cryptogeal germination and other seedling adaptions to the burning of vegetation in savanna regions:...

Cryptogeal Germination and Other Seedling Adaptions to the Burning of Vegetation inSavanna Regions: The Origin of the Pyrophytic HabitAuthor(s): George JacksonSource: New Phytologist, Vol. 73, No. 4 (Jul., 1974), pp. 771-780Published by: Wiley on behalf of the New Phytologist TrustStable URL: http://www.jstor.org/stable/2431248 .

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New Phytol. (I974) 73, 77I-780.

CRYPTOGEAL GERMINATION AND OTHER SEEDLING ADAPTIONS TO THE BURNING OF

VEGETATION IN SAVANNA REGIONS: THE ORIGIN OF THE PYROPHYTIC HABIT

BY GEORGE JACKSON

Department of Botany, University of Ibadan, Ibadan, Nigeria

(Received 2o December I973)

SUMMARY

Following a study of Butyrospermum paradoxum (Jackson, I968), observations on the germination of several savanna shrubs and trees have been made. Plumule burying (cryptogeal germination) occurs in a number of species in widely separated families. It is suggested that this feature has arisen as a result of evolution in a habitat that has long been subject to annual burning. The problem remains as to whether the fires are to be regarded as natural or as due to the widespread use of burning by man.

INTRODUCTION

Hofmeyer (I92I) recorded plumule burying in Elephantorrhiza burchelli Benth., (Papi- lionaceae) a savanna suffrutex of southern Africa. Jackson (I968) showed how Butyro- spermum paradoxum, in the manner of hypogeal germination, produces an apparent radicle from which in due time the buried plumule arises. The term cryptogeal was suggested for this type of germination which results in new shoots arising from below the ground even though the seed germinated on the surface. Exell (I970) recorded the phenomenon in Combretum. In California, Schlising (I969) observed that the cucurbit Marah oreganus and other Marah species have the same kind of germination which he regards as an adaptation that reduces water loss.

The present paper describes observations made on the germination of seeds of a number of West African savanna shrubs and trees and discusses them in relation to the origin of the pyrophytic habit.

OBSERVATIONS

Germination of Combretum species Species of Combretum have been grown extensively for this study and this genus

makes a convenient start for comparison with other species. Since Exell (I970) and Exell and Stace (I972) do not give drawings, Combretum will first be described from my in- vestigations.

Germination tests were made with the fruits lying on the soil surface since this is how Combretum fruits germinate in the wild. They are rarely buried except sometimes by termite activity. It appears that Exell (I970) and Exell and Stace (1972) buried the fruit (or seed) and this may account for his statement that the cotyledons arise, rather than that the cotyledon stalks are pushed, below ground.

77I



772 (EORGE JACKSON

Combretum binderanum and C. sericeum were collected at Bida (North Western State of Nigeria) in January I969 and planted at Ibadan in the same month.

C. binderanum is a small savanna tree whose fruits ripen during the dry season and they are wind dispersed into areas which will usually have been burnt. They lie on the soil surface or are blown about until the rains begin when, if conditions are favourable and the seed has survived, they will germinate.

(o)i (b)~~~M (C) I

/l { = b / 1 /f

co~f 1X / -,

-s~~~~~~~~S

2 a-

/at e t ,ah d cross-section, cntinuing ds(in section)

77 j 1 -

ff I P

Fig. i. Seedlings of Combretum species. (a) i and ii, C. molle; (b) i and ii, C. fragrans; (c) i and ii, C. binderianum. f, Foliar cotyledon; s, cotyledon petiole; ss, fused cotyledon petioles; p, plumule.

On germination (Fig. ic) an apparent radicle emerges from the fruit coat and grows down into the ground for about 4-6 cm. During the period of growth of the apparent radicle, two foliar cotyledons fused at their bases are drawn out of the fruit coat. At this stage germination has apparently followed a normal mode of epigeal germination. How- ever, in the place where the plumule bud is expected, there is a cavity which dissection reveals to be a tube, star shaped in cross-section, continuing down into the apparent hypocotyl. After a period of several weeks (the time period varies greatly) a shoot develops which breaks through the side of the tube and grows up to the soil surface



Cryptogeal germination 773 where normal leaves develop on it. This shoot often appears several centimetres away from the expanded part of the cotyledons.

