revisionary work extended knowledge of the syncarp

structure to nearly all species of the genus and made it possible to place the varia-

tions observed in a more detailed taxonomic framework.

If one turns first to the morphology, it is found that in Artocarpus the com-

pound inflorescence of the Moraceae is condensed into capitate, unisexual inflores-

cences in which each of the numerous perianths contains a single stamen or ovary.

In the male inflorescence the perianths remain free (as they do in both sexes in the

allied genus Prainea) but in the female head the perianths are more or less com-

pletely fused. Where the fusion is only partial it occurs in a highly specialized

manner, which is not evident until the syncarp is dissected. It can then be seen that

each perianth has a proximal free tubular region with a broad lumen enclosing

the ovary. Distally, however, the perianths are early adnate to their neighbours,

either fusing with them completely or leaving the perianth apex free. They thus

form a continuous external wall to the syncarp which has considerable mechanical

strength and is pierced only by the narrow lumen in each perianth through which

the style is exserted. Passing from the axis to the outer surface, each perianth thus

has either two or three zones, free—fused or free—fused—free. The latter condition

was illustrated by Corner (1939) for A. integer (Thunb.) Merr. and A. hetero-

phyllus Lam. The varying internal structure of the syncarp and some aspects of

its external appearance are illustrated below.

In other species, however, the fusion between the perianths is complete or,

alternatively, it may be said that the ovaries are enclosed in cavities in a receptacle

in which axial and floral elements are not clearly distinguishable.

This then is the basic structure of the compound syncarp of Artocarpus, but

such a highly specialized and apparently restrictive ground plan can, nevertheless,

allow considerable morphological and biological diversity, especially in those

species in which the perianths remain free proximally. Monographic study of

Artocarpus showed that these variations could be linked with the taxonomic sub-

division of the genus in which other characters, especially details of leaf anatomy,

were taken into consideration, although it also became evident that some parallel

evolution had occurred in the syncarp.

Thus a primary taxonomic subdivision into two subgenera, Artocarpus and

Pseudojaca, which can readily be made on the basis of spirally arranged versus

alternate and distichous leaves, and amplexicaul versus lateral stipules, can be

35

36 Gardens’ Bulletin, Singapore — X XIX (1976)

ee a ae et ee et ee a

S

LFF

LH}

\, «AY

(

cue

*, Wr eeet te,

im a .

: >

as

eet cons: g

Fig. 1. The syncarp in Artocarpus. Subg. Artocarpus. A. hispidus. a, b, longitudinal section

and tangential section in plane x-y at anthesis, X 10; c, longitudinal section at maturity,

x 4; d, part of the same (1, fruiting perianth; 2, ovary; 3, testa; 4, umexpanded perianth),

xX 1. A. elasticus. e, submature head, X 4. Subg. Pseudojaca. A. peltatus Merr. f, oblique

section at anthesis (perianths free proximally), X 24; g; longitudinal section at maturity, X 4.

A. fulvicortex Jarrett. h, oblique section at anthesis (perianths completely fused), X 1; i, part

of the same, X 3. a-—d redrawn from Jarrett (1959a).

correlated quite closely with syncarp characters, In subg. Artocarpus the syncarp

is usually ellipsoid or cylindric and the perianths are nearly always free both

proximally and at the apex. Most species can in fact be identified by the perianth

apices alone (cf. Jarrett, 1959b, f. 16). In subg. Pseudojaca, on the other hand,

the syncarp is much more uniform in appearance. It is either subglobose or

shallowly lobed with a smooth or papillate surface and although in most species

the perianths are free proximally, there are several in which they are completely

fused.

Artocar pus subg. Artocarpus was further subdivided (Jarrett, 1959b) into two

sections based mainly on characters of the inflorescence, including those of the

embryo, and into several series based primarily, though not solely, on the distinc-

tive, microscopic, capitate hairs on the leaves. Considered biologically and morpho-

logically, three different syncarp types can be recognised in the subgenus corres-

ponding with one or more of these taxonomic subdivisions, while subg. Pseudojaca

forms a fourth type to which three species from subg. Artocarpus (ser. Rugosi)

should also be referred.

The biological evolution of the syncarp has apparently proceeded in two

different directions. It is, of course, indehiscent and is broken down only by the

frugiferous mammals and birds that feed upon it or by decay. Nevertheless it can

be attractive either as a whole, if the entire syncarp is more or less fleshy, or for

the individual fruiting perianths in species where the free proximal region of the

perianth is hypertrophied.

Syncarp of Artocarpus 37

The least specialized condition of the syncarp would seem to be found in a

number of species in subg. Artocarpus sect. Artocarpus in which the distal regions

of the perianths forming the external wall of the syncarp and the free perianth

apices are fleshy but more or less firm while the free proximal regions are thin-

walled or only slightly hypertrophied (but sweet and juicy at least in A. elasticus

Blume and A. sericicarpus Jarrett). In contrast with this comparatively undifferen-

tiated internal structure the external appearance of these syncarps is remarkably

varied, depending on the shape and indumentum of the perianth apices. They

range from scarcely projecting so that the surface appears areolate, each areola

representing the tip of a perianth, to long drawn-out and flexuous, giving the

figurative appearance of the head of a Medusa. Such elongation of the perianth

apices is often associated with dimorphism. There is then usually a marked

contrast between the short, perforate apices from which the styles emerge and the

intermingled solid processes, which may bear distinctive hairs — long, appressed

and silky in A. sericicarpus but short and patent in A. elasticus (Terap in Malaya) and

recurved in A, tamaran Becc. and A. multifidus Jarrett. In A. teysmannii Miq., on

the other hand, comparatively few of the perianth apices are elongate and inter-

mediates occur. It is interesting to note that this dimorphism is found in one or

more (but not all) of the species in each of the three series in Sect. Artocarpus

(Incisfolii, Angusticarpi and Rugosi) which have this type of syncarp and that it

apparently represents parallel evolution.

The fourth series in this section (Cauliflori) possesses the most remarkable

syncarps in the genus. The enormous fruits of A. heterophyllus Lam. (Jack) and

A. integer (Thunb.) Merr. (Chempedak), which are borne on the trunk and larger

branches, may measure as much as one metre in length and half a metre across.

The very numerous seeds are enclosed in the strongly hypertrophied proximal free

region of the perianths and in the Chempedak (but not the Jack) these separate

from the wall and the core at maturity, falling out when the baggy syncarp is cut

open. The taste and smell is highly characteristic of each species and was described

by Corner (1939) as “‘sickly sweet” in the Jack and much stronger (‘‘of durian

and mango”’) in the cultivated Chempedak (but lacking in the wild var. silvestris

Corner). The syncarp surface is covered by firm, but not indurated, conical

perianth apices.

The smaller, globose or short-cylindric, armoured fruits of sect. Duricarpus

representing the third type of syncarp in subg. Artocarpus, have seeds that are

likewise surrounded by succulent, hypertrophied perianths. The free tips of the

perianths are, however, woody and, while in some species such as A. lanceifolius

Roxb. (Keledang) and the pinnate-leaved A. anisophyllus Mig. they are merely

cylindric, in others such as A. rigidus Bl. (Monkey Jack) and the related A.

hispidus Jarrett, they form tapering spines.

The smooth or papillate, fleshy syncarps of subg. Pseudojaca (Tampang in

Malay) present a strong contrast to those just described and, as already stated,

there is relatively little variation in appearance and morphology. Only in A.

styracifolius Pierre from southern China is the surface covered by flexuous pro-

cesses and these appear to be formed from enlarged interfloral bracts. (Bracts are

present among the flowers in most species of Artocarpus at least in juvenile

inflorescences but their heads are usually minute and discoid or infundibuliform.)

As regards internal structure, where the proximal portion of the perianths is free

it is thin-walled, but in several species, including A. fulvicortex Jarrett among

Malayan species (Orange-Barked Tampang in Corner, 1940), the perianths are

completely fused. Finally a few species in subg. Artocarpus such as A. kemando

Miq. have small fleshy fruits which should be classified biologically with this group.

The biological significance of the syncarp in Artocarpus was taken up by

Corner is his discussion of the Durian Theory, in which the genus was frequently

mentioned (1949, 1954a, 1954b). Vegetatively it shows both massive pachycaul

38 Gardens’ Bulletin, Singapore — X X1X (1976)

and slender leptocaul construction and, in particular, the association of the latter

with cauliflory in A. integer and A. heterophyllus, The compound syncarp, more-

over, shows striking parallels in some species with fruits of the Durian type. The

surface may be armoured but here this is by perianth apices rather than by simple

spines; the fruit may be strong smelling as, for example, in A. elasticus, A. hetero-

phyllus and A. integer; and; finally, fleshy perianths can take on the function of

an aril (Corner, 1962). However, other parallels may also be seen in the genus

since the fleshy syncarp. of subg. Pseudojaca can be compared with a berry,

although the flesh is formed from the perianths and axis rather than from the

carpel wall. It may be added that in the allied genus Prainea, in which the

perianths remain free in the female inflorescence, the few that form seeds and

project from the surface each resemble a single-seeded berry in which, again, the

flesh is formed by the perianth.

It might be assumed that these biological variations in the syncarp would be

reflected in marked differences in the animals acting as distributors. However,

while differences do exist they are not verv clear-cut. Precise information is scanty

and mainly derived from cultivated trees, which is not surprising since in the forest

Artocarpus is usually widely scattered. However, it is clear from observations

gathered together by Ridley (1930) and others made by Corner (1939, 1940) that

it is the attractive flesh, variously dispersed in the syncarp, that brings about the

distribution of the seeds. Arboreal mammals, especially monkeys and civet cats

break open the larger fruits, nibbling the juicy perianths and scattering at least

some of the seeds. Docters van Leeuwen (1935) also records several species

including two of the most important cultivated species, Chempedak & Breadfruit.

as being eaten by bats, a fact first mentioned by Rumphius. Ridley suggests that

the cauliflorous fruits are eaten by wild pig, cattle and elephants. The smaller

fleshy fruits may be eaten by birds or bats and could be carried off whole and

thus more widely distributed. However the distribution patterns of the species,

which were mapped in my monograph, suggest that water is a strong barrier to

dispersal, as might be expected with such large seeds lacking in dormancy.

The uniqueness of the syncarp in Artocarpus lies in the partial fusion between

tubular perianths which exists in most species. This character has made possible

the differentiation for attractive or protective functions of the proximal and distal

regions of the perianth and hence the remarkable biological parallels between this

compound fruit and syncarps derived from a single flower. It is evident that field

observations are still needed to enrich our biological knowledge of this diverse

genus.

REFERENCES

CORNER, E. J. H. 1939. Notes on the systematy and distribution of Malayan

phanerogams, IT. The Jack and the Chempedak. Gdns’ Bull., Singapore 10:

56-81.

1940. Wayside Trees of Malaya, Vol. 1. Govt. Printer, Singapore.

770 pp.

1949. The Durian Theory or the origin of the modern tree. Ann.

Bot. N.S. 13: 367-414.

— 1954a. The Durian Theory extended — II. The arillate fruit and

the compound leaf. Phytomorphology 4: 152-165.

1954b. The Durian Theory extended — III. Pachycauly and

megaspermy — Conclusion. Phytomorphology 4: 263-274.

1962. The classification of Moraceae. Gdns’ Bull., Singapore 19:

187-252.

:

:

Syncarp of Artocarpus 39

DOCTERS Van LEEUWEN, W. M. 1935. The dispersal of plants by fruit-eating

bats. Gdns’ Bull., Singapore 9: 58-63.

JARRETT, F. M. 1959a. Studies in Artocarpus and allied genera, I. General

considerations. J. Arnold Arbor. 40: 1-29.

1959b. Studies in Artocarpus and allied genera, III. A revision of

Artocarpus subgenus Artocarpus. J. Arnold Arbor. 40: 113-155, 298-368.

1960. Studies in Artocarpus and allied genera, IV. A revision of

Artocarpus subgenus Pseudojaca. J. Arnold Arbor. 41: 73-140.

RIDLEY, H. N. 1930. The Dispersal of Plants Throughout the World. Reeve,

London. 774 pp.

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The Origin of the Afroalpine

Pachycaul Flora

and its Implications

by

D. J. MABBERLEY

Botany School, Oxford

Summary

The morphological, anatomical and biogeographical implications of the apparently

primitive nature of the forest pachycaul form in Senecio and Lobelia are discussed. The

preadaptation of high altitude swamp pachycaul forms for temperate rhizomatous vegeta-

tion and the adaptations of hyperpachycaul forms to the conditions of the tropical alpine

belt are stressed.

Fig. 1. Lobelia rhynchopetalum in the High Simien of Ethiopia during von Riippell’s

expedition of 1833. (From von Riippell, 1840: t. 6 i issi

University Librarian, Cambridge. a Petr Romer eee ie be olecunn

perder charakterisert diese Zone eine sehr fremdartige Pflanze, die einer Aloekrone

oy * welche auf einem mannshohen hohlen Stengel aufsitzt. Ihr Landesname ist Gibarra,

int systematische Stelle die Familie der Lobeliaceen. Da sie nur an der Schneegranze

vork6mmt, und doch in der Form eini i it mi i i

. uae uge Ahnlichkeit mit den der warmsten Tropenvegetation

eigenthiimlichen Pflanzen hat, so gibt dieses der Landschaft einem hochst fremdartigen

Charakter.

Eduard von Riippell (1836).

4]

42 Gardens’ Bulletin, Singapore — XX1X (1976)

Introduction

With the baobab and Welwitschia, the Giant Groundsels and Lobelias are

perhaps the most famous botanical curiosities of Africa. The layman’s familiarity

with herbaceous senecios and lobelias, the unfamiliar habit of the ‘giant’ plants

and their exotic tropical montane home have given the Giant Groundsels and

Lobelias an exalted place in botanical travelogues, popular horticultural works and

other writings and made them a tourist attraction attained by few members of the

vegetable kingdom.

The adjective ‘giant’ in botanical works has connotations of teratology or

polyploidy and is used here only in the nicknames ‘Giant Groundsels’ for Senecio

L. subg. Dendrosenecio Hedb. and ‘Giant Lobelias’ for Lobelia L. sect. Rhyncho-

petalum (Fres.) Benth. & Hook.f., the general term ‘“pachycaul’ being used for

those plants with massive primary construction, large buds and large leaves, of which

fine examples are provided by the Giant Groundsels and Lobelias (Corner, 1949).

Pachycaul senecios have been known from Africa since the eighteenth century;

those first brought back to Britain were not from the continent but from the

isolated Atlantic island of St. Helena, 900 km east of the Mid-Atlantic Ridge

(Mabberley, 1975b). Later, pachycaul species were discovered in West Africa and

Ethiopia where the first pachycaul lobelia was collected (Fig. 1); finally the

mountains of tropical East and Central Africa were rediscovered and the famous

Giant Groundsels and more Giant Lobelias collected for the first time, in the latter

half of the last century.

Meanwhile the alpine belts of the Andes yielded the pachycaul “‘Frailejones”

(Espeletia spp.) and puyas, and although pachycaul plants are not restricted to

islands and mountain-tops (Corner, 1949), their conspicuous appearance in such

situations, and the superficial correlation between their presence and the ‘insular

situation’ had aroused considerable discussion. The study of the floras and faunas

of islands, continental and oceanic, and of insular situations, geological and

altitudinal, has been of continuous interest to biologists, for much evidence for the

theory of Natural Selection was derived from it by Darwin, whose observations in

the Galapagos Islands paved the way to modern ideas on evolution:

“The principle which determines the general character of the fauna and flora

of oceanic islands, namely that of the inhabitants, when not identically the

same, yet are plainly related to the inhabitants of that region whence colonists

could mostly readily have been derived — is of the widest application

throughout nature .... For alpine species, excepting in so far as the same

forms, chiefly of plants, have spread widely throughout the world during the

glacial epoch, are related to those of the surrounding lowlands.”

Charles Darwin, Origin of Species (1859: 342)

The fallacy in the blind comparison of ‘altitudinal islands’ and oceanic islands

has been explored by White (1971). Nevertheless, certain families, e.g. Campanu-

laceae and Compositae are represented by pachycaul forms on islands both

geographical and altitudinal. One genus in each of these families viz. Lobelia and

Senecio is similarly distributed. Within their respective families, these genera are

large, Lobelia with perhaps 350 species (Wimmer, 1956, 1968) and Senecio, as

understood at present, is perhaps the largest of flowering plant genera with 2000-

3000 species (Willis, 1973). Unlike other genera with arborescent forms in these

predominantly herbaceous families, Lobelia and Senecio have herbaceous as well

as woody forms (Good, 1974: 85) and almost the whole gamut of life-forms

represented in their families is to be found in them. If the genera, or sections of

them, are monophyletic, then it should be possible to discern evolutionary trends

within them and hence investigate the relationship of the pachycaul habit to that

4

f

*

9

Afroalpine Pachycaul Flora 43

of the herbaceous habit. It is only in the mountains and on the islands of Africa

that pachycaul species of both genera grow together. Thus it was felt that a study

of these ‘Giant Lobelias and Groundsels’ would throw considerable light on the

evolution of the woody pachycaul in florally advanced families. Currently seven

pachycaul species of Senecio (Mabberley, 1973a; 1974a; 1975b) and seventeen

pachycaul species of Lobelia (Mabberley, 1974c) are recognized. Revisions had

been made piecemeal before those, but the origin of the pachycaul habit was

undecided through the lack of either developmental studies or the comparison of

pachycaul with herbaceous forms. In consequence, two opposing theories had been

proposed. Fries & Fries (1922) suggested that the pachycauls were primitively

forest plants of the Tropics, whereas Cotton (1944) argued that they had arisen

from temperate plants which had reached the Tropics along mountain chains and

elaborated pachycaul construction there. Recently these arguments have been

voiced by Coe (1967) and Carlquist (1965: 199) respectively.

Besides in these speculations, the Giant Groundsels and Lobelias appeared in

a more profound work, the Durian Theory of Corner (1949-54b; 1964), the

pachycaul construction which they exhibit being a keystone of much of the theory,

which argues the origin of leptocaul trees from pachycaul ancestors. Are they

relics of those from which the leptocaul and herbaceous evolved and multiplied

to populate the temperate zones, or are they rare elaborations of herbaceous groups

selected for their longevity in ‘insular situations’?

Senecio

The first African pachycaul senecios to be discovered were S. leucadendron

(Forst.f.) Hemsl. and S. redivivus Mabberley, the He—- and She— Cabbage Trees

respectively, first collected by Banks on St. Helena on Cook’s Endeavour voyage

in 1771 (Mabberley, 1975b). No pachycaul species from the mainland was collected

until 1859, when Sir John Kirk collected scraps of a woody Senecio on Living-

stone’s Zambezi Expedition; his specimens were not received at Kew until 1867,

by which time the tree had been discovered on Clarence Peak, Fernando Po in April

1860 by Gustav Mann, whose name it bears, Senecio mannii Hook.f. It is now

known from Nigeria, Cameroun and from Zaire to Ethiopia and Tanzania,

Mozambique and Angola (Mabberley, 1973b). In June 1864, the Middle East

botanist Wilhelm Georg Schimper collected a related species, S. gigas Vatke, on his

third expedition in Ethiopia.

It was not until the Royal Society and the British Association put the ‘Kilima-

Njaro Expedition’ of 1884 into the field with the energetic Harry Hamilton

Johnston as its leader that the first Giant Groundsel was collected and named

S. johnstonii Oliv.; later many collections from the other mountains were also

given specific rank, but with S. johnstonii these are now considered to constitute

three species in all (Mabberley, 1973a), the second being S. keniodendron R.E.

& T.C.E. Fr., an hyperpachycaul tree of Mt. Kenya and S. brassica R.E. & T.C.E.

Fr., a ‘creeping tree’ of Mt. Kenya and the Aberdare Mts. of Kenya. The African

pachycaul senecios are thus: Senecio leucadendron, S. redivivus, §. mannii, S.

gigas, S. johnstonii comprising eight geographical and altitudinal subspecies includ-

ing subsp. refractisquamatus (De Wild.) Mabberley and subsp. barbatipes (Hedb.)

Mabberley, §. keniodendron and S. brassica.

In Hoffmann’s treatment of Senecio (1892), all the Giant Groundsels then

known as well as the Cabbage Trees and S. mannii and S. gigas were included in

the ‘Arborei’, an heterogeneous assemblage of species put together merely on their

woody habit; some leptocaul shrubs of Madagascar were also included. Recent

44 2 Gardens’ Bulletin, Singapore — XX1X (1976)

study of the details of the flowers (Mabberley, 19742) has shown that the

allegiance of the Giant Groundsels is with the herbaceous sect. Crociserides, that

of S. gigas and S. mannii with the lianoid and herbaceous ‘Crassocephalum-Gynura’

complex, whilst S, leucadendron is quite isolated in the genus as is S. redivivus. It

is more easily argued (Mabberley, 1974a) that the tropical pachycauls with the

primitive ‘Dendrosenecio-branching’ are relics of a pachycaul ancestry for the

herbaceous group than that they are sporadic arborescent innovations from primarily

herbaceous stocks. This is supported by the observation that pachycaul trees with

this branching habit are to be found in other alliances in Senecio in New Zealand,

Mexico, Cuba and the Canary Islands.

It was argued that in the Dendrosenecio-Crociserides assemblage, evolutionary

trends within the Giant Groundsels provided a clue to the origin of the herbaceous

forms by the stem’s becoming a ‘truncus superficialis’ as in S. brassica and thence

a subterranean rhizome suited to perennation and the invasion of the temperate

zones (c.f. ‘herb-making’ in Hedysarum, etc. analyzed by Gatsuk, Dervis-Sokolova,

Ivanova & Shafranova (1974) ). The massive alpine pachycauls, ‘hyperpachy-

cauls’, are seen as dead ends as far as evolution of temperate vegetation is con-

cerned, but adapted to the exacting climate of the afroalpine belt in elaborating

characters such as leaf-movements etc. (see below). By contrast the creeping form

adapted to the swampy habitat is seen as pre-adapted to a seasonal climate.

ALPINE PACHYCAULS

In the pachycaul alpine species are elaborated certain characteristics which are

weakly developed in the forest forms. Marcescence is more marked; Hedberg

(1964) has shown that the marcescent collars of leaves act as efficient insulators,

the temperature around one tree dropping to —4°C, whilst remaining + 1.8°C

within the ‘collar’. This warm microhabitat is exploited by animals, e.g. the frills of

S. keniodendron provide a night shelter for the chironomid midges which breed in

the buds of Giant Lobelias, and for many beetles and spiders (Coe, 1967) whilst

the groove-toothed rat, Otomys orestes orestes Thomas burrows up into the

marcescent leaves and leaf-bases (Coe, 1967). In another tree, Hedberg (1964)

found that the pith remained at + 3°C whilst the temperature dropped to —5°C

outside. If the collars are removed, Hedberg suggests that the tree may die. In

S. johnstonii subsp. barbatipes, an alpine plant of Mt Elgon, the rdle of the frills

is taken by the highly developed bark, which is again exploited by animals. As

Dendrosenecios are hygrophilous, they are often to be found in hollows which are

frost pockets, where insulation is even more important than in the plants of the

steep slopes. The movements of the leaves which protect the bud (Diels, 1934: 68)

and the production of antifreeze slime are also exploited by the invertebrate fauna

which overnight in the ameliorated micro-habitat thus provided, e.g. snails and

insects which also receive shelter from desiccation by day (Coe, 1967).

The marked xeromorphy of alpine forms (Hare, 1941) is linked with the

severe alpine climate; the thick leaves may be important in preventing water loss.

The pubescence of the leaves of many forms may reflect incoming radiation

(Hedberg, 1964), but several alpine forms, e.g. S. keniodendron have glabrous

leaves. The shiny adaxial surface may be of importance in reflection of radiation.

The abaxial surface of the leaves of S. brassica may protect the bud at night when

closed over it by preventing outward radiation, as has been discovered by the

scarlet-tufted malachite sunbird, Nectarinia johnstonii johnstonii Shelley, which

gathers the hairs to line its nest (Coe, 1967). There is marked endemism in the

insects paralleled by their host distribution patterns. Further, there is an increase

in flightlessness with altitude, probably associated with the alpine habitat stadtives

‘cryptozoic’ modes of life (Salt, 1954).

Afroalpine Pachycaul Flora 45

Lobelia

The first pachycaul Lobelia from Africa was collected by the zoologist, Eduard

von Riippell, in the High Simien in Ethiopia in 1833 (Fig. 1). Now seventeen (one

undescribed) such species are known and all are referable to sect. Rhynchopetalum

(Fres.) Benth. & Hook.f. (Mabberley, 1974c), in subsect. Haynaldianae E.

Wimmer, subsect. Nicotianifoliae Mabberley and subsect. Rueppellianae Mabberley.

The Haynaldianae are a Brazilian group with three African outliers. The Nicotiani-

foliae are found from eastern Africa to S.E. Asia with closely related taxa in

Hawaii (Mabberley, 1974c). They include L. giberroa Hemsl. of montane forest

and clearings and L. bambuseti R.E. & T.C.E. Fr. of the upper forest belt. The

alpine species are the creeping L. deckenii (Asch.) Hemsl. and L. rhynchopetalum

Hemsl. of the Rueppellianae and, of the Nicotianifoliae, L. wollastonii Bak.f. and

L. telekii Schweinf., which seem to be parallel alpine types as is L. nubigena Anth.

of Bhutan in the L. nicotianifolia [Roth ex] R. & S. complex. All seem to be derived

from forest ancestors (Mabberley 1974c, 1975a). In the Far East the Nicotianifoliae

include the rhizomatous L. sumatrana Merr. of high mountains.

ALPINE PACHYCAULS

The stems of the forest species of Giant Lobelia are usually bare of marcescent

foliage; the stems of the alpine species are either prostrate, as in the paludal

L. deckenii, acaulescent as in L. telekii, or erect, with a conspicuous frill of

marcescent foliage like that of a Dendrosenecio as in L. wollastonii. The base of

the leaf has a plug of corky tissue which holds the withered lamina to the stem.

Erect flowering shoots of L. deckenii are also thus clothed as figured by Hedberg

(1964). Diurnal leaf movements of the leaves also protect the buds which are

bathed in antifreeze slime as in Senecio.

Coe (1967) reports that chironomid midges shelter in the closed rosettes of

Lobelia deckenii subsp. keniensis and that the larvae are found in the slimy water

therein. The water is said never to dry up, even in cultivation (McDouall, 1927)

and does not freeze solid except at very low temperatures: the larvae are thus

protected. Hedberg (1964) measured the temperature outside and inside the bud

of Lobelia telekii and found it to drop to -3.5°C outside, whilst falling no lower

than +1.0°C within.

Scott (1935) worked on the assemblages of Coleoptera restricted to the

pachycaul lobelias. Some species, e.g. a silphid, spend their entire life cycle in a

Lobelia plant as do certain bibionid flies in Lobelia flowers (Coe, 1967). The

distribution of the associated species of Trechus (Coleoptera) matches that of the

lobelias (Scott, 1958). As with those of the Dendrosenecios, many of the insects are

flightless and ‘giant’ within their own genera.

Dendrosenecio, Rhynchopetalum, and Altitudinal Distribution

The study of the pachycaul Lobelioideae and Senecioneae of Africa has given

support to Croizat’s (1962: 257) forecast of ‘similar’ evolutionary patterns in the

Giant Groundsels, Lobelias and the South American espeletias. This study has

supported the view of the origin of alpine forms from forest ones in parallel as

eh by Humbert (1935) for Dendrosenecios and Fries & Fries (1922) for

elia.

Dendrosenecios occur on the wet mountains of eastern Africa at altitudes

over 2100 m, but only on those mountains higher than 3300 m. Although found

on the Cheranganis (c. 3400m), they are not found on the nearby Mau Massif

(3050m); the difference between these two appears to be critical. Similarly, the

difference between the Aberdares (3940m) and the Cheranganis may be critical

for Lobelia telekii, which is absent from the latter range.

46 Gardens’ Bulletin, Singapore — X X1X (1976)

Dendrosenecio and Lobelia telekii distributions may be explained by the

hypothesis of Wood (1971), wherein former amelioration of climate would have

forced the Senecio and Lobelia belts to higher altitudes; those mountains, which

were high enough to harbour them then, still possess them, now that the vegetation

belts are once more depressed. The adaptive radiation of the Dendrosenecios seems

not to have proceeded as far as that in Lobelia in the East African mountains, It

may be that the longer life-cycle of the Dendrosenecios has permitted slower change

(c.f. Arber, 1928).

Argument

Starting from the pachycaul members of both genera, interpretations of many

morphological and ecological features are possible. Can as much be explained if

herbs are taken as the primitive condition and the pachycaul as the advanced?

Starting from herbs in the Crassocephalum-Gynura and Crociserides alliances

of Senecio, it is necessary to postulate a mechanism for increasing woodiness (that

so far suggested (Carlquist (1962) ) seems to be untenable (Mabberley (1974b) ),

and for postponing flowering. All the available evidence points to a forest ancestry

for the creeping swamp pachycauls and the erect alpine ‘hyperpachycauls’ so that

there would be no indication of how the presumed herbaceous ancestors attained

the forest pachycaul condition. S$. brassica would be a ‘herb’ for the second time

in its evolution (c.f. Arber, 1928). It would have to be argued that the characteristic

‘Dendrosenecio-branching’ (‘Modéle de Leeuwenberg’ of Hallé & Oldeman, 1970)

had been attained in herbaceous, succulent, woody, lianoid and pachycaul groups

independently; furthermore, in the wholly pachycaul groups, there would be no

indication of their presumed herbaceous ancestors.

Similarly, it must be argued that several herbaceous lines of distinct appearance,

e.g. in Lobelia, plants like L. sumatrana and L. deckenii, have colonized the

Tropics and produced very similar pachycaul plants in America and Africa as well

as India and Hawaii. It must also be assumed that the inflorescence has become

more complicated, the fruit baccate, the seeds winged and the leaf-size increased,

all in several lines. If this is so, then wind-pollination and dispersal must be

antecedent to bird and insect pollination and dispersal, the short-lived temperate

herb antecedent to the tropical pachycaul (c.f. Mabberley 1975a).

No sense can be made of phytogeography, associations with animals or the

origin of a range of life form within plant genera. It is simpler, then, to follow the

easier line of argument, and, in short, arrive at the same conclusion as Corner

(1967b) working with the woody genus Ficus, for if the herb (Senecio, Lobelia)

or leptocaul tree (Ficus) is primitive and the pachycaul advanced, then:

(i) The primitive species are the most common and widespread, contrary to

much of biogeography which would have the primitive as relics;

(ii) the pachycauls are advanced but make least contribution to tropical forest

(Ficus) or temperate floras (Senecio, Lobelia) which the flowering plants have

been evolving;

(iii) the most leptocaul trees (Ficus) or herbs (Senecio, Lobelia) have the

simplest inflorescences, supplying no evidence of their evolution.

As Corner continues, morphological series, [whether i in Ficus, the Crociserides,

‘Crassocephalum’ or Rhynchopetalum] can be read in either direction; the ecologi-

cal factor is ‘time’s arrow’. In the case of Ficus, the arrow is aimed at tropical

rainforest via leptocaul trees; in the Crociserides it is aimed at the conquest of the

temperate zones via preadapted rhizomatous perennials, in ‘Crassocephalum’ at

filling the secondary habitats of the African Tropics with fast-growing plants and

in Rhynchopetalum it is aimed at both.

Afroalpine Pachycaul Flora 47

The hypothesis

The hypothesis is that Lobelia sect. Rhynchopetalum and Senecio sect.

Crociserides are derived from pachycaul ancestors and that, in parallel, these groups

have given rise to herbs which have reached the temperate zones, and to

extreme ‘hyperpachycaul’ forms which have conquered the tropical mountains

of Africa, living in wet situations above the treeline away from other arborescent

competition. The hypothesis implies that there have been physiological and

morphological adaptations for simplification and overwintering in the herbs and

remarkable elaborations of characteristics of the forest plants in the hyperpachy-

cauls adapted to the alpine environment.

The evolution of subg. Dendrosenecio and sect. Rhynchopetalum in Africa

can be seen as the conquest of the highlands, either by becoming hyperpachycaul

with marcescent foliage, reduction of hydathodes, enhanced pubescence, etc., or by

becoming prostrate and lying down in wet places. The latter is the method which

has permitted the colonization of the temperate zones in these groups. The marked

increase in pachycauly with altitude may have an ecological explanation, for

Daubenmire (1947: 186) has shown that massive organs may withstand short

periods of extreme temperatures better than less massive ones. Hyperpachycauls

are thus adapted to diurnal climate fluctuations, whereas rhizomatous plants with

intermittent growth are adapted to a seasonal climate. It becomes clear then, why

no Lobelia of North Africa and the Mediterranean is of the Rhynchopetalum

alliance compared with the Crociserides with many Asian and European relatives,

for, in Africa, the alpine species which reaches furthest north is the hyperpachycaul

L. rhynchopetalum with a highly peculiar structure; herbaceous Rhynchopetala are

the result of ‘miniaturisation’ (Hallé & Oldeman, 1970: 150) in the Far East.

On the other hand, sect. Rhynchopetalum has reached the Pacific as fast-

growing pachycauls from both east and west, such that the presence of pachycauls

on both sides of the Pacific is readily explicable (Mabberley, 1975a). Indeed, the

immigration of the ‘pachycaul starter’ has permitted the development of herbaceous

plants from Japan to Sumatra. By contrast the Crociserides seem to have spread

very little as pachycauls but have romped and excelled in the temperate zones as

coarse herbs.

Sect. Rhynchopetalum and ‘Crassocephalum’ have elaborated fast-growing

pachycauls, which have thus become ‘nomads’ (van Steenis, 1958) of the sub-

montane forests of Africa, and India, incidentally predisposing them to cultivation

as shamba [small-holding] hedges (S. mannii) (Mabberley, 1974a) and as pot

plants (L. nicotianifolia [Roth ex] R. & S. (Anon., 1904) etc.) in Victorian green-

houses. By contrast, subg. Dendrosenecio with a longer life-cycle has ascended the

mountains to make woodlands above the ‘treeline’.

In general, then, there is factual support for the predictions of the Durian

Theory, with the important proviso that the groups here studied are capable of

hyperpachycauly under the selective pressure of the alpine environment.

Implications

According to our hypothesis, then, such statements as “... highly probable

that the development of the arborescent habit and delayed flowering among the

tree Senecios and Lobelias of the East African Mountains, was a photoperiodic

response ... fixed by Natural Selection”, (Melville, 1953) and “‘The ancestors of

the equatorial alpine rosette trees are temperate zone herbs, which arrived on the

equatorial peaks by long distance dispersal just as did the ancestors of island

rosette trees” (Carlquist, 1965: 200) seem to be unsubstantiated by the available

evidence. On the contrary, it is more easily argued that the pachycaul state is the

primitive, which leads to the following considerations.

48 Gardens’ Bulletin, Singapore — X XIX (1976)

GROWTH HABIT

Herbs

The primitive growth-form in the Senecioneae appears to be Dendrosenecio

branching, examples of which are found scattered throughout the tribe; it appears

that it represents the ‘pachycaul starter’ condition for ‘Senecio’. The aerial parts

of the Crociserides, so difficult to describe in ‘cauline’ terms appear to be inflores-

cences and are more readily comparable with one another and other life-forms

once this is recognized. Similarly, the creeping lobelias like L. sumatrana show that

the aerial parts of many lobelias are also merely ‘inflorescence’.

Hyper pachycauly

Enhanced pachycauly exemplified in the alpine hyperpachycauls is a feature

of both genera. It appears to be associated with the basally growing leaves in these

families. Thus, under the selective forces of the alpine environment, there are

hyperpachycaul Dendrosenecios and lobelias in Africa, Pachypodium in the

Malagasy Mts. (Koechlin, 1969), espeletias in the Andes (Smith & Koch, 1935),

Saussurea gossipiphora D. Don and Rheum nobile Hook.f. & Thom. in the

Himalaya (Anthony, 1936) and, under the selective forces of the horticulturalist,

the hyperpachycaul vegetables such as lettuce and cabbage, large European and

Asiatic varieties of which are figured by Herklots (1972: 190-224).

