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Edred John Henry Corner, 1972. photograph by Ismail bin Ahmad
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,
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WO WS SS
SSS
~
NS Ss
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: @ 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.
SELECTED BIBLIOGRAPHY ALLEN, B. M. 1967. Malayan Fruits. Donald Moore Press Ltd., Singapore. pp. 94-99.
BURKILL, I. H. 1935. A Dictionary of Economic Products of the Malay Peninsula. Vol. 1, 871-875. Crown Agents for the Colonies, London.
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 & Sons Inc., N. Y. pp. 59-60.
Durio Zibethinus, Reproductive Biology 33
FAEGRI, R. & L. van der PIJL 1966, The Principles of Pollination Ecology. Pergamon Press, London.
HEASLETT, E. A. 1972. Durio mualaccensis Planch. with pink-tinged flowers. Malay. Nat. J. 25, 39.
HO, C. C. 1971. Status of conservation of genetic resources of indigenous crops in Malaysia. Pl. Introd. Rev, 8. C.S.1.R.O. Australia, 28-49.
JONG, K., B. C. STONE & E, SOEPADMO 1973. Malaysian Tropical Forest: An underexploited genetic reservoir of edible-fruit tree species. Proc. Symp. Biol. Res. & Nat. Dev., Mal. Nat. Soc., 113-121.
KOCHUMMEN, K. M. 1972. Bombacaceae. In T. C. Whitmore (Ed.), Tree Flora of Malaya, 1: 100-120. Longman Malaysia Sdn. Bhd., Kuala Lumpur.
KOSTERMANS, A. J. G. H. 1958. The genus Durio Adans. Reinwardtia 3: 357-460.
LAI, ANDREW K. K. 1974. The economics of establishing a 400-acre fruit orchard in Peninsular Malaysia. Malay. agric. J.: 49: 421-432.
MEIJER, W. 1969. Fruit trees in Sabah (North Borneo). Malay. Forester 32: 252-265.
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}
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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
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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’.
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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.
et
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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