Comparison with normal germination shows that the apparent radicle is cotyledonary and, that on its initial growth and expansion, it carries the undeveloped plumule below ground. The true radicle is also carried below ground by this initial cotyledonary expansion where it later develops normally into a strong tap-root system.

This type of germination is found in C. binderanum, C. apiculatum, C. zeyheri (from Malawi), C. glutinosum, C. hartmannianum (K. Wickens, personal communication), C. hypopilinum and C. fragans (Fig. ib).

(a)

(b)

Fig. 2. Stages in the germination of Combretum molle (half the fruit coat has been removed). Planted 7 March 1973 (a) to i6 March 1973 (d).

C. molle, a tree, widespread in savanna and derived savanna areas, shows a difference. On germination two strands joined at their tips emerge from the fruit and on elongating caTrry the fused tip below ground. Two separate cotyledons are withdrawn from the fruit coat and are carried on separate stalks above ground (Fig. 2). When the cotyledon stalks cease to grow, the plumule develops and grows to the soil surface forming a shoot with normal leaves while the true radicle develops below ground (Fig. ia). This type of germination is present in C. molle, C. collinum (K. Wickens, personal communication) and C. psidioides (K. Wickens, personal communication).

C. sericeum is a savanna suffrutex which is found extensively in Daniellia oliveri savanna and is expecially characteristic of areas of cultivation and disturbance. The flowers appear in late December or early January and soon produce the pink or red fruits which, on ripening, are shed into grassy areas, that are usually burnt over, or into cultivations in various stages of preparation for the oncoming wet season.

On germination two cotyledon stalks, fused at their tip and so protecting the young plumule, emerge and grow I-2 below ground after which the plumule and radicle develop



774 GEORGE JACKSON

normally (Fig. 3a, b). In contrast to the species described above the leafy parts of the cotyledons are not withdrawn from the fruit and seed coats and thus the germination resembles the normal hypogeal method.

Combretumpaniculatum, a climber of forest and derived savanna areas, was germinated and grown for comparison (Fig. 4). In this species a short split structure emerges from the fruit coat but a true radicle grows immediately from the fused tip and the plumule

(a) (b) (c)

/777' 77 ~~~~~~~~~~~~~ ~- 7/727

Fig. 3. (a) and (b) Stages in the germination of Combretum sericeum. (c) Original plumule damaged, resulting in the growth of the cotyledonary axillary buds from the root crown. (a) 4 January I969; (b) i6 January I969; (c) 8 June I969.

f~~~~~~~~~~

(aX

(b) N ~~ ~~S (d) (e) (b-) ~

Fig. 4. Combretum paniculatum: (a) and (b) four winged fruit typical of parts of the genus; (c)-(e) stages in germination.

develops from the join of the cotyledon stalks. Foliar cotyledons are not withdrawn from the fruit coat and the plumule is not at any stage pushed below ground. It is interesting, however, that the short cotyledon petioles emerge from the fruit before the plumule elongates, a method similar to that of C. sericeum. K. Wickens (personal communication) reports a similar type of emergence in C. microphyllum, a savanna scrambler of East African distribution.



Cryptogeal germination 775 Other genera of the Combretaceae

Guiera and Quisqualis demonstrate plumule burying to some extent. Guiera senegalensis is a shrub, usually small, but which grows under woodland condi-

tions in Cameroun as a much taller plant. It is mostly found in the drier areas and on overgrazed or overcultivated lands where it can form extensive communities. It flowers in

(a)' (I)11 (a)iii (a)iv f

\)< (6 if'. if<f \j! (

-h h h~~~~~S-

(b) i (se

ft (d) i

f~ ~~~~~~~~/f /

s ~~~~~~~~~~~~~~~~~h h~~~~~~~~~

77

(b)i 61

IFig. 5. (a) Gardenia erubescens: i, Young seedling; i,seedling showing emergence of plumule from the cotyledonary tube; iii, apparently normal seedling; iv, dissection of the cotyledonary tube with plumule within. (b) Guiera senegalensis: i, seedling; ii, cup-like base of cotyledon stalks slightly cut to show base of plumule. (c) Pterocarpus erinaceus: i, seedling; ii, base of cotyledonary stalks grooved to fit around the plumule base. (d) Piliostigma thonningii: i, seedling showing cotyledons lying close to the soil surface; iv, single fleshy cotyledon.

the dry season. Its germination resembles the Combretum molle type with the plumule just below ground in a small cup of tissue where the bases of the cotyledon stalks fuse (Fig. 5b).