The pachycaul construction of massive buds permits the tolerance of the

Tageszeitenklima (Troll, 1947) of the tropical alpine belts by ‘arborescent’ plants

above the tree-line, e.g. besides Senecio and Lobelia in Africa, Puya ramondii

Harms and Lupinus weberbaueri Ulbr. in the Peruvian Andes (Pontecorvo, 1972),

Lupinus alopecuroides Desr. (Heilborn, 1925), puyas and espeletias in the

Colombian Andes (Fosberg, 1944) as well as the Andine Ceroxylon (Corner,

1966: 289) and even Cyathea in the Papuan mountains (Wardle, 1971), but not

their spread beyond the Tropics into a seasonal climate. Such diurnal fluctuations

in deserts may favour pachycauly e.g. Cactaceae, succulent Euphorbia species,

Yucca spp. etc., and fire may favour pachycaul forms with wide cortex and hence

deeply seated or weakly developed cambium, e.g. Xanthorrhoea spp. in Australia,

Aloe capitata Bak. var cipolinicola H. Perr. in the ‘prairies’ of Madagascar and

again Cyathea in New Zealand and New Guinea. In the dicotyledonous examples

there is a reduction in branching, and in Puya, the inflorescence is unbranched in

P. ramondii. Similar simplification of structure is to be found in Echium (Bram-

well, 1972a). In that genus, and other ‘temperate’ genera, the pachycauls of the

Canary Islands appear to represent relics of the pachycaul starters which initiated

the herbaceous lines so common in Europe, e.g. Echium (Meusel, 1952; Bramwell,

1972a), Sonchus (Bramwell, 1972b), Carlina (Meusel, 1952). Similarly, species

of Erysimum, Crambe, Aeonium, Chrysanthemum, Campanula, Bupleurum,

Dendriopoterium, Bencomia, Digitalis and Limonium (‘Statice’) appear as pachy-

caul relics in the Atlantic Islands (Meusel, 1952).

STEM ANATOMY

In general, the anatomy of the herbs in Senecio and Lobelia is a good deal

simpler than that of their pachycaul relatives — fewer cell-layers, leaf-traces, ducts,

less modification in the pith and cortex with aerenchyma etc. The seedlings of the

pachycauls are more ‘conventional’; the differences arise when the apex increases

in size.

Cortical and medullary bundles

Associated with hyperpachycauly, there is the appearance of the phyllodic

leaf-base and cortical bundles in Lobelia; some species have relic medullary

bundles showing that the medullary bundle condition is the primitive one in

Afroalpine Pachycaul Flora 49

Lobelia, and the cortical bundle condition the advanced. Davis (1961) points out

that in the Compositae, medullary bundles are particularly abundant in the

Cichorieae, especially in those plants with the ‘rosette-habit’.

In Lobelia, the medullary bundles serve the base of the primitive ‘forest leaf’;

the cortical bundles are often associated with the phyllodic leaf. In a similar way,

cortical bundles are often associated with leaves of the ‘monocotyledonous’ type

in the Dicotyledons, e.g. Eryngium spp. of the monocotyledonous habit (Metcalfe

& Chalk, 1950: 717), Gentianaceae-Gentianoideae (ibid.: 933) and groups with

leaves which have few costae, e.g. Melastomataceae (ibid.: 637).

The appearance of cortical bundles seems to be a ‘way out’ in evolutionary

lines where a larger leaf is being favoured and yet the number of traces to serve

such a leaf has been lost; hence in Lobelia, the cortical bundles are found in the

most massive pachycauls (Rueppellianae), whose massiveness has been selected

for by the alpine and swamp environments. Such bundles also give support to those

massive inflorescences formed by the reduction of branching of a forest form, and

for which the capacity for supporting lignification has been lost.

It has recently been suggested (Zimmermann & Tomlinson, 1972) that the

regular dicotyledonous ring of vascular bundles may be the equivalent of the outer

of the monocotyledonous systems seen in some woody monocotyledons. If this is

indeed the case, then Lobelia sect. Rhynchopetalum may demonstrate how the two

systems as exemplified by L. giberroa may give rise to the typical dicotyledonous

system as seen in L. bambuseti by loss of the inner system and the origin of a

‘monocotyledonous’ system as shown by L. rhynchopetalum with the appearance

of a ‘new’ cortical system associated with basally growing leaves (c.f. Burtt, 1974).

Hyper pachycauly

Selection has favoured the hyperpachycaul in the extreme alpine climate; the

hyperpachycaul is marked by its massive apex and reduced branches compared

with its forest relatives. Dominance of the apex over lateral meristems is found

in the absence of suckers in L. wollastonii, the unbranched inflorescences of the

alpine L. rhynchopetalum, L. wollastonii, etc. with the basipetal inflorescence

gradient (Mabberley, 1975a) lost etc., the untoothed leaves of alpine Nicotiani-

foliae and the large capitula on weakly branched inflorescences of the alpine

Dendrosenecios; in short, there is a common constraint determining the morpho-

logy of the hyperpachycaul ‘syndrome’ (c.f. Beketoff, 1858; Uittien, 1928; and

the particular case of Sonchus (Bramwell, 1972b) ). The balance of growth factors

determining differentiation in the tissues must be tipped in favour of apical

dominance. Such may be an increase in ‘auxin’ as has been suggested by Cotton

(1944) and was discovered in Aster by Delisle (1937) who found that there was

more auxin in the apices of the inflorescences of A. novae-angliae L. than in those

of A. multiflorus Ait. which is much more branched, (c.f. also Smith, 1967).

LEAF

Venation

The venation of Senecio (Mabberley, 1973a) and Lobelia (Mabberley 1974c)

leaves is mainly or entirely basipetally formed. In Dendrosenecio, the fraction of

the leaf formed acropetally is very small; some herbaceous species have a larger

part of the lamina thus formed and may be amphipetal.

In the East African Lobelias, my studies have shown a series demonstrating

the loss of teeth and acropetally formed venation. This series is interpreted as the

failing of the marginal meristem in the leaf with the consequent loss of teeth, and

the increasing importance of the spreading growth of the ‘midrib’, giving the

phyllodic leaf-base. The reduction of toothing in both Senecio and Lobelia reduces

the number of hydathodes per leaf. The action of hydathodes is not well understood;

50 Gardens’ Bulletin, Singapore — X X1X (1976)

despite their supposed efficiency in extruding water, the hydathodes of the toothed

leaves of L. assurgens L., a pachycaul of Jamaica, investigated by Shreve (1914)

could not prevent the ‘injection’ of the leaves by water during heavy rain.

The reduction of the acropetal venation would appear to be irreversible.

Vassal (1970) has shown the appearance of the phyllodic leaf in Acacia to be

polyphyletic and formed in various ways, but that there is a progressive loss of

pinnae, with a ‘mucro’ left in some species, as in Senecio and Lobelia.

On the other hand, there appears to be a constraint on the number of primary

costae derived from basipetal development of the lamina. In Senecio, the largest

leaves have about 18-20 veins in Dendrosenecio; most herbaceous species have

costal numbers lower than 18. However, some coarse herbaceous species of Uruguay,

e.g. S. bonariensis Hook. & Arn., appear to have very large numbers of costae; on

close examination, it can be seen that the intercostals have been ‘pulled out’ during

development, thus increasing the apparent costal number, as in S. keniodendron,

(Mabberley, 1973a).

Abscission

Abscission is not a common characteristic in the Compositae (Bentham,

1873), and is almost restricted to those shrubby and arborescent plants of leptocaul

construction with narrow leaf-bases, e.g. Brachylaena, These characters tend to be

associated with the discrete midrib and looped costae, early-formed venation

consummate with compact buds and the sudden expansion of intermittent growth,

making them comparable with other tree leaves. The insulating marcescent frills

and persistent leaf-bases of Dendrosenecio and Lobelia wollastonii are conspicuous

in the afro-alpine flora. When young, however, al! Dendrosenecios and Lobelia sect.

Rhynchopetalum display this phenomenon, as do herbaceous species, e.g. L. urens

L., where the rootstock is covered with persistent leaf-bases (Brightmore, 1968).

How widespread is the absence of abscission and the persistence of leaf-bases?

Within Senecio, all herbs examined have persistent leaves and it appears very com-

monly in the herbaceous Compositae but is more familiar to flower arrangers than

to monographers. The shrubby S. hypargyraeus DC. (Madagascar), the climbing

S. maranguensis O, Hoffmann (Tanzania) and the leaf-succulent species are

exceptions. Their small-based leaves are easily lost, even during drying in the press.

In the shrubby Compositae, leaf-fall is often not clear-cut and the marcescent

foliage makes a useful: character for recognizing sterile Compositae in ‘the bush’.

The leptocaul Brachylaena loses leaves as others are formed (Humbert, 1962: 45)

or may lose them altogether in the cold season (Lecomte, 1922). However,

marcescence is a general feature of herbs and pachycauls of Compositae, e.g. the

pachycaul Espeletia in the Andes and pachycaul Conyza vernonioides (A. Rich.)

Wild of East Africa. Such persistent leaf-bases cover the ‘stock’ of many herbs,

e.g. Andryala spp. and Senecio asperulus DC. (Hutchinson, 1946: 255), and make

the climbing hooks of Mikaniopsis (Exell, 1956). Comparable contrast of leptocaul

and pachycaul and herb is to be found in the Boraginaceae (s./.) with pachycauls,

e.g. Echium spp. of the Canary Islands, and herbs, e.g. Myosotis, with marked

SEEN. compared with the leaf-dropping trees, Cordia and Ehretia, of the

ropics.

Much has been written of the ‘abscission layer’ with regard to marcescence,

but Gawadi & Avery (1950) pointed out that abscission is not always associated

with such a layer and that the layer is a protective feature of the cicatrice; indeed,

it sometimes appears after abscission. Nevertheless, the range of forms of marces-

cence and abscission in monophyletic groups shows that abscission has been gained

or lost many times in the angiosperms.

Afroalpine Pachycaul Flora 51

Many young tropical trees retain their leaves in the dry season (Schaffalitzky

de Muckadell, 1959) rather like the beech (Knight, 1795) in winter or when kept

horticulturally short as a hedge. It is one of a syndrome of ‘juvenile’ characters

(Schaffalitzky de Muckadell, 1959) which appear to represent a primitive condition

in wood anatomy etc. (Mabberley, 1974 a-b).

If it is postulated that the primitive pachycaul had marcescent leaves, it seems

reasonable to argue that such marcescence may have been selected against with

the increasing trunk size due to increasing wood formation through secondary

thickening, but elaborated where such a mantle would act as an insulator, e.g. in

hot conditions the Joshua Tree (Yucca brevifolia Engl.) of the deserts of S.W.

United States (Menninger, 1967: 2) and in the cold, Espeletia in the Andes. The

origin of the leptocaul tree in many lines according to the Durian Theory must

have been accompanied by the origin of the small leaf with abscission which seems

to have been achieved in various ways (Gawadi & Avery, 1950); especially

efficient abscission mechanisms would have been selected for in seasonal conditions,

such as ‘savanna’ and the temperate zones.

EUROPEAN FLORA

The ecological preference of lobelias for wet places (Woodhead, 195la) is a

direct result of a wet tropical ancestry through upland swamp habitats to the

temperate zones; the predominance of aerenchyma and hydathodes in Lobelia is

thus explicable as is the remarkable habit of the aquatic L. dortmanna L. The

rare branching of L. dortmanna inflorescences (Woodhead, 1951b) is explicable

as an ancestral trait, and the minute undeveloped flowers at the apex and smaller

cell-size in the upper leaves (Tenopyr, 1918) are to be expected from the primitive

‘die-away growth’ (Corner, 1949) of the primitive tropical pachycaul ancestor.

Pachycaul Outlook

We need to know more of pachycaul plants (Corner, 1967a). In the Com-

positae, we want to know how some tribes have elaborated leptocaul trees as in

Dicoma and Brachylaena; the latter genus has even reached the ‘willow pattern

stage’ (Corner, 1964: 143), the ultimate in leptocauly, in B. neriifolia R.Br.

(Hutchinson, 1964: 228). Such pachycaul-leptocaul trends are not open to simple

computer analysis, for they are in parallel within related phylads. Are the principles

governing pachycauly in Compositae and Campanulaceae of general application?

In Compositae, we need to know more of hyperpachycauly and _ the

reappearance of the big leaf when the acropetal venation has been lost, as in the

lettuce in cultivation, and why the basipetal venation of Compositae never seems to

exceed about eighteen major costal pairs. We need to know more of the pachycaul

Dendrocacalia of the Bonin Islands (Tuyama, 1936) and of the Siberian Petasites

the petioles of which are higher than a man (Gilbert-Carter, 1947: 143). We need

to know more but we are almost too late: introductions of continental plants to the

islands of Hawaii and St. Helena, and the introduction of animals to those islands

and to Kerguelen have had disastrous effects on the passive native pachycauls, In

the mountains, the puyas are being grubbed up by shepherds, for lambs can get

entangled in Puya spines (Pontecorvo, 1972) and in Africa, the Dendrosenecios

of Kilimanjaro are becoming rare through excessive cutting (Hedberg, 1969).

Having fled the rising forests of leptocauly to reach the refuge of islands and

mountain, the pachycauls are now cornered by Man the Explorer and Exploiter.

We scarcely have time to begin to follow the leads to an understanding of plant

evolution provided by the Durian Theory.

52 Gardens’ Bulletin, Singapore — XX1X (1976)

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The Underground Forests of Africa:

a preliminary review

by

FRANK WHITE

Departments of Botany & Forestry, University of Oxford

“Evolution in Ficus is from the thick to the thin’ — E. J. H. Corner in litt. 27. ii. 74.

‘Evolution in Barotseland is from the thin to the thin’. Abbridged summary of this paper.

Summary

The growth-form of the geoxylic suffrutex, which has massive, woody, underground

axes but only annual or short-lived shoots above ground is described. The species considered

are all related to large forest or woodland trees or lianes and occur in genera with no

herbaceous members. They are confined to tropical and subtropical savanna regions. Their

distribution and ecology are considered. Geoxylic suffrutices are most diversified in Africa,

where they have independently evolved in 31 families. Very few occur in the Sudanian

Region and they are rare there. Most are endemic to the climatically similar Zambezian

Region where they are centred on the Kalahari Sands which cover much of the upper

Zambezi basin and its periphery. Arguments are developed which suggest that the growth

form of the geoxylic suffrutex has evolved, not primarily in response to fire, nor to frost,

as has been previously supposed, but as a response to the unfavourable edaphic conditions

provided by extremely oligotrophic, seasonally waterlogged sandy soils in a region of

extremely low relief.

Introduction

Corner’s fruitful hypothesis, that the proto-Angiosperm was of pachycaul

construction with an unbranched or sparsely branched stem, monopodial growth,

massive apical meristem, wide pith and cortex, sparse secondary xylem, very short

internodes and large compound leaves, illuminates the early adaptive radiation of

the vegetative architecture of the Angiosperms and has inspired a number of

important detailed studies (e.g. Hallé & Oldeman, 1970; Mabberley, 1974 a, b).

The further diversification of the leptocaul descendants of pachycaul plants,

however, has received much less consideration. The purpose of this short account

is to draw attention to a group of geoxylic suffrutices, which, despite their short

stature and quasi-herbaceous habit are closely related to large forest or woodland

trees or lianes, and, despite their exiguous subaerial parts, usually have massive

woody subterranean structures. Most of them are trees which, for some reason,

now live underground. It is interesting to enquire how this has come about.

Geoxylic suffrutices with this kind of phylogenetic relationship to large woody

plants are almost confined to those parts of the tropics with a markedly seasonal

distribution of rainfall, and where the prevalent vegetation is ‘savanna’ in which

woody plants and grasses occur together in various proportions. The term savanna

is used here in the general sense of Chapman & White (1970: 82) and not as a

precise classificatory unit. Today savanna vegetation is everywhere subjected to

extensive man-made fires and consists largely of pyrophytic species. It has probably

always been subjected to natural fires which were formerly less frequent and more

localized. Some authors, e.g. Exell & Stace (1972), believe that the suffruticose

57

58 Gardens’ Bulletin, Singapore — XX1X (1976)

habit in savanna regions has evolved largely as a response to fire. Fire has

certainly played a part in the evolution of the geoxylic suffruticose habit, but its

relative importance and significance seem to have been misunderstood.

The distribution of geoxylic suffrutices within the savanna regions of the world

is very uneven. Their greatest concentration is in south-central Africa on the

Kalahari Sands which cover most of the Upper Zambezi basin and its periphery.

Since other elements in the Zambezian flora also show a similar distribution, White

(1965) recognized a Barotse centre of endemism, which takes its name from the

ancient Kingdom of Barotseland, situated near its heart.

Within the Barotse centre the most characteristic habitat of these suffrutices

is a sparse open grassland which burns much less fiercely than most savanna vege-

tation. They are scarce or absent from the more fiercely burning types. This fact,

and their localized distribution within the fireprone savanna regions, suggests that

their origin should be sought not exclusively in relation to fire but that other factors

should be considered.

A few suffrutices, which occur on Kalahari Sand, also extend their range into

the Highveld grassland of the Transvaal, and a few others are endemic there. This

is a part of Africa where frost is severe, a fact which led Burtt Davy, writing at a

time (1922) when the flora of Barotseland was completely unknown, to suggest

that the suffruticose habit had been moulded in response to frost.

For the majority of suffruticose species occurring in the Zambezian Region

Speciation appears to be complete. Either their geographical ranges overlap with

those of closely related large woody species, with which they presumably share a

common ancestor, or they are taxonomically isolated and have no very close

relatives. For a significant minority, however, speciation is incomplete. Within a

single species some populations are suffruticose, whilst others are trees, shrubs or

lianes. By studying these species, together with non-suffruticose species in the same

general area, which have proceeded part-way towards the suffruticose habit, or

show, perhaps sporadically, some of the attributes suffrutices must acquire, it is

possible to reconstruct the probable ancestry of this particular growth form.

Evidence is presented in this paper which suggests that, in Africa, the geoxylic

suffrutex originated primarily as a response to extremely unfavourable edaphic

conditions, but that for some species, at least occasionally, fire is necessary for

vigorous growth. The suffrutex is better adapted to frost than the tropical trees and

lianes which gave rise to it, but it is unlikely that frost played any significant part

in the evolution of the habit.

Literature on geoxylic suffrutices is sparse and scattered. Only Burtt Davy

(1922) has attempted a general review.

Growth Forms

There are many kinds of suffrutex and the term is often loosely or erroneously

applied. The stems of a suffrutex are woody at the base and persist for several

years, giving rise to less persistent shoots, which die back after a relatively short

time, sometimes each year, sometimes after a longer interval. The suffrutices dealt

with here are unusual, in that, at least under present-day conditions, their stems are

burnt back almost to ground-level nearly every year. Suffrutices are clearly adapted

to this condition. Shortly after burning and well before the onset of the rainy

season they send out new shoots, which often produce flowers precociously at the

base of the shoot before it is fully developed. The associated grasses and other

herbs, which when fully grown may completely conceal the suffrutices, do not

begin their vegetative development until after the rains break, by which time the

suffrutices have finished flowering.

Underground Forests of Africa 59

The suffrutices dealt with here are very sensitive to fire. Even if their shoots

are only lightly singed, they die back to the base. A severe fire might kill all the

subaerial parts, in which case renewal is from subterranean stems and the plant

behaves as a geophyte. Normally, however, the basal parts of the subaerial stems

remain and the plant behaves as a chamaephyte.

Different species of suffrutex, and sometimes different populations within species,

behave differently when they are protected from fire. In some species there is a

considerable die-back every year almost to the base. In other species there is a

limited amount of upward growth which may continue for a few years. In obligate

suffrutices, however, upward growth is severely restricted and ultimately the

subaerial parts become moribund. Few flowers are produced and there is pro-

gressive die-back towards the base. In Parinari capensis all herbarium specimens

from the northern Transvaal are less than 15 cm. tall. Burtt Davy transplanted P.

capensis “‘to more favourable conditions of temperature and soil moisture’’ but it

““did not show any change of habit after several years’. North of the Limpopo,

when individuals escape fire, they are capable of attaining a height of 40 cm. but

no more. At the extreme south-eastern limits of its range in southern Mocambique

and northern Natal it can grow up to a height of 2 m.

All the suffrutices dealt with here have massive woody underground parts and

the term ‘geoxylic’, used by Du Rietz (1921) in a somewhat different context, is

appropriate. In the majority, several axes radiate just beneath the surface of the

soil from the main vertical subterranean axis, which, except in young plants, is

relatively poorly developed. Sometimes they extend for a distance of several metres.

In some species these axes can reach a diameter of 10 cm. or more. They are

usually very hard and consist mostly of secondary xylem, the total amount of which

is probably no less than that of a medium-sized woodland tree growing in the same

general region. These radiating axes are usually referred to as ‘rhizomes’. Their

true nature, however, requires careful investigation since the arboreal relatives of

some suffrutices are said to sucker freely from their extensive superficial roots. The

suffruticose Parinari capensis, for instance, looks very similar to a suckering clump

of the tree species P. curatellifolia Planch. ex Benth. though their proportions are

different.

Some species, e.g. Erythrina baumii Harms, have specialised water-storing tissue

(Duvigneaud, 1954), but this does not seem to be a general feature.

Some species are not rhizomatous or only slightly so and the underground part

consists of a large vertical axis which may be greatly expanded at ground level

where many annual shoots arise. Rawitscher & Rachid (1946) describe these for

Cochlospermum insigne St. Hil. and a palm, of the genus Acanthococos. They call

them ‘xylopodia’ and say they are stems. This type seems to be rare in Africa.

This account is confined to suffrutices which not only are closely related to

large trees or lianes and have presumably evolved from large trees or lianes, but

Occur in genera which except for their suffruticose members consist exclusively of

large woody plants. Suffrutices of similar habit, though usually with smaller under-

ground parts, which belong to otherwise shrubby groups are excluded from con-

sideration. Similarly the suffruticose species of genera which include true herbs and

trees, e.g. Cassia and Phyllanthus are omitted.

Fig. 1 illustrates Euclea crispa a typical “‘rhizomatous” geoxylic suffrutex. In

this polytypic species some subspecies, like the one illustrated are obligate suffruti-

ces, whereas others are always trees. The latter sometimes occur as single-stemmed

individuals, but sometimes form thickets of trees which arise from suckers from the

superficial ‘roots’.

60

Gardens’ Bulletin, Singapore — X XIX (1976)

Fig. 1. Euclea crispa (Thunb.)

Giirke. A typical rhi

geoxylic suffrutex. Note the cha

remains of last-year’s stems.

Underground Forests of Africa 61

Distribution and Ecology

General distribution

Geoxylic suffrutices are a conspicuous feature of the campos cerrados of the

Planalto of Central Brazil, and are recorded in the classical literature (Schimper,

1898: 376; Warming, 1892). No general review has been published but information

can be gleaned from a scattered literature — Andira inermis Mart. and Anacardium

pumilum St. Hil. (Rawitscher et al, 1963) Jacaranda decurrens Cham., Cochlo-

spermum insigne St. Hil. and Acanthococos sp. (Rawitscher & Rachid, 1946),

Byrsonima verbascifolia Rich. ex Juss. (Aubréville, 1961), Chrysophyllum soboli-

ferum Rizzini (Mangenot, 1969), Licania dealbata Hook. f. and Parinari obtusifolia

Hook. f. (Prance, 1972), and Caryocar brasiliense Cambess. subsp. intermedium

(Wittmack) Prance & Freitas da Silva (Prance & Freitas da Silva, 1973).

It appears that geoxylic suffrutices are fewer in species in South America than

in tropical Africa, and that taxonomically isolated, obligate suffrutices are pro-

portionally less well represented.

In Asia it appears that there are very few geoxylic suffrutices. From Australia

they seem to be absent, though many multiple-stemmed, tall-shrubby species of

Eucalyptus have large woody underground parts (mallee).

It is in tropical Africa that this growth form is found in its greatest diversity.

Here there are no less than 109 species belonging to 56 genera occurring in 31

families. These are listed systematically in an appendix.

Distribution in Africa

In Africa geoxylic suffrutices are almost confined to the two great savanna

regions — the Zambezian and Sudanian. Only a few species occur in the transitional

region to the south of the Zambezian Region, the prevalent vegetation of which is

grassland and wooded grassland. There are also a few others in the southern part

of the Indian Ocean coastal belt, the Tongaland-Pondoland Region, which is a

mosaic of savanna-like and forest formations (Fig. 2). Since very few species are

confined to the Tongaland-Pondoland Region it is not considered further.

The Sudanian Region occurs as a wide band north of the equator between the

rainforests of the Guineo-Congolian Region and arid and semi-arid regions to the

north. The Zambezian Region occupies a comparable position south of the equator.

In area these two regions are comparable. Their vegetation which consists mainly

of woodland, wooded grassland and various types of edaphic and secondary

grassland, is broadly similar, as is their climate. The mean annual rainfall varies

from 500 to 1500 mm. and the dry season lasts from 5 — 7 months. The Zambezian

Region, however, is somewhat more diverse in its physiography and climate. In

both regions dry season fires are an annual occurrence over extensive areas. Neither

region can be said to be more fire-prone than the other.

The representation of geoxylic suffrutices in the two great savanna regions is

very uneven. Only 7 species belonging to 2 genera in 2 families are known from

the Sudanian Region, whereas 102 species in 55 genera in 30 families occur in the

Zambezian Region. Of the 7 Sudanian suffrutex species, 6 belong to the genus

Combretum and 5 of them are closely related. 4 species are of very restricted

distribution and are confined to upland areas such as Fouta Djallon and the Jos

Plateau. Another species, C. sericeum G. Don f., is of uncertain taxonomic status and

is connected by intermediates to a climbing species, C. paniculatum Vent.

The Sudanian and Zambezian Regions are so different in their suffruticose

floras that an explanation must be sought, either in their unequal opportunities for

the evolution of suffruticose species or in those for the survival of a suffruticose

flora which was formerly common to both.

62 Gardens’ Bulletin, Singapore — XX1X (1976)

It is well known that the flora of the Sudanian Region is, in general, much

poorer than that of the Zambezian Region. In two analyses of the larger woody

plants occurring in the two regions, White (1962, 1965) has shown that the flora

of the Zambezian Region is probably between two and four times as rich as that

of the Sudanian Region. He suggests (1962) that this may, at least in part, be due

to differential extinction during the Pleistocene. A region as physiographically

diverse as the Zambezian offers better opportunities for migration and survival

than does a region of low general relief such as the Sudanian. There is much

phytogeographical evidence to support this idea. Several species which are wide-

spread in the Zambezian Region, e.g. Ochna schweinfurthiana F. Hoffm., Protea

a

FROMONTE

OG

ees

bes

Fig. 2. Map of Africa showing chorological regions referred to in the text.

Underground Forests of Africa 63

madiensis Oliv., Terminalia mollis Laws., are very sporadic in the Sudanian Region.

Their distributions suggest that in the Sudanian Region they have only just avoided

extinction due to climatic change. If they have only just managed to persist, is it

not likely that some of their former associates have perished? Similar considerations

might apply to the suffrutices, but here the discrepancy between the two regions is so

much greater — the Zambezian suffruticose flora is 15 times as rich as the

Sudanian and, at the generic level, 22 times as diversified — that the explanation

must surely be sought in differential opportunity for speciation. This leads us to a

consideration of the ecology of geoxylic suffrutices.

Ecology in Africa

The most characteristic habitat of the geoxylic suffrutex in the Zambezian

Region is seasonally anaerobic grassland, mostly on sandy, extremely oligotrophic

soils, which are waterlogged and badly aerated for part of the year and dry out at

least in their upper layers during the dry season. Such conditions are inimical to

the growth of trees. Even the growth of the grasses, which share dominance with

Cyperaceae, is sparse and wiry.

The best-known occurrences of this habitat are at the edges of dambos, the

seasonally waterlogged grassy depressions which are such a characteristic feature

of the unrejuvenated plateau surface representing the African cycle of erosion

(King, 1951) which occupies a large part of the Zambezian Region.

By far the most extensive occurrences, however, are on the Kalahari Sands

which occupy the Upper Zambezi basin and its periphery, and extend northwards

as a narrow belt far into the Guineo-Congolian Region (fig. 3.). The relief of this

region is so gentle that waterlogged soils occur very extensively in the Zambezi

basin on the virtually flat interfluves between the lower reaches of the tributary

rivers of the Zambezi, and, locally, on watersheds of higher elevation which in

general are better drained.

This type of anaerobic grassland with suffrutices is the most widespread

vegetation type in the upper Zambezi basin (White, in press). Apart from the

dambos mentioned above, it does not occur anywhere else in Africa, except very

locally. There are small areas associated with impeded drainage in places near the

coast in the Tongaland-Pondoland Region, which is contiguous with the Zambezian

Region, and a few suffrutices occur there.

In the Sudanian Region anaerobic grasslands on sandy oligotrophic soils com-

parable to those of Zambezia are fragmentary in the extreme, because the land

surface has reached a different stage in the cycle of erosion. Apart from a few

small patches scattered along the coast they are confined to small areas, each only

a few acres in extent, on the flat tops of mesa-like hills where the drainage is

impeded by the occurrence of hardpan near the surface (J. B. Hall, in litt.). Under

these circumstances it is difficult to see how a suffruticose flora could have evolved.

Geoxylic suffrutices are normally absent from secondary grassland following

the destruction of forest or woodland. They are only plentiful on soils which are

sO impoverished that they can only support sparse secondary grassland which in

composition and luxuriance is similar to edaphic suffruticose grassland. This occurs

chiefly in montane areas and on Kalahari Sand.

Chapman & White (1970) present evidence which indicates that during the

last 1000 years extensive areas of montane forest in Malawi have been destroyed

by fire and replaced by grassland which owing to soil erosion has become pro-

gressively shorter and less luxuriant. The ultimate stage is a sparse grassland in

which suffrutices such as species of Protea and Parinari capensis are often con-

spicuous. According to Fanshawe (1969: 45) sparse grassland with abundant

suffrutices, which has spread from the waterlogged interfluves and depressions, may

represent the last stage of degradation of Kalahari forest and woodland following

clearing and persistent burning.

64 Gardens’ Bulletin, Singapore — XX1X (1976)

Kalahari Sand formerly covered a much larger area than it does today as is

shown by the many residual patches which still survive.

The great majority of geoxylic suffrutices occurring in the Zambezian Region

are either confined to the main occurrence of Kalahari Sand centred on Barotse-

land, e.g. Trichilia quadrivalvis C. De. (fig. 3), or have their centre of distribution

there, or occur within the range of the former distribution of Kalahari Sands.

The most abundant species on Kalahari Sand is Parinari capensis, which is also

the most widespread Zambezian geoxylic suffrutex (fig. 3). It occurs beyond the

former limits of Kalahari Sand on other types of sandy soil, not only the sandy

@ 100 200 300 400 500 800 MiLES

—————— ee

eS Map of Africa showing distribution of (a) Kalahari Sand (broken line); (b)

[richilia quadrivalvis C. DC. (continuous line); (c) Parinari capensis Harv. (solid circles).

:

Underground Forests of Africa 65

edges of dambos but also on shallow sandy soils surrounding granite inselbergs in

the Transvaal and on maritime sands of the Tongaland coastal plain. Most Zambe-

zian geoxylic suffrutices have distributions intermediate between those of Trichilia

quadrivalvis and Parinari capensis.

Evolution

The significance of fire

In the absence of fire, some, perhaps most, suffrutices are capable of a limited

amount of upward growth, but eventually the shoots become moribund and die

back. Fire destroys this slowly dying, not very floriferous, material, and stimulates

the production of numerous precociously-flowering shoots. This response to fire is

clearly adaptive. Flowering takes place some weeks or months before the associated

grasses, which eventually conceal the suffrutices, begin their growth. Their flowers

are visible and accessible to pollinating insects and much of the season’s growth is

completed before competition for light becomes a serious factor.

It is difficult, however, to see how the suffruticose habit arose in response to

fire. Chorological and ecological evidence are both against it.

We have seen that in Africa geoxylic suffrutices have a very uneven distribu-

tion. The great majority are concentrated in part of the Zambezian Region. The

Sudanian Region, with various qualifications mentioned elsewhere, is comparable

in size, climate and flora to the Zambezian. The incidence of fire is the same in

both, or, if anything, greater in the Sudanian, and yet the latter is almost bereft

of suffrutices.

Because of the climatic vicissitudes of the Pleistocene, the Sudanian Region has

suffered more extinction than the Zambezian, but the disparity between the two

suffruticose floras, compared with that of some other growth forms, is so great,

that differential extinction from a former common suffruticose flora provides an

unlikely explanation.

Within the Zambezian Region geoxylic suffrutices show a very uneven

distribution in relation to the intensity of burning. Their most characteristic habitat

is edaphic grassland, This is a fire-sensitive community and is frequently burnt. But

it does not burn fiercely, in contrast to most types of secondary grassland occurring

in the same general area. Suffrutices are conspicuously absent from the latter. It

has been demonstrated experimentally (Trapnell, 1959, White, unpublished) that

when Zambezian woodland is subjected to annual fires at the end of the dry season,

when the burn is more intense, the trees are progressively eliminated, and the grass

becomes more luxuriant. Suffrutices are not normally found under these conditions.

Whether fire or competition with the coarse grasses is the primary cause is

uncertain. The trees may be eliminated as trees, but they are not always killed

outright. The underground parts survive, and, each year, after the fire, produce an

annual crop of non-flowering coppice shoots. Even after 40 years of yearly late

burning, the rootstocks survive and, were the fires to cease, could give rise to trees

again. Burning as prolonged and intense as this far exceeds the destructive effects

of natural fires, or fires started in connection with land clearance and farming.

Lawton (1972) has shown that under the latter conditions many tree species, even

some which are relatively fire-sensitive, can become established from seed in

secondary grassland which is subjected to fierce, though not necessarily annual,

fires. The inescapable fact is that the woodland trees of the Zambezian Region are

well-adapted to withstand fire — even to withstand a fire-regime far fiercer than

anything they have experienced in their whole evolutionary history. They have no

need to evade a menace which does not exist. In some cases the tree which is

adapted to fierce fires and the related suffrutex which evades them are so similar

in everything other than pattern of growth and habit that identification is difficult

66 Gardens’ Bulletin, Singapore — XX1X (1976)

when the habit is unknown. Examples of such pairs of sibling species are Parinari

curatellifolia Planch, ex Benth. (tree) and P. capensis, and Diospyros batocana

Hiern (tree) and D. chamaethamnus Dinter ex Mildbr. It is perhaps significant

that Parinari curatellifolia is as common in the Sudanian Region as it is in the

Zambezian, but has not given rise to a suffrutex there.

The significance of frost

Burtt Davy’s early account (1922) was concerned with the Highveld in the

Transvaal. Here the prevalent vegetation is grassland “bare of trees except in the

shelter of rocky kopjes and even there only a few scattered individuals are met

with’. A few suffrutices, which also occur on Kalahari Sand, e.g. Dichapetalum

cymosum, Elephantorrhiza elephantina and Parinari capensis extend into the High-

veld grassland. A few other suffrutices, e.g. Elephantorrhiza obliqua, Erythrina

zeyheri and Eugenia pusilla, are more or less confined to it. The winters on the

Highveld are cold with considerable extremes. Frosts are a regular feature. Killing

frosts fall as early as March and as late as October. Burtt Davy suggests that in

the Transvaal the suffruticose habit has evolved in response to frost. This could

very well be so for the endemic species, but probably less than 10% of the

suffrutex flora of South Central Africa occur mainly in frosty regions and many

species occur in or are confined to frost free regions. Other chorological and

ecological evidence points in another direction.

Edaphic control

We have seen that in Africa the great majority of geoxylic suffrutices occur

on the mantle of Kalahari Sand centred on Barotseland, or within the region of its

former extent. They are mostly found on sandy soils on very gently sloping or

almost flat surfaces. The sands, some of which have been redistributed by water,

are extremely poor in nutrients. Because of the low relief and seasonal climate,

the sandy soils are seasonally waterlogged and seasonally dry. The fluctuating

water-table causes the formation of impervious horizons near the surface, This

accentuates the seasonal differences in soil-water content and restricts the rooting

environment and hence the nutrient supply of woody plants. In general, seasonally

waterlogged soils in the same general region favour the growth of grasses vis a vis

woody plants, but the Kalahari Sands are sometimes so deficient in nutrients that,

even in the absence of competition from woody plants, the grass growth is sparse.

The trees of the Zambezian Region cannot withstand seasonal waterlogging

followed by seasonal drying out of the soil. Under such conditions on the Kalahari

Sand, and at the sandy edges of dambos on the Central African plateau, trees are

replaced by suffrutices. Where flooding is prolonged, woody plants are completely

excluded.

Except when the suffrutices are flowering, the communities they occur in have

the appearance of grassland and are usually described as such. The phytomass of

the suffrutices however greatly exceeds that of the grasses.

The correlation between the edaphic conditions just described and the distribu-

tion of geoxylic suffrutices is so great, and the correlation between the incidence

of fire and the incidence of frost and the occurrence of suffrutices so weak, that

we must postulate a causal connection for the former. We must also look for

confirmatory evidence.

Although edaphic grassland with suffrutices is the most extensive vegetation

type in the upper Zambezi basin, dry forest (now largely destroyed) occurs on the

deeper well-drained sands, and is separated from the edaphic grassland by an

ecotone of woodland and wooded grassland,

I

;

Underground Forests of Africa 67

Within the upper Zambezi basin there is a complex mosaic of different edaphic

conditions largely dependent on effective depth of soil and its water-relations. It

is under circumstances such as these, especially where soil fertility is at a critical

low level, that one would expect to find intermediate stages in the evolution of the

suffruticose habit. The best example is provided by Baikiaea plurijuga Harms.

Baikiaea is a small genus of trees which is confined to the Guineo-Congolian

Region, except for B. plurijuga which dominates dry semi-deciduous forest on deep

well-drained Kalahari Sand in the lower half of the upper Zambezi basin. The

northernmost occurrences of B. plurijuga are separated from the Guineo-Congolian

Region by an interval of 600 km. B. plurijuga is normally a tree 20 m. or more in

height. There are no suffruticose species of Baikiaea, but B. plurijuga has recently

(Fanshawe & Savory, 1964) been found to occur on sites which appear to be

intermediate between typical forest sites and typical suffruticose grassland. Here

Baikiaea forms dwarf forests less than 2 m. tall. “If the root is excavated a

candelabra effect is exposed”. Just below the soil surface the original tap root gives

off a number of comparatively short twisted branches from the ends of which

tufted shoots arise. The latter apparently persist for no more than 4 years. This

life-form of Baikiaea is very similar to that of a rhizomatous geoxylic suffrutex.

Fanshawe and Savory suggest that the curious growth-form of Baikiaea might be

due to a peculiarity of nutrient status but is more likely to be due to impeded

drainage. A more detailed study of the edaphic conditions would be most

instructive.

A change in growth-form as drastic as that between a forest tree and a

geoxylic suffrutex could not be caused by the tree invading a new and very

different habitat under a stable environment, followed by its descendants gradually

adapting to the different conditions by mutation and selection. The original invader

would be eliminated by selection from the start. Such a change is much more likely

to happen if the environment of a population undergoes a gradual change to which

the population gradually adapts. In a region of such low relief and imperfect

drainage as Barotseland, relatively little change, either climatic or physiographic,

would be necessary to bring this about. Indeed, in another publication, Fanshawe

(1969b) discusses evidence which suggests that in one part of Barotseland the

water-table is at present rising and causing the deaths of trees over a large area.

It is currently fashionable to interpret most patterns of plant distribution in

Africa and some patterns of taxonomic relationship, especially where closely

related species are involved, in terms of climatic events of the Pleistocene, very

often in terms of the most recent phases, involving a period of no more than

20,000 years. Much, doubtless, can be interpreted in this way, but much cannot.

It is likely that edaphic conditions favourable for the evolution of suffrutices were

greatly extended in Barotseland during the pluvial periods of the Pleistocene, but

this does not mean that the suffrutices originated then. Quite small physiographic

events such as minor warping of the earth’s crust or the capture of major tributary

rivers could produce, over quite extensive areas, the kind of edaphic change

required for transformation in growth form. This could have happened repeatedly

over a very long period of geological time. The genus Parinari, which has figured

sO prominently in this discussion, is well represented in tropical America, Africa

and Asia, and occurs in Madagascar. In its leaves, flowers and fruits it is remarkably

uniform, and has diversified little since the breakup of Gondwanaland. Is it

necessary to postulate that its speciation occurred in the Pleistocene? Is it not more

likely that the tumultuous events of that period have merely sharpened the edges

of taxa which began their differentiation a very long time before?

68 Gardens’ Bulletin, Singapore — XXIX (1976)

APPENDIX

Systematic List of Obligate and Facultative Geoxylic Suffrutices occurring in Africa.

S — occurring in Sudanian Region. T-P — occurring in Tongaland-Pondoland Region.

Z — occurring in Zambezian Region.

ANACARDIACEAE

Z. Heeria nitida Engl. & v. Brehm. and

c. 8 other species

Z. Lannea edulis (Sond.) Engl.

Z. L. gossweileri Exell & Mendonca

Z. L. katangensis Van der Veken

Z. L. virgata R & A. Fernandes

Z. Rhus kirkii Oliv. and c. 4 other

species

ANNONACEAE

Z. Annona stenophylla Engl. & Diels

APOCYNACEAE

Z. Chamaeclitandra henriquesiana (K.

Schum. ex Warb.) Pichon

Z. Landolphia gossweileri (Stapf) Pichon

— facultative; liane

Z. Rauvolfia nana E. A. Bruce

Z. Strophanthus angusii F. White

ARALIACEAE

Z. Cussonia corbisieri De Wild.

CELASTRACEAE

Z. Salacia bussei Lozs. — facultative;

shrub

Z. S. luebbertii Loes.

T-P. S. kraussii— (Harv.) Harv. — facul-

tative; shrub

CHRYSOBALANACEAE

Z. Magnistipula sapinii De Wild.

Z. Parinari capensis Harv.

COCHLOSPERMACEAE

S. Cochlospermum tinctorium A. Rich.

COMBRETACEAE

Z. Combretum argyrotrichum Welw. ex

Laws.

brassiciforme Exell

. harmsianum Diels

. lineare Keay

. platypetalum Welw. ex Laws.

. relictum Hutch & Dalz.

. sericeum G. Don f.

viscosum Exell

DICHAPETALACEAE

Z. Dichapetalum bullockii Hauman

Z. D. cymosum (Hook.) Engl.

Z. D. rhodesicum Sprague & Hutch.

NwANYY

QAAANAANAA

DILLENIACEAE

Z. Tetracera masuiana De Wild. & Th.

Dur.

EBENACEAE

Z. Diospyros chamaethamnus Dinter ex

Mildbr.

, T-P. D. galpinii Hiern

, I-P. D. lycioides Desf. — faculta-

tive; shrub, small tree

D. virgata (Giirke) Brenan

Euclea crispa (Thunb.) Giirke —

facultative; shrub, small tree

FLACOURTIACEAE

Z. Caloncoba suffruticosa (Milne-Redh.)

Exell & Sleumer

GUTTIFERAE

Z. Garcinia buchneri Engl.

Z. Psorospermum mechowii Engl.

IXONANTHACEAE

Z. Ochthocosmus candidus (Engl. &

Gilg) Hall. f.

LECYTHIDACEAE

Z. Napoleona gossweileri Baker f.

LEGUMINOSAE: CAESALPINIOIDEAE

Z. Brachystegia russelliae Johnston

Z. Cryptosepalum exfoliatum De Wild,

— facultative, small tree

Z. OC. maraviense Oliv.

LEGUMINOSAE: MIMOSOIDEAE

Z, T-P Elephantorrhiza elephantina

(Burch.) Skeels

Bs E. obliqua Burtt Davy

T-P E. woodii Phillips

Ph Entada dolichorrhachis Brenan

7 E. nana Harms

LEGUMINOSAE: PAPILIONOIDEAE

Z. Erythrina baumii Harms

Z. EE. zeyheri Harv.

NN NN

LINACEAE

Z. Hugonia gossweileri Bak. f. & Exell

ex De Wild.

LOGANIACEAE

Z. Strychnos gossweileri Exell — facul-

tative; liane

MALPIGHIACEAE

Z. Sphedamnocarpus angolensis (A.

Juss.) Planch. ex Oliv.

MELIACEAE

Z. Ekebergia pumila 1. M. Johnston

Z. Trichilia quadrivalvis C. DC.

Underground Forests of Africa

MORACEAE

Z. Ficus pygmaea Welw. ex Hiern

Z. F. verruculosa Warb. — facultative;

small tree

MYRTACEAE

Z. Eugenia angolensis Engl.

T-P E. capensis (Eckl. & Zeyh.) Sond.

— facultative; tree

Z. E. pusilla N. E. Br.

Z. Syzygium guineense (Willd.) DC.

subsp. hAuillense (Hiern) F. White

OCHNACEAE

Z. Brackenridgea arenaria (De Wild. &

Dur.) N. Robson — facultative;

shrub.

Ochna confusa Burtt Davy & Green-

way

O. katangensis De Wild.

O. leptoclada Oliv.

O. macrocalyx Oliv. — facultative;

shrub

O. manikensis De Wild.

Ochna mossambicensis Klotzsch —

facultative; shrub

O. pygmaea Hiern

O. richardsiae N. Robson

PASSIFLORACEAE

Z. Paropsia brazzeana Baill. — faculta-

tive; shrub

PROTEACEAE

Z. Protea angolensis Welw.

Z. P. heckmanniana Engl.

Z. P. paludosa Welw.

Z. P. trichophylla Engl. & Gilg

RHAMNACEAE

Z. Ziziphus zeyherana Sond.

NN NN NNN N

69

RHIZOPHORACEAE

Z. Anisophyllea quangensis Engl. ex

Henriques

RUBIACEAE

Z. Ancylanthus rubiginosus Desf.

Gardenia subacaulis Stapf & Hutch.

Leptactina benguelensis (Welw. ex

Benth. & Hook. f.) R. Good

Morinda angolensis (R. Good) F.

White

Pachystigma pygmaeum_ (Schlecht.)

Robyns

Pavetta pygmaea Brem.

Psychotria spp.

*Pygmaeothamnus concrescens

Bullock

P. zeyheri (Sond.) Robyns

Tapiphyllum spp.

Tricalysia cacondensis Hiern

T. suffruticosa Hutch.

SANNA NNN & NP

SAPINDACEAE

Z. Deinbollia fanshawei Exell

TILIACEAE

Z. Grewia decemovulata Merxm. —

facultative; shrub

Z. G. falcistipula K. Schum. — faculta-

tive; shrub

Z. G. herbacea Welw. ex Hiern

VERBENACEAE

Z. Clerodendrum buchneri Giirke

Z. C. lanceolatum Giirke

Z. C. milne-redheadii Moldenke

Z. C. pusillum Giirke

Z. C. triplinerve Rolfe

* This genus only has suffruticose members. It is however very closely related to the

arborescent Canthium.

70 Gardens’ Bulletin, Singapore — X XIX (1976)

References

AUBREVILLE, A. 1961. Etude écologique des principales formations végétales

du Brésil, Centre Techn. For. Trop. Nogent-sur-Marne,

BURTT DAVY, J. 1922. The suffrutescent habit as an adaptation to environment.

J. Ecol. 10: 211-219.

CHAPMAN, J. D. & F. WHITE. 1970. The evergreen forests of Malawi. Comm.

For. Inst, Oxford.

DU RIETZ, G. E. 1931. Life-forms of terrestrial flowering plants, I. Act. a

phytogeogr. suec. 3: (1).

DUVIGNEAUD, P. 1954. Une Erythrine 4 xylopode des steppes du Kwango.

Lejeunia 15: 91-94.

EXELL, A. W. & C. A. STACE. 1972. Patterns of distribution in the Combretaceae.

In VALENTINE, D. H. (ed.) Taxonomy, phytogeography and evolution.

Academic Press, London & New York.

FANSHAWE, D. B. 1969a. The vegetation of Zambia. For. Res. Bull. 7. Kitwe,

Zambia.

1969b. The vegetation of Kalabo District. For. Res. Pamphl. 22.

Kitwe, Zambia.

& B. M. SAVORY. 1964. Baikiaea plurijuga dwarf-shell forests.

Kirkia 4: 185-190.

HALLE, F. & R. A. A. OLDEMAN. 1970. Essai sur l’architecture et la dynamique

de croissance des arbres tropicaux. Coll. Monogr. Bot. 6. Paris.

KING, L. C. 1951. South African scenery, ed. 2. Oliver & Boyd, Edinburgh.

LAWTON, R. M. 1972. An ecological study of miombo and chipya woodland with

particular reference to Zambia, Thesis, Oxford University.

MABBERLEY, D. J. 1974a. Branching in pachycaul Senecios: the Durian Theory

and the evolution of Angiospermous trees and herbs. New Phytol. 73: 967-975.

1974b. Pachycauly, vessel-elements, islands and the evolution of

arborescence in ‘herbaceous’ families. New Phytol. 73: 977-984.

MANGENOT, G. 1969. Réflexions sur les types biologiques des plantes vascu-

laires. Candollea 24: 279-294.

PRANCE, G. T. 1972. Fl. Neotropica Monogr. 9, Chrysobalanaceae. Hafner, New

York.

& M. FREITAS da SILVA. 1973. Fl. Neotropica Monogr. 12,

Caryocaraceae. Hafner, New York.

RAWITSCHER, F. K., M. G. FERRI & M. RACHID. 1943. Profundidade dos

solos e vegetacdo em campos cerrados do Brasil Meridional. Anais. Acad.

bras. Cienc. 15: (4).

& M. RACHID. 1946. Troncos subterrancos de plantas Brasileiras.

Anais. Acad. bras. Cienc. 18: 261-280.

SCHIMPER, A. F. W. 1898. Pflanzen-Geographie auf physiologischer Grundlage.

Fischer, Jena.

Underground Forests of Africa 71

TRAPNELL, C. G. 1959. Ecological results of woodland burning experiments in

Northern Rhodesia. J. Ecol. 47: 129-168.

WARMING, E. 1892. Lagoa Santa.

WHITE, F. 1962. Geographic variation and speciation in Africa with particular

reference to Diospyros. Syst. Assn Publ. 4: 71-103.

1965. The savanna woodlands of the Zambezian and Sudanian

Domains: an ecological and phytogeographical comparison. Webbia 19:

651-681.

(ed.) (in press). Vegetation map of Africa. UNESCO, Paris.

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Notes on Rain-Forest Herbs

by

B. L. BURTT

Royal Botanic Garden, Edinburgh

Concise summaries of views on the herbaceous plants of rain-forest have been

given by Richards (1952, pp. 96-102) and by Walter (1971, pp. 118-122). The

present notes are an attempt to expand the subject a little further, by recording

some observations on the growth patterns of dicotyledonous herbs and emphasising

the contrasts both with monocotyledons and with temperate forest dicotyledons.

At present the relation between structural features of the leaves and physiological

function is, in general, rather uncertain, and this is not the field for a taxonomist

to enter. Nevertheless I have ventured a few remarks, if only as a reminder of the

questions a field-botanist wants to ask. These notes are inevitably limited by my

personal experience, which wholly excludes the New World and is derived largely

from collecting trips in Sarawak.

The importance of the massive tropical palms (Palmae) and screw-pines

(Pandanaceae) in attaining a balanced appreciation of monocotyledons as a group

is now widely recognized. But even at the level of rain-forest herbs a comparison

between monocotyledons and dicotyledons illuminates some fundamental differences

more brightly than a similar study in temperate forests. When these are brought

into the picture, it is immediately apparent that, under the impact of a strongly

seasonal climate, the contrast between monocotyledon and dicotyledon has been

lessened.

First let us look at growth-habits, particularly at the underground parts. In

temperate forests rhizomes or stolons with scale-leaves are frequent, both amongst

dicotyledons and monocotyledons: for instance, Mercurialis (Euphorbiaceae — see

Mukherji, 1936) or Paris (Liliaceae — see Kirchner, Loew & Schroter, 1934) in

Europe; Podophyllum (Berberidaceae — see Holm, 1899) or Medeola (Liliaceae

— see Bell, 1974) in North America. Examples could easily be multiplied.

Of the herbs of tropical rain-forest Richards (1952, p. 98) says “ ... plants

with underground rhizomes are frequent, but the rhizomes are adapted for multi-

plication and migration rather than perennation”. He is echoed, despite a slightly

different concept of perennation, by Walter (1971, p. 118): “‘the herbs are often

equipped with underground perennating organs such as rhizomes and tubers. But

these serve less as storage organs for reserve food than as a means of vegetative

reproduction”. These statements need some qualification. They might seem to

imply, no doubt unintentionally, that the rhizomes of temperate forest herbs do

not serve for spread or vegetative reproduction; of course, they clearly do so.

Secondly, in my experience, rhizomes may be common on tropical monocotyledons

but they are certainly very rare amongst the dicotyledons. In considering rain-forest

herbs the two groups must be distinguished.

It may be as well to restrict the words “storage” and ‘‘perennation” to use

when a seasonal dormancy is accompanied by complete die-back of aerial shoots.

Then the situation found in most non-seasonal rain-forest herbs with underground

rhizomes may be described as the accumulation of food-reserves. The importance

of this must not be underestimated in the monocotyledons. The rhizomes of many

73

74 Gardens’ Bulletin, Singapore — X XIX (1976)

Zingiberaceae eventually throw up massive new leaf-fronds anything from 1.5 to

9 metres in height. This can scarcely be achieved without the backing of some

accumulated reserves, even though there is continuity through the rhizome or stolon

to older actively photosynthetic fronds. Very often the tip of the rhizome becomes

decidedly swollen when it turns up to form the new leaf-frond.

Some Zingiberaceae grow in tight clumps, and these, of course, have short

slow-growing rhizomes; others form dense or diffuse patches, and in these the

rhizome is extended as a far-ranging stolon. Apart from question of size, the

patterns are those of rhizomatous herbs in temperate forests.

Dicotyledonous herbs also form patches in the rain-forest, but this is achieved

without the aid of scale-clad underground rhizomes or stolons. A characteristic

pattern of growth can be observed in Cyrtandra radiciflora C.B.Cl. (Gesneriaceae).

This species forms stands with erect leafy shoots keeping a more or less even height

of about 0.75 metre. These shoots are evergreen and their duration is unknown.

Flowering is axillary and basal, at or near ground level. The terminal bud remains

vegetative and produces a succession of leaves. What prevents the shoots from

growing higher and higher?

It seems that the average height is maintained because, as upwards growth

proceeds, the lower part of the stem becomes more and more decumbent. If a

handful of shoots are pulled up it will be found that they are linked by pieces of

prostrate, sometimes buried, stem. Buds on the prostrate stems give rise to new

shoots that help to thicken the patch, and the process of becoming prostrate helps

to expand it. At all times the main growing points of the shoots are aerial and are

directed upwards. There is no horizontal (diageotropic) growing point like that

of a rhizome or stolon.

The pattern just described for Cyrtandra radiciflora is found in a number of

species of this genus (which is very large and very varied in growth-patterns), and

in other genera where some species have axillary inflorescences: Argostemma

(Rubiaceae), Elatostema (Urticaceae), Linariantha (Acanthaceae), Gomphos-

temma (Labiatae) come to mind. Other rain-forest herbs (e.g. some Acanthaceae)

have terminal inflorescences; these plants retain their herbaceous stature by dying

down to near the base after fruiting and form new shoots from basal buds: scars

of old shoots are often visible, though I have never noticed a dead shoot in situ.

Observations on the death-patterns of tropical herbs are badly needed: there are

indications that the fruiting shoot may die slowly, so that its leaves are still

photosynthetic long after the seeds are shed. This could be a necessary feature, in

the absence of underground storage organs, to support the growth of a new shoot:

but that is speculation until careful studies can be made. This pattern of growth

is shown in some forest species of Pseuderanthemum (Acanthaceae); other members

of the genus do not die back but produce shoot-buds from the axils of leaves just

below the dead infructescence — and become shrubs, Another genus of Acanthaceae

which has terminal inflorescences and dies down is Cosmianthemum; it is unusual

in having somewhat fleshy roots; otherwise the roots of these forest herbs are thin

and wiry.

By no means all the dicotyledons with axillary flowers become decumbent at

the base. A very frequent habit is a stiff erect unbranched stem with the leaves

tending to be in the upper part, sometimes in a distinct cluster near the top —

rather the habit of a miniature palm tree. Once again we have no knowledge of the

duration of such plants. This habit is found in a number of genera, for instance

Didymocarpus, Didissandra and Cyrtandra (Gesneriaceae), Sonerila (Melasto-

maceae) and Neckia (Ochnaceae).

A simple modification is found when species grow horizontally from vertical

cliff faces; then the terminal tuft of leaves is eccentric, the leaves on the lower side

being longer; in Cyrtandra mirabilis C.B.Cl. the longest leaves may be as much as :

Rain-forests herbs 75

70 cm, and as they are thin and delicate this would be an impossible size on an erect

stem. In this habitat, too, is found an elaboration of the simple pattern; the stem

is branched, each branch having its characteristic tuft of leaves: in a form of

Didymocar pus gracilipes C.B.Cl. there may be as many as 20 leaf-tufts. Again it

is difficult to envisage this pattern being successful as an erect stem. Cliff-plants

with these fans of pendulous leaves are found in both Asiatic and American

Gesneriaceae (cf. Resia H. E. Moore, 1962), and also in such genera as Steenisia

(Rubiaceae).

Another variant is the plant with an erect fan of leaves sometimes found on

steep slopes and banks in the forest. Here the stem is short, or the lower part

becomes prostrate keeping the leaf tuft near ground level. Such a fan of leaves,

each about 30 cm long, is beautifully shown in Cyrtandra penduliflora Kraenzl. and

is associated there with marked anisophylly—one leaf of each pair is reduced to a

small stipule-like structure — and the development of prop roots, perhaps 20-30 cm

long and 2 mm diam. quite rigid and branching only when they have reached the

soil. These are of obvious value in supporting the plant in steep habitats.

It might seem that the simple erect stem and the decumbent, branched, patch-

forming type stand widely apart. However, Didymocarpus malayanus Hook. f. is

a plant of the Malay Peninsula which occurs in two forms: one has an erect

unbranched stem, but the leaves show rather less apical aggregation than charac-

teristic of that pattern, while the other is a prostrate mat-forming type, the shoots

never being more than about 6 inches above the surface of the ground. Although

the inflorescences of the erect plant carry many more flowers, there appears to be

no essential difference between the two: if eventually separable as distinct species,

they are at least very closely allied.

One noteworthy type of growth that I have not personally encountered in

Sarawak (and I think it is not recorded there) is the much branched monocarpic

herb represented by several species of Strobilanthes (Acanthaceae). These plants

are well known for their gregarious habit and their periodic simultaneous flowering.

Records for Sumatra and Java are summarized by van Steenis (1942); they include

S. kunthianus Benth. from open grassy places and S. cernuus Bl. and others which

are “‘hygrophytes of rather dark mountain forests’. The habit is best known in

species of Strobilanthes found in the seasonal forests of India, and also occurs in

other genera of Acanthaceae (Isoglossa, Mimulopsis) in the evergreen but distinctly

seasonal forests of eastern and south-eastern Africa.

In these seasonal forests underground storage organs become much more

frequent in dicotyledons: climbers with annual stems and tubers become prominent

(Gerrardanthus, Cissus fragilis Harv., Tacazzea in Natal) and genera which lack

storage organs in rain-forest, or in the always-damp habitats in these seasonal

forests, develop them: for instance Begonia. In south-east Africa Impatiens

duthieae L. Bolus is found in always-damp situations in the forest and has no

storage organs, J. flanaganae Hemsl., more exposed to seasonal change at the forest

margin, has tubers; in northern Malaya Impatiens mirabilis Hook. f., a plant of

the somewhat seasonal forests on the limestone, has a thickened storage trunk

resembling an Adenium.

Two genera of monocotyledons that range from the seasonal monsoon forests

of south-east Asia down into the rain-forest are particularly interesting. These are

Arisaema (Araceae) and Hedychium (Zingiberaceae). By far the greater number

of the species of Arisaema live under markedly seasonal conditions: they have an

underground corm which produces leaves and inflorescence annually and has a

distinct period of rest. This pattern is found also in Arisaema fimbriatum Mast. of

the Langkawi Islands, N. Malaya, where the forest is largely evergreen, but with

a proportion of deciduous species and a distinctly dry and cool winter. Species

are found further south on the mainland (A. anomalum Hemsl.) and in Borneo

76 Gardens’ Bulletin, Singapore — X XIX (1976)

and Java (A. umbrinum Ridl., A. filiforme Bl. etc.), which have a thick fleshy

rhizome, rather than a corm, and these plants have leaves present all the year

round. Hedychium is rhizomatous throughout its range, but in the northern seasonal

area all the leaf fronds die down in winter and the plant is dormant; in the

Bornean H. cylindricum Ridl. there are leaf fronds present throughout the year.

Another aroid, Amorphophallus, seems to be somewhat anomalous in its

behaviour. It has a large corm and Walter (1971, p. 118) reports that in Africa,

where it grows in seasonal areas, it flowers before it leaves. In Sarawak, where

it is by no means uncommon, a corm will produce a flower in one year, a leaf in

another: adjacent corms are in growth simultaneously so that flowers and leaves

may be found together. However there is probably no strict alternation of flowering

and leafing years: it seems likely that flowering only takes place at intervals of

several years; one can see 50 plants in leaf for every one with an inflorescence, In

any case Amorphophallus is, I think, unique among the rain-forest herbs in having

a well-marked annual dormancy.

To return to the comparison of monocotyledons and dicotyledons, we find that

rhizomes and stolons with scale leaves are virtually restricted, in the rain-forest,

to the monocotyledons. The dicotyledons lack subterranean, or superficial, shoots

with scale leaves and diageotropic growing points. As these features are well known

amongst the dicotyledons of temperate forests, it is reasonable to suppose that they

have been developed there in response to a markedly seasonal climate. In the

monocotyledons they seem to be part of the normal developmental pattern of the

plants: their well developed scales represent only the sheaths of the mature leaf

and remind us that in the monocotyledons the sheath is a much more important

part of the leaf than it is in the dicotyledons, where it is well-developed only

sporadically in quite diverse families (Umbelliferae, Polygonaceae etc.). The

important role of the rhizome in monocotyledons is perhaps another aspect of

growth linked to their fundamentally hypogeal pattern of germination (cf. Burtt,

1972).

Many of the dicotyledonous herbs of the forest floor have small seeds; such

are all the Gesneriaceae, Begonia, some Rubiaceae and a few Acanthaceae (e.g.

Staurogyne). Such seeds are probably dispersed by rainwash or by carriage on the

feet of animals, and these two methods probably provide the best chance of

dispersal under rain-forest conditions. Small seeds may also be favoured by the

fact that they do not offer a desirable food-store to seed-predators. Salisbury’s

comparative study of seed size in relation to open and woodland habitats in

temperate Europe showed that amongst closely related species those of shady

habitats had larger seeds. Such a comparison is scarcely possible in Sarawak where

the primary vegetation of virtually the whole country is forest.

The advantages of small seeds in rain-forest, suggested above, may be enough

to outweigh the limitations imposed by the seedling having to start life with a very

small capital of food reserves. These limitations would, however, exert a selection

pressure in favour of any seedling strategy that evaded or ameliorated them, I have

suggested elsewhere (Burtt, 1970) that this is just what is achieved by the continued

post-germination growth of one cotyledon in Gesneriaceae. The enlarged photo-

synthetic surface enables the seedling to build up energy for the organization of the

plumular bud, which is delayed by comparison with its rapid appearance in most

plants. The fungal association formed by the roots of the microspermous orchids

is, Of course, another way in which this difficulty is overcome, and the same

argument may be applied to a widespread dicotyledonous saprophyte of the Malesian

rain-forest, Cotylanthera (Gentianceae). In another microspermous family of

monocotyledons, Burmanniaceae, both (fully?) autotrophic (Burmannia longi-

folia Becc.) and heterotrophic species (B. sphagnoides Becc., etc.) are found in the

forest, but here the heterotrophic association is with blue-green algae, not with

fungi.

Rain-forests herbs 77

Begonia is a microspermous genus of herbs in tropical forests all over the

world. It does not seem to have any means of offsetting this disadvantage of small

seeds: yet although Begonia plants are common, and seed-setting apparently

prolific, seedlings are in my experience (which I admit is inadequate) curiously

rare — especially as collected seed germinates freely in the greenhouse. This, of

course, is not a situation affecting Begonia alone. Seedlings of herbaceous plants

are so uncommon in the rain-forest that very little can be said about them. However

the situation is similar, but perhaps a little less pronounced, in temperate forests,

so this is not a rain-forest peculiarity. Nonetheless their rarity in the very open

vegetation of the forest floor is noteworthy and needs investigation.

To this seedling rarity there are a few exceptions. Seedlings of two genera of

Gesneriaceae are not infrequent, sometimes very prolific, in rocky forests on

limestone. These genera are Monophyllaea and Epithema, We do not know the

exact duration of the normal life cycle of these plants but it is certain that in both

genera it is relatively short. In other words seedlings occur plentifully when they

are necessary for the maintenance of the species. We are reminded that the

biennial Digitalis purpurea L. produces seedlings freely in European woodlands,

while young plants of Primula vulgaris Huds. need to be carefully sought. Similarly

in subtropical evergreen kloof forests near Durban, Natal, the short-lived mono-

carpic Streptocarpus molweniensis Hilliard (Gesneriaceae) produces myriads of

seedlings. Thus reproduction by seed seems to present similar problems for investi-

gation in forest herbs under a wide range of climatic conditions.

If there is one lesson to be learnt from the history of botany, it is surely that

attempts to give physiological explanations of leaf-structure without adequate

physiological experiment are extremely hazardous. And physiological experiments

in tropical rain-forest have so far been quite inadequate both in precision and in

the range of subject used. All I can do here is to abstract some current thought

from the physiological literature and try to relate it to the features I have seen in

rain-forest herbs. If it spurs someone to write an authoritative account I shall be

more than satisfied.

Even the physical measurements of the environment are very difficult in rain-

forest (cf. Schulz, 1960); however it seems probable that the following conditions

often obtain near the forest-floor. There is a low or very low saturation deficit; the

carbon dioxide concentration is somewhat above normal (though not as high as

was at one time suggested); average light intensities are low; and the incidence and

intensity of sun-flecks, leading to sudden rises in leaf-temperatures, are a factor

of great physiological significance (Evans, Whitmore & Wong, 1962). In this latter

connexion Evans (1972, p. 34) has emphasized the extreme complexity of leaf

temperatures, the extent of changes and their effects.

As to the plants’ behaviour under these conditions, the early hypothesis of

Stahl (1896) has now been abandoned: it was that a high transpiration rate was

necessary to permit adequate salt absorption from weak soil solutions, and he

interpreted various structural peculiarities as aiding this high transpiration rate.

It is now known, from greenhouse studies, that an increase in the CO, concentration

not only enhances assimilation, but lowers the transpiration rate (Hughes 1966;

Meidner & Mansfield 1968, p. 76). Plants on the forest floor actually have very

low transpiration rates (McLean 1919, Walter 1971): so this feature harmonizes

with the higher CO, concentrations found there.

Rain-forest herbs have typical shade-leaf histology in that they are thin and

the palisade often consists of only a single layer of shallow cells. However a more

specifically rain-forest feature is the frequent occurrence of a well-developed water-

storing hypodermis, or in its absence the epidermis itself is large-celled and aqueous

(for notes on Cyrtandra see Bokhari & Burtt, 1970). It has been shown (McLean,

1919) that development of conducting tissue in rain-forest herbs is relatively weak.

78 Gardens’ Bulletin, Singapore — XX1X (1976)

One is tempted to link water storage to the sudden effects of sun-flecks on the one

hand and poorly developed xylem on the other: but no experimental work in this

field is known to me. Nor, as far as I am aware, has the working of stomata on

raised “turrets” (common in Gesneriaceae, and see the illustration of Ruellia in

Strasburger, 1965) been studied experimentally. Until we know how they affect

transpiration when they are open, and how often they are open, speculation can

only be wild.

Leaf-surface is of considerable interest amongst rain-forest herbs. Not

infrequently the upper surface is thrown up into numerous small peaks with

corresponding hollows below; this is the condition usually described as “‘mammil-

late’. It occurs, at least, in some species of Cyrtandra and Didymocarpus

(Gesneriaceae), and Begonia (Begoniaceae), and in Tropical America species of

Pilea (Urticaceae) show the same feature. The palisade tissue is continuous over

these peaks and thus its quantity is increased within a given leaf area. Although

the direct incident light on that area remains the same, it may be that this type

of surface permits the plant to make better use of the lateral component of the

lighting. It would be interesting to compare the assimilation of smooth and

mammillate leaves when direct illumination is excluded.

Another well-known feature of certain plants growing in deep forest shade is

their blue-green iridescence. Lee & Lowry (1975) have recently returned to a study

of this phenomenon and now suggest that the iridescence is produced by a

structural layer in the wall of the epidermis which increases the reflection of light

rays in that part of the spectrum that is of least value in photosynthesis, but

enhances the penetration of the most useful wavelengths. Selaginella is probably

the commonest plant showing this iridescence, but it is also found in flowering

plants such as Begonia and is very well-marked in Mapania (Cyperaceae).

Leaf colour in forest herbs is a subject that has attracted much speculation;

but I have not found much detailed information in the literature on its occurrence.

The phenomena generally discussed are red coloration in general and red-green or

silver-green mottling; adaptive advantages have been sought for these conditions.

It is therefore worthwhile to put on record that any advantage that they do confer

on the plant has often been inadequate for them to become constant within the

species concerned. For instance, closely adjacent or mixed populations of Sonerila

tenuifolia Bl. (Melastomataceae) may be found with green or purple leaves, either

colour being with or without whitish blotches; some Begonia species occur in

colonies showing a mixture of blotched and unblotched leaves; Sonerila borneensis

Cogn. may have leaves of plants growing within a short distance of one another

silver-streaked or plain green, and the same applies in Monophyllaea glauca C.B.Cl.

var., in which silvering, when present, is more conspicuous in the seedling phase.

Similarly in Cyrtandra splendens C.B.Cl. plain green leaves, leaves mottled in darker

and lighter green, leaves flushed or wholly coloured red on the underside or leaves

red on both surfaces seem to occur indiscriminately. It is also well known that

some ‘forms’ of the species popular for greenhouse cultivation have leaves more

spectacularly coloured than others (e.g. cultivars of Episcia reptans Mart. —

Gesneriaceae — and Bertolonia — Melastomataceae). Little emphasis has been

placed on the implication of intraspecific variation when considering the possible

adaptive significance of these colour patterns. This is not to deny that they may

be adaptive, and in some species (e.g. in Dossinia marmorata Bl., or in the

light and dark green mottling of many species of Paphiopedilum, both Orchidaceae)

they do seem to be constant, But the examples of inconstancy within a species are

too frequent to be ignored.

Rain-forests herbs 79

One thing is clear in this physiological uncertainty: that the forest-floor

environment in evergreen tropical forest is far from optimal. Richards (1952,

p. 98) has emphasized this, and points to the relatively low number of families

represented in the herbaceous flora. It will have been noted how often the genera

Begonia, Cyrtandra, Didymocarpus, Argostemma, Sonerila have recurred as

examples; this is partly due to my limited experience but it does also demonstrate

that these large genera have shown parallel evolutionary diversification to cover

several successful growth-forms. There is scope for an interesting study in assessing

how many groups of genera have representatives in, or are wholly confined to,

the herbaceous flora of the rain-forests and the extent of their diversification there.

References

BELL, A. 1974. Rhizome organization in relation to vegetative spread in Medeola

virginiana. J. Arnold Arbor. 55: 458-468.

BOKHARI, M.H. & B. L. BURTT. 1970. Studies in the Gesneriaceae of the Old

World XXXII: Foliar sclereids in Cyrtandra. Notes R. bot. Gdn Edinb.

30: 11-21.

BURTT, B. L. 1970. Studies in the Gesneriaceae of the Old World, XXXI: Some

aspects of functional evolution. Notes R. bot. Gdn 30: 1-10.

1972. Plumular protection and some related aspects of seedling

behaviour. Trans. bot. Soc. Edinb. 41: 393-400.

EVANS, G. C. 1972. The quantitative analysis of plant growth. Blackwell, Oxford.

EVANS, G. C., T. C, WHITMORE & Y. K. WONG. 1962. The distribution of

light reaching the ground vegetation in a tropical rain-forest. J. Ecol.

48: 193-204.

HOLM, T. 1899. Podophyllum peltatum: a morphological study. Bot. Gaz.

27: 419-434.

HUGHES, A. P. 1966. The importance of light compared with other factors

affecting plant growth. In Bainbridge, R., Evans, G. C. & Rackham, O.

Light as an ecological factor, pp. 121-146. Blackwell, Oxford.

KIRCHNER, O. von, E. LOEW & C. SCHROTER. 1934. Lebensgeschichte der

Bliitenpflanzen Mitteleuropas 1 (3): 645.

LEE, D. W. & J. B. LOWRY. 1975. Physical basis and ecological significance of

iridescence in blue plants. Nature (Lond.) 254: 50-51.

McLEAN, R. C. 1919. Studies in the ecology of tropical rain-forest. J. Ecol

7: 5-54, 121-172.

MEIDNER, H. & T. A. MANSFIELD. 1968. Physiology of stomata. McGraw

Hill, London.

MOORE, H. J. 1962. Resia — a new genus of Gesneriaceae. Bot. Mus. Leafl. Harv.

Univ. 20: 85.

MUKERII, S. K. 1936. Contribution to the autecology of Mercurialis perennis L.

J. Ecol. 24: 36-81.

RICHARDS, P. W. 1952. The Tropical Rain Forest. University Press, Cambridge.

SCHULZ, J. P. 1960. Ecological studies on rain forest in northern Suriname.

Meded. bot. Lab. Herb. Rijks-Univ. Utrecht No. 163.

80 Gardens’ Bulletin, Singapore — XX1X (1976)

STAHL, E. 1896. Uber bunte Laubblatter, ein Beitrag zur Pflanzenbiologie. Annls

Jard, bot. Buitenzorg 13: 137-216.

STEENIS, C. G. G. J. van. 1942. Gregarious flowering of Strobilanthes

(Acanthaceae) in Malaysia. Ann, R. bot. Gdn Calcutta, 150th Anniv. vol.

pais. 7

STRASBURGER, E. 1965. Textbook of Botany. New English ed. from 28th

German ed, Trans. P. R. Bell & D. E. Coombe. Longmans, London.

WALTER, H. 1971. Ecology of Tropical and Subtropical Vegetation. Trans.

D. Mueller-Dombois. Oliver & Boyd, Edinburgh.

Comparison of the Phytomass Structure of Equatorial “Rain-Forest”

_in Central Amazonas, Brazil, and in Sarawak, Borneo

by

E. F. BRUNIG

Chair of World Forestry, University of Hamburg

H. KLINGE

Max Planck Institute of Limnology, Department of Tropical Ecology, Ploen/ Holstein

Introduction

The ombrophilous predominantly evergreen lowland forests parts of Sarawak

and Amazonia grow on very similar geologic formations, on similar soils and in a

similar climate. The one author enumerated very intensively the phytomass

structure on a 0.2 ha rectangular plot, 64 km from Manaus on the Itacoatiara road

(Klinge and Rodrigues, 1971, 1973; Fittkau and Klinge, 1973; Klinge, 1972, 1973a;

Klinge et al., 1973). The other author enumerated similarly, except without weighing

phytomass, 55 rectangular 0.2 ha plots on a wide range of sites in Sarawak and

Brunei, two 20 ha full enumerations on podzol soils on Tertiary and Quarternary

parent materials respectively and a 0.04 ha plots random sampling of 60 plots on a

Holocene terrace (Brunig, 1968, 1970, 1974). The purpose of the Amazonian project

was the analysis of phytomass structure, of the Bornean study the analysis of diver-

sity within and between stands and of the diversity/site interrelationship (Ashton

and Brunig, 1975; Brunig, 1973a, b). General information on forest types, flora, and

ecological conditions in the Amazonian area is given by Duke and Black (1953),

and by Hueck (1966), in the Bornean area by Ashton (1964), Richards (1974)

and Brunig (1975).

In this paper the term ‘Central Amazonia’ and ‘Central Amazonian rain

forest’ are used according to Fittkau (1969) who defines ‘Central Amazonia’ as

a geochemical-ecological unit which is clearly distinguished from other parts of

Amazonia.

The Sample Stands

The Amazonian plot is typical for mixed “terra firme’ forest on well drained

loamy soils (Anon., 1969). Bleached sands and podzols occur in the neighbourhood

at some distance but not in the plot area (Klinge, 1965, 1968, 1973b). Close to

the plot were short steep slopes and alluvial valley bottom which carry different

types of forest (Takeuchi, 1961).

Plots were selected from the Bornean material to represent a wide range of

site conditions and of stand structure, and also to indicate the size of within-stand

variation of essential phytomass features against which the Amazonian plot could

be assessed. The selected plots are briefly characterized in tab. 1. The plots selected

from the 20 ha sampling area in Sabal Forest Reserve have not yet been fully

analysed as they are intended for comparison with data from the San Carlos

“MAB” project area, Amazonas, Venezuela, which is being enumerated in

1975-1976.

81

d [cm]

35

30

25

20

15

@ 103

bi

7 138

Lecythidaceae

© 210

@ 212

Leguminosae coesaip,

@ 233

* 235

Leguminosae

@ 286

Moraceae

@ 323

Myrtaceae

@ 345

Palmae

a 381

Rubiaceae

a 416

Sapotaceae

@ 449

Violacece

e 490

x 491

40 hm)

Fig. 1. Diameter —

height correlation for

representatives of

plant families which

according to theif

number of species

and/or individuals are

the most important

ones in the Central

Amazonian rain forest

(acc. to Klinge &

Rodrigues). Top =

whole stance,

= enlarged for u

growth.

83

Phytomass structure, equatorial rain forests

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84 Gardens’ Bulletin, Singapore — X XIX (1976)

Forest Structure

Stratification and stand height

Our data indicate overlapping ranges of height in the various strata (tab. 2)

and consequently indistinct storey formation of diameter/height relationships. The

question whether tropical rain forest is stratified or not is controversial and views

are conflicting (Rollet, 1973; Whitmore, 1975). While geometric stratification is

often indistinct and obscure in mature stands on well-drained normal sites and

soils, addition of floristic variation and plant geometry often produces more

distinct layering in terms of overall diversity variation pattern. Distinct layering

with discernible gaps between two or more layers is common on sites with

extremes of environmental conditions or in some phases of development (Brunig,

1970, 1975; Ashton and Brunig, 1975). For Amazonian rain forest Klinge and

Rodrigues (1968), Aubréville (1961) and Soares (1957) describe the existence of

storeys in general terms but the information is not supported by quantitative

analysis. Maximum heights of 35 and 40 m are reported by Klinge and Rodrigues,

Rodrigues, and by Takeuchi, and of 25 to 30 m by Aubréville, and Soares.

The following general description of the stratification of the forest is mainly

based on our own data, amended by data of the other authors:

A-layer: a few very large trees overtowering the following

B-layer: a non-continually, vertically ill-defined upper tree layer

C,-layer: lower tree layer composed of mainly young or suppressed indivi-

duals of species which are dominant in the upper tree layer.

Occasionally, there are palm-trees.

Almost all trees of the A-, B- and C,- layers show stem-rot increasing in

severity from smaller to thicker stems.

C,- and D-layers: a rather continual, vertically illdefined upper shrub layer

with many saplings and with especially many acaulous palms.

E-layer: dominated by acaulous palms and composed predominantly of

saplings and seedlings; real herbs being scarce.

All layers are heavily interlaced by lianes, many of which have thick stems.

Vascular epiphytes are rare; there are some hemi-epiphytes, saprophytes, and

parasites. Old palm fronds and old leaves of many tree species are heavily covered

with algae and bryophytes. Crowns of the upper layer are up to 40 m wide; in the

lower layers crowns have narrower conical forms.

In comparison, Bornean forests on similar sites are taller, the A and B strata

are more complex, and generally exhibit much diversity of structural characteristics

in relation to site and phasic development.

Number of trees

The total number of trees, lianes, palms and herbs per unit area varies very

widely in tropical moist forests as a result of differences in site, in stage of phasic

development and spatial distribution pattern. In the Manaus plot the density per

ha of all trees and palms above 20 cm height is 94,000 individuals (tab. 3). This

agrees very well with the 73,000 trees and 6,000 palms recorded by Aubréville.

Both figures do not include lianes, vascular epiphytes etc. Much lower figures for

tree and palm density or total density were found by Takeuchi. Lechtaler’s figure

745 stems (dbh 8 and more cm) agrees well that of Takeuchi.

In the Bornean plots (nos. 43 to 53) the total number of trees > 2 cm d

varies between 8028 and 12,133 per ha which indicates the scale of variation in

number of trees which is of about the same order as the variation of basal area

(35.3 to 50.9 m?/ha in the selected plots, sample mean of all 55 plots 36.5 m?/ha

with a range of 27.0 to 88.0 m?2/ha).

Phytomass structure, equatorial rain forests 85

Table 2. Stratification of the Central Amazonian rain forest on level terra firme acc. to

Klinge & Rodrigues (plot size 0.2 ha)

Lower crown height

| Upper crown height

(m)

(m)

Stratum | Individuals

ivy botkier ofl H.tisive bon per ha

Mean Range | Mean Range

A 35.40 38.10 — 32.10 | 23.70 29.00 — 20.00 50

B 25.90 30.50 — 20.40 | 16.70 24.60 — 8.70 315

=. 14.50 21.90 — 10.05 | 8.40 8.70 — 2.70 775

ee 5.90 11.00 — 2.70 3.60 7.80 — 0.70 2,920

D 3.00 4.50 — 1.55 1.70 2.90 — 0.20 6,070

E 1.00 1.50 — 0.20 | 0.10 0.20 — 0.05 83,650

93,780

Bole diameters

Height/breast-height diameter (h/d) ratios vary with species, site and age.

Emergent trees frequently have ratios between 25 and 50, trees in the B-layer about

50 and trees in the lower canopy between 60 and above 100. Ratios vary strongly

even within one species in a stand and even more between species often obscuring

any existing tendency to layer formation.

Fig. 1 shows the relationship between total height and d for 14 plant families

which according to numbers of species and/or individuals are the most important

in the Manaus plot. The wide scatter in the taller strata is typical and agrees with

observations in the Sarawak plots (Brunig, 1975, fig. 11d).

Table 3. Plant density per height class and ha in the terra firme rain forest of Central

Amazonian acc. to Aubréville (plot size 500 m2 (1) and 175 m2 (2), respectively)

| | | 2

Height class |

(m) |

| Trees Palms ! Trees Palms

ae ia |

> 15 | 340 60 | 514 0

po. . 0S 300 20 | 629 57

>? 2,940 1,560 | 3,714 1,143

/ |

Pach BE | 3,580 1,640 | 4,857 1,200

x1 | ? ? | 68,229 5,029

pak

|

Total — — 73,086 6,229

Linas >I mi. 880 | 1,254

simi, ? | 7,467

Herbs <Imh_. v4 / 6,327

|

!

Total | eas | 94.363

86 Gardens’ Bulletin, Singapore — X XIX (1976)

The ecological significance of stand curves (tree frequency distributions over

d) in tropical forests has been recently reviewed by Rollet (1973). The shape of

the stand curves is subject to many environmental influences and to intrinsic

properties of the stand; variation between stands and sites, and within stands with

time, is correspondingly large (Ashton and Brunig, 1975; Brunig, 1975). The

Manaus plot shows a strongly truncated distribution, the largest diameter being

only 55 cm, compared with a site related range of 50 to 100 cm in the 5 Bornean

plots.

Phytomass

The phytomass data from the Manaus plot are the only available precise

figures for the Amazonian lowland forest. The data are summarized in tab. 4. The

Table 4. Fresh phytomass of the Central Amazonian rain forest acc, Klinge & Rodrigues

(size of study plot 0.2 ha)

Fraction Phytomass (t/ha)

Trees and palms, A 190.2

— above ground B 399.5

Cc. 77.2

C, 15.7

D 4.7

E 1.5

— below ground 255

Lianes, epiphytes, etc. 89

Total | 1,033

corresponding volume of tree boles in m3/ha is 385 > 15 cm d and 304

> 25 cm d. These volumes and the corresponding fresh phytomass lie within the

range of data reported by authors (tab. 5) and by the data of the FAO inventories

south of the Amazon River. Compared with other tropical moist forests, the

amount of stem volume and, consequently, of stem wood volume is rather low in

the Central Amazonian rain forest. However, the terra firme forest of the Manaus

area is not the most luxurious forest in Amazonia (Rodrigues, 1967). The total tree

Table 5. Fresh phytomass of the Central Amazonian rain forest stands calculated under

the assumption of a phytomass content equal to that in the Manaus plot.

Fresh phytomass

Authors (t/ha) Remarks

Soares 360 Average of 2 surveys of 9 and 36 ha

respectively .

Rodrigues 413 Average of 27 ha

Aubréville 510 Average of 2 surveys of 500 and 175 m2

respectively

Lechthaler 1,000 1 survey of | ha

Klinge-Rodrigues 1,000 1 survey of 0.2 ha

Takeuchi 1,350 0.16 ha section of 3 surveys comprising

0.185 ha

tne

Mean 770

Phytomass structure, equatorial rain forests 87

volumes above ground estimated as V = G - 0.5 h (where G = basal area

per diameter class, h = height of the diameter class) in the 55 sample plots in

Borneo range between 195 and 1760 m3/ha. Determining factors are again site,

developmental phase and the presence or absence of gregarious species which

successfully reduce competitors on certain, often extreme and difficult sites. The

mean value is 778 m3/ha (mean basal area 36.5 m*/ha of trees above 2 cm d).

The fresh weight of phytomass is of the same order in t/ha as the volume

estimator in m3/ha, and varies in the same range. The tree volumes naturally vary

not only in relation to natural factors, but also to the size and shape of the plots.

Variation increases as the size of the sample plots decreases, and deviations are

less for transects than for squares.

Maximum and minimum figures for total above-ground phytomass of living

trees and palms in layers A-D were calculated for sub-plot sections which vary in

size and shape (fig. 2). These figures indicate that sampling the phytomass distribu-

tion of an area by transects apparently gives a better representation than by blocks.

It can also be seen that the curves for maximum and minimum phytomass figures

are not symmetrical.

Fresh phytomass

(metric t/ha)

@ square plots

© fectangular transects

1,000

500

Extent

of study plot

0" 400 400 500 900 1,600 2,000

Fig. 2. Maximum (upper curve) and minimum figures (lower curve) for fresh phytomass

of layers A—D, calculated for square blocks and rectangular transects of different

extent within the 0.2 ha plot of Klinge & Rodrigues, in the Central Amazonian rain

forest.

Assuming the above-ground living phytomass in layers A-D to be 68.7 % of

the total living above-ground phytomass, the total living above-ground phytomass

reported by Aubréville (0.05 ha plot) as 350 t/ha is less than the figure of 415

t/ha which we obtain in a corresponding transect. Takeuchi’s 0.16 ha transect

would include 927 t/ha which is more than the 710 t/ha we get in the Manaus

plot for a square block of equal area. The figures of Lechthaler and Klinge &

Rodrigues are identical despite the fact that Lechthaler’s plot is 5 times larger

than Klinge & Rodrigues’ plot. Very low figures are obtained for the data of

Rodrigues (27 transects of 1 ha each), and of Soares (9 and 36 transects, respecti-

vely, of 1 ha each): 284 t/ha for Rodrigues’ plot, and 247 t/ha for Soares study.

88 Gardens’ Bulletin, Singapore — X XIX (1976) |

Number h >150em,d > Tem

of species

500

0,1 0,5 area 1,0 ha

d incm

> 25

735

756

300

>15

100

Oj 9 27 36

area in ha

Fig. 3. Species number as a function of diameter class, size and shape of study plots in

the Central Amazonian rain forest.

Upper part: plots up to | ha in size.

Lower part: plots up to 36 ha in size.

89

Phytomass structure, equatorial rain forests

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90 Gardens’ Bulletin, Singapore — X XIX (1976)

These low figures are possibly caused by site heterogeneity, The 5,000 m long

transects of both authors in addition to latosol also included groundwater-

influenced valley soils, bleached white sands and podzols, and flanks of valleys.

Floristic structure

Sample plots contain architectural and floristic variation of small-scale (tree

groups in the order of 0.1 ha) and medium-scale (stands of 1 to several ha)

(Brunig, 1975; Ashton and Brunig, 1975). Accordingly, in addition to the wide

variation in architectural features (basal area, height, layering, diameter, frequency),

there is considerable floristic variation (species complement and species dominance

pattern, species for a number of reasons often occurring vicariously) between plots

which is governed by chance the more the smaller the plot size. As a result, family,

generic and species dominance figures for small plots are only meaningful if they

are supported by data from larger-scale sampling of the wider surrounds on the

same site types (Brunig, 1973). However, some features of floristic structure are

somewhat more general and more consistent even in small plots, such as species-

area and species-dominance curves.

In the Manaus plot the 5 leading plant families Moraceae, Lauraceae,

Leguminosae, Lecythidaceae and Sapotaceae on an average represent 50 to 60 %

of all species, and 50 — 70 % of all individuals. Leguminosae and Lecythidaceae

strongly exceed Lauraceae, Moraceae and Sapotaceae. The other authors for the

reasons given above report different proportions and family dominances, e.g. in

Takeuchi’s survey the Guttiferae are conspicuous, the Olacaceae in Lechthaler’s

plot and Olacaceae and Euphorbiaceae in Rodrigues’ survey.

Generally in Central Amazonia, second in number of species and/or indivi-

duals are the Apocynaceae, Annonaceae, Rosaceae (Chrysobalanaceae), Bur-

seraceae, Euphorbiaceae, Myrtaceae, Olacaceae, Celastraceae, Humiriaceae, and

Myristicaceae. These 10 plant families on an average represent 20 — 40 % of the

number of species and 20 — 50 % of the individuals.

The group of rare plant families is the Guttiferae, Caryocaraceae, and

Bombacaceae, and 40 plant families are very rare.

Palms as a family are generally well represented. The acaulous species belong

to the lower strata of the forest and are included only when the survey includes

small sizes. A few palm species are cauliferous and intrude the middle forest

layers; their heights may measure up to about 15 m.

The Central Amazonian rain forest is composed of about 55 families and

about 500 more common tree species (fig. 3). Rare species or families increase these

figures for more extensive areas. Despite this high number of species and plant

families, the Central Amazonian rain forest is poorer in species and less diverse

than the Bornean Mixed Dipterocarp forest in Sarawak (Brunig, 1973a).

Including small palms and woody species of low habit, herbs of the ground

vegetation, and epiphytes, the total number of plant families in the Central

Amazonian rain forest is supposed to be about 70, and its number of species

about 700. There is no information on the number of cryptogam and vascular

cryptogam species and families. The latter group is not well represented, but the

cryptogams are very numerous, especially in the phyllosphere.

We used data of the other authors for the construction of various species-area

curves. The curves for the girth classes of 25, 35, and 56 cm rise steeply and

smoothly (lower part of fig. 3). The curve for the next lower girth class (15 and

more cm) is in its lower part above the curve of the 25 cm dbh class and its

inclination is stronger. The curves for area below 1 ha are reproduced at larger

scale in the upper part of fig. 3 which also includes the curve for dbh of 8 cm

Phytomass structure, equatorial rain forests 91

or 10 cm. It also includes >1 cm d or >150 cm h, which increase extremely

rapidly to 0.2 ha and then flattens. It eventually would cross the curves for girth

classes 25, 36 and 56 cm at plot sizes of 30 — 35 ha and species numbers of

about 500. This agrees with the contention of Brunig (1968 and 1973a) that small

plots cover the total species population satisfactorily, if very low diameter limits

below or of 1 cm are adopted. Larger minimum sampling sizes require very much

larger plot sizes if the less common and rare species should be adequately sampled.

A diameter limit of 25 cm requires plot sizes of 30 and more ha. Intermediate

diameter limits between 10 or 15 cm require about 15 to 20 ha, provided the

forest and site are reasonably uniform.

In the same sections of our 40 x 50 m plot, previously used for maximum and

minimum phytomass calculations, maximum and minimum numbers of species

were counted (tab. 6 and fig. 4). Differences between maximum and minimum

species numbers are much smaller than the differences between maximum and

minimum phytomass. The number of species is somewhat larger in transects than

in blocks of similar size.

n Species

5

e square plots

© rectangular transects

3

Extent

of study plot

0 100 400 500 900 1,600 2,000

Fig. 4. Species number as a function of plot size in the Central Amazonian rain forest acc.

to Klinge & Rodrigues.

Upper curve: maximum figures for species number.

Lower curve: minimum figures for species number.

The shape of species-areas curve is strongly influenced by site heterogeneity.

In the Sabal sampling area, Sarawak, the increase of species number with transect

length (20 x 500 m) is first steeper but then flatter in more xeric, oligotrophic and

relatively homogeneous parts with tendency to single-species dominance (transect

pairs 251-275 and 276-300 in fig. 5). It is first flatter but continues to rise steeper

On more heterogeneous medium sites (1-25, 26/50), but again similar

to the first pair on transitions to red latosols where again one species attains strong

dominance (Dryobalanops beccarii Dyer). This is discussed in detail in an earlier

paper (Brunig, 1973a).

Floristic and phytomass structure

The floristic and phytomass structure of a stand can simultaneously be

expressed by the species-dominance curve. The curve for this purpose represents

the contribution of each species to the stand basal area. The species are plotted

in order of their contribution in percent of the stand total. The starting point of

each curve is chosen arbitrarily so that crossing of the curves is avoided. One

advantage of the species-dominance curve for putposes of comparison is that its

significance is independent of the chances of species presence which is useful for

small plots in floristically heteregeneous, diverse stands. The species-dominance

92 Gardens’ Bulletin, Singapore — XX1X (1976)

curves of a number of plots in different forest types in Sarawak (incl. sample plot

43) is shown in fig. 6. The stands are arranged in order of improving site and soil

conditions from the left (SP 40, Dacrydium pectinatum Delaubenf. bearing

Kerangas on peat bog) to the right (SP 16, Dryobalanops beccarii bearing Mixed

Dipterocarp forest). The dominance of the leading species is strong to the left

(Shorea albida Sym, in SP 27 and Agathis dammara (Lamb.) L. C. Rich. in SP

43) and weak to the left. Increasing flatness indicates that the mutual exclusion

principle weakens and random distribution of ecological niches prevails. The

species-dominance curve of the Manaus plot shows by comparison the least degree

of species dominance and the flattest trend of the curve. This means that distribu-

tion is largely governed by chance and more so than in the Bornean plots. This

result cannot, however, be generalized because the Bornean plots, including SP

16, are on less favourable soils than the terra firme plot at Manaus.

Figures for both phytomass and species numbers in sections of different size

and shape of the original 40 x 50 m plot were calculated separately for each layer

as percentages of the figures for the total plot (fig. 7 — blocks; fig. 8 — transects).

The minimum figures for phytomass and the corresponding numbers of species are

shown in the upper part of both figures and the corresponding maxima and species

numbers in the lower part. Figs 7 and 8 indicate that the lower forest layers

represent a low proportion only of the phytomass, but a very large proportion of

the total number of species. Therefore, the overall distribution of species within

the plot is much more homogenous than the distribution of the phytomass. This

observation agrees with the finding of Webb ef al. (1972) in the subtropical forest

of eastern Australia.

n species

Species- Area Curve

Sabal pm cai

yr 1-25

476-500

100 —

—_— 5

Yj | aa oe 276 -300

P< o

y

//

0 5 10 15 20 25

Number of chain-squares

150

50

Fig. 5, Species-area lines for pairs of transects, each 20 x 500 m, in the Sabal sampling

area, Sarawak. For plot description see tab. 1.

93

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Phytomass structure

SLOId JIdGNVS S NI SSAYND ALISYSAIC - JONVNINOG

94 Gardens’ Bulletin, Singapore — X XIX (1976)

The inverse importance by phytomass and by number of species of the

various size classes or stand strata is general for tropical moist forests. Fig. 9

shows the same relationship for SP 43 as an example of a stand in which a single

species attains extreme dominance, and fig. 10 for SP 53 with a more balanced

floristic structure. The two samples again demonstrate the wide variation of

structural parameters which exists in tropical moist forests. This is supported by the

summaries of the cumulative species/size class and cumulative biomass/size class

%

100

pe

ss A

oO e A

eee species ;

2a

oO

50

biomass ~~

aD oe “"B

eee ee ———

0 DO NG ae B A

e square blocks, 40 x 40 m a 4 square blocks, 30 x 30 m © + square blocks, 10 x 10 m

re

biomass

D C5 Cy B A

Fig. 7. Increase of species number and phytomass of layers A-D in square blocks of different

size, as per cent of the totals in the 40 x 50 m plot of Klinge & Rodrigues. The

curves delimit the variability range of the figures.

Above: minimum figures of phytomass and corresponding species numbers, and

minimum species number and corresponding phytomass.

Below: maximum figures of phytomass and corresponding figures of species number,

and maximum species number and corresponding phytomass.

Phytomass structure, equatorial rain forests 95

curves for the 5 selected Bornean sample stands (fig. 11 and 12). These examples

show clearly that efficient biomass sampling can be done with a relatively large

minimum diameter limit which may be as high as 20 cm in stands such as in

SP 43 or 10 cm in SP 53. But efficient sampling of species composition would

require much lower minimum diameter limits close to zero. It was for this reason,

that such low limits were chosen in the sampling of the 55 plots in Borneo which

in fact covered an estimated 90.3 % of the species which are present in the associa-

tion group of Kerangas and Kerapah forests (Brunig, 1973a, 1975).

%

100

a en gn

exo

50

fet 3

D C5 C, 8 A

——_———————

De

= x rectangular transects, 40 x 10m @ 0 rectangular transects, 10 x 50 m

%

10 0 ——————— noe

See oe ae

n Species e

°

g

8

Biomass

Sa iis et

D Co C, 8 A

Fig. 8. Increase of species number and phytomass of layers A-D in rectangular transects of

different size and direction, as percent of the totals in the 40 x 50 m plot of Klinge

& Rodrigues.

The curves delimit the variability range of the figures.

Above: minimum figures of phytomass and corresponding species number, and

minimum species number and corresponding phytomass figures.

Below: maximum phytomass figures and corresponding species number, and maximum

species number and corresponding phytomass figures.

96 Gardens’ Bulletin, Singapore — X XIX (1976)

Table 7. Percentages of plant families on total numbers of species and individuals in

the Central Amazonian rain forest acc. to Klinge & Rodrigues (dbh 15 and more cm)

Lechthaler (dbh 16 and more cm), and Soares (dbh 15 and more cm) :

Klinge & Rodrigues Lechthaler Soares(2)

3

Plant families (3)

0.2 ha 1 ha 9 ha.

Moraceae l.

Lauraceae l.

Leguminosae 20.

Lecythidaceae S.

Sapotaceae yA

(6.5) 0.7 (17)

(27.4) 14 (11.2)

(11.6) 2.1 (9.4)

2 ee

———————

lst Subtotal 54.6 (44.3) 60.7 (69.7) 4.3 (22.3)

Apocynaceae 3.6 5.4 ae

Annonaceae 1.8 3.6 1.9

Celastraceae 1.8 (1.4) 1.8 es M fi Cs

Euphorbiaceae 10.9 1.8 ae

Olacaceae 3.6 3.6 (4.7) o

2nd Subtotal 21.8 (31.4) 161° AN 0.7 (1.9)

Anacardiaceae

Burseraceae

Combretaceae

Cucurbitaceae

Flacourtiaceae

Guttiferae

Myristicaceae

Rosaceae

Rubiaceae

Sapindaceae

Simaroubaceae

3.6 (8.4) 0.7 (7.7)

RA

0.7 (2.4)

1.8 (2.3)

x KKKXKXKXXKXXK X

Vochysiaceae

Violaceae

Humiriaceae

Icacinaceae

Myristicaceae

Caryocaraceae

Nyctaginaceae

Myrtaceae

Bombacaceae

(5.7)

(4.3)

(2.9)

WW I

N WW

Reese

a Rba2e

| xxxxXx

3rd Subtotal 23.6 (24.3)

|

N

\o

=

oo

SL

Total

n families 18 21 11

N species 55 56 140

n individuals 70 215 2250

Palmae

species l

individuals 1 ; ‘

*

Phytomass structure, equatorial rain forests 97

Plot 43

Fig 9 Sample Plo % Fig. 10 Sample Plot 53

Species Species

Biomass

oe] 1 2 3 4 5 6 7 8

10cm diameter Class

10 diameter class

Fig. 9. Cumulative relative species number and phytomass (biomass) with increasing diameter

class in an Agathis dammara bearing Kerangas forest on Deep Humus Podzol, SP.

43, Sarawak,

Fig. 10. Cumulative relative species number and phytomass (biomass) with increasing

diameter class in a mixed Kerangas forest on Grey-White Podzolic clay soil, SP. 53,

Sarawak.

"lg # BIOMASS

Fig 12 Sample Plot 43,44,51,52,53

Fig. 11 Sample Plot 43,44,51,52,53

10-cm diameter class

10cm diameter class

Fig. 11. Cumulative relative species number with increasing diameter class in 5 selected

sample plots, 0.2 ha each, in Sarawak.

Fig. 12. Cumulative relative phytomass (biomass) with increasing diameter class in 5 selected

sample plots, 0.2 ha each, in Sarawak.

The variation of phytomass between 5 square 20 x 20 m subplots in the two

sample plots SP 43 and SP 53 is illustrated in fig. 13 and fig. 14. The figures show

Clearly the common feature: variation is much smaller in the lower size classes

than in the larger size classes, but variation in the single-dominant stand

(SP 43) is again less in the dominant emergent layer (71-80 cm d). It is interesting

that the latter feature disappears again in the course of phasic development along

a time-related ecological gradient which culminates in sample plot 44 (fig. 15).

The strong dominance of A gathis dammara has weakened. The top canopy is more

mixed, the stand structure more diverse and the stocking more variable between

subplots. Obviously, such features have important significance not only for biomass

and species sampling, but also for the structure and functioning of the ecosystem

as a whole (Brunig, 1970, 1973b).

Conclusion

Available information on the Central Amazonian and Bornean rain forest

permits the conclusion that relatively small plot sizes, such as the 40 x 50 m and

20 x 100 m plots we used, have advantages for sampling both species composition

and its phytomass. The small size is time and labour saving and cost-benefit

efficient. Very large plots are proportionally costly and time consuming, and

require an inordinate amount of facilities and organization because of the enormous

BASAL AREA PER SQUARE AND

OIAMETER CLASS

G inm2

S$P.63

G inm? BASAL AREA PER SQUARE AND

DIAMETER CLASS

SP. 43

$a. 6

4

3

2

1

; 1SQ = 404.7 m?

1 SQ = 404.7m2

15

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ne OO} (3 Cy

SLA LX J is all

O-6 6-10 11-20 21-30 31-40 41-50 51-60 «81-70 71-80 oe, 6 oe Os 8 68 ee ee

Fig. 13. Basal area in m2 in each of the 5 Fig. 14. Basal area in m2? in each of the

subplots (1 sq. ch.) of sample plot 5 subplots (1 sq. ch.) of sample

SP. 43, Sarawak. plot SP. 53, Sarawak.

G in m2

BASAL AREA PER SQUARE AND

DIAMETER CLASS

2.5 SP. 44

Fig. 15. Basal area in m2 in each of the

5 sub-plots (1 sq. ch.) of

sample plot SP. 44, Sarawak.

The plot follows in a succes-

1 SQ = 404.7 m2

1,5 sion-related catena on SP. 43.

The X — axis denotes diameter

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Phytomass structure, equatorial rain forests 99

number of individuals and the greater number of species especially if site and

forests are not homogeneous. However, if emphasis is on the rare or very rare

species, plot sizes must be very large and diameter limits low. If only the forest

phytomass is studied, small plots are adequate, especially with respect to the lower

layers of the stand, and minimum diameter limits can be larger. The smaller

material can be conveniently subsampled without much loss of precision.

Our conclusion is in agreement with Lang et al. (1971) who studied tropical

forest at Barro Colorado, Panama, and found that almost a 100 % sample is

needed if the objective is to sample the rare species with high precision. The more

common species are however adequately documented even if the sample comprises

only a tiny portion of the total area. The examples from Borneo also confirm our

earlier contention and Ashton’s (1964a) opinion that between-stand diversity and

site diversity limit the useful size of vegetation sampling plots to around 0.2 to 0.5

ha if within-plot homogeneity is desired. Expansion of plots beyond this size introdu-

ces excessive heterogeneity by including different site and stand conditions. The

variation of biomass parameters is of such magnitude and its pattern so complex

that sampling of stand biomass and other structural stand features in natural

virgin tropical rainforest must be done:

by using small area plots if biomass is to be measured directly

by rigorously stratifying the sampling design according to site conditions,

phasic development and species composition

——— by supplementing the biomass sampling in intensively studied plots by a

survey of the wider plot surround with respect to the variations of biomass-

related parameters such as basal area, stand height, tree shape, tree density,

tree frequencies per diameter class and species composition.

Unless these conditions are met, the results of studying small biomass

sampling plots, as of other types of yield observation plots, will produce meaning-

less, because uncoordinated, information.

Acknowledgments

Thanks are due to W. A. Rodrigues, Botany Department, Instituto Nacional

de Pesquisas da Amazonia, Manaus, Amazonas, Brazil, who made some of his

staff available for the fieldwork from June to November 1970, and who also helped

in many other ways.

The Amazonian data have been obtained through cooperation between the

INPA, Manaus, and the Department of Tropical Ecology, M.P.I., Ploen. The

Bornean data have been processed with financial assistance from the German

Research Foundation. (DFG).

Literature

ANON. 1969. Os solos da area Manaus — Itacoariara. IPEAN, Série Estudos e

Ensaios 1, Manaus, 116 pp.

ASHTON, P. S. 1964a. A quantitative phytosociological technique applied to

tropical mixed rainforest. Malay. Forester 27 (3): 304-317.

1964b. Ecological studies in the Mixed Dipterocarp Forest of

Brunei State. Oxford Forestry Memoir 25, Oxford.

— and BRUNIG, E. F. 1975. The variation of tropical moist forests in

relation to environmental factors as key to ecologically oriented land-use

planning. Mitt. BundForsch-Inst. Forst-u. Holzw. 109: 59-86.

100 Gardens’ Bulletin, Singapore — XX1X (1976)

AUBREVILLE, A. 1961. Etude écologique des principales formations végétales

du Brésil et contribution 4 la connaissance des foréts de l’Amazonie brési-

lienne. Centre Technique Forestier Tropical, Nogent-sur-Marne, 268 pp.

BRUNIG, E. F. 1968a. Some observations on the status of heath forests in

Sarawak and Brunei. Proceedings, Symp. on Recent Advances in Tropical

Ecology, Varanasi, 1967. Int. Soc. Trop. Ecol., Varanasi: 451-457.

1968b. Der Heidewald von Sarawak und Brunei. Mitt. Bund.

Forsch-Anst. Forst- u. Holzw. Nr. 68, Bd. I u. If, 431 pp.

1970. Stand structure, physiognomy and environmental factors in

some lowland forests in Sarawak. Trop. Ecol. 11 (1) 26-43.

1973a. Species richness and stand diversity in relation to site and

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293-320.

1973b. Biomass diversity and biomass sampling in tropical rain

forest. In: IUFRO Biomass studies, Univ. Maine, Orono.

1975. Ecological studies in the Kerangas forests of Sarawak and

Brunei. Borneo Lit. Bureau, Govt. Printer, Kuching (in press).

DUCKE, A., and BLACK, G. A. 1953. Phytogeographical notes on the Brazilian

Amazon. Anais Acad. Bras. Ciénc. 25: 1-46.

FITTKAU, E. J. 1969. The fauna of South America. In: E. J. Fittkau, J. Illies,

H. Klinge, G. H. Schwabe, and H. Sioli (Editors): Biogeography and Ecology

in South America, Junk, The Hague. Vol. II: 624-658.

FITTKAU, E. J., and KLINGE, H. 1973. On biomass and tropic structure of

the Central Amazonian rain forest ecosystem. Biotropica 5 (2): 2-14.

HUECK, K. 1966. Die Walder Siidamerikas. Fischer, Jena, 422 pp.

KLINGE, H. 1965. Podzol soils in the Amazon basin. J. Soil Sci. 16 (1): 95-103.

1968. Report on tropical podzols, 1st draft. F.A.O. Rome, 88 pp.

1972. Biomasa y materia organica del suelo en el ecosistema de la

pluviselva centro-amazonica. Acta cient. Venez. 24: 174-181.

1973a. Struktur und Artenreichtum dez zentralamazonischen

Regenwaldes. Amazoniana 4 (3): 283-292.

1973b. Root mass estimation in lowland tropical rain forests of

Central Amazonia, Brasil. I, Trop. Ecol. 14: 29-38; II. Anais Acad. bras.

cienc. (1975, in press).

KLINGE, H., and FITTKAU, E. J. 1972. Filterfunktionen im Okosystem des

zentralamazonischen Regenwaldes. Mitt. deutsch. bodenk. Ges., Gottingen.

16: 130-135.

KLINGE, H., and RODRIGUES, W. A. 1968. Litter production in an area of

Amazonian terra firme forest. Part I, Litter-fall, organic carbon and total

nitrogen contents of litter. Amazoniana 1 (4): 287-302.

1971. Matéria organica e nutrientes na mata de terra firme perto de

Manaus. Acta amazon., Manaus 1 (1): 69-72.

1973. Biomass estimation in a Central Amazonian rain forest.

IUFRO Biomass studies, Univ, Maine, Orono.

Phytomass structure, equatorial rain forests 101

KLINGE, H., RODRIGUES, W. A. BRUNIG, E. F., and FITTKAU, E. J.

1973. Biomass and structure in a Central Amazonian rain forest. In: Ecological

Studies, II. Tropical Ecological Systems. Springer, New York & Berlin.

LANG, G. E., KNIGHT, D. H., and ANDERSON, D. A. 1971. Sampling the density

of tree species with quadrats in a species-rich tropical forest. Forest Sci.

17: 395-400.

LECHTHALER, R. 1956. Inventario das arvores de um hectare de terra firme

da zona Reserva Florestal Ducke, Municipio de Manaus. Inst. Bras. Biblio-

grafia e Documentacdo, Rio de Jan. Botanica, Publ. 3, 7 pp.

RICHARDS, P. W. 1974. The tropical rain forest. 5th Ed. Cambridge Univ. Press.

RODRIGUES, W. A. 1967. Inventario florestal pil6to ao longo da estrada Manaus

— Itacoatiara, Estado do Amazonas: Dados preliminares. Atas Simpdsio

sdbre a Biota Amaz6énica, Belém 1966, 7: 257-267.

ROLLET, B. 1973. L’architecture des foréts denses humides sempervirentes de

plaine. Centre Techn. For. Trop., Nogent sur Marne, 298 pp.

SOARES, R. O. 1957. Inventario florestal Reserva Florestal Ducke. Relatorio.

Mimeogr., 26 pp.

TAKEUCHI, M. 1961. The structure of the Amazonian vegetation. II. Tropical

rain forest. J. Fac. Sci. Tokyo Univ. Sect. 3, Bot., 8 (1/3): 1-26.

WEBB, L. J., TRACEY, J. G. and WILLIAMS, W. T. 1972. Regeneration and

pattern in the subtropical rain forest. J. Ecol. 60 (3): 675-695.

WHITMORE, T. C. 1975. Tropical rain forests of the Far East. Clarendon Press,

Oxford, 282 pp.

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Autonomous Evolution in Plants

Differences in plant and animal evolution

by

C.G.G.J. VAN STEENIS

Rijksherbarium Leiden

CONTENTS

Page

Summary - - - - - - : - - 103

1. Introduction . - - - - - - - - 104

2. Survival level and patio ludens - - . - - - : 107

Anatomical features and structural fitness of Gymnosperms - - 109

3. Pre-adaptations in plants - - - . . - - 111

4. Early differentiation - - - - - - - - 112

5. Saltatory evolution in plants - . - - - - - 113

6. Gliding evolution in animals - - - - - - - 117

7. Co-evolution of animals and plants” - - - - - - 119

Evolution of orchids - - . - : - : - 121

Evolution of figs’ - - - - - - - - 122

8. Reticulate phylogeny - - - : - - - - 123

9. Embryology and ontogeny” - - - - - - - 124

References - - - - - - . - - 125

Summary

It is argued that after ’decisions’ were made in the early stages about the basic matrix of

plant life later evolution followed in an autonomous way, not as a consequence of the

competition /selection principle.

Evolution of plants is characterized by their passive tolerance and lack of active aggres-

sion. Their main struggle is to evolve against the environment; mutual competition is no

agency for their evolution. Animal evolution has, besides this same struggle, a second

impetus by competition.

_ Under this dual pressure animal evolution is proceeding more rapidly and form-making

is more abundant, and has led to more complicated specialized structural and behavioural

development than in plants because of sexual selection, which is absent in plants.

_ Competition and survival of plants is more passive and mainly directed against the

inanimate environment. This tolerance led to a slower and conservative evolution.

The survival level, which tops all requirements necessary for survival for a certain place

and time, lies much lower in plants than in animals and allows for plants a greater free

space (‘patio ludens’) for structural development of non-adaptive characters, which fall beyond

competition, selection, and adaptation. This free space in animal development is generally

considered to be very narrow.

So-called ‘pre-adaptations’ in plants have not come into existence because of competition

pressure, and is a misleading term in evolutionary sense.

In early differentiation structural decisions for later phyla may well have been made by

chance, or these characters may have had in those early stages a lower ‘genetical weight’

than they got during later establishment.

In ‘plants, the usual way of evolving evolutionary development is through sudden

(saltatory) change which is amongst others proved by preponderance of allopolyploid and

aneuploid chromosome numbers.

This saltatory evolution proceeded through a small number of specimens.

103

104 Gardens’ Bulletin, Singapore — XX1X (1976)

Saltatory development may also have occurred through sudden change of a few genes

which physiologically upset pathways to morphogenesis, partly through neoteny, and gave

rise to systematical teratologies, and thus to creation of isolated taxa.

Racial segregation may have led to new species but in plants only in exceptional cases

(in long isolation): the term micro-evolution used for this development should be abandoned

for plants.

It seems not possible as yet to translate structural changes in genetical terms and define

the constancy in genetical weight of genome structure, though there must be a considerable

genetical difference between characters common to phyla and those common to families,

genera and species. It is peculiar that by a sudden saltation of a ‘physiological gene’ a very

constant structure may be upset, for example by a peloric form in an orchid.

In animals on the other hand ‘gliding evolution’ by gradual accumulation seems to be

the usual way of development. This is attributed to competition and sexual selection, and

it goes by populations, through convivia, commiscua and comparia.

Mutations irrelevant to divergent survival may be possible but they will play a minor

role, as patio ludens is for animals a very narrow measure. Saltations, if they occur, must

be quite exceptional.

Co-evolution of plants and animals is usually a one-sided affair, in which changes in plant

structure occur first, and adaptation by animals follows. Except for negligible exceptions

plant evolution goes independent of animal evolution in an autonomous way; novelties

arising in plants are exploited by animals for their evolution and specialization.

This does not exclude that in a restricted number of cases plants got into a situation

where animal action became a vital factor for their survival, as in orchids and figs. In these

cases animal populations have forced their way of gliding evolution on that of plants, but

even in these cases changes of plant structure do not arise perforce of competition among the

plants themselves. their changes remain autonomous, it is the animals which adapt themselves.

It is argued that, whereas in the gliding, divergent evolution of animals there will be

hardly any chance of reticulate phylogeny, though their will be of course reticulate affinity.

In plants, however, it has been shown that reticulate phylogeny has played an important

role in their evolution.

Finally attention is given to the basic difference between animals and plants in their

embryological and ontogenetical development which must have had essential implications

for their evolution.

1. Introduction

It is, I believe, generally accepted that evolution in plants and animals is

caused by similar impulses and that its mechanism(s) has been the same for both.

It should be remarked that this holistic principle is philosophically an extremely

attractive axiom. It should, however, also be remarked that the development of

evolutionary theory has largely been in the hands of zoologists and zoo-palaeon-

tologists. They had of course no reason to check whether the axiom is fully valid

for plants or whether there are differences, either in degree or in quality.

From the side of botanists there have been, as far as I can remember,

remarkable few queries about the validity of the holistic axiom. And those I know

of concern only the proportional speed of evolution.

J. D. Hooker (1859: xii, footnote) pointed to the marked contrast of the

showy, vivid differentiation of the fauna as compared with the conservative, rather

monotonous development of the plant kingdom, writing: “the much narrower

delimitation in area of animals than plants, and greater restriction of Faunas than

Floras, should lead us to anticipate that plant types are, geologically speaking,

more ancient and permanent than the higher animal types are, and so I believe

them to be, and I would extend the doctrine even to plants of highly complex

structure’. The idea that changes in the development of the Angiosperms have

been extremely slow was also stressed by Hamshaw Thomas (1961: 3).

It appears in fact, that certain types of life, especially among the bacteria and

algae, have persisted over immense periods, some two, or at least one and a half

billion years, before showing further evolutionary development.

Autonomous Evolution 105

It is true that this observation relates only to the quantative aspect, the speed

of evolutionary progress, but it leads nevertheless to consider the qualitative

aspect, even if this would mean a re-appraisal of the holistic principle.

Therefore we have to consider the mechanism(s) of evolution gradually

developed through the ideas of Buffon c.s., Lamarck, Hutton, Malthus, Lyell, and

finally synthesized by Darwin & Wallace, by whom the gradually grown idea of

adaptation was more closely defined as adaptation caused by selection on the basis

of competition, more popularly explained as survival of the fittest.

Competition, resulting in selection, must of course have been a powerful agent

through the history of life. It is supposed to have been already present on the

abiotic level. Probably already at this stage was it effective, with the understanding

that ‘decisions’ were made resulting in a restricted number of initial organic

compounds (see Quispel, 1968). The same principle of competition is held res-

ponsible for the evolution at the akaryotic and later karyotic stages at the biotic

level. It is clear that competition results in restriction of the pre-existing variability,

either by adapting the mechanism of segregation or by preferential elimination of

less adapted individuals.

In these early stages, again, ‘decisions’ were made about basic features of

structure which became the matrix of later evolution. One may well imagine that,

if ‘decisions’ had materialized in different ways, other matrix structures would have

originated. Thus, the impact of these early competitions must have contained a

very important factor of chance. Chance is in this context of course to be under-

stood as causal, but it includes the possibility that matrix structures of genomes

could have been different. The early ‘decisions’ made, must thus have had a

decisive, hence restrictive influence on later evolutionary lines for further develop-

ment. Once a stable basic matrix pattern of genome design was established, the

fate of further evolution based on this design was curbed, the stakes of its

potential boundary being set out, comparable to ‘evolution’ of basic designs in

industrial tool and machine development.

This implies that only part of the potentially possible organic structures really

have got into actual existence as viable living organisms. We cannot fathom what

other basic designs could have had viability, and so, questioning what percentage

of the total potentiality of living matter was ever realized, becomes an impossible

and useless exercise.

The main basic design for plant evolution must have been the unicellular

algae and bacteria*, probably soon followed by fungi. They must have been

capable of conquering the earth, as they still do. They coupled plasticity against

environmental factors with diversification, resulting in the occupation of all niches,

as they still do. This diversification consisted of the origin of species adapted to the

environmental niches of an unimaginable variety: freshwater, seawater to brine,

arctic to tropical conditions, rock faces and snow, even extremely high water

temperatures. It seems doubtful whether this can be explained or that it needs to

be explained by the competition/selection axiom; the world was bare and niches

unoccupied, it was free for all.

Our unique planet once occupied by bacteria and algae, we are confronted

with the question why there was any ecological or adaptational need or necessity

for evolution to more complicated organisms according to the competition/

selection axiom as the mechanism of evolution.

*I have always been surprised that virus is usually advanced as more primitive living matter,

due to a more simple design. Since virus is inert matter, only capable of multiplication as

a parasite in the protoplasm of more complicated real organisms, they cannot have preceded,

or be ancestral to, the latter.

106 Gardens’ Bulletin, Singapore — X XIX (1976)

It is likely that the unicells were followed by thread-like, branched and

foliar algae, which also needed space. They may have locally shaded out, but not

replaced all the unicells. They were received as affiliated newcomers, to belong

to one happy family. Under favourable environmental conditions there is no end

to the extension of the family, as is e.g. shown by the tropical rainforest, the flora

of the Cape or of New Caledonia or Western Australia which are not only very

rich, but where also each family and each genus is represented by many species

thriving peacefully together. |

Here we glimpse a first difference, the passive tolerance of plants as compared

with animals. Plants are tolerant living beings, they do not eat their close allies,

they do not hunt and kill in order to survive, they do not need all sorts of devices

towards upmanship in order to live. This passive tolerance, lack of active aggres-

sion, suffering in silence, subdued happy-go-lucky mode of living, just waiting what

will happen, this inertia as compared with animals, is characteristic of plants. To

no mean degree this is due to the sedentary bond with the terrestrial substratum.

Animals show generally motility, they show aggression, they are out to

exterminate rivals, show competition and intolerance, and are for a great deal

not sedentary and bound to the substratum, but move around. It should be

mentioned that among the most highly evolved animals, viz. birds and mammals,

there are striking examples of tolerance within the species, mutual aid, and even

birth control by various sophisticated devices. Still, these are exceptions, and

especially tolerance towards the members of other species is very rare.

These two opposite tendencies, passivity and activity, must, I believe, have

the important corollary, that animals are under greater pressure to develop steadily

more complicated means and ways, including structures in order to keep up with

competition and have to use all possible advantages, which by mutation occur, in

order to survive. Their structure becomes in this way adapted to competition,

leaving hardly room for organs or other features which are useless or irrelevant

to survival. Their organization is thus changing rather rapidly; organs once useful

have been superseded by others and though they often do not disappear entirely,

they soon are hidden away and can only by careful comparative anatomy be traced

as insignificant vestiges.

Thus I believe that, while the competition/selection axiom is valid for animal

life, plants behave more conservatively, as they do not suffer from similar pressure.

They develop more slowly and give free way to inventiveness in forms and struc-

tures which are irrelevant to competition/selection, creating features which some-

times are called adaptively-neutral.

It should be noted of course, that rudimentation in flowering plants, due to

saprophytism, parasitism, or secondary aquatic life, is comparable to rudimentation

in animals. Nevertheless, it seems to be less stringent in general, and it seems to

proceed much more slowly.

Competition and survival in plants is passive; it is mainly caused by or

directed against the inanimate environment, heat and cold, drought and water,

seasonal desiccation, exceptional soil types, and presence of toxic minerals, etc. A

few exceptional cases of allelopathic behaviour mean only that certain plants may

not tolerate others in their immediate vicinity, but there is plenty of room for them

elsewhere. Besides, allelopathy does not concern competition between allied species,

but rather implies an influence of exudates of non-related species. Parasitic plants

may destroy or harm their hosts, but they usually come to a balance agreeable

to the survival of both host and parasite, sometimes even to a parasitical symbiosis _

(Rafflesia, Balanophora, etc.). In their strife for light plants may shade out others, _

but there are always open places where the shade-giving plants cannot thrive and 4

have to give way to the smaller ones.

Autonomous Evolution 107

There is no case known to me that a so-called better adapted plant completely

outrooted another allied species. It has been shown that seedlings of one species

may have an advantage over those of an other in experiments, but I doubt whether

these experimental conditions can be applied to germination in nature, and if it

were so, in nature it will always turn out to be a mere question of proportional

abundance, not of extinction through competition. This can hardly be otherwise, as

each plant species has its own ecology, including resulting abundance: no two

species have exactly the same ecology. To be precise, and to quote a simple

example: very few closely allied species of plants will be able to survive in a peat

bog of high acidity, or in soils loaded with heavy metal ions, but we never observe

that one species eliminates all others.

In conclusion, it appears that intra- and inter-specific competition as well as

natural selection (in the sense of elimination of weak individuals by stronger ones)

among plants is insignificant. The occurrence and abundance of plants is almost

entirely defined by environmental factors.

Against animals in search for food, the plants behave passively. Many may

contain poisonous substances, or elaborate structural devices which seem to be

effective in keeping off some of the potential predators, but even in these cases

it is the animals which adapt themselves; as a matter of fact the most toxic plants

have animals which feed on them. Thus, it is essentially a question of equilibrium,

based on mutual adaptation.

Animals on the other hand have the problem of surviving two kinds of

struggle for life. The first struggle is the same as that of plants, against the

inanimate environment, but the second is against each other. Instead of the basic

autotrophy of plants there is a food chain in animals, often very complicated, in

which besides plants other animals take part. This dual struggle means a high

degree of competition among animals, and thus a much higher pressure towards

upmanship. This must inevitably lead to more rapid change and development, that

is, evolution.

A third point is that the number of niches for animals is much greater than

for plants, and far more finely knit, enabling them to develop through the pressure

of competition/selection an immensely greater display of form-development and

specializations.

A fourth, though minor, point is that animals can occupy certain environments

unfit for plants, such as the depths of the oceans, the atmosphere, caves, etc.

Concluding, this concise discussion may serve to explain the observation

Hooker made, that the variety in the animal kingdom is far greater than that in

the plant kingdom.

What is more important, it throws also doubt on the holistic view of evolution

in animate nature, in particular on the intensity of competition in the struggle for

survival.

2. Survival level and Patio Ludens

The views exposed in the introduction lead to certain consequences which I

have alluded to in my essay on plant speciation in Malesia (1969), viz. that there

is a difference in the situation of the survival level in plants as compared with

animals. I have illustrated this in a generalized schematic figure (Fig. 1).

108 Gardens’ Bulletin, Singapore — XX1X (1976)

Plants

Patio ludens

Fig. 1. For explanation see the text.

The rectangles represent the total potential space for structural development,

in conjunction with the degree of the minimum requirements necessary for survival.

indicated by the hatched space. The demarcation is marked by a line, which I call

the ‘survival level’; beneath it one has to think of all structures and functions

compulsory for survival.

Above the survival level there is ‘patio ludens’, represented by the blank space

which can be occupied — but will not always be necessarily fully occupied — by

structures which are irrelevant to survival, hence fall beyond competition, selection,

and adaptation.

Through the more intense competition and more complicated life of animals,

I believe that patio ludens is for animal life only a narrow zone as structural

development is under high pressure of competition/selection, and development is

more acutely directed towards trying to employ and adapt any new feature which

it can use for its survival. The survival level in animals lies thus considerably

higher. It should be admitted though, that adaptive-neutral features have occurred

in animals as well, at very primitive levels, e.g. when the divergence started in

arthropods into the insect and arachnid phyla, but also at the level of speciation,

as exemplified e.g. by protuberances (often allometric in behaviour) in protozoans,

arthropods, vertebrates, etc. See p. 112. Also I would not exclude the possibility

of a lower survival level in primitive groups of animals.

In plants the survival level must generally lie much lower and primary struc-

ture equipment is more primitive. There is no such competitional strife in perfection

of adaptive structures as among animals. Consequently there is ample allowance

for the possibility of structural features (form development) which are irrelevant

to competition and adaptation.

These irrelevant or adaptatively neutral characters in plants concern both

gross morphological characters and internal characters. It is for a woody plant

not a matter of competition whether it develops into a tree or liana or a scrambler;

or whether a liana twines to the right or to the left. Phyllotaxis seems also a quite

irrelevant character, all types are equally well fit to let a plant live and survive.

Presence or absence of stipules can equally not be attributed to have special

function for survival. To prevent any misunderstanding: functional adaptations are

very important, but they are not in any way restricted by neutral basic features

like e.g. phyllotaxis.

Merousness of flowers also seems a matter of chance choice. Thus it would

be a far-fetched idea to postulate that 5- or 4-merous flowers have a competitive

value, the one better than the other, or 3-merous ones over 2-merous flowers (cf.

also Bateson, 1894: 67). Monocotyledons are characterized by 3-merous flowers,

but 2-merous ones do equally well (Stemona, Paris, etc.).

Autonomous Evolution 109

In the flower the number and position of anthers, obdiplostemony, etc. is an

often systematically very constant structure, but it seems futile to ascribe com-

petition value to such structures. In a very uniform genus, such as Tristania, the

number ranges from 5 to very many (and then in phalanges); in Borneo many

species grow together and none of them is crowding out the others.

As to gynoecium, its position: superior or inferior, its merousness, the position

of ovules, erect or pendent, axial or parietal, seems not to have any bearing on

competition. It just happens that in families like Theaceae one or a few have by

exception an inferior ovary (Anneslea) and in Rubiaceae some have a superior

ovary (Gaertnera). Or this may vary even within one genus (Mastixiodendron).

A similar situation prevails with the seed. It could not be argued with good reason

that the presence of two cotyledons would be of any competitive value above the

presence of one cotyledon, or for that matter of more than two. The same holds

for the place where reserve food is stored, in the cotyledons or in albumen, or in

both, or whether seeds are large or small. They all come up equally well ecologic-

ally. As a matter of fact any systematic structure (systematic character) may be

constant in one group and vary in an other; properly none of them have absolute

value.

In this context it is noteworthy what A. C. Smith remarked, when he spoke

of the phylogenetic systematy of the Monimiaceae (1973: 55): “The basic

complex with which we are here concerned, within the Ranales, is characterized

by having comparatively primitive xylem, ethereal oil cells, monocolpate pollen

or pollen derived from that type, and unilacunar nodes. Incidentally, these are not

glaringly apparent characters, but they are some of the basic characters that

taxonomists concerned with Angiosperm evolution must use if they seek to

understand (phylogenetic) relationships”’.

In all these structures plants do not compete, their only concern is to stand

certain primary minimum conditions under the survival level.

_ Concluding, it must be well understood as a major point that it is precisely

these ‘technical characters’ which serve for the schemes of the evolutionary

system of the Angiosperms, that is, that they reflect phylogenetic affinity and are

employed for the reconstruction of their ancestral relations and derivation. Though

these structures have no adaptive value, the way of evolution is traced by them.

And this shows their importance.

Anatomical features and structural fitness of Gymnosperms

Even for anatomical features the evidence that complicated, specialized

structures would have originated as a result of competition/selection to enhance

their functional value, is dubious, if we try to measure their success.

One might imagine that vessels for transport of water, assimilates and minerals

would mean a great advantage over tracheids. This rough assumption is, however,

not borne out by the facts, as among both groups are the highest trees known to

exist, and the oldest in life-span are even among those without vessels. Furthermore,

it is not so that among the vesselless trees growth need to be hampered by

absence of vessels and thus growth would be slower. Saplings of certain conifers

may show a very rapid upgrowth indeed, comparing favourably with that in

eucalypts. Conversely it is not so that saplings or trees with vessels always show

a rapid upgrowth; some grow extremely slowly. This whole matter is dependent on

several factors, sometimes individually on soil and climate conditions, and

Structure and capacity of root system, but mainly on the ecological capacity of the

different tree species of each group, irrelevant of presence or absence of vessels.

110 Gardens’ Bulletin, Singapore — XX1X (1976)

A conclusion is sometimes made about the better adaptation by presence of

vessels with reference to the palaeontological experience that Gymnosperms have

very gradually been partly replaced by Angiosperms, in the sense that terrestrial

space now occupied by Angiosperms was in pre-Cretaceous time the domain of

Gymnosperms. This is certainly true, but it is doubtful whether this generality

can be explained by improved ‘adaptive values’. On the one hand it should be

remarked that anatomically and functionally the Jurassic Ginkgo was obviously

a success, but similar things can be said of Araucaria, Metasequoia, Cycadaceae,

and others. On the other hand trees equipped with Angiosperm-type wood

from the Cretaceous had also to make place for newcomers. In addition it should

be remarked that anatomists tell us that various anatomical features seem to be

without function. Finally, the ‘decline’ of Gymnosperms is, I feel, slightly

exaggerated; they are still responsible for a high percentage of all organic matter

produced on our globe. This idea of ‘decline’ may, possibly in part be due to the

proportionally low form-development which is indeed negligible if compared with

the enormous diversity in structural development of Angiosperms.

But this is altogether another matter than inadequacy or deficiency of

structural and functional fitness. This matter belongs to the question one can also

put for structural development of many phyla and groups: why some are ancient

but remained small and others grew to great diversified groups. Even in the

Mezozoic the Gymnosperms as to number of genera and species were probably

always fewer in number than the Angiosperms are today. The only guess one can

make in this obscure field of speculation is that the basic genome pattern of groups

remaining small was ‘rigid’ and did not allow for abundant form-development, and

that the genome pattern of so-called more successful groups or phyla was more

suitable or ‘versatile’ and had the promise of more potentialities. Similarly as in

chemistry certain atoms (for example C, Si, etc.) have more potentialities as the

basis of compounds than others: or in terms of plants, certain species appear to

be fit to be ‘developed’ into a large number of edible or ornamental variations,

while others simply resist this and do not possess genome potentialities fit to be

exploited by domestication.

In chemistry potentialities of chemical evolution — in the sense of capacity

of producing compounds — can be foretold. This should then also be possible for

the chemical compound named genome-structure. But this is so complicated that it

will never be possible to compute why the pattern in the Linaceous genus

Ctenolophon, which existed already in the Upper Cretaceous, persisted all the time

in the tropical forests (now extinct in the neotropics) but produced at most three

species, while the obviously much later evolved Compositae, Acanthaceae, etc.

showed an astounding diversification though they are structurally very homogeneous

from the taxonomic point of view.

I may mention a few other examples of old genera which are known from the

Upper Cretaceous or Palaeocene which have never evolved into large groups, e.g.

Pachysandra, Nypa, Knightia, and Gingko; contrasting these with Ilex, Quercus,

Nothofagus, Alnus, Symplocos, etc., we cannot account for the latter’s successful -

development, taxonomically and geographically, \:

I do not believe that it will ever be possible to compute the causality

structural development or account for the potentialities of the genome matrices an

show that it could not have been otherwise and could be foreseen, or at leas

expected.

Autonomous Evolution 111

I have stressed (1969) that a congenial, equable climate, such as the tropical

rain forest, which has persisted ecologically unhampered for aeons, has the lowest

competition pressure, hence the lowest survival level in all habitats for plants, hence

for them the widest patio ludens. Consequently the tropical rain forest offered the

longest and largest opportunity towards form creation on the globe, for all kinds

of structural developments which came up to survival conditions. It became the

cradle of the development of Angiosperms as well as many other groups of the

plant kingdom. This is also the reason why the tropical flora contains so many

isolated genera and, besides, the frame-work of all larger families, which swarmed

out later to other parts of the globe.

3. Pre-adaptations in plants

This term has sometimes been loosely applied in an evolutionary sense, to

explain for example the structure of seeds and fruits on the sandy beach.

These fruits and/or seeds, which are all provided with some buoyancy device,

are either hard-shelled, or have their seed surrounded by a stone and/or fibrous

tissue and thus protected against the surf and grinding on sand, rock, coral and

pebbles. But it must be kept in view that the representatives of the beach and the

tropical beach-forest are just single or very few beach-specialized species of large

inland genera which all display the same fruit-seed structure in inland

vegetation, whether it be the hard-shelled Leguminosae (Caesalpinia, Canavalia,

Desmodium, Erythrina, Pongamia, Sophora) or species of for instance the genera

Barringtonia, Calophyllum, Casuarina, Clerodendrum, Colubrina, Cordia, Cycas,

Cyperus, Dodonaea, Euphorbia, Fimbristylis, Guettarda, Hernandia, Hibiscus,

Ipomoea, Ischaemum, Morinda, Pandanus, Scaevola, Spilanthes, Terminalia,

Tournefortia, Wedelia, etc.

To bring their morphological capacities in conjunction with adaptation, as

so-called ‘pre-adaptation’, seems to me a serious misleading of evolutionary

thought, as it suggests the childish idea of pre-sighting on the part of the plants

that it might be useful to develop such structures, just in case it might be helpful

to cope with the exigency of sharing the future life of a beach-comber, These

structures were already there in the genera and have nothing to do with the axiom

of competition/selection pressure. Invading the beach just meant for these genera

invading new terrain, in part unoccupied. The effort often was not even

considerable, as they remained for their root system largely freshwater plants,

and for several genera the hot beach conditions did not differ much from their

main development in dry inland savannahs.

I could for many other specialized habitats give a similar picture, in the way

that so-called pre-adaptations were already represented in existing structures

outside these specialized habitats. A development of large hypocotyls with food-

reserve in the seed, is for example represented in many tropical inland trees; it

developed strongly in the littoral Rhizophoraceae, but certainly not as a result of

competition/selection pressure. In passing: this feature is also not necessary at all,

as the tiny seed of Sonneratia mangrove trees does not show anything of the kind.

A similar picture is displayed in almost all ecological specializations, be it

rheophytes, therophytes, etc.

It should be added that, whereas the survival level scheme holds for one

species or group at one time and in one place, the corollary is that patio ludens

characters may, in later stages, or during migration of a taxon to other places with

112 Gardens’ Bulletin, Singapore — XX1X (1976)

different environments be ‘pushed down’ under the survival level as they become

essential for survival in these stages or places where their latent existence is

activated. Such characters may be physio-ecological as well as morphological.

In conclusion: (1) structures originate and may suit more than one ecological

class or niche, necessarily leading to the peopling of specialized habitats with an

array of unrelated, ‘generic waifs’ coming up to the minimum requirements of the

habitat.

(2) ‘Pre-adaptation’ is often used in a misleading way, as a fancy term

invented through pre-occupied thought. It should be defined more clearly, as in

most instances in plants it has nothing to do with adaptation. It should preferably

be replaced by the neutral term: ‘pre-disposed structure’.

4. Early differentiation

The survival level scheme set out in fig. 1 is, of course, meant for one time

of each plant or animal in one place: it is dynamic, because in the course of time

the significance of characters will, or at least may change. Structural characters

as they appear today to belong to a rigid scheme may, in the far past, in primitive

ancestors not have had the organizational significance they have now. Such

characters may have been then irrelevant not only in plants but also in animals,

because the more primitive the organisms are the lower is their survival level and

the larger their patio ludens must have been.

I have in this context questioned zoologists in asking why in the great phylum

of Arthropoda the Insecta are based on an organization scheme with 6 feet, while

the Arachnoidea are based on a scheme with 8 feet, and whether they assume that

such a basic structure has been the result of competition and natural selection; their

answer was in the negative. Similar questions can be asked about the fact that

Vertebrates all have 4 extremities, Cephalopods have either 8 or 10 arms, that the

basic scheme of Echinodermata is 5-merous (in an exceptional small group

‘running wild’ towards an 11-merous structure) and why this would have advantage

over a 3-, 4-, or 6-merous structural scheme which would equally have been

feasible. In corals, on the other hand, there are again two large classes, the Octo-

corallia and Hexacorallia; why are there no Pentacorallia? With the exception

perhaps of the quadrupedal organization which may be the most ‘economical’

solution from the structural point of view as well as for neuro-locomotor organiza-

tion, these numbers like many others in animals (e.g. 5 fingers in tetrapods, 21

scleral elements in sauropsids) and like merousness in flowers, appear to be quite

accidental and devoid of adaptive or selective significance. These structural

schemes must have been fixed at initial stages, but the agency which caused the

‘decision’ seems very obscure. Still this decision was extremely important, being

decisive for later phylogenetic organization.

It seems a far-fetched idea that this decision had anything to do with com-

petition/selection; to me it appears a matter of casual structural development for

which the potential was already embedded in the basic genome matrix, Once

triggered development could not proceed otherwise.

In the initial primitive stage these basic structures may well have been patio

ludens characters of the group concerned, irrelevant of competition/selection

pressure, similar as must have been the case with many phylogenetic characters of

plants, as has been advanced earlier in the preceding chapter.

Autonomous Evolution 113

This leads then to consider the genetical status of the merousness, and to the

question: were these characters which have now class or phylum value at the early

initial stage of much lower genetical value and apt to variation, maybe even at

species level? How could it then be understood in the genetical sense that, what

initially was possibly defined by a few genes could later develop into a strictly

fixed bond characteristic of a whole phylum, and obviously so essentially integrated

in its genome structure that it was not liable to be influenced by later mutations?

In fact, except for rudimentation, secondary changes of such accidentally fixed

primitive numbers are very rare indeed.

5. Saltatory evolution in plants

It is axiomatic that structural development is always proceeding stepwise, never

completely gradual. In this point there can be no difference in inanimate or animate

chemical compounds: both energy and matter are discontinous, ‘molecular’:

quanta, atoms, genes, and so their changes must be discontinuous.

The changes brought about by evolution in organisms can of course be small

or large; if the steps are very small, the process looks to us gradual and one can

speak of ‘gliding evolution’; a mutation concerns at least one gene change. But

if the changes are larger steps, one speaks of saltatory changes and development.

As in animals evolution in plants starts with divergence, and divergence must

start from diversity, often called variability, of a genetical nature.

The first major step to evolution is speciation, that is, changes on the species

level. This holds for all levels, as the first representative of the suprageneric taxa

must also belong to a species. The origin of species is thus the most important

phenomenon in evolution. But what is the criterion for a species, especially its

delimitation? In two previous essays (1949, 1957) I have extensively treated the

causes of variability and species delimitation respectively. I have come to the

conclusion that there are essentially two ways of speciation, viz. through racial

segregation and through saltation.

With racial segregation a species population segregates in the course of the

slow process of dispersion into spatially (ecologically or geographically) isolated

(replacing = vicarious genetically differentiated ecotypes, races and subspecies,

in response to the ecological environments in the new lands (see van Steenis,

1949: xliv—l, and 1957: clxxxili—cxcvi).

Such raciation may finally result into a compound string or array of ‘beads’

representing convivia in Danser’s sense.

Such races differ from one another in their gene combinations, but these

differences usually concern only a restricted number of genes and in the intervening

border zone where two adjoining races meet there is a transition zone where fertile

hybridization takes place and intermediary specimens occur. On the borders

marginal differentiation takes place by pioneer advances (genetic drift).

The general experience in plants is that raciated species populations form

together one commiscuum (syngameon of Lotsy) in Danser’s sense (1929). Such

a commiscuum is really a net of interfertility, as all races are miscible with the

adjoining ones. Even if widely spaced races may become isolated through circum-

stances, fertility usually remains intact. There are many cases to support this. For

instance the Pleistocene glacial period has broken up many populations, but through

this cause now widely disjunct ‘species’ of, for example, Platanus and Campsis, in

East Asia and America are still miscible; properly they should be treated as races

of one species population and classified taxonomically as subspecies.

114 Gardens’ Bulletin, Singapore — XX1X (1976)

The possibility that the furthest remote races have accumulated so many

hereditary differences that they prove incompatible if brought artificially into

contact cannot be excluded. They may still be crossable but not miscible any more,

that is, in hybridization will not go beyond the sterile F, hybrid.

I would not go so far as to exclude the possibility that accumulating differences

in gene composition may, after a long period of isolation, in a restricted number

of cases lead to new species. This possibility is still more likely if partial popula-

tions survive in isolation on islands.

But the general impression is that in plants speciation through racial segrega-

tion must be a rare phenomenon and that this so-called ‘micro-evolution’, however

interesting it may be for an understanding of the variability within a species is,

in plants, of little significance in phylogenetic evolution. Racial segregation is a

restricting agency, pruning variability; it is in phylogenetical sense not a creative

agency. Goldschmidt (1933) defined this in saying concisely: ‘‘Geographische

Variation ist weder eine Vorstufe noch ein Modell des Artbildungsvorganges”’.

Saltatory evolution appears, on the other hand, to be the common way in

which form-making in plants takes place, and this can easily be observed from the

still growing, important body of facts about chromosome numbers. Scanning these

it is obvious that a very large number of species are polyploids, either autoploids

or alloploids. Still more interesting is the fact that this increasing information shows

within families the frequent occurrence of dysploid, aneuploid and allopolyploid

numbers which are not seldom characteristic of genera of higher taxa. Genera can

have allopolyploid genomes, as occurs e.g. in Gossypium.

Cultivated cotton is generally tetraploid (52 chromosomes), and is supposed

to be an allotetraploid of Gossypium arboreum L. x G. thurberi Tod. (or some

other Asian and American diploid species) (Brown, 1951). Note that the cultivated

types are natural allotetraploids and that they behave as diploids. The product

arboreum x thurberi is not quite similar.

Stebbins (1971: 179-201) emphasized the important creative role of

polyploidy in Angiosperm phylogeny and concluded (I.c.: 198) that “extensive

polyploidy must have taken place during the early evolution of woody Angio-

sperms. The most probable hypothesis, therefore, is that the polyploidy which gave

rise to the basic numbers of woody plants took place at various times during the

Cretaceous and the earliest part of the Tertiary Period, while the diversification

of species on the basis of secondary basic numbers is largely a product of the

Tertiary and Quaternary periods’. He cited many examples of tropical taxa in

this context and estimated that between one-fourth to one-third of the flowering

plants are polyploid with reference to their nearest relatives.

In some families taxonomic affinities can thus be supported cytogeographically

and attempts can be made towards a reasonable reconstruction. See for instance

the most interesting papers on Australian Proteaceae by Johnson & Briggs (1963),

on Pomoideae by Challice (1974), on the Casuarinaceae by Barlow (1959), the

Loranthaceae by Barlow & Wiens (1971), the Oleaceae by Briggs (1970), and the

Malvaceae by Bates (1968). ‘

There are at least two processes by which chromosome changes are brought ;

about, viz. hybridization (proved in many cases) and obviously irregularities in

meiosis (translocation or ‘centric fusion and fission’, aneuploidy, duplication);

there may be others.

The main point is, that major genomic rearrangements of the type quoted

above, occur in a single generation, indubitable proof that saltatory form-making

has been the major feature in plant evolution. See fig. 2.

Autonomous Evolution 115

comm.6

0

E

E

(eo)

oO

|

|

|

comm.1

—

— eee

Fig. 2. Scheme of saltatory evolution in plants by individuals.

Commiscuum I has produced the daughter commiscua 2, 7, and 8. Commiscuum 2 has

produced the daughter commiscua 3, 4, and 5.

Commiscua 1, 7, and 8 show mutual affinity and so do commiscua 2, 3, 4.

Commiscuum 6 is an allopolyploid between commiscua 3 and 5; it shows affinity with

several other commiscua but is also an example of reticulate phylogeny.

Even though they may not become established at once, they certainly re-occur

with a given probability and sooner or later will result in a population of indivi-

duals with novel characteristics. Thus, the idea seems justified that evolution in

plants is largely of a saltatory type. For instance, polyploidy undoubtedly has been

instrumental in many cases, in producing new forms. Some botanists claim that

autopolyploids are side-products of evolution, being variations on a given level

only, whereas evolutionary progress occurs on the diploid level. There is on the

other hand no doubt that amphidiploid combinations are significant in evolution.

More importantly, saltatory genomic changes in the diploid range are well-

documented, especially in the genus Clarkia (Lewis, 1953).

In any case it appears that such evolutionary changes have nothing to do with

competition pressure or selection of the fittests.

Naturally, the fit survives, the new plant arisen must come up to survival level

and be able to germinate, grow, and propagate, but that is all there is to it, harmless

extras are allowed.

116 Gardens’ Bulletin, Singapore —- X XIX (1976)

It is admitted that not all families show an important array of ploidy variation,

e.g. Pinaceae or Lauraceae seem to be exceptions. In the Lauraceae the family

number seems to be x = 12, including the vegetatively aberrant parasitic, herba-

ceous genus Cassytha, according to Okada & Tanaka (1975). Incidentally, this

number seems to be common in primitive Angiosperms. In such cases the number

of chromosomes does not tell much, and information would be needed about the

internal structure (chemical composition) of the chromosomes and also about the

way in which these ‘internal’ differences have come about. The same should be said

about genera in which the number of chromosomes is very constant; sometimes

differences in size and shape already reveal this in a superficial way. The study of

the genome architecture in plants is of course a most difficult field to explore and

we are only beginning to enter it, for instance by measuring DNA hybridization.

Finally I would here also remark on the phenomena of teratological and

neotenous forms, for which I refer to my essay of 1969. Teratological forms arise

as sports all of a sudden. With teratological forms it is clear that physiological

chain-reactions in plants have undergone change. Classes of terata so much resemble

taxonomical characters (prolification, antholysis, enations, cohesions, fasciation,

laciniation, adesmy, reduction, petaloidy, scyphogeny, and ceratomania) that they

cannot simply be ignored or waved away. Some terata are known to be inherited

and due to a single gene mutation. Bringing terata and: phylogeny in line means

that they should be hereditary (see e.g. Stubbe, 1966).

The concept of terata is mostly accepted as something ‘abnormal’ or

‘monstrous’, and should be disposed of as meaning inferior. This appears to me a

very superficial, emotional evaluation. Many evolutionary processes are brought

about by reduction, suppression, fusion, etc.: a panicle of separate flowers changes

into a head or fig, or is reduced to a raceme, or even a single flower; meristems are

suppressed and contraction follows; or they are joined to other meristems and

fusion follows (ovaries of Morinda; epiphyllous flowering; concaulescence in

Solanum, etc.); leaf production is suppressed on twigs which grow into thorns:

lateral branches do not develop inflorescences and are metamorphosed into curved

hooks for climbing (Uncaria). There is no end to these metamorphoses, each of

which represents an ‘abnormality’ or ‘malformation’ if compared with that of the

immediate ancestor which did not possess the new structure. Thus the ‘concept’

of terata has a very definite structural meaning in biology, viz. a sudden change

of structure which differs from the taxon from which it evolved.

Comparing trees of the Naucleeae with the miserable Uncaria, a climbing plant,

of which part of the flower-bearing side-branches are flowerless and deformed into

curved hooks, the latter is an abnormality; but surely Uncaria has found its niche,

proved its vitality and developed into quite a large genus. Considered unemotio-

ese from a broad outlook, systematical teratologies are really hereditary terato-

ogies.

Many of these changes are morphological reductions or suppressions, and

that stamps them to belong to neotenous behaviour, that is: reaching maturity

before all parts have developed as in the immediate ancestral form, Precocious

flowering may turn a woody plant into a herb; precociously flowering herbs may

be reduced to flower production on the cotyledons of the seedling (Monophyllaea).

For plant evolution I ascribe (1949, 1969) great importance to neoteny

which I regard as one of the two crucial processes in their evolution. Takhtajan

(1954) spoke of ‘phylogenetic teratology’ and correctly generalized and applied

it to all contractions and reductions, as a vital element in form-making.

Systematical teratologies originated in all probability suddenly as saltations,

in one or more steps and survived if they were viable in the sense that their

ecological and reproductive capacity reached survival value, with their morpho-

logical caprices tolerated.

Autonomous Evolution 117

In contrast with the chromosome ‘mutations’ caused by hybridization or other

mutative changes I have the conviction that important changes in morphogenesis

might often have been caused by not too integral genetical changes. I derive this

from the fact that fasciation (as in Celosia cristata L.) or pelorial flowers (as

occur in Scrophulariaceae, Orchidaceae, etc.), which give a fundamental change

to structure, seem to be based on presence or absence of one or very few vital

genes only.

I once discussed with a famous botanist how he thought that a pitcher of

Nepenthes might have originated. To my surprise he said that this might have been

gradually built up, may be by a thousand gene mutations. Obviously he was

ignorant of scyphogenous structures in the cultivated ‘crotons’, fancy varieties of

Codiaeum variegatum (L.) Bl., in which the rough skeleton of a Nepenthes pitcher

can be observed, the blade, tendril (naked midrib) and at the end a pitcher with an

appendage (the lid).

If such a structure can be formed in a ‘sport’ of one known species, little

imagination is necessary to assume the origin of a pitcher, through scyphogenous

action, in a few saltatory steps. Once the initial step was made, autonomous

perfection can be imagined in a few more orthogenetic steps.

Blocking of certain vital genes by mutation may cause development to follow

another physiological pathway in the chain-processes leading to morphogenesis

and production or reduction of proteins, hormones or other substances controlling

form-development.

I have talked about this matter with geneticists, both on the matter of stability

of structure and obviously responsible genome patterns on one hand, and sudden

changes in a few vital genes on the other hand, but it seems that these seemingly

contradictory phenomena cannot easily be translated in genetical terms of

molecular biology. They find this a most complicated matter about which even

generalized ideas of morphogenesis in genetical terms can not yet be given.

However unfortunate this may be, I hope the meaning of the arguments given

above is clear. They lead to the following conclusions:

(i) In both major causes of evolution of plants, that is either changes in the

gross chromosomal patterns (allopolyploidy, dysploidy, aneuploidy) or the

physiological function changes of morphogenesis by neoteny, the changes are

sudden, saltatory.

(ii) The saltatory steps are at least at species level, but higher categories, for

instance genus level, may also be involved.

(iii) The conclusions given above imply that evolution of plant structure is

essentially not caused by competition but is an autonomous process in which

chance plays a distinct rdle.

(iv) For form-making the gradual accumulation of gene changes resulting

into raciation may not be excluded as a cause of segregation of species but should

be considered as of minor importance, while also their competition is not the

overwhelming agency as frequently supposed.

In fig. 2 I have drawn a scheme reflecting the above considerations.

6. Gliding evolution in animals

As explained in the introduction the mechanism of evolution in animals must

be much more complicated than in plants, as in addition to autonomous develop-

ment in patio ludens at early stages it must include competition. As in most plants

raciation in species populations easily occurs, sympatric and allopatric, the main

difference with plants being that such raciation is largely a matter of competition

partially for food and shelter, but with the additional agency of sexual selection,

118 Gardens’ Bulletin, Singapore — X XIX (1976)

which is absent in plants. Through these combined factors and competition racial

segregation will in animals usually develop more rapidly than in plants. By this

sexual selection partial populations drift apart and become in the practical sense

incompatible, and thus a start is given to divergent development. In several cases

it has been shown experimentally by artificial insemination that recognized good

species of insects, which in nature keep strictly apart, are factually compatible.

But through their isolation by sexual selection and then occupation of a specialized

ecological niche they will finally drift apart, by populations, to such degree that they

become incompatible genetically. Thus they start as convivia but gradually become

commiscua and finally comparia, to stand on their own for future development.

Mutations irrelevant to survival will be possible, but these will play a much smaller

role than in plants as patio ludens in animals allows for much less free form

development than in plants by predominant competition and sexual selection

pressure: any new feature arising is ‘tested’ on its usefulness for competition.

See fig. 3. The reader may recall that a prominent zoologist and geneticist,

R. Goldschmidt, has put forward the idea that in the macro-evolution of animals,

saltatory re-arrangements of the genome, and ‘teratological’ mutations “‘the hopeful

monster’) have been important. But there seems to be little evidence to support

this concept.

Fig. 3. Scheme of two initial stages of divergence in the gliding evolution of animals by

populations.

A. A mother population (m.p.) starts to form a convivium (c.v.); it is still loosely con-

nected and compatible with the mother population by a transition zone (f.z.) of rare misci-

bility.

B. In a further stage the convivium of fig. A has developed into a new independent

commiscuum (comm.) which has become incompatible (indicated by a ‘gap’) with the mother

population (m.p.). This new commiscuum is undergoing in its turn a similar differentiation

and has formed a new convivium (c.v.’) comparable to the scheme in fig. A.

The main conclusions on the differences of animal evolution as compared with

plants appear to be fourfold:

(i) Evolution in animals will be gradual, through accumulation of competition /

selection characters by ‘gliding evolution’, through separation of divergent popula-

tions, raciation with practical incomptability into convivia which gradually develop

into truly incompatible commiscua, and finally into comparia.

(ii) Evolution of animals goes in general by populations and not by individual

specimens as usual in plants.

(iii) There is little opportunity for patio ludens characters to develop, as all

are tested on usefulness for competition and survival, and are subject to sexual

selection which is unknown in plants.

Autonomous Evolution 119

(iv) Saltatory steps are not excluded, but they must be extremely rare in

proportion to their frequent occurrence in plants,

In fig. 3 a scheme has been drawn reflecting these considerations.

7. Co-evolution of animals and plants

As I have emphasized in the first chapter plants were the first organisms of

all organic evolution by their capacity of assimilation, capturing and storing

energy. Animal life developed later, and never became independent. Food chains

always have to go back on plant life.

Animals could in a broad sense be considered to lead a parasitic life; they

browse and feed on plants which make their life possible.

Except for negligible exceptions plants play the passive rdle, and the organic

matter they produce is at the disposal of animals which are specialized for taking

advantage of anything they can find, even the most indigestible organic products.

From this follows that plant evolution goes independent of animal evolution and

that novelties arising in plants are secondarily exploited by animals. Notable

exception: a large part of Angiosperm evolution has been aligned to pollination

‘symbiosis’ with animals.

Apart from the plant bodies themselves, used as food, animals are attracted

to them by colours, scents, and obvious shelter. Evolutionists seem generally to

assume that glands, floral and extra-floral, give competitive advantage to plants

through the prowling animals. They have theorized that in such a way the

competition/selection principle was forced on the plants, inducing plants to excrete

more nectar or other substances, and thus induce numerical advantage over those

which produced less, or less abundant, attraction to animals.

This is a very crucial problem indeed, and it seems difficult to prove or to

disprove whether the assumption of this advantage is true or not, and that it

worked under natural conditions.

For one thing, experiments lack of course the factor time. Even if it were

proved that there was advantage to plants by animals this would mean that this

assumed advantage would result into greater numbers of the plants (higher popula-

tion density) which had the advantage. It is hard to believe, however, that this

would mean extinction of those which offered less benefit. The latter would have

a lower population density, but we can observe that precisely such a phenomenon

is ubiquitous in the plant kingdom. In each genus certain species are rarer than

others, but it would be a far-fetched idea that all the rare or rarer ones are nearer

to, or nearing extinction. This is largely a matter of ecology, available niches, etc.,

not an immediate result of competition pressure: each species has its own ecology,

including frequency of occurrence.

For another thing experiments never reflect the situation in nature. Imagine

an experiment in which seeds of two allied species were sown together with the

result that the seedlings of the one crowded out the other. Would it be conclusive

to speak of higher competitive value and selection? It would certainly not be

conclusive, except for the experimental conditions, the soil used, etc., and not for

the varied conditions nature offers to the two, where such situations as in the

experiment will hardly ever occur, and then only extremely locally, if ever. The

very existence of the two species disproves already the assumption: in nature both

occupy obviously their own particular ecology, otherwise one of the two would

not exist.

Excretion in plants is mostly a physiological necessity. Dripping from

hydathodes occurs when evaporation is insufficient: organic and mineral substances

excreted in this way may serve animals. A similar reasoning could be held for

excretions by glands.

120 Gardens’ Bulletin, Singapore — X X1X (1976)

Shelter is ‘offered’ by plants to animals, in many ways.

On the under-surface of leaves a fairly large number of woody plants develop

domatia in the axils of the main nerves. The physiological] function of these domatia

is not known, according to Jacobs (1966), who published a classic paper on

them. They do not excrete and are not glands; they appear often only when seedl-

ings have reached a certain age. Their distribution in the plant kingdom is large

but restricted; they have never been found in plants of arid countries. They were

not infrequently termed ‘acarodomatia’, derived from the observation that small

arthropods seek shelter in these small cavities. It is proved that they originate

irrespective of animal irritation and appear to be a whim of plant structure. The

fact that animals exploit them as shelter means nothing special: animals will of

course exploit anything they find favourable for their comfort and survival,

animate or inanimate, just as primitive man would employ anything which he

found useful or of advantage. Our urgent strife of locating useful things is of course

not different from the same urge in animals. In fact we and the animals are

completely possessed by this strife. But from a strictly detached point of view

there is every reason to accept that domatia are an irrelevant structure in plants

which is secondarily exploited by animals. That is, if we really want to detach

ourselves from the inherent prejudice that all characters of animate nature must

have some useful meaning.

I am of course by no means the first who ventilates criticism and in this

context I want to refer to Bateson (1894: 12) who “undertook the study of

adaptation as a test to the theory of natural selection and the hypothesis that there

is a tendency for useful structures to be retained and for useless parts to be lost.

We have no right to consider the utility of a structure demonstrated, in the sense

that we may use this demonstration as evidence of the causes which have led to

its existence. In absence of correct and final estimates of utility, we must never use

the utility as a point of departure in considering the manner of its origin. It thus

happens that we can only get an indefinite knowledge of adaptation, which is not

an advance beyond the original knowledge that organisms are more or less adapted

to their circumstances. No amount of evidence of the same kind will carry us

beyond this point’’,

If we cannot perform this mental effort towards objectivity we will have to

account for the presence of hairs, stipules, phyllotaxis, etc. etc. as well as for their

absence in terms of utility. ““No doubt’, Bateson (1894: 79) says, “that ingenious

persons would find ecological explanations of all these characters, for on this

class of speculation the only limitations are those of the ingenuity of the author’’.

Various kinds of shelter are employed by ants in tropical plants, In these

myrmecophilous plants the devices may be very simple, stem-appressed leaves of

root-climbing plants (Hoya, Dischidia), reflexed appressed lowest pinnae of palm

fronds (Calamus sp.), palm-sheaths (Korthalsia), appressed stipules, saccate

domatia (several neotropical Melastomataceae, Callicarpa saccata van Steenis),

but also pithy stems (Cecropia, Endospermum spp., Clerodendrum fistulosum

Becc.) and pithy branches in a large number of Malesian trees of various families,

the tendril of one species of Nepenthes, and stipular thorns of Acacia, in which the

pith is removed to shelter ant colonies, The most spectacular shelter is offered by

the root tubers of the epiphytic rubiaceous genera Myrmecodia, Hydnophytum and

some allied genera. These tubers have large labyrinth-like cavities inhabited by

ant colonies where they tend fungal gardens as food.

There is a host of literature on this subject, a survey of which would fill a

book in itself. The essential question turns round the adaptation theory of Beccari

(1884-1886) and Schimper (1888) who advanced that such structures in plants

arose by the mutual action of plants and animals to the advantage of both. And

they tried to collect data to show the advantage of ants for plants. The latter

evidence appears, however, very dubious indeed.

Autonomous Evolution 121

One crucial point has been cleared by Treub (1883) who showed that the

cavities in the Myrmecodia tubers originate already in seedlings without any action

of ants and excellent upgrowth follows without them. Whether these cavities have

any ecological meaning to the plant is uncertain; they may physiologically serve

for aeration or evaporation for regulation of temperature, but this has not been

proved.

It is doubtful even, whether they are essential to the ants. We note in this

context, that certain European ants build their nests around the base of plants.

preferably Rosaceae and Umbelliferae, but they survive equally well without them.

It stands to reason, however, that in an objective view there is no necessity to

assume co-evolution, if we advance that these structures would also have been

developed by plants without any ants in existence. Why should not leaves be

appressed to stems in root-climbers, stipules leave cavities, leaves have domatia,

pinnae be reflexed, stems and thorns have pith, all representing structural develop-

ments sui generis?

Conversely, it is clear that if ants evolved and would find these structures,

they would employ them and take full advantage. Some species might even become

entirely dependent.

Plant structure evolves first and it is the animals which will adapt themselves

and often will evolve to greater specialization. This principle applies to chemical

differentiation as well.

It has sometimes been advanced that the supposed profit the plants would have

from the ants would consist of protection against other predators, but this is

proved to be a fallacy. For Myrmecodia the profit for the plant was supposed to

consist in accumulating minerals etc. for growth, but there are many large woody

epiphytes without ants showing that in this aspect epiphytes can well manage this

themselves. Then it was advanced that for several other myrmecophytes the ants

are attracted by their seeds with their oil-containing elaiosome, which seeds are

deposited in their nests. This is true and may locally add to their frequency, but

none of these ant plants is confined to ant nests and their seeds can germinate on

any suitable bark.

It must be concluded that the co-evolution of ants and plants is only a one-

sided evolution, namely for the ants.

I fully agree with von Ihering (1907: 710) who said that Cecropia needs its

ants as much as a dog its fleas.

Evolution of orchids

The spectacular development of Orchidaceae is of course a classic of

co-evolution. Leaving apart a fairly considerable number of orchids which are

self-fertilizers or are cleistogamous, the majority is compulsory cross-fertilized by

insects and this has led to most ingenious devices of the orchid labellum.

Systematically the queer fact is that in orchids so many generic hybrids are

found, and that still more can be made by artificial insemination. The definite

impression is that the whole of the family is genetically only one comparium with

many commiscua, and that the species are usually convivia, They maintain their

distinction by the grace of compulsory cross-pollination and the use of selected

Insect species to achieve that goal. Orchid evolution thus reflects insect evolution.

_ As soon as in the variability range of an orchid a deviation, differing only

in a few genes presumably, occurs, it may be favoured with an insect form from

the variability range of the latter’s population and the two will consequently form

a couple of consorts. This is the first step towards more specialized couples of

orchid /insect.

122 Gardens’ Bulletin, Singapore — X XIX (1976)

Here again, however, the deviating plant structure comes first; if there is no

suitable insect partner, it will probably succumb; if there is a more or less suitable

partner attracted by colour, shape, scent, etc., within the range of variability of the

insect population, the couple is formed and the new plant is saved and lives on by

the grace of the pollinating insect. The latter is of course in no way dependent on

the orchid for its survival.

It cannot be the reverse, as there can be no stimulant or inductive influence

emanating from an insect causing a plant towards a gene combination which it

wants to have. Plant structure comes first, animal adaptation may follow.

Though we conclude that thus evolution in orchids will have been effected in

a gliding way, imitating that of animals, saltations may occur by hybridization, It

is namely known that insects may, incidentally, make errors in pollination by

which even intergeneric fertile hybrids may occur. Their offspring will in subsequent

generations produce a host of new forms which may again start couples with other

insects and consequently lead to further form-development.

This sudden occurrence of hybrids may be termed ‘saltatory’, but for the

essential difference that the saltation is of a much lower status than that discussed

for other plants, as all the offspring remains within the orchid comparium in a net

of interfertility.

A further curious observation can be made in orchids, viz. that by a single

other ‘saltation’ the orchid flower does not develop in the proverbial bisymmetrical

way, but as a normal regular monocotyledonous flower. Such ‘peloric’ forms, of

which I have formerly listed some from the tropics (1949: xli-xlii), are only

recognizable vegetatively by comparison, otherwise they are unidentifiable, even

by first-grade specialists.

Whereas pelorias are generally caused only by one or a very few gene

changes, this tallies with the considerations above that obviously the most

remarkable build-up of the orchid labellum may be a beautiful facade, but that

it is genetically and hence, taxonomically, not such a stable component.

It shows also that few genes may, in cases, bring about a sudden radical

change in morphogenesis,

Evolution of figs

The evolution of figs is a culmination point of co-evolution, as here the

pollinating wasps have still more specialized relations with the plant in that also

their life is bound to the figs in a most intimate way, a compulsory symbiosis. This

is certainly not so with orchid insects, not even in the highly specialized cases of

pseudo-copulation, Much of what I have said about the relations between orchids

and insects will hold here too.

New forms of Ficus will arise and succeed if from the variability of the insect

populations a more or less suitable mate is available. If it is available, adaptation

of a new insect population will follow. Much of this evolution seems not to have

been competitive. Evolution seems to have resulted from the “‘extremely gradual

alteration of the Ficus-protoplasm’”’ (Corner, 1961: 113). In this aspect it is

noteworthy that all species of Ficus seem to have the same chromosome

number, x = 13. )

If this assumption is true it would theoretically follow that artificial insemina-

tion of closely allied species of figs would in all probability lead to fertile hybrids. —

I am not aware that such crucial, certainly difficult experiments have ever been ©

carried out. hs

A conclusion on this chapter on co-evolution runs as follows:

(i) In a large number of situations attributed to co-evolution, evolution is —

primarily of the animals. Plant structures are utilized by animals for their benefit

Autonomous Evolution 123

and they specialize. The plant structures arose sui generis and not in so-called

‘response’ to animal agency.

(ii) Even in the vital association of insects and flowers in orchids and insects

and figs in Ficus plants change (evolve) independently in an autonomous way

and insects adapt themselves.

(iii) Speciation in orchids and figs imitates (follows) the gliding evolution

as is usual in animals. Small changes accumulate in populations which diverge and

gradually develop into races, subspecies and species respectively which in nature

gain (ecological) isolation through the coupling with the particular insects. Insects

are thus secondarily stimulated towards further evolution themselves.

(iv) Saltatory evolution in both groups, more especially in orchids, may occur

incidentally through hybridization.

8. Reticulate phylogeny

I have termed this chapter reticulate phylogeny instead of reticulate affinity,

because it concerns real ancestry which is meant here.

In general plant evolution through speciation will run divergent as in the

branching mode of a tree, similarly as in animal evolution. Fig. 2.

There are, however, many instances known of allopolyploid species hybrids

which are truly new species; they certainly in part share the characters of the two

parent species but exhibit also new characters of their own.

By definition genetical contacts are prohibited between comparia. In plants

a comparium is not rarely equivalent with a subgenus or genus, and as a rule

species of different genera are incompatible and merging or exchange of genetical

material is excluded.

However, exceptions occur, and there are several cases known where clearly

through previous hybridization different generic genomes were blended through

allopolyploidy. In the Cruciferae an allopolyploid generic hybrid was made between

Brassica and Raphanus. Many genera are supposed to have originated in this way,

e.g. Armoracia, and certain allopolyploid species known in Gramineae from

parents belonging to different genera, such as Aegilops and Triticum, Agropyron

and Elymus, etc. As early as 1881 Focke mentioned generic hybrids from the

families Amaryllidaceae, Cactaceae, Campanulaceae, Compositae, Ericaceae,

Gesneriaceae, Rubiaceae, and Scrophulariaceae; others have been found since.

This opens the possibility for allopolyploidy.

_ I would certainly not suggest that all cases of reticulate affinity, a phenomenon

which occurs frequently in plants, should be deemed to be the result of reticulate

phylogeny.

On the other hand I suppose that in very many cases allopolyploid genera and

species have as yet not been recognized as such and my estimate is that there is

a fair number of them.

Allopolyploid blending means that two divergent ‘twigs’ of the ancestral trees

are joined which caused a local ‘netting’ of its ‘canopy’. There is good reason to

suppose that this ‘intertwining’ has also acted in the past during the ancestral

development of the plant kingdom. See fig. 2.

I emphasize that these allopolyploids may be extremely important in plant

evolution, as from them other types, aneuploid, dysploid, or polyploid, may have

originated.

_Compared with plants such reticulate phylogeny may be tacitly assumed to

be in the great minority in animal evolution. This is quite obvious, because sexual

selection will prohibit to no mean degree genetical contacts at the level of species

124 Gardens’ Bulletin, Singapore — X XIX (1976)

and genus. It makes it especially unlikely, or very rare, because in animals sexual

behaviour, attraction and structure of the sexual organs play such an important

role in the divergence of populations. Many ‘experimental’ specific and few generic

hybrids are known, especially among insects, birds and mammals. But they are

sterile as a rule, and even hybrids on a racial or sub-species level in the animal

kingdom are very often sterile, a situation which is exceptional among plants.

9. Embryology and ontogeny

The fact that embryological and subsequent ontogenetic development in

animals is so different from that in plants must have had evolutionary implications.

In animals the development of the embrvo leads via metamorphoses, even-

tually alternated by larval generations, to the mature stage, but from the start it

concerns the whole individual and its complete organization. This changes and

grows and differentiates by a long series of internal structural transformations;

it is a closed system. It is thus quite conceivable that for animals the subsequent

stages in ontogeny can to a certain degree reflect the sequence of phylogenetic

stages, as defined in Haeckel’s principle or law of biogenetics. It can also be

assumed that genetical changes may occur at all stages of this ‘centripetal’

development.

This is essentially different in plants where development is centrifugal and

structure is proportionally so simple. Though the individual in statu nascendi is

as the embryo contained in the seed coat, the internal development concerns only

the development of the archegonium to a mature seed, There is no question of

further internal transformation; it is an open system, Reserve food is stored either

in albumen or cotyledons or both, but there is no reason to assume that either of

the two is a reflection of ancestry in shape or otherwise. It should be admitted that

a few ancestral characters e.g. primary vascularization, may be preserved as vestiges,

as in plants all parts are end-products preserved thanks to the presence of cell-

walls.

Also the first leaves above the cotyledons cannot be seen as reflecting

ancestral shape. The ancestral, primitive shape of the leaf in Angiosperms is, as

Corner (1954) has argued, in all probability the compound leaf, as still retained in

many tree families as a primitive character, token of possible derivation from

compound-leaved seed ferns. It is not impossible that also the seed ferns had

seedlings with simple leaves and that the whole complex of vegetative upgrowth

of seed fern ancestors is grosso modo retained in certain woody families of

Angiosperms,

Under this point of view the simple leaf is among Angiosperms a derived

stage. Such reduction should be considered as a manifestation of neoteny

(see p. 116) by which principle is meant that the new form is simplified as

compared with its ancestor at attaining the fertile stage. Neoteny causes ontogeny

to be condensed; it is probably as frequent in plants as it is in animals.

The matter considered in this essay has lingered in my thoughts for many

decades, in fact since I was a student and studied Carl von Naegeli’s ‘Mechanisch-

physiologische Theorie der Abstammungslehre’. I realize very well that it will be

provocative to those thinking in neo-Darwinistic terms.

For these reason I felt it not unnecessary to feed some ideas to the biological

world in honour of Professor Corner as a token of my admiration for his immense

achievement in botany from his studies in the tropics and his admirable attempts

to pour new wine in old vessels of biological theory.

I feel much indebted to my friend and colleague, Prof. Dr. H. Gloor, Geneva,

for improvement of the text.

a

Autonomous Evolution 125

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On Speciation in the Humid Tropics: some new data

by

ANDREY A. FEDOROV

Komarov Botanical Institute, Leningrad

During the author’s travels to Sri Lanka (Ceylon) and to Indonesia and,

particularly, in the course of his examination of herbaria and botanical iconography

pertaining to Dipterocarpaceae (see Foxworthy, 1927, 1932; Van Slooten, 1932,

1940, 1941, 1942, 1952; Symington, 1943; Ashton, 1962, 1964, 1967, 1969) he has

already established many facts elucidating speciation in the humid tropics on the

basis of the Law of Homologous Series in Hereditary Variation discovered as early

as the beginning of this century by N. I. Vavilov (1920, 1922), elaborated by him

somewhat later (1930, 1935) and subsequently by his numerous collaborators and

pupils.

As is well known, Vavilov established this law mainly in the course of his

studies on cultivated plants, his attention being attracted by their infraspecific

diversity. But Vavilov had no opportunity to observe this phenomenon in a

sufficiently large number of species of wild plants, nor those belonging to perfectly

homologous genera.

Vavilov was sure that no homologous series of hereditary variation had been

discovered in our wild holarctic genera and species merely because, in this respect,

they had been extremely poorly studied.

In the Holarctic it is difficult to find homologous variation not only at the

specific level, but at the infraspecific level as well. Many wild species occurring

there appear to be surprisingly homogeneous. The cause of the apparent homo-

geneity is associated with their heterozygosity as has been pointed out by Vavilov

himself (Vavilov, 1936, pp. 78-79) with cross-pollination, with the latent state of

their recessive characters. However, the latent diversity of characters can be made

apparent by means of compulsory self-pollination, or inbreeding. This fact is well

known by all the geneticists and plant breeders.

Besides the actual homogeneity there is a delusive homogeneity. A conviction

is very widespread among taxonomists about the perfect homogeneity of many

widespread species over vast areas. The reason is that many botanists work mainly

with herbarium material. The uniformity of herbarium specimens, sometimes

accumulated in large numbers can be explained by the fact that many collectors

involuntarily discarded specimens inconvenient on account of their dimensions or

some other characteristics and thus made collections of standard specimens suitable

for drying and mounting on standard sheets of herbarium paper.

As I know, tropical herbaria differ in this respect from holarctic ones. It is

difficult to sort out series of standard samples in the tropics, even though the

desire to do it be very keen, since many species, particularly large trees are so

Sparsely scattered in a tropical forest, that sometimes herbaria contain only their

type or isotype specimens, This precludes the possibility of revealing infraspecific

Systems of hereditary forms in these plants by means of sheer observation even if

they actually exist in nature.

There are at least a few genera of plants indigenous to the northern part of

the Holarctic in which homologous series are observed not within species but

127

128 Gardens’ Bulletin, Singapore — X XIX (1976)

among the species of the given genus. Such are the genera Verbascum and Celsia

(Scrophulariaceae) and Astragalus and Oxytropis (Leguminosae). It is true that

here the taxonomic delimitation of these genera is not perfectly reliable, however.

The state of affairs in the humid tropics is very interesting. I venture to assert

that, within the family Dipterocarpaceae. almost all the representatives of which

are confined to tropical rain forests of Southern and South-Eastern Asia, the law

of homologous series is conspicuous in all the genera and numerous species belong-

ing to this family, including the monotypic genus Upuna, the single species of

which, U. borneensis, also exhibits homology, at least in the leaf structure, as do

the species of the other genera of this family.

It should be pointed out that Vavilov anticipated all this on the basis of his

theoretical considerations with respect to plant taxa of almost any rank, having

emphasized the universal significance of the law he had formulated, but practically

he had no opportunity himself to encounter such interesting material for investiga-

tion as the Dipterocarpaceae.

The genetic affinity of the genera of Dipterocarpaceae is so close, that almost

all the characters pertaining to the shape and structure of leaves, fruits and other

organs and parts are subjected to homologous variation except the main generic

characters felicitously designated by Vavilov as “generic radicals”.

It is only the existence of such radicals, sometimes not quite distinct and also

transgressive (e.g. genera Shorea, Hopea, Doona) that made it possible to classify

the Dipterocarpaceae family, comprising a total of up to 580 species, into 15

genera.

Owing to the indistinctness of certain generic radicals (or, more precisely,

unsuccessfully distinguished genera) taxonomists classifying Dipterocarpaceae were

compelled to reduce to synonyms certain taxa described earlier at the rank of

genus. Thus disappeared such generic names as Pachynocarpus, Richetia and some

others.

When I am writing about the family Dipterocarpaceae, I have in mind only its

Asiatic subfamily Dipterocarpoideae comprising the greatest number of genera and

species, leaving aside for the time being the African subfamily Monotoideae (48

species of the genus Monotes and 4 species of the genus Marquesia), since I have

not the necessary material at my disposal. The law of homologous series is manifest

within the Dipterocarpaceae with the utmost distinctness and cogency in the first

place in consequence of the numbers of species in many of its genera (see Ashton,

1964; Willis, 1966).

Shorea ie ba ... 180 Doona bm sain

Hopea (including Balanocarpus) .... 90 Parashorea ... «sb fou

Dipterocarpus rit ... 76 Dryobalanops sf 9

Vatica a4! re ... 76 Cotylelobium 5

Vateria (incl. Stemonoporus) + sneha tls nf CM acme wide a 3

Anisoptera on ... 13 Monoporandra 2

Upuna ... ne De

If all these genera of Dipterocarpaceae were arranged in a table following the

sample of similar tables presented in Vavilov’s works, it would at once become

obvious that with respect to all the characters (studied up to the present time)

species within each genus form homologous series.

The table does not show the combinations of characters of particular species,

but only lists individual characters and their occurrence in the genera. Further-

more, they are only the most conspicuous ones, revealed either from herbarium

material or from drawings published in the botanical literature. Many characters,

Speciation in the tropics 129

such as the leaf pubescence, the details of venation etc., are still to be studied. It

is important to point out, that the characters of many species presented in the

table were observed in isotype specimens a fairly great abundance of which is

available in the Herbarium (LE) of the Komarov Botanical Institute of the

Academy of Sciences of the USSR in Leningrad. The numbers of isotype specimens

found there are 30, 15, 22, 13, 12, 5, 8, 3, 2, 3 and 2 for the genera Shorea,

Hopea, Dipterocarpus, Vatica, Vateria (= Stemonoporus), Anisoptera, Doona,

Parashorea, Dryobalanops, Cotylelobium and Monoporandra respectively. This is

some guarantee against errors in the identification of numerous other specimens

deposited in the Herbarium as ‘ordinary’ specimens and examined in the course of

my investigations.

The table, the principle of composition of which is described here does not,

of course, deal with the infraspecific homologous variation as yet unstudied at all

in the representatives of the Dipterocarpaceae. My purpose was to demonstrate

homologous series of species within genera, which in their turn are also homologous

to the same extent. Thus, I do not merely repeat what has been done by Vavilov,

but, as far as possible, endeavour to develop his theory.

Homologous characters are given in Latin terminology. The best illustrations

of these characters might have been the drawings or photos, but, unfortunately

they would have been too numerous and there would not be enough place for all

of them in the table.

Unfortunately the names of the examined species not indicated are omitted

but I hope I shall be able to add them in the very near future in a separate paper.

Similar to infraspecific systems of the forms of cultivated plants studied by

N. I. Vavilov, the homologous characters in species belonging to the genera of

Dipterocarpaceae exhibit in many cases independence of other characters, but in

approximately 50% of species a rather distinct correlation is observed; for instance,

between the characters of leaves on the one hand and, on the other the characters

of fruits, with respect to their general similarity of appearance in the first place,

and to their equal relative and absolute dimensions as well.

Being perfectly aware of the significance of the law he formulated, Vavilov

quoted the remarkable, indeed prophetic, words of de Candolle (A. de Candolle,

1888, La Phytographie, p. 80) who wrote, that a day will come, when science will

interpret the elements of a species as the elements of a genus, as the

elements of a family, and all these groups will be coordinated according to a

definite uniform system. Vavilov was perfectly justified in his conclusion: ‘This

day has come” (Vavilov, 1936, p. 79).

The tropical family of arborescent plants, Dipterocarpaceae, is a good

illustration for the ideas of Alphonse de Candolle and Nikolay Ivanovich Vavilov.

All the taxonomic ranks of this family follow the law of homologous series that is

common for all plants and, in fact, for all organisms. The genera of the Diptero-

carpaceae are so closely allied to one another, that they can be regarded as initial

species, as it were, evolved up to the generic level.

Thus, it is not only the infraspecific systems of hereditary forms of cereals,

legumes, Cucurbitaceae and other cultivated plants, but also the species of gigantic

tropical trees belonging to the Dipterocarpaceae that form homologous series. As it

is illustrated by the example of this family, the Law of Homologous series in

Hereditary Variation is directly associated not only with the initiation of new forms

within a species as in the case of cultivated plants, where the action of the natural

selection is superseded by artificial selection and where many forms and varieties

of plants therefore have good chances for survival but also with speciation.

__ The obvious fact of the abundance of species characteristic of the genera of

Dipterocarpoideae, particularly, of such genera as Shorea, Hopea, Dipterocarpus

130 Gardens’ Bulletin, Singapore — XX1X (1976)

and Vatica almost confined to the tropical rain forests of Southern and South-

Eastern Asia should be explained.

Earlier I assumed (Fedorov, 1966) and this provoked some criticisms in the

botanical literature (see Van Steenis, 1969, pp. 108-109; Ashton, 1969) that in a

tropical rain forest the abundance and diversity of species within many genera and

families of trees is explained by the fact that there natural selection does not

eliminate indifferent characters; these characters remain in the populations, their

frequency being governed by genetic drift. Of these forms possessing such

characters, those having the rank of species survive. As it becomes clear at present,

the possibility of initiation of such characters is afforded by the law of homologous

series: being indifferent, they are homologous to the corresponding characters that

are useful in certain closely allied forms. Despite the abovementioned criticisms

of my views, I am still convinced, that if the speciation in the humid tropics was

accomplished only by means of natural selection, without participation of genetic

drift, there too, similarly to the northern zone of the Holarctic, each genus of wild

plants would be represented by fragmentary group of species that would not form

any perceptible homologous series.

One of the good examples of parallel (according to my concept, homologous)

series, probably also formed by genotypic factors, within subgenera and other

infrageneric taxa of the tropical genus Ficus having an extremely wide range

(comprising about 900 species) is pointed out by E. J. H. Corner (1959, pp.

106-108), who designated this phenomenon, after Darwin, parallel evolution. Here

the characters pertaining to the form of inflorescences and their position on a shoot

are subjected to parallel (homologous) variation, as well as ramiflory and cauliflory

and also geocarpy. The forms of growth or life forms in the subgenera of the genus

Ficus also exhibit parallel (homologous) variation manifested in all the types

from pachycaul trees to leptocaul trees. Epiphytic species of Ficus occur in at least

three series. Creeping forms occur in five series in various combinations with

epiphytic. Still more diverse are the homologous forms pertaining to the structure

and venation of leaves, as well as to their size, both relative and absolute. Corner

(l.c.) emphasizes that there can be no doubt in the convergent origin of all these

forms, since parallel (homologous) species of different genera differ distinctly

from one another in the structure of flowers, by the characters of which the main

taxonomic subdivisions of the genus Ficus are delimited.

Corner makes an important reservation, that for instance, the case of a parallel

(homologous) appearance of species of the genus Ficus with narrow leaves

resembling the leaves of willow occur in the groups of the genus Ficus indigenous

to different phytogeographical regions (Corner, 1961, p. 108; Corner, 1967, p. 33).

The same phenomenon in different families of tropical plants had already

been mentioned by C. G. G. J. van Steenis (1948-1954, pp. LVII-LVIII).

As yet the mechanism of the origin of homologous series in different genera

and families of plants in the humid tropics is not quite clear. The assumption that

it is to a great extent based on mutagenesis leading to genotypic changes is quite

justified, although, undoubtedly, many specific examples can also be phenotypic.

Since allied species possess homologous characters, it is most probable that the

genes responsible for these characters are also homologous or even identical at

least within the same family. It was Vavilov himself (Vavilov lI.c.) who referred

to the facts of induction of artificial mutations in species of Drosophila that followed

the law of homologous series.

Recombinations resulting from hybridization, serving, like mutations, as it

were as raw material for natural selection, hardly played any significant role in

speciation with respect to tropical trees, since hybrids occur rarely here (see Van

Speciation in the tropics 131

Steenis, 1969, p. 111). Chromosome numbers, for example, in different genera of

the family Dipterocarpaceae, the object of my interest, in many cases prove to be

the same. In most species of the genus Dipterocarpus studied (as yet not many) the

prevailing chromosome number is 2n = 20 (see Fedorov, ed. 1969, p. 262; Moore,

ed. 1973, p. 274).

Corner (1954, pp. 33-34) was the first to assume that selfpollination prevails

in the trees of tropical rain forests. Later I advanced a similar hypothesis (Fedorov,

1966) although I overlooked Corner’s priority. Quite recently, as the result of the

investigations of Bawa (1974), as well as of Bawa and Opler (1975) various types

of pollination became known for both the tropical and temperate regions. By the

way, it was revealed, that many trees apparently having bisexual flowers are

actually dioecious in many cases, since either gynoecium or androecium prove to

be underdeveloped, or their development proves to be asynchronous. Other details

of the “‘reproductive biology” as it is designated by these authors and Ashton

have been elucidated. Ashton quite recently published (Ashton, 1975, p. 109) an

abstract of a paper on the existence, in tropical rain forest trees, of both panmixis

and apomixis. It should be pointed out, that all the details of these phenomena in

Tropics are as yet insufficiently studied by far, but only one fact, but a most the

important one, should be apparently recognized to be beyond doubt: interspecific

hybridization is a very rare event in tropical rain forests.

Nature itself has established many almost insuperable obstacles to spontaneous

hybridization between species of tropical trees which would lead to heterozygosity.

This fact was mentioned in my earlier paper (Fedorov, 1966). The difficulty of

such hybridization is, in the first place, the consequence of non-coincidence of the

time of flowering, particularly, in the equatorial zone where there are no seasons

of the year. This non-coincidence is observed even among individuals belonging

to the same species, let alone those belonging to different species; another obstacle

is the prolonged and irregular period of sterility, sometimes lasting for several

years, then the low population density of many species, up to almost perfect

dissociation of separate individuals of these species, i.e. their spatial isolation, and

also biotic isolation and, in general, the diversity of biological niches.

The survival of a large number of species belonging to the genera of Diptero-

carpaceae and their resistance to the pressure of natural selection can be explained

by the early development of isolation from one another of the most diverse types.

This problem was successfully studied by P. W. Richards (1969, pp. 149-153)

and by F. R. Fosberg, who delivered a paper on this topic at one of the symposia

of the XIth International Botanical Congress held in Seattle (Fosberg, 1969, p. 62).

Th. G. Dobzhansky (1950, pp. 219-221), in his study especially devoted to

the problem of evolution in the tropics, correctly emphasizes, that in the temperate

and in the cold zones such elementary factors as the sufficient or insufficient

quantity of food and the degree of resistance to low winter temperatures played

the most important rdéle in the process of natural selection. In the humid tropics

the interrelations with the environment are more complicated; its requirements are

more refined, while the response of organisms is more diverse and complicated; the

role of the biotic environment is significantly more important, than in temperate

and cold regions.

Polyploidy, apparently, also played a certain role in the speciation in tropical

trees. At least polyploids have been found in some species belonging to the families

Leguminosae, Simaroubaceae, Meliaceae, Anacardiaceae, Sapindaceae, Bombaca-

ceae, Sterculiaceae and to some other families, represented in the flora of tropical

semideciduous forests of Costa Rica (Bawa, 1973, pp. 422-434). However, poly-

ploid series are very rare in these cases.

132 Gardens’ Bulletin, Singapore — XX1X (1976)

The counts of chromosome numbers in species belonging to the genera of

Dipterocarpaceae were commenced only quite recently. Chromosome numbers have

been determined for only thirty species (see Fedorov, ed. 1969, p. 262; Moore,

ed. 1973, p. 274). If it is remembered that this family comprises 580 species, it

would be clear, that any conclusions concerning the rdle of polyploidy in the

evolution of this family would be as yet premature. Nevertheless, the prevailing

chromosome number being 2n = 20 (genus Dipterocarpus), cases have already

been recorded of diverse numbers in certain species of the genus Shorea, where

the chromosome number is 2n = 14 or 28. There are cases when 2n = 12

(Pentacme), while in the genus Dipterocarpus rarely occur species with 2n = 30.

The main ‘x’? numbers in different genera of the family are probably close to

5-7-11.

It is possible to interpret from a new point of view the phenomenon of

convergence, which is very conspicuous and widespread in the trees of a tropical

rain forest. This convergence pertains to the shape of leaves, inflorescences and

other parts of plants belonging to different genera and families, particularly in the

tropical Lauraceae, Annonaceae, Sapotaceae, Fagaceae and many others. This

convergence is adaptive, but probably it is based on the law of homologous series

in hereditary variation as dealt with in this paper.

Genera Dipterocarpacearum

A] 2] 3] 4).4 [6b | Af ting

Homologous

characters

3

oO

OQ,

°o

ae

Folia late-elliptica vix

acuminata, obtusa vel

retusa ca 20 cm. longa

et 15 cm. lata

Dipterocarpus

+, | Vatica

+ | Vateria

Doona

Parashorea

Dryobalanops

Cotylelobium

Pentacme

Monoporandra

4.

a

Praeced. similia, ca

10-15 cm. longa et 5-7

cm. lata

Praeced. similia, ca

5-10 cm. longa et 3-5

cm. lata

Folia oblongo-elliptica

vix acuminata, ca

25-35 cm. longa et

10-15 cm. lata

Praeced. similia, ca}| + | +] +] +

10-15 cm. longa et.

3-7 cm. lata

+

eee

fit

Speciation in the tropics 133

Homologous

characters 2

p.

a

8

7k eh s

_— Q, ——

ro) S| a

o = _—

wa bia | G

oa

Folia late-ovata acumi- +

nata, ca 10-15 cm.

longa et 6-8 cm. lata

Praeced. similia, ca + ier b+ +/+

5-10 cm. longa et 3-7

cm. lata

Folia obovata vix +

acuminata, 10-20 cm.

longa et 5-6 cm. lata

Praeced. similia, ca +

3 cm. longa et 2 cm.

lata

Folia obovata obtusa,

ca 4.5 cm. longa et 3

cm. lata

Folia rotunda obtusa, +

ca 15 cm. longa et lata

Folia rotunda _ vix 2

acuminata, ca 15 cm.

longa et lata

Genera Dipterocarpacearum

N

Ww

>

ae

oo

\o

_

oO

—"

—

—

Ne

Anisoptera

Parashorea

Monoporandra

Vatica

Fa el

Ba |

+ + +

Cee toa |

et ees & | |

See ee BIT

Bie tes Pee | po

Ree et oP | Ss

$5) SE Be

Mei ae

Folia fere rotunda vix

acuminata, ca 3 cm.

longa et 2.8 cm. lata

+

Folia late lanceolata + + | +

acuminata, ca 20 cm.

longa et 5 cm. lata

Praeced. similia, ca 7 oe + +

cm. longa et 4 cm. lata

Folia elliptica apice + | + + > +

caudata, ca 7 cm.

longa et 3 cm. lata

ao

+

134 Gardens’ Bulletin, Singapore — XX1X (1976)

Genera Dipterocarpacearum

Homologous b

characters 3 a 5 s

ee Po ec Be =

bel oO xs o e

§ o ww & ro) fo)

gia] § = | & & | 2). 8.8 0

a a. ~ oO n 3 ° > ~~ r=

Shoe poe «3 | a = | £2 oe

wm im|aA >< & | Oo) Oor eee

ms

+ | Doona

evber TL

oo

ob

+ | Vatica

Praeced. similia, ca 6

cm. longa et 2-3 cm.

lata

Folia late ovata apice

caudata, ca 6 cm.

longa et 2.5-3 cm. lata

Folia oblanceolata ob-

tusa, ca 10-15 cm.

longa et 4.5 cm. lata

Praeced. similia, ca} +

3-5 cm. longa et 1-3

cm. lata

SDs

a[rmvwmme [efel [ele [=| [11

open ae

Sete 9S

25 | Lamina foliorum om-

nino glabra

26 | Lamina foliorum plus- | + +] + +

minusve pilosa, tomen-

tosa vel hirsuta

27 | Fructus magni, ca] + + + + T+

10-15 cm. longi

28 | Fructus 5 Ape ca

5-7 cm. longi

29 mig oa parvi, ca 2-3

cm. longi

30 | Calycis lobi post an-

thesin accrescentes

Calycis lobi abbre-| + | + | + | +

viati, fructus globosi

Speciation in the tropics 135

References

ASHTON P. S. 1962. Some New Dipterocarpaceae from Borneo. Gdns’ Bull.,

Singapore 19: 253-319.

1964. Manual of the Dipterocarp trees of Brunei State. Univ. Press,

Oxford.

———_——— 1967. Taxonomic notes on Bornean Dipterocarpaceae, 3. Gdns’

Bull., Singapore 22: 259-352.

1969. Speciation among tropical forest trees: some deductions in

the light of recent evidence. Biol. J. Linn. Soc. 1: 155-196.

1975. The reproductive biology of some rain forest trees and their

evolution. Abstract of the paper presented at the XII Internat. Botan.

Congress, Leningrad.

BAWA K. S. 1973. Chromosome numbers of tree species of a lowland tropical

community. J. Arnold Arbor. 54: 422-434.

1974. Breeding Systems of the species of a lowland tropical

community. Evolution 28: 85-92.

—— P. A. OPLER. 1975. Dioecism in tropical forest trees. Evolution

29: 167-179.

CORNER E. J. H. 1954. The evolution of tropical forest. In: J. Huxley, A. C.

Hardy, and E. B. Ford (eds.). Evolution as a process. Allen & Unwin,

London.

1961. Evolution. In: A. M. McLeod and L. S. Cobley, Contem-

porary botanical thought. Oliver & Boyd, Edinburgh.

1967. Ficus in the Solomon Islands and its bearing on the post-

Jurassic history of Melanesia. Phil. Trans. R. Soc. Lond. B. 253: 23-159.

DOBZHANSKY, Th. 1950. Evolution in the Tropics. Am. Scient. 38: 209-221.

FEDOROV, An. A. 1966. The Structure of the tropical rain forest and speciation

in the humid tropics. J. Ecol. 54: 1-11.

1969. (Ed.). Chromosome numbers of flowering plants. Leningrad.

FOSBERG, F. R. 1969. The problem of isolation in the lowland tropical rain

forest. Abstracts of the papers presented at the XI Intern. Botan. Congress,

Seattle.

FOXWORTHY, F. W. 1927. Commercial Timber Trees of the Malay Peninsula.

Malayan Forest Records 3.

1932. Dipterocarpaceae of the Malay Peninsula. Malayan Forest

Records 10.

MOORE, R. J. 1973. (Ed.). Index to plant chromosome numbers 1967-1971.

1.B.P.T., Utrecht.

RICHARDS, P. W. 1969. Speciation in the tropical rain forest and the concept of the

niche. Biol. J. Linn. Soc. 1: 149-153.

SLOOTEN, D. F. Van 1932, The Dipterocarpaceae of the Dutch East Indies, 6.

The genus Dryobalanops. Bull. Jard. bot. Buitenzorg Ser. 3, 12: 1-45.

136 Gardens’ Bulletin, Singapore — XX1X (1976)

1940-1949. Sertulum Dipterocarpacearum Malayensium I, II,

Il, 1V. Bull. Jard. bot. Buitenzorg, Ser. 3, 16: 430-454 (1940); Ibid. 17: 96-138

(1941); Ibid., 17: 220-225 (1942); Ibid. 18: 229-269 (1949).

(1952). Sertulum Dipterocarpacearum Malayensium 5. Rein-

wardtia, 2: 1-68.

STEENIS, C. G. G. J. Van 1948-1954. Flora Malesiana, Ser. 1, 4.

1969. Plant speciation in Malesia, with special reference to the theory

of non-adaptive saltatory evolution. Biol. J. Linn. Soc. 1: 97-133.

SYMINGTON, C. F. 1943. Foresters’ manual of Dipterocarps. Malayan Forest

Records 16.

VAVILOV, N. I. 1920-1935. The law of homologous series in variation (in

Russian). Saratov (1920). Idem in J. Genet. 12 (1) (1922). Idem in Theoretical

basis of plant selection, 1 (1) (in Russian). Revised and enlarged edition by

the author (1935).

1930. Linnean species as a system (in Russian). Trudy po

prikladoni botanike, genetike i selektsii 26 (3).

WILLIS J. C. 1966. A Dictionary of the Flowering Plants and Ferns, 7th edition.

Revised by H. K. Airy Shaw. Univ. Press, Cambridge.

The Morphology and Systematics of Pandanus Today

(Pandanaceae)*

by

BENJAMIN C. STONE

Department of Botany, University of Malaya, Kuala Lumpur,

Malaysia

Summary

More than 500 species of Pandanus are now known, and 70% of these have been

described since 1900, nearly half since 1939, and new ones are being discovered. Many

obstacles have prevented the completion of a monograph (dioecism, large structures, remote

locales) but perhaps the most serious has been ignorance of morphology and morphogenesis.

Studies of these are thus of critical importance. Micromorphological-anatomical data and

cytotaxonomic data have recently become available, permitting data integration not previously

possible, This has resulted in a new detailed infrageneric classification which can contribute

to understanding of the phylogeny. This classification recognizes 8 subgenera, 62 sections,

and 22 subsections covering 468 species and numerous synonyms. Chromosome numbers

are 2n = 60 (1 species of Pandanus, P. spiralis R. Br., has 2n = c. 120). Remarkable stomate

variability is tied almost exclusively to systematic relationship.

I. Introduction

The Pandanaceae is a family now generally conceded to be the sole member

of the Order Pandanales (Monocotyledonae). The Typhaceae and Sparganiaceae

(formerly included) are not closely related to Pandanaceae and form a distinct

Order Typhales.

Although known to botanists for some three centuries, the Pandanaceae

accounted for in Warburg’s Monograph (1900) were 180 species of Pandanus,

about fifty spp. of Freycinetia, and one of Sararanga. No further genera have been

discovered but the number of known species has grown and there are about 700

binomials currently, The foremost students of the family since 1900 have been

Martelli, Merrill, Pichi-Sermolli, and St. John. More vigorous exploration in the

Palaeotropics has vastly increased the available study material; much fieldwork

has significantly augmented the herbarium study.

But many problems remain which impede full understanding of the family,

in particular the largest genus Pandanus. With over 500 species, Pandanus posed

severe difficulties in establishing interspecific relationships and an infrageneric

classification.

II. Traditional taxonomic characters and unresolved problems

The salient features of previous taxonomic work on Pandanus was the virtually

complete dependency on the characters of the ripe fruits. Nearly all described

species and infrageneric taxa were based on fruit-characters. Since all the plants

are dioecious, this resulted in almost sure ignorance of the males. Staminate

specimens could seldom be identified. The problem was brought about by the

* Based on a paper read at the International Botanical Congress at Leningrad, 1975

(Abstract in [A. Takhtajan (Ed.),] Abstracts of the papers presented at the XII International

Botanical Congress July 3-10, 1975 (1):100).

137

138 Gardens’ Bulletin, Singapore — X XIX (1976)

rarity of good staminate material in herbaria (in turn the result of the ephemeral

nature of the male flowers in nature), and the difficulty of correlating staminate

and pistillate specimens both in the field and in the herbarium. Sterile material

was impossible to identify.

Clearly, a taxonomic system which relied entirely on fruit characters, in a

genus of strictly dioecious plants, was inadequate both for practical identification

and for studies of phylogeny. For the purposes of most botanists, identification of

Pandanus was either uncertain or impossible.

In view of this situation it was obviously desirable to seek taxonomic

characters which were shared by both staminate and pistillate plants, i.e. vegetative

characters, including those revealed by micromorphology and anatomy. During the

past two decades our efforts have been turned to solutions to the problems

described. The main features of the work, carried out by various persons at several

institutions, are described below.

III. New Investigations and their Results

A. Gross Morphology. — In general three main aspects have been developed:

(1) Fuller quantification of characters, particularly of vegetative structures.

Example: the mainly qualitative descriptions of leaves have been replaced by

analyses giving data such as tooth (prickle) size and spacing, vein number,

variation in leaf length and width, etc. (2) The discovery and correlation of

staminate with the pistillate-plants of the same species, and full descriptions and

taxonomic use of staminate characters. Example: field work yielding field know-

ledge of population structure, phenology, breeding behaviour, and ecological

distribution, has often led to correct correlation of sexes. Pollen characters have

been studied only to a limited extent but may throw some light on species relation-

ships, as has been demonstrated in a few cases (e.g. Pandanus sigmoideus St. John).

(3) Habit and morphogenetic field characters supplementing the existing herbarium

knowledge, made possible by augmented collection techniques, photography, field

analysis of individuals in various growth stages, etc.

B. Morphogenesis and architecture (habit). — Work in this field has revealed

the changes which occur in ontogeny from seedling to adult and has necessitated

the recognition of ‘juvenile’ states which may differ radically from adult states,

even in the same species. Progressive changes in anatomical features are correlated

with the external changes in size and form, and indicate that anatomical characters

must be derived from adult structures for reliable use in taxonomy and classifica-

tion. Habit classification has become possible through the analysis of growth phases

and it is now clear that adult form can be a major taxonomic character, This is

especially clear in the case of Pandanus Sect. Acanthostyla, of Madagascar, a group

of species which share the ‘coniferoid’ habit. Further studies of habit have been

carried out by Guillaumet (1973), based on the more general work of Hallé and

Oldemann (1970; 1975). The ‘lateral’ inflorescences of Sect. Cauliflora and Sect.

Tridens are similar examples of habit specialization which offer taxonomic utility.

C. Anatomy. — Anatomical studies of Pandanus date back at least as far as

Solla (1887) but their significance in relation to taxonomy was not appreciated.

With resumption of such studies by Tomlinson (1965), Kam (1969), Gineis

(1969), and now especially by K. L. Huynh (1974), the correlation between —

anatomical features and other characters became clear. It is now evident that, in —

general, anatomical characters form a fairly reliable basis for the discrimination

of species-groups, and furthermore, it has become clear that these species-groups

usually correspond to sections. Occasionally, single species stand out on anatomical

grounds, and there are_some cases in which anatomy seems not to offer clear

support to sectional discrimination, but in a great majority of cases the anatomical

data has had a beneficial and significant effect on infrageneric taxonomy. The

Pandanus, Morphology and Systematics 139

anatomical characters used have been chiefly from the leaves, and as demonstrated

by Kam, only fully adult organs could be compared. Within these limits the

appearance of particular anatomical features seems sufficiently constant and in rare

cases may be diagnostic.

The tissues which furnish the characters are especially the epidermis, the

stomatal complex, the hypodermis, the crystal cells, the chlorenchymatous layers,

the fibrous strands and the vascular bundles. In particular, the range of variation

in the epidermal tissues (including the stomata) proves to be of very great value.

In order to rationalize the variation found, Tomlinson founded a classification of

stomatal types, based on progressive complexity. This system was used by Kam

and others and shown to correlate well with sectional taxa. More recently (1974)

the classification has been refined by Huynh, who defines seven stomatal types and

in turn finds a remarkably good correspondence with the infrageneric classification

being developed by Stone. In fact, the anatomical data became the test by which

the infrageneric taxa could be evaluated; where serious disharmony in anatomical

features was revealed within a section, it was usually found to indicate an artificial

classification which could be remedied by remodeling the Section e.g. by dividing

it, or by reassigning some of its supposed component species to other sections. The

anatomical data thus often revealed a ‘hidden’ flaw in previous taxonomic systems.

Examples of the variety of stomatal-complex structures revealed that all retain

the basic tetracytic pattern but vary in relation to the production of elaborations,

which are commonly in the form of papilliform protuberances arising from the

cells of the stomatal complex and of the epidermis proper. The simplest arrange-

ment is an essentially flat epidermis, the stomate flush with the surface, the

epidermal cells merely forming a tessellate pattern. On adaxial surfaces of leaves

the epidermis may be zoned or not; zonation involves differing cell shape and

presence or absence of stomata in alternating bands corresponding to veins and

inter-vein spaces. Such zonation produces a further character that may be used in

addition to the stomatal type. Increasingly complex stomatal types develop as

various cells produce papillae, and the entire epidermal surface or all the relevant

zonal bands, may thus become papilliferous. The papillae themselves may be

limited to one per cell, or may occur in sets on a cell: they may be of various

simple forms or in more elaborate forms such as forked or dendritic. Papillae may

form a stockade around the stomate, or around a group of stomata. The stomata

may become considerably sunken below the general level of the epidermis.

The hypodermis may be of one or more cellular layers and may include

crystal cells in various patterns and in various orientations. The crystals may be

trhomboidal or occur as raphides; the former usually are more common in leaves,

and may exist in two distinct forms, and in various sizes. The patterns of distribu-

tion of the crystal cells may be of some taxonomic value.

The chlorenchyma may be continuous or interrupted, and this distinction

sometimes has a taxonomic significance.

The association of fibrous strands with particular tissues may also be constant

enough for taxonomic use.

A considerable number of other anatomical features occur, some of which

may on occasion have a taxonomic use, e.g. stomatal size and stomatal index, the

occurrence of papillate stockades, etc.

Wherever data from anatomy conflicts considerably with a traditionally

established taxonomic group it is likely that the latter is heterogenous and a

re-evaluation of all the constituent species and their characteristics is in order. By

application of this method the infrageneric classification can be established on a

broader, firmer basis than otherwise possible. The concrete result of such applica-

tion has been put forward as a new infrageneric scheme (Stone, 1974). In this

system, eight subgenera are established (these are further grouped into four

140 Gardens’ Bulletin, Singapore — X XIX (1976)

unnamed groups of 3, 2, 2 and 1 subgenera respectively). Each subgenus consists

of one or more (up to sixteen) sections. Altogether, 62 sections are recognized.

These in turn are in some cases divided into subsections, There are 468 species

accounted for, i.e. probably 90% of the total (the remainder are excluded

temporarily as either probable synonyms or because data is quite insufficient for

placement).

D. Cytology. — The predominant chromosome number found in Pandanus

is 60 (somatic): but one tetraploid (P. spiralis R. Br.) is known. However,

only some 30 species have been ‘counted’. The foremost workers in this field

have been Tyjio, Harada, Cheah (1969) and the work is being continued by Jong.

The only discovery of some taxonomic significance is that in some cultivars (e.g.

P. spurius Miq.) some cells at least may be aneuploid (with such numbers as 59

or 61 chromosomes). So far however, there is no significant input from chromosome

studies, but the work has probably not progressed far enough to be sure that this

will remain true. It is at least potentially interesting that the one case of tetraploidy

occurs at the margin of the generic distribution (Northern Territory, Australia)

where it seems to be the case that habitat and climatic conditions are marginal.

The karyotype analysis by Cheah shows that the chromosomes are very small.

There may be 0-4 pairs of SAT-chromosomes, and many are short rods which are

hardly discriminable,

E. Embryology. — Pandanus is peculiar in that the mature embryo sac in

the few species so far studied, has a condition of supernumerary nuclei (over and

above the usual eight): these nuclei, as was shown by Fagerlind (1940), migrate

in from the surrounding tissue at a late stage. Recently this has been reconfirmed

in two Malayan species (Cheah and Stone, 1975). The other genera of the family

do not appear to show this phenomenon. The significance, if any, to taxonomy,

has yet to be discovered. However, circumstantial evidence for a few species

indicates that reproduction may be apomictic: it is conceivable that this is related

to the ‘nuclear migration’ as first noticed by Campbell and demonstrated by

Fagerlind, but this remains to be investigated.

F. Palynology. — The pollen morphology has yet to be investigated in detail.

Present evidence suggests that some variation exists and thus some taxonomic

information may arise from studies of pollen. It is hoped to investigate this with

the Scanning-Electron Microscope now available in the University of Malaya.

IV. Synopsis of the infrageneric taxa of Pandanus'

Group 1

Subgenus 1. Rykia

Sections:

(1) Rykia (with subsec- (2) Asterodontia (7) Kaida

tions Rykia, Bidens, (3) Hombronia

Malaya, Multispina, (4) Mydiophylla

Calcicola, Atroden- (5) Rykiopsis

tata, Gressittia) (6) Solmsia

Subgenus 2. Lophostigma

Sections:

(1) Lophostigma (7) Perrya (13) Bernardia

(2) Megastigma (8) Cauliflora (14) Asterostigma

(3) Karuka (9) Barrotia (15) Tridens

(4) Maysops (10) Liniobtutus (16) Cheilostigma

(5) Metamaysops - (11) Brongniartia

(6) Paralophostigma (12) Veillonia

1. See Stone (1974) for bibliographic citations.

Pandanus, Morphology and Systematics

Subgenus 3. Kurzia

Sections:

(1) Kurzia

(2) Microstigma

(3) Jeanneretia

(4) Pulvinistigma

Subgenus 4. Vinsonia

Sections:

(1) Vinsonia

(2) Barklya

(3) Mammillarisia

(4) Dauphinensia

(5) Stephanostigma

141

(5) Curvifolia

(6) Involuta

(7) Marginata

(8) Cristata

(9) Kanehiraea

(10) Utilissima

Group 2

(6) Heterostigma (9) Acanthostyla

(7) Souleyetia with (10) Rykiella

subsections Souleyetia (11) Lonchostigma

and Sussea (12) Platyphylla

(8) Foullioya (13) Eydouxia

Subgenus 5. Martellidendron

Sections:

(1) Martellidendron

Subgenus 6. Pandanus

Sections:

(1) Pandanus, with Sub-

sections Pandanus,

Austrokeura, and

Insulanus

(2) Fagerlindia

(3) Elmeria

(4) Athrostigma

Subgenus 7. Coronata

Sections:

(1) Coronata

Subgenus 8. Acrostigma

Sections:

(1) Acrostigma, with

Subsections

Acrostigma,

Scabridi,

Dimissistyli,

Ornati,

Y. Future work needed.

(2) Seychellea

Group 3

(5) Intraobtutus

(6) Australibrassia

(7) Semikeura with

Subsections

Semikeura and

Elaphrocarpus

Excavata

(9) Megakeura

(8)

Group 4

Glaucophyllae,

Parvi,

Papilionati,

Alticolae, and

Pumili

(2) Fusiforma

(3) Pseudacrostigma

(4) Epiphytica

A. Functional significance of micromorphological-anatomical characters: The

great variation in anatomical structure which correlates so well with classification,

seems so far to resist an ecological or physiological explanation. For example, the

more elaborate stomatal types (five in Tomlinson’s, six or seven in Huyhn’s)

142 Gardens’ Bulletin, Singapore — X XIX (1976)

suggest xeromorphy. Nonetheless, various species of Pandanus which are taxono-

mically unrelated and which have very different stomatal types, may occur

sympatrically in exactly the same microhabitat, i.e. fresh-water swamps.

B. More precise developmental studies to determine the basis of different

habit categories, as well as to provide a means to compare ontogeny in pandans

with that in other plants.

C. Further cytological studies to determine if other examples of polyploidy

exist, whether they correlate with classification and/or habitat, and whether they

tend to cluster at the margin of the generic distribution as is apparently the case

and would be expected theoretically on the basis of the evolutionary studies of

e.g. Stebbins.

D. Palynological work as a basic survey and to correlate with taxonomy and

with fossils, particularly to see whether palynomorphic form genera such as

Pandaniidites can be in fact accepted as pandanaceous.

E. Distributional analysis as a partial basis of phylogenetic interpretation.

References

CHEAH, C. H. 1969. M.Sc. thesis, University of Malaya.

———— 1973. Chromosome studies of Pandanus. Bot. Jahrb. Syst. 93:

498-529.

——— & B. C. STONE. 1975. Embryo sac and microsporangium

development in Pandanus. Phytomorphology 25: 228-238.

FAGERLIND, F. 1940. Stempelbau und Embryosackentwicklung bei einigen

Pandanazeen, Annls Jard. bot. Buitenz. 49: 55-78.

GINEIS, C. 1969. Etude anatomique de la plantule de Pandanus sp. Bull. Inst.

Fr. d’ Afr. noir 31 A, 2: 325-339.

GUILLAUMET, J.-L. 1973. Formes et development des ‘Pandanus’ Malgaches.

Webbia 28: 495-519, 6 figs., 10 pls.

HALLE F. & R. A. A. OLDEMAN. 1970. Essai sur Il architecture et la

dynamique de croissance des arbres tropicaux. Masson & Co., Paris.

1975. Essay on the Architecture and Growth Dynamics of Tropical

Trees. English translation by B. C. Stone. University of Malaya Press, Kuala

Lumpur,

HUYNH, K. -L. 1974. La morphologie microscopique de la feuille et la taxonomie

du genre Pandanus. Bot. Jahrb. Syst. 94: 190-256.

KAM, Y. K. 1969. M.Sc. thesis, University of Malaya.

1971. Morphological studies in Pandanaceae III. Comparative

systematic foliar anatomy of Malayan Pandanus. Bot. J. Linn. Soc. 64:

315-351.

& B. C. STONE. 1970. Morphological studies in Pandanaceae IV.

Stomate structure in some Mascarene and Madagascar Pandanus and its

meaning for infrageneric taxonomy. Adansonia n.s. 10: 214-246. se

SOLLA, R. F. 1884. Contribuzione allo studio degli stomi delle Pandanee. Nuovo —

G. bot. ital. 16: 172-182. |

STONE, B. C. 1974. Towards an improved infrageneric classification in Pandanus

(Pandanaceae). Bot. Jahrb. Syst. 94: 459-540.

TOMLINSON, P. B. 1965. A study of stomatal structure in Pandanaceae. Pacif.

Sci. 19: 38-54, _.

WARBURG, O. 1900. Pandanaceae, in A. Engler, Das Pflanzenreich, 3, IV.

9: 1-97, Engelmann, Leipzig.

Ternstroemia corneri (Theaceae)

by

HsuAN KENG

Department of Botany, University of Singapore

In preparing a systematic account of the Malayan Theaceae for volume 3 of

the Tree Flora of Malaya, I came across an obviously undescribed species of Tern-

stroemia from southern Johore. It is represented by several specimens collected

by Professor E. J. H. Corner and others, all deposited at the Herbarium of the

Botanic Gardens, Singapore, of which one (Corner SFN 27840) was sent to Kew

as early as 1935 for identification and returned with an annotation sheet stating

that it was “‘Not matched in Kew’’, signed by Mr. Fisher in 1936. Its large, obovate

or oblanceolate leaves and ellipsoid fruits with a pointed apex are so characteristic

that it can be readily differentiated from other large-fruited Ternstroemia species

of Malaya and indeed those of the rest of the Malaysian region. The new species,

dedicated to Professor Corner, is described below.

Ternstroemia corneri H. Keng, sp. nov.

Arbor 12-20 metralis, ramulis teretibus. Folia coriacea, auguste obovata vel

oblanceolata, 20-28 cm longa, 7-8.5 cm lata, apice rotundata vel mucronata, basi

longa attenuata, margine integerrima, nervis 13-15 paribus; petiolis circa 1 cm

longis, incrassatis. Flores solitarii, proxime positi, pedicellis 2—2.5 cm_longis,

bracteolis 2, suboppositis, lineo-lanceolatis, 5 mm longis, sepala 5-6, obovato-

rotundata, 5-6 mm longa, petala 5—6, oblongo-obovata, 8-10 mm longa; stamina

numerosa (circa 80), 5-7 mm longa, ovarium conicum, 2-4 mm longum, 2-loculare,

loculis 2 plusve ovulatis. Fructus ellipsoideus vel auguste ellipsoideus, 4.5-5 cm

longus et 2—2.5 cm diametro, seminibus 2-4.

Small to medium-sized tree, 12-20 m tall. Bark greyish, no stilt roots or

buttresses. Branches and branchlets terete. Leaves 3-4 in a false whorl, coriaceous

or thin coriaceous, narrowly obovate or oblanceolate, 20-28 x 7-8.5 cm; lateral

veins 13-15 pairs; apex rounded or abruptly and bluntly mucronate; base long-

attenuate; petiole 1 cm long, stout. Flowers solitary, in axils of fallen leaves,

2-2.5 cm across if fully expanded, peduncles 2-2.5 (—3) cm long; bracteoles 2, sub-

opposite, a short distance below the calyx; sepals 5-6, obovate-rounded, 5-6 mm

long; petals 5-6, oblong-obovate, 8-10 mm long; stamens about 80, in 3-4 series,

the connective produced and pointed; ovary conical, 2-4 mm long, 2-loculate, with

2 ovules per locule, the style 2-forked. Fruit baccate, ovoid or narrowly ovoid,

4.5-5 cm long, 2—2.5 cm in diameter, seeds 2-4, ellipsoid, flattened.

Known only from southern Johore, Peninsular Malaysia, in lowland swamp

forests.

Specimens examined: Johore, Sungei Berassau, Mawai-Jemuluang Road,

Corner SFN 28740 (Type) (in swamp forest), 6 February 1935; Sungei Sedili,

Corner s.n. in March 1932 (a tree, up to 50 feet); Mawai, Corner SFN 30888 (60

feet, leathery leaves, yellowish green beneath); Sungei Kayu, Kiah SFN 32158;

Sungei Kayu, Mawai-Jemuluang Road, Corner SFN 32245; Mawai, Nagadiman

SFN 34736; Sungei Gambut, Corner SFN 36815 [all SING!].

143

144 Gardens’ Bulletin, Singapore — XX1X (1976)

A simple dichotomous key to the four Peninsular Malaysian Ternstroemia

species with larger flowers (over 1.5 cm across) and larger fruit (over 2 cm long)

follows:

1. Normal leaves over 20 cm long; mature fruit distinctly ellipsoid and attenuate

toward both ends, over 4.5 cm Jong ...............ccceeeee eee eees T. corneri H. Keng

1. Normal leaves less than 15 cm long; mature fruit rounded or ovoid, less than

3.5 cm long

2. Flower (and fruit) stalk slender, 3.5-4 cm long; leaves elliptic obovate,

12-18 x.6-8 CM) i siaiventionitn.- pe a eee T. penangiana Choisy

2. Flower (and fruit) stalk stout, 1-1.5 (-2) cm long,

3. Bracteoles immediately below and clasping the calyx; mature fruit

ovoid-rounded, 3-3.5 x 2.5-3 cm; leaves elliptic to narrowly elliptic,

8-11 x0235-5.5. €m \2.208:5). aad. ZW. Se T. bancana Miq.

3. Bracteoles a short distance away and free from the calyx; mature fruit

rounded, 2.5-2.75 cm across; leaves narrowly elliptic, 12-16 x 3.5-5

os Pert: eer eters Peet Firs ce rhe oe po T. wallichiana Engler

I am grateful to the Director of the Botanic Gardens, Singapore, for the

herbarium and library facilities kindly provided and to Mr. D. Teow for the

photographs reproduced in this paper.

Facing plate: Ternstroemia corneri H. Keng

A branch with unfolded flowers (type, eres SFN 28740). Upper inset: fruits cut into

halves showing the seeds (Ngadiman SFN 34736); lower inset: dissected flowers(type).

All scales in cm.

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Thelypteridaceae Allied to Phegopteris in Malaya

by

R. E. HOLTTUM

Royal Botanic Gardens, Kew

Summary

Following the revised scheme of genera in the family Thelypteridaceae proposed by the

author in 1971, a revised account is here given of the genera Macrothelypteris, Pseudophego-

pteris and Metathelypteris in Malaya; these three genera, together with Phegopteris (sensu

Ching 1963) appear to form a natural group. Some corrections to the nomenclature of the

author’s book Ferns of Malaya (1955) are made, with revised descriptions where necessary,

and the addition of two species Metathelypteris decipiens (Clarke) Ching and M. flaccida (B1.)

Ching, not previously recorded for Malaya.

In my book on the ferns of Malaya (1955) I described 46 species of the family

Thelypteridaceae, but (as stated on p. 236) no natural delimitation of genera had

then been devised; those adopted were genera of convenience. It was clear to me

that much more detailed observation of plants throughout the oriental tropics was

necessary before a better arrangement of genera could be found. Subsequently

R. C. Ching (1963) and K. Iwatsuki (1963-65) proposed new systems of classifica-

tion, but both were mainly based on species of mainland Asia, whereas the family

is far more diversified in the Malayan region and the Pacific. For the past eight

years I have devoted most of my time and thought to a study of the family through-

out the Old World, including Africa, with a glance also at the New World where

A. R. Smith of Berkeley is attempting a similar survey. In 1971 I arrived at a new

system of genera in the Old World, based on Ching’s scheme but with considerable

extensions. Since then I have prepared a series of monographs covering all species

of individual genera; the series is not yet complete.

My present estimate is that Malaya has at least 54 species belonging to the

family; this is about 10% of the total number of species in the Old World, with

representatives of most of the genera; most of the missing genera have their main

distribution in mainland Asia, but one of them is Amauropelta which is mainly

American and extends across Africa to the Mascarene Islands.

The object of the present paper is to give a revised account of the Malayan

species of a small group of genera which are distinguished by the following com-

bination of characters which was first recognized by Ching: midrib of pinnae

prominent but not grooved on the upper surface, and veins not reaching the margin.

They also agree in having sori mainly exindusiate, and all genera except Phegopteris

have some species with amply bipinnate fronds; such fronds do not occur in other

genera of the family. I judge that the four genera form a natural group; if anyone

wished to unite them, they would collectively bear the generic name Phegopteris

(which in the strict sense of Ching does not occur in Malaya), but I prefer to

maintain them as separate genera. They differ cytologically as follows: Phegopteris

n = 30; Macrothelypteris and Pseudophegopteris n = 31; Metathelypteris n = 35.

These numbers are based on several counts of plants from different sources, and of

more than one species, in each case. Thus Metathelypteris has the same chromo-

some number as Thelypteris s.str., but the two groups differ in many ways and are

certainly not closely related. Phegopteris has three species, two of them widely

distributed in north temperate latitudes, one in southern China, extending to Tonkin

145

146 Gardens’ Bulletin, Singapore — XX1X (1976)

and Taiwan, with only one Malesian record, in Celebes; I found it to be easily

maintained in cultivation at Penang, but it did not propagate itself from spores.

The name Phegopteris derives from Polypodium phegopteris Linn. It was first

used as a generic name to distinguish terrestrial ferns which have exindusiate sori

resembling those of Polypodium, and was used in the 19th century to cover various

different groups of such ferns. The present limitation of the genus is due to Ching

(1963: 312). Its distinctive characters are: stipe-scales with marginal acicular hairs

but no such hairs on the surface; fronds simply pinnate, pinnae connected by a

wing along the rachis, the wing forming semicircular lobes between pinnae.

In the following statement I have not attempted to give a full synonymy for

each species, but I do give the following in all cases: (a) the basionym; (b) the name

used in my book of 1955; (c) names used in conjunction with previous descriptions;

(d) the correct name in Thelypteris, if such has been published. A full synonymy

for Pseudophegopteris and Macrothelypteris will be found in my paper of 1969

cited below; it will be given for Metathelypteris when I prepare a monograph.

KEY TO THE GENERA IN MALAYA

Fronds simply pinnate; sori distinctly indusiate ..................... 1. Metathelypteris

Fronds mostly bipinnate; sori exindusiate or with very small indusia:

Slender spreading acicular hairs consisting of several cells, abundant on lower

surface of axes of frond; spores with a very fine raised reticulum not distinguish-

able ‘with’ light ‘micrOscope’ soc dak we uatec tok sc cores tose eee 2. Macrothelypteris

Hairs on lower surface all unicellular; spores with a slightly raised surface reticulum

of: rather large: meshes.iu.2 07. hand. bas oad am te dor 3. Pseudophegopteris

1. Metathelypteris Ching 1963: 304. Holttum 1971: 26

Rhizome short, suberect. Fronds simply pinnate with deeply lobed pinnae (in

two non-Malayan species bipinnate); veins often forked, not reaching margin; hairs

on lower surface acicular or capitate, always unicellular; sori indusiate; no hairs or

glands on body of sporangia.

Distribution: about 14 species, widely distributed but few of them anywhere

abundant; San Thomé and Fernando Po; Madagascar; Ceylon; N.E. India to China

and Japan; throughout Malesia on mountains; Solomon Islands.

Specimens from the islands of the Gulf of Guinea have been identified with

the Madagascan M. fragilis (Bak.) Holtt. but may represent a distinct species. No

specimens have been reported from Madagascar since the original specimen, a

single frond, reached Kew in 1877. Another specimen, still undescribed and possibly

originating from Nigeria, is the only evidence that plants of this genus now exist

in mainland Africa. Only one species of the genus was described in Holttum 1955;

two more are here added.

KEY TO THE MALAYAN SPECIES

Lobes of at least the lower pinnae lobed half-way towards costules or more deeply

tre yine magne nae sagen’ Heine <opeieide nienmuiice~ Tarsxismeuunaame tana nan nen 1. M flaccida

Lobes of pinnae entire or crenate:

Pinna-lobes (except basal acroscopic lobe) entire; pinnae commonly to 6 x 2 cm;

veins often simple in smaller pinna-lobes ..............s0+cseeeeeeeeees 2. M. decipiens

Pinna-lobes of large pinnae crenate; pinnae commonly larger; almost all veins

POT ooo occ cncceecens cence ee epee eeswisseveasipnayuniinellig ie Uns simnnIeInnnn 3. M. dayi

T hely pteridaceae 147

1. Metathelypteris flaccida (BI.) Ching 1963: 306.

Basionym: Aspidium flaccidum Bl., Enum. Pl. Jav. (1828) 161. Racib. Fl. Btzg 1

(1898) 176.

Synonyms: JLastrea flaccida Moore, Ind. Fil. (1858) 92. Bedd. Ferns

S. India (1864) t.250; Handbook (1883) 244. — Dryopteris flaccida (Bl.) O. Kuntze,

Rev. Gen. Pl. 2 (1891) 812. v.A.v.R., Handb. Mal. Ferns (1908) 195. — Thelypteris

flaccida (Bl.) Ching, Bull. Fan Mem. Inst. Biol. 6 (1936) 336.

Rhizome short, erect. Stipes to 25 cm or more long, pale, hairy in the groove;

basal scales 3-4 mm long. Lamina 25 cm or more long, with rather widely-spaced

subopposite pinnae, to 10 pairs, thin; basal pinnae narrowed towards base on basi-

scopic side. Largest pinnae of Malayan specimens 10 x 2.5 cm, acuminate, lobed

almost to the costa; largest lobes lobed 4 way to costule or more deeply; costules

to 4 mm apart; veins pinnate in the larger lobules of pinna-lobes, distal veins

forked; lower surface of rachis, costae, costules, veins and surface of lamina bearing

slender pale erect acicular hairs to } mm long; upper surface of costules and veins

bearing scattered hairs as those on costa. Sori 1-3 in each lobule of a pinna-lobe,

small; indusia thin with short acicular hairs.

Distribution: West Java (type); Sumatra (?); Malaya; Ceylon & S. India; N.E.

India to West China.

In 1969 I found plants of this species on sheltered earth banks by a road at

5000 ft near Brinchang, Cameron Highlands; specimens were also collected some-

what earlier by Abdul Samat bin Ali (no. 363) on Maxwell’s Hill, Perak. The

Malayan specimens are all rather small and have shorter hairs on the lower surface

than those from Java and from N.E. India. Prof. Manton found that in Ceylon

the species occurs in both diploid and tetraploid forms (Phil. Trans. R. Soc. B,

238:137. 1954). Herbarium specimens from Ceylon at Kew can be separated into

those with longer and with shorter, less abundant hairs on lower surface; the

Cameron Highlands specimens correspond with the latter. It seems likely that this

species will spread in northern Malaya as clearing provides suitable habitats.

2. Metathelypteris decipiens (Clarke) Ching 1963: 306.

Basionym: Nephrodium gracilescens (Bl.) Hook. var. decipiens Clarke, Trans.

Linn. Soc. Il, Bot. 1 (1880) 514, t.65, fig. 2.

Synonyms: Lastrea gracilescens var. decipiens Bedd., Handb. Suppl. (1892) 51. —

Thelypteris decipiens Ching, Bull. Fan Mem. Inst. Biol. 6 (1936) 335.

Rhizome short-creeping or suberect with fronds closely tufted at its apex.

Stipe 15-25 cm long, pale except for darkened base, very-short-hairy; scales narrow,

2 mm long, bearing short hairs. Lamina to 30 cm long, with about 12 pairs of free

pinnae; basal pinnae sometimes a little reduced, often narrowed at the base on

basiscopic side; texture thin. Largest pinnae on Indian specimens 9 X 2.5 cm,

commonly 6 x 2 cm, on Malayan specimen 5 x 1.3 cm, short-acuminate with

upcurved tip, lobed almost to costa; basal acroscopic lobe often enlarged and

crenate, other lobes entire, slightly oblique, hardly falcate; costules to 3} mm apart;

veins to 6 pairs, those in acroscopic basal lobes mostly forked, in other lobes mostly

simple; lower surface of rachis, costae and costules bearing scattered short hairs,

also short brown linear scales; upper surface of costae densely hairy, scattered

similar hairs on costules and veins. Sori medial or a little supramedial; indusium

small, pale, with minute capitate hairs.

Distribution: Darjeeling district; Khasia Hills in Assam; in Malaya only found

once on rocks in opening of mossy forest, by waterfall, Gunong Batu Brinchang,

6000 ft (Molesworth Allen 5005).

148 Gardens’ Bulletin, Singapore — XX1X (1976)

This species is very near M. gracilescens (Bl.) Ching, differing in broader

pinna-lobes of the largest fronds, with acroscopic basal lobes enlarged and crenate,

and in having some veins forked in the larger pinna-lobes. The Malayan plant

matches specimens from the Khasia Hills very closely; it is not mentioned in the

appendix to the second edition of my book. M. gracilescens (type species of the

genus) has a wide distribution on mountains in the Malayan region (Sumatra, Java,

Borneo, Philippines, New Guinea) also Taiwan and southern Japan; it has not yet

been found in Malaya.

3. Méetathelypteris dayi (Bedd.) Holttum 1976: 117.

Basionym: Nephrodium dayi Bedd., Journ. Bot. 25 (1887) 323.

Synonym: Lastrea dayi Bedd., Handb. Suppl. (1892) 54.

Misapplied name: Thelypteris singalanensis sensu Holttum 1955: 243, fig. 138.

I have no corrections or addition to the description of 1955, but here provide

a correction of the name. The type of Nephrodium singalanense Bak. represents a

Sumatran species distinct from the Malayan one; it has abundant minute capitate

glandular hairs all over the lower surface and the fronds are thinner in texture,

drying a darker green. It may be a forest plant, whereas the Malayan M. day

grows in rather open places, not in full forest shade. A plant from Taiping Hills

investigated by Prof. Manton proved to be tetraploid; the Sumatran M. singalanensis

might be diploid.

Distribution: Sumatra, Malaya, West Java, Borneo, Philippines, New Guinea.

2. Macrothelypteris Ching 1963: 308. Holttum 1969: 25

Rhizome short, prostrate or suberect; scales at base of stipes narrow, thickened

near their bases, with short acicular or capitate marginal and superficial hairs;

fronds amply bipinnate-tripinnatifid with adnate pinnules; scales on rachis (if

present) often with thickened bases, sometimes with marginal hairs, always with an

acicular hair-tip, usually grading to septate hairs on distal parts of frond; sori small,

with small indusia obscured by ripe sporangia; sporangia bearing capitate hairs;

spores with a very fine surface-reticulum not distinguishable in detail with the

light microscope, sometimes with slight wing-like outgrowths.

Distribution: about 9 species, from the Mascarene Islands to warmer parts of

mainland Asia, throughout Malesia, widely in the Pacific. In Malaya only one

species, which needs no new description but has an earlier name than that cited

in Holttum 1955.

Macrothelypteris torresiana (Gaud.) Ching 1963: 310. Holttum 1969: 27.

Basionym: Polystichum torresianum Gaud. in Freycinet, Voy. Bot. (1824) 333.

Synonym: Thelypteris torresiana (Gaud.) Alston, Lilloa 30 (1960) 111.

Name in Holttum 1955: Thelypteris uliginosa (Kunze) Ching.

This species is at once distinguishable by its glaucous stipe with dark narrow

basal scales and by the presence of slender acicular hairs more than 1 mm long

and consisting of several cells, which take the place of scales on the lower surface

of axes of the frond. It is distributed almost throughout the range of the genus and

has also become established through human agency in various parts of the American

tropics. It is not a common species in Malaya, except in the north, in open places

in the lowlands, though easy to cultivate in Singapore.

T hely pteridaceae 149

It would not be surprising if M. multiseta (Baker) Ching, described from

G. Matang near Kuching, Sarawak, and occurring at c. 3000 ft in the Padang High-

lands of Sumatra, were to appear in open places on the mountains of Malaya. This

species has larger fronds than M. forresiana, with reddish stipes and copious stiff

spine-like scales throughout stipe and rachises.

3. Pseudophegopteris Ching 1963: 313. Holttum 1969: 12

Rhizome various, in the Malayan species erect, in P. aurita (Hook.) Ching

long-creeping and slender. Stipe and rachis usually reddish, basal scales thin,

red-brown when dry, edges not ciliate; scales on frond usually few, appressed,

reduced to a single row of short cells with red transverse walls. Lamina usually

large (smallest in the Malayan P. rectangulare), much longer than wide, with +

reduced lower pinnae; in bipinnate fronds the lamina of pinnules adnate to

pinna-rachis; hairs on frond acicular or short-capitate, always unicellular. Sori

exindusiate, often spreading a little along the veins; sporangia sometimes bearing

acicular hairs near annulus; spores pale, with a slightly raised reticulum of rather

large meshes.

Distribution: 21 species, distributed from the islands of St Helena and San

Thomé (Atlantic Ocean) to Hawaii; in Malesia only on mountains in open places.

The two Malayan species are named Thelypteris oppositipinna and T. brunnea

in my book of 1955. Both names must be changed, and a new description of the

latter is provided. The only other species which might occur in Malaya is P. aurita

(Hook.) Ching, which was described from N.E. India and has been found on Mt

Kinabalu and the highlands of eastern New Guinea; it might occur on the exposed

upper parts of Gunong Tahan. In New Guinea this species was found to be tetrap-

loid, but in Ceylon it is diploid.

Pseudophegopteris rectangularis (Zoll.) Holttum 1969: 19.

Basionym: Polypodium rectangulare Zoll., Syst. Verz. (1854) 37, 48.

Name in Holttum 1955: Thelypteris oppositipinna (v.A.v.R.) Ching.

Distribution: N.E. India; Sumatra, Malaya, Borneo, Java, at 3000-5000 ft.

The name rectangularis was based on a specimen from Java, the later name

Oppositipinna on a specimen from Sumatra; the species also received other names

elsewhere (see Holttum 1969 for full synonymy). The few Malayan specimens have

been found in rather dry exposed ground in or near stream-beds, whereas plants of

P. paludosa (see below) grow in wet ground by streams. It would be interesting to

transplant P. rectangularis to see whether different environmental conditions would

cause it to vary from its normal characters as described and figured in my book.

Pseudophegopteris paludosa (BI.) Ching 1963: 315. Holttum 1969: 23.

Basionym: Polypodium paludosum Bl., Fl. Jav. Fil. (1851) 192, t. 90.

Name in Holttum 1955: Thelypteris brunnea in part, excluding Indian plants.

Correct name in Thelypteris: T. paludosa (Bl.) K. Iwats., Acta Phytotax. Geobot.

19 (1961) 11.

Rhizome erect, massive in well-grown plants. Stipe 50 cm or more long glab-

rescent, reddish; basal scales to c. 10 x 2 mm, very thin. Lamina to 120 cm or

more long; free pinnae to c. 15 pairs, opposite, lower pinnae somewhat reduced

and more widely spaced, basal pinnae 25 cm long on a frond with largest pinnae

33 cm; basal basiscopic pinnule or pinna-lobe longer than acroscopic. Pinnules

broadly adnate to pinna-rachis, usually connected by a very narrow wing, grading

distally to the deeply lobed apical part of the pinna; largest pinnules (apart from

basal ones) about 4 x 1 cm, deeply lobed, veins pinnate in the lobes; lower surface

150 Gardens’ Bulletin, Singapore —— XX1X (1976)

of pinna-rachis and costae of pinnules bearing stiff spreading slender acicular hairs

2-3 mm long, shorter and thicker hairs on upper surface. Sori usually 2 pairs in

each pinnule-lobe, round or nearly so; sporangia lacking hairs near annulus.

Distribution: Malesia, Sumatra to New Guinea, on mountains at 4000-7000 ft,

in open wet ground by streams; rather few collections.

When writing my bok of 1955 I had only seen one plant of this species, which

I found in an early clearing (for the trout hatchery) near Brinchang at Cameron

Highlands in the 1930’s; I also saw a plant collected by Mrs Allen at Fraser’s Hill.

As Mrs Allen has reported (Gard. Bull. Sing. 17: 260. 1958) the species increased

greatly in the later large clearings at the Highlands, and I saw it growing abundantly

by streams above Brinchang village in 1969; these Malayan plants certainly agree

closely with specimens from the mountains of West Java, whence Blume had the

type of his species.

The name Thelypteris brunnea applied to the Malayan species by me in 1955

was based on Polypodium brunneum Wall., published without a description in a

list of the specimens in Wallich’s herbarium. The earliest valid name for the Indian

species is Phegopteris pyrrhorhachis Kunze, based on a specimen from the Nilgiri

Hills in southern India; the rhizome is somewhat prostrate and the fronds are never

so large as in P. paludosa. In Ceylon Prof. Manton found both tetraploid and hexa-

ploid forms of this species. Malayan plants of P. paludosa look very uniform at

Cameron Highlands.

Mrs Allen remarked that she had found P. rectangularis and P. paludosa

growing together, and it would not be surprising if intermediates were found. It

should be noted that, apart from the great difference in size (which would not apply

to young plants of P. paludosa) the two species differ constantly in the presence of

stiff hairs on the sporangia P. rectangularis (see Holttum 1955 fig. 137) and their

absence in P. paludosa.

The plants from Mt Kinabalu mentioned by Mrs Allen in her note on Thelyp-

teris brunnea above-mentioned are Pseudophegopteris aurita (Hook.) Ching.

References to literature cited

CHING, R. C. 1963. A re-classification of the family Thelypteridaceae from the

mainland of Asia. Acta phytotax. sinica 8: 289-335.

HOLTTUM, R. E. 1955. A Revised Flora of Malaya, 2, Ferns of Malaya. Govern-

ment Printer, Singapore.

1968. Ibid., second edition, with appendix of corrections and addi-

tions.

—_—_—— 1969. Studies in the family Thelypteridaceae, I. The genera Phegop-

teris, Pseudophegopteris and Macrothelypteris. Blumea 17: 5-32.

1971. Studies in the family Thelypteridaceae III. A new system of

genera in the Old World. Blumea 19: 17-52.

1976. Some new records of Thelypteridaceae for the Philippines.

Kalikasan 5: 109-120.

IWATSUKI, K. 1963-65. Taxonomy of the thelypteroid ferns, with special refer-

ence to the species of Japan and adjacent regions, Parts 1-4, Mem. Coll, Sci.

Kyoto Univ. B, 30: 21-51; 31: 1-40, 125-197.

Tremellales with Tubular Hymenophores Found in Singapore

by

A. DAVID! & M. JAQUENOUD

Laboratoire de Mycologie, associé au Achlenstr. 30, CH-9016 St Gall.

CNRS, Villeurbanne, France Switzerland

Summary

The authors describe a new species of pore-bearing Tremellales: A porpium hexagonoides,

and discuss a collection of a species closely related to A. dimidiatum David.

Until recently, the poroid Tremellales were only represented by a resupinate

species, Aporpium caryae (Scw.) Teix. & Rog. In a recent paper (David, 1974).

a new species was described from Guadeloupe and named A. dimidiatum David.

The author believed that the existence of Tremellales in the form of polypores

might be far less exceptional than had been previously supposed. This opinion

was confirmed by a short stay in Singapore? in July 1974 devoted to the study of

the island’s polypores, when several poroid fungi with longitudinally divided

hypobasidia were collected. On one hand the stay in Singapore was very profitable

as far as the number of species collected was concerned, but on the other we were

disappointed in the results of trying to culture them. From the spore samples

made on the spot in Singapore, we should have got polyspermous and mono-

spermous mycelium on our return to Lyon, but only a low percentage of germinating

spores were found, probably due to the 7-15 days’ lapse before culturing.

Are spores of equatorial species, developing in a climate which is always

favourable for germination, particularly sensitive to drying out? The failure of the

cultures, especially of monosperms, is to be regretted, because ome specimen

collected in Singapore shows, apart from its size, many characteristic features of

A. dimidiatum described from Guadeloupe: no microscopic difference could be

discerned. On the other hand other specimens certainly represent a new species —

Aporpium hexagonoides David & Jaquenoud, sp. nov.

Fructificationes parvula*, solitaria, subdimidiata vel dimidiata, in statu recenti

coriacea elastica; in statu sicco dura cornia, 2—3 cm lata, 1—1.8 cm ad radium,

0.3-0.85 cm crassa. Facie superiore (Plate Ib) applanata vel leviter convexa,

albida ad marginem, alibi pallide ochracea, 10 YR 8/6 7/6 7/8,4 molliter veluta

(aut tomentosa) vel hispida in statu recenti; in arescendo corrugantur. Margine

obtusa. Facie inferiore hymeniale (Plate la) pallide alutacea, 10 YR 8/2-2.5

Y 8/2. Pori magni, angulosi, plus minusve hexagonales, ca. Imm diam. Multi

fasces hyphacei ex hymenio eminentes, sub lente visibiles. Tubuli contexto

concolori neque aparte separati. Systema hypharum dimiticum: hyphae sceleticae

1Assisted by B. Dequatre, collaborateur Sexhtallaens du CNRS.

2We are much indebted to the Chairman, Nature Reserves Board, Singapore and to Dr Chang

Kiaw Lan for all the help given to us during our stay in Singapore.

3We are very grateful to Dr. H. M Professor at the Cantonal G -School of

iso gon’ tee voce etzger, anton rammar-School o

4See “Code Munsell Book ps Onles” (1950), Baltimore. Maryland.

151

152 Gardens’ Bulletin, Singapore — XX1X (1976)

hyalinae (3-) 4-5 » diam., crassis tunicatis usque ad 1 w hyphae generativae

hyalinae tenuiter tunicatae, 2—3 » diam., cum articulis longissimis, ut fibulae

rarae atque difficiles visu sunt (Fig. lb). Basidia claviformia 20 X 8 un, longi-

tudinaliter septata in parte superiore (Fig. la), 4 sterigmatis subulatis, 10-12

longis. Basidiospori hyalini, non cyanophili, non amyloidi, non dextrinoidi, sub-

cylindreati, plus minusve depressi, cum regione apicali, Congo ammoniacali

adhibito valde colorescente, 9-11 xX 4-5 y» (Fig. Ic). Inter basidia paraphysoidi

subsunt simplices plus minusve ramosi.

Haec species facile cognoscitur, quod pori magni saepe hexagonoides fiunt.

Praeterea ab utraque alia specie nota magnitudine basidiorum atque spororum

differt, et quod probasidium non prius quam in partibus superioribus dividitur.

LY AD 1763 (holotypus in herbario A. David, Univ. Lugduni), ad truncum

profunde in humo infossum, in margine silvae, Jungle Fall Valley Path, post

casam, Bukit Timah Reserve, Singapore, 28.7.1974.

Fruiting bodies small, solitary, subdimidiate to dimidiate, leathery and

flexible when fresh, hard and horny when dried, 2—3 cm long, radius of 1—1.8

cm, and 0.3 — 0.85 cm thick. Upper surface (Plate 1b) applanate to slightly convex,

light ochraceous 10 YR 8/6 7/6 7/8 except towards the margin which is whitish,

velutinous to hispid when fresh, becoming strongly radially wrinkled on drying.

Hymenial surface pale brown between 10 YR 8/2 and 2.5 Y 8/2. Pores big

angular, more or less hexagonal, about 1 mm. diam (Plate la). Numerous

fascicles of hyphae emerging from the hymenium and visible under the hand-lens.

Tubes and context concolorous and not distinctly separated. Hyphal system

dimitic: skeletal hyphae hyaline (fig. 1b), 4-5 » diam., with walls up to

1 » thick. Generative hyphae hyaline, with thin walls, about 2—3 yp», with very

long cells, so that the clamp connections are rare and difficult to see. Basidia

clavate, 20 X 8 », divided up longitudinally in the upper part (Fig. la), with 4

sterigmata which are subulate and 10-12 y» long. Basidiospores hyaline, neither

cyanophilous, nor amyloid, nor dextrinoid, with thin walls, subcylindric, more or

less depressed, with one apical region which can be dyed strongly with ammoniacal

Congo, 9-11 X 4-5 wu (Fig. Ic).

This species is easily recognizable by its big pores which are often hexagonal.

It differs from the other two known species of A porpium by the size of the basidia

and of the spores, and by the fact that the probasidium is only divided up longi-

tudinally in the upper part.

Ecological and geographical distribution

LY AD 1763 (holotype in the herbarium A. David, University of Lyon), on

prostrate trunk, partly buried in the ground, at the edge of the forest, Jungle Fall

Valley Path, behind the hut, Bukit Timah Reserve, Singapore. 28.7.1974. LY AD

1820 on section of a trunk, within the edge of the forest, McRitchie Jungle,

Singapore. July 1974.

An Aporpium sp. very similar to A. dimidiatum

This species, which we collected only once in Singapore presents so many

similarities with Aporpium dimidiatum that we prefer to be cautious and not to

make it a new species, at least for the time being. It differs from A. dimidiatum in —

the small size of its fruiting bodies, the smaller pores, and in being constantly —

sulcate. Fruiting bodies, many, small, dimidiate to effused-reflexed, solitary or more

or less confluent in longitudinal stripes, 2.5-3 cm long, radius 1.5 cm, 0.7-8.0 cm —

thick, becoming very hard after drying. Upper surface convex, not hairy, but —

showing a fine tomentum under the hand-lens, beige to light rust 10 YR 8/3 7/3

7/4. Marginal area usually with 2-3 concentric grooves, the rest of the upper

surface more or less scrobiculate. Context leathery, strongly zoned with brown

Plate 1. Fruitbody of Aporpium hexagonoides (x3)

a: hymenial surface, b: upper surface.

Tremellales 153

stripes of cartilaginous consistency corresponding to growing layers. Hymenial

surface greyish white, becoming brown when touched: (5—) 8-10 pores per mm.

Microscopic characters: all identical to those of A. dimidiatum.

BAO

3 a

Fig. 1. a: fragment of the hymenium squashed after one night in ammoniacal Congo (x 2000)

b: skeletal and generative hyphae (x 2000).

c: spores (x 3000).

Reference

DAVID, A. 1974. Aporpium dimidiatum, nouvelle tremellale porée. Bull. trimest.

Soc. mycol. Fr. 90: 179-185.

ea rani Muti FIC] ticlisabondn

ete: 28

= i ae EF Pat

Sur Un Nouveau Bolet Tropical 4 Spores Ornées

par

JACQUELINE PERREAU et RocER HEIM

Laboratoire de Cryptogamie, Muséum National d'Histoire Naturelle, Paris

Résumé

Originaire du Gabon, ie Boletus cornalinus est un Xerocomus entiérement moucheté du

méme rose-pourpre que celui qui teinte les pores, tandis que la chair et les tubes se révélent

incarnats; il posséde des spores brun jaunatre 4 ornementation peu accentuée, d’irréguliérement

et densément fovéolée 4 verrucoso-cristulée. I] s’apparente 4 d’autres bolets appartenant aux

sous-genres Phylloporus et Xerocomus dont certaines espéces montrent des spores non lisses;

ses affinités plus lointaines pourraient se trouver du cété des Piperati.

Summary

Boletus cornalinus, originating from Gabon, is a Xerocomus entirely spotted with the

same purple rose colour that characterizes its pores, with the flesh and tubes being incarnate.

Spores yellowish brown, finely ornamented; ornamentation irregularly and densely foveolated

to verrucose-cristulate. Related to other Boletes, especially of subgenera Phylloporus and

Xerocomus where some species exhibit non-smooth spores. Its remote affinities could be

traced to the Piperati group.

A laube du XXéme siécle, on ne connaissait guére qu’une quinzaine de bolets

a spores ornées avec, parmi eux, le cosmopolite Boletus strobilaceus Scop. ex. Fr.

sur lequel Berkeley créa, dés 1851, le genre Strobilomyces et le Boletus ananas

Curtis qui devint le type du genre Boletellus établi, en 1909, par Murrill. Actuelle-

ment, il est possible d’en compter plus de soixante-dix, découverts notamment au

fur et 4 mesure que se développait l’étude des flores tropicales: ils se trouvent

répartis dans plusieurs coupures génériques ou sous-génériques selon les con-

ceptions des Auteurs sur la systématique des Bolétales. Bien qu’ayant la

caractéristique commune de présenter une ornementation sporale, ces espéces se

rattachent 4 des groupes différents au sein de ]’ensemble formé par les champignons

charnus 4 hyménophore tubulé et, si les indications tirées de leurs spores ne

peuvent étre seules décisives pour leur classement, du moins suggérent — elles

souvent des regroupements, affinités ou tendances; ainsi en est-il pour la forme de

ces éléments, leur pigmentation et les particularités architecturales de leur paroi

qui se manifestent essentiellement au niveau de l’exospore.

Tous ces bolets montrent justement une assez grande diversité dans les

motifs de décoration exosporique : 4 cété de réseaux serrés et profonds, d’une

ordonnance presque réguliére, ou d’épaisses nervures longitudinales, on observe des

verrues plus ou moins massives, des crétes, des ailes élevées ou de fines stries,

des nappes fovéolaires d’une extraordinaire variabilité, des réseaux contournés,

incomplets ou formés d’amples alvéoles. Evidemment, selon les espéces, l’orne-

mentation ne présente pas la méme importance et apparait parfois si faible

qu’on la distingue 4 peine au microscope photonique et qu'il faut étudier ses

détails en microscopie électronique a balayage.

_ Tel est le cas chez un bolet recueilli, 4 plusieurs reprises, par M. Gérard

Gilles, dans la forét de la Mondah, prés de Libreville, au Gabon, forét qui abrite

une flore fongique particuliérement riche et intéressante, peu connue encore.

Entiérement rose pourpré a incarnat, comme I’est la variété de calcédoine appelée

cornaline, cette espéce nouvelle a recu le nom de Boletus (Xerocomus) cornalinus.

155

156 Gardens’ Bulletin, Singapore — X XIX (1976)

20 ym

Cc

Fig. 1. Boletus cornalinus: a — Carpophore et coupe dans le chapeau; b — spores, dont |

pleurocystides; d — |

une en coupe optique, vues au microscope photonique; c —

hyphes du revétement piléique.,

Un Bolet Tropical 157

Description

Caractéres macroscopiques

Chapeau de 20-60 mm de diamétre et jusqu’ a 20 mm d’épaisseur, convexe,

puis convexe-aplani, régulier, sec, entiérement moucheté de flocons rose pourpré,

vieux rose, rose vineux (Séguy 82 et 83)* sur un fond plus clair, rosé (S 80),

Yensemble passant lors de la dessiccation 4 un brunatre mélé de tons rouillés-

cuivrés; marge arrondie, trés légérement excédante, parfois de teinte plus pale;

revétement non séparable.

Chair de 5 4 10 mm d’épaisseur, séche, d’un blanc-rose pourpré, incarnat,

proche de S 130, jaunissant a l’air en deux a trois minutes.

Hyménophore tubulé, horizontal ou faiblement ventru, échancré autour du

sommet du pied selon des lamelles décurrentes en filet sur celui-ci; tubes longs

de 5-15 mm, blanc rosé (S 130), immuables, mais devenant brun-jaune lorsqu’ils

sont poudrés par la multitude des spores, 4 pores arrondis au début, puis suban-

guleux, assez réguliers, de 0,6-1 mm de diamétre, rose vineux (S 82), nettement

plus vermillon (S 93-94) sur exsiccata.

Pied relativement gréle, de 50-100 mm de longueur, atteignant 6-8 mm de

diamétre et 10 mm 4 la base vers laquelle il se dilate progressivement, fibreux,

plein, entiérement couvert de flocons et de courtes fibrilles rose pourpré (S 82); la

base est plus ou moins enveloppée d’un manchon de mycélium beige rosé d’ot

partent quelques rhizomorphes brun noiratre assez gros et tenaces (Fig. 1, a).

Couleur des spores en masse : brun jaune.

Odeur inconnue.

Saveur légérement acidulée.

Caractéres macrochimiques

NH,OH : instantanément jaune-brun verdatre sur le revétement et la chair —

Acides : réaction nulle — FeSO, : immédiatement brunatre sur la chair piléique

— lode (Réactif de Melzer) : réaction nulle sur la chair.

Caractéres microscopiques

Basides sub-ellipsoides, de 25-30 X 10-12 um, portant quatre stérigmates

effilés, peu arqués, longs de 5 »m en moyenne.

Spores de (13) — 13,5 — 15 X 4,5 — 5,5 — (6,2) um, ellipsoides-fusiformes,

longuement atténuées vers le sommet arrondi, subtilement aplati parfois; avec, a

maturité, une dépression supra-appendiculaire accentuée, la face dorsale offrant

souvent une convexité, puis une légére concavité juste au-dessus de l’appendice

hilaire petit et subcylindrique; 4 gouttelettes lipidiques assez nombreuses; 4 paroi

ornée, jaune brunatre; non amyloides.

Au microscope photonique (Fig. 1, b), l’ornementation, peu accentuée, apparait

composée de multiples ponctuations délicates et de taches un peu arrondies ou

étoilées-divariquées, parfois disposées en alignements, brunatres ou jaune

réfringent selon la mise au point. En coupe optique, cette ornementation se traduit

par des échancrures festonnées dans une exospore colorée, alors qu’épispore et

endospore sousjacentes demeurent d’épaisseur réguliére. Toutefois, certaines spores

montrent des plages pratiquement lisses.

Naturellement, les observations en microscopie 4 balayage précisent les détails

d'un relief qui, dans ces conditions, se révéle moins masqué par la périspore et

Yectospore. En voyant les nombreuses fossettes ou anfractuosités plus ou moins

fusionnées, isolant de petites crétes contournées et irrégulitrement anastomosées ou

des protubérances versiformes (PI. I, A-D), on ne peut que penser aussitét a

une nappe fovéolaire. Toutes les caractéristiques de ce type ornemental sont

*— BE, Séguy — Code universel des couleurs. P. Lechevalier, Paris, 1936.

158 Gardens’ Bulletin, Singapore — XX1X (1976)

d’ailleurs réunies puisque l’on retrouve des plages de surface sporale lisses,

surtout au sommet, ou a peine scrobiculées comme sur la zone entourant l’appendice

hilaire (en B); a l’opposé, l’aspect déchiqueté et “‘cunéiforme”’ de la décoration se

remarque sur toutes les photographies de la planche.

Pleurocystides fusiformes 4 sommet étiré-atténué, parfois capité, toujours

émoussé (Fig. 1, c), de 50-65 xX 12-15 wm, 45 pm au col, a paroi fine, a

contenu jaune brunatre, légérement flexueuses, émergentes, relativement abondantes

(547 par 100 pm?).

Cheilocystides peu différenciées sur l’aréte des tubes, larges de 7-15 pm,

tres nombreuses et couvertes de granulations polygonales-arrondies, de 0,2-0,5

um de diamétre, rouge orangé vif trés réfringent.

Trame des tubes de type Phylloporus et Xerocomus; hyphes hyalines, larges

de 5-7 pm, non bouclées, 4 peine divergentes.

Revétement piléique constitué d’hyphes entrecroisées, incrustées, de largeur

variable (5-16 »m), étranglées aux cloisons et dont les articles terminaux, longs de

30-35 ym, sont cylindracés ou clavulés.

Ces hyphes que |’on voit également en bouquets dans les flocons du pied, sont