Quisqualis indica grows along the banks of the wide sandy-bedded rivers of northern



776 GEORGE JACKSON

Nigeria where the vegetation burns in the dry season. It is a scrambling untidy shrub with a tendency to climb. On germination the cotyledons are retained within the seed coat but unequal elongation of the cotyledon stalks carries the plumule slightly downwards and below ground. There is some indication, however, that if the seed is buried, the direction of growth of the cotyledon stalks can be upwards (Fig. 6b).

Other families Sapotaceae. Butyrospermum paradoxum is a savanna tree which becomes con-

spicuous in certain areas when it is selectively preserved during felling operations pre- ceding cultivation. The germination has been previously described (Jackson, I968) and differs from the above in that the cotyledons remain fused inside the hard-shelled seed on the ground surface (Fig. 6a).

ff )'(b)i

ss ~~~~~~~~sssS 1.5cm

((11

(b)ii

Fig. 6. (a) i and ii, Stages in the germination of Butyrospermum paradoxum. ss, Fused cotyledon stalks; sss, cotyledon stalks broken up into strands in late stages of growth of plumule; ff, the cotyledons remain within the fruit coats; r, radicle. (b) i and ii, Seedlings of Quiisqualis indica.

Rubiaceae. Gardenia erubescens is a savanna shrub of widespread distribution but recent work (G. Jackson, unpublished) shows a clear relationship between its distribution and cattle movement; thus this species occurs frequently in cattle areas and along cattle trails. Its germination can be compared with that of Combretum binderanum except that usually the developing plumule does not break through the cotyledonary tube but ascends inside the tube. The mode of germination can therefore easily be mistaken for normal epigeal germination, but dissection reveals the true origin of the shoot (Fig. 5a). In many individuals the tube is broken or split to a varying degree and the shoot emerges from it (Fig. 5a, ii).

Ochnaceae. Lophira lanceolata is a savanna tree, flowering and fruiting in the dry



Cryptogeal germination 777 season. Its germination resembles Combretum paniculatum in that the cotyledon stalks extend out of the seed coat and bury the young radicle to a slight degree.

Papilionaceae. Pterocarpus erinaceus is a widespread savanna tree, flowering and fruiting in the leafless state during the dry season. Its germination (Fig. 5c) resembles that of Guiera in that a cup of tissue below ground protects the young plumule (Fig. 5c, ii). There is later formation of the swollen type of tap root from the crown of which subsequent shoots develop after fire damage to the original plumule.

Caesalpinaceae. Piliostigma is a savanna genus, with P. thonningii growing in the climatically wetter areas and P. reticulatum in the drier, but with considerable overlap of the species. Both are associated with cattle dispersal. They do not bury the plumule but the hypocotyl grows down into the soil and the cotyledons come to lie very close to soil surface (Fig. 5d). The petioles are short and succulent and form a protective cup for the developing plumule similar to that in Pterocarpus erinaceus. The radicle soon becomes swollen to several times the diameter of the hypocotyl and shoot, and damage to the shoot results in proliferation from the root crown.

DISCUSSION

The types of germination described here result in the burial of the plumule of the seedlings so that new shoots arise from well below the ground even though the seeds or fruits germinate on the soil surface. This type of germination, which has been termed cryptogeal, is seen to be widespread in savanna species. A characteristic feature of savanna is the high incidence of fires in the dry season. Such fires may be caused naturally (e.g. by lightning) but they are now most frequently made by man. Most fires are started in the middle to late dry season either by hunters to flush game or by pastoralists to encourage new green growth. It is of interest to consider how the behaviour of the savanna trees and shrubs fall into this pattern of burning.

The dry season is the time of flowering and fruiting for many savanna species. The timing of events varies, for example in Pterocarpus erinaceus the yellow flowers appear whilst the tree is leafless and the fruits are often almost ripe by the time the tree is in new leaf. In Nigeria flowering is from November to February and fruiting until March. On the other hand, in Isoberlinia doka the flowers appear with the new leaves between November and March. Butyrospermum paradoxum flowers in February and fruits in May, the leaves showing several flushes in the year. Whatever the variation, however, fruits are ready for dispersal after the fires and before the rains.

'Exell and Stace (I972) correlate dry season fruiting with the pyrophytic habit whereby the ground is clear to some extent for easy dispersal of seed, particularly for those species adapted to wind dispersal. Animal dispersal of Piliostigma and Gardenia erubescens may well, however, be related to a similar factor in that, after grass fires have removed herbage, cattle tend to utilize persistent pods and fruits for fodder and at the same time are obliged to forage far afield, thus effecting wide dispersal. There is, however, a marked tendency for denser populations of browse plants in cattle holding areas or along trails, since these plants are valued by herders, as is shown by the fact that Fulani herdsmen will knock off pods to feed stock and even climb trees to lop-off fruiting branches in the dry season.

Fruit and seed dispersal is followed by germination and growth, presumably in the period of early rains immediately after fruiting and dispersal and after fires have swept the herbage. Established seedlings will therefore usually have 6-9 months before being



778 GEORGE JACKSON

subjected to a first burn. Where germination involves the burying of the plumule or hypocotyl, the root crown develops well below soil surface and buds upon it will be protected from fires (see Fig. 3c). In addition that part of the true stem which is also under- ground will bear buds in the axils of scale leaves; these buds are also protected and can give rise to new shoots when the shoots above ground are burnt off. Jackson (I970) compared this type of survival in grassy areas to the suffrutex habit but since an escape from fire damage would result in perennial lasting stems, the method should perhaps be termed pseudo-suffrutex. This kind of survival in savanna trees is not confined to the plumule-burying species but is found in many others which may also survive in cultiva- ted ground by persistent regrowth from root suckers. Survival through fire and cultivation are thus achieved by similar adaptations.

The origin of the pyrophytic habit When we consider the numbers of species in savannas with advanced pyrophytic

features there can be little doubt that the occurrence of regular fires has played a major role in their evolution. The question remains as to the origin of the fire factor.

Man is known to have existed as a hunter on the continent of Africa some 6o,ooo years ago and to have been using fire as a means of driving game. As an iron-tool cultivator man has been active for about 3000 years, during which time the use of fire would be intensified for the various cultural activities associated with shifting cultivation and tree and trash burning. He was also a herder of animals and presumably used fire as a means of flushing green grass in the dry season.

The effects of the three types of fires have some features in common but there are differences which can lead to varying fire-climax communities.

Hunting fires are most similar to those that would occur naturally. The seasonal timing of the fire will vary according to the game movements, the type of game and the type of country. It is improbable that they will take place at exactly the same time and at the same location each year. The effect is therefore that of a patchwork burn which will do little damage to established vegetation. This type of patchwork burn, particularly when employed early in the dry season, is the kind of burning recommended and used by many foresters and by road maintenance workers as least damaging to woody species and least dangerous.

Cultivation fires are varied in purpose. In initial clearing and cultivating fierce local burns are achieved by cutting and stacking timber and debris and using the ash as a fertilizer. After cultivations harvest trash is often burnt to facilitate subsequent cultivations. These fires tend to weaken or fully destroy woody plants and any regrowth is by sucker or coppice. Therefore on fallowing regeneration will involve, to some extent, invasion from neighbouring vegetation types. Under shifting cultivations the early years of fallowing result in grass regrowths which are burnt annually either deliberately or unintentionally; being grass without tree cover, they will provide a considerable amount of fuel for the burning. Invasion of woody species in such areas will thus be confined to pyrophytic types.

Pastoralists use burning to obtain a green growth from herbage when range fodder becomes scarce. The burn tends therefore to be late in the dry season, often on a large scale, and occurs mostly in the lower lying areas. Where cattle are wide ranging the burns will probably not be in the same area each year. However, if there is a tendency to restricted traditional grazing lands, the burn will frequently take place at the same locality each year and this, in turn, leads to a concentration of cattle in these areas. The burn being



Cryptogeal germination 779

late will be fierce and will tend to destroy woody plants at the expense of grasses unless overgrazing and overexploitation reduce the sward.

The indigenous peoples of Africa recognize two types of savanna woodland which probably arise as a direct result of the various types of burning. One has long grass cover and broad-leaved pyrophytic trees. The species list for such woodlands is long and in- cludes Piliostigma thonningii, Combretum spp., Cussonia kirkii, Pterocarpus angolensis and Parinari curatellifolia. It is called Chipeta by the Achewa of Malawi.

The other has a relatively sparse grass layer because the trees suppress the herbs and one can clearly see through the woodland. This is called miombo in East Africa, typified by Brachystegia and Julbernardia.

The thinning of miombo woodlands increases the yield of the grass layers without increasing the basal ground cover. Ivens (I967) estimated that the dry herbaceous yield increased four-fold. This extra herbaceous growth is often burnt when dry to attempt the control of Brachystegia-Julbernardia regrowth which is considered to be fire tender by Trapnell (I959). Fire resistent trees such as Pterocarpus angolensis and Parinari curatellifolia are then favoured. Elimination or suppression of miombo-type woodland dominated by Isoberlinia doka and the proliferation of Terminalia avicennioides has been noted in northern Nigeria following the burning of long grass phases subsequent to fallowing. For example, in Zaria district the nearer one is to the towns the more frequent the Terminalia communities become whilst the Isoberlinia types are characteristic of the protected forest reserves.

In Malawi in the Nkhata Bay area, in a semi-evergreen forest vegetation, abandonment of cultivation gives rise to communities of savanna woodland affinities with Pterocarpus angolensis, Parinari curatellifolia and Burkea africana, all pyrophytic species (Jackson, I 968).

In the Sudanian zone long-established cultivations in the neighbourhoods of the towns and major rivers have developed into cultivation parklands with various types of protected trees. One of these parklands is that with numerous individuals of Butyrospermum paradoxum which is an advanced plumule-burying species.

In northern Cameroun, at Be, it has also been recorded that Gardenia erubescens is often concentrated around the edges of wide grassy valleys where dry season grass burning and cattle grazing take place, thus associating the distribution of a pyrophytic species with cattle-keeping activities.

In southern Nigeria, at the boundaries of the forest zone, the savannas are fire derived and revert to forest if protected. These areas are dominated by pyrophytic species such as' Lophira lanceleolata, Parinari curatellifolia, P. polyandra, Pterocarpus erinaceus, Butyrospermum paradoxum and Combretum molle.

It seems therefore, in view of the time scale, natural or hunting fires may have been responsible for the widespread occurrence of pyrophytic features and types of vegetation but that recent pressures from cultivation and grazing practices may well have reinforced habit and encouraged further spread of pyrophytic species.

ACKNOWLEDGMENT S

The author is grateful to Dr (Mrs) J. Lowe for her continued interest and valuable criticism of the manuscript and to Mr H. A. Egbedi for the typing. He also thanks Mr K. Wickens of the Herbarium, Kew for making available information on Combretum seedlings. Also Professor P. J. Syrett of University College, Swansea.



780 GEORGE JACKSON

APPENDIX

Authorities for species mentioned in the text Burkea africana Hook. Cussonia kirkii Seemann Butyrospermum paradoxum (Gaertn. f.) Hepper Elephantorrhiza burchelli Benth. Combretum apiculatum Sond. Gardenia erubescens Stapf and Hutch. C. binderanum Kotschy Guiera senegalensis G. F. Gmel. C. collinum Fresen. Isoberlinia doka Craib and Stapf C. fragrans F. Hoffm. Lophira lanceolata Van Tiegh. ex Keay C. glutinosum Perr. ex DC. Parinari curatellifolia Planch. ex Benth. C. hartmannianum Schweinf. P. polyandra Benth. C. hypopolinum Diels Piliostigma reticulatum (DC.) Hochst. C. microphyllum Klotzch P. thonningii (Schum.) Milne Redhead C. molle R. Br. ex G. Don. Pterocarpus angolensis DC. C. paniculatum Vert. P. erinaceus Poir. C. psidioides Welw. Quisqualis indica Linn. C. sericeum G. Don. Terminalia avicennioides Guill. et Perr. C. zeyheri Sond.

REFERENCES

EXELL, A. W. (1970). Summary of the Combretaceae of Flora Zambesiaca. Kirkia, 7, 159. EXELL, A. W. & STACE, C. A. (1972). Patterns of distribution in the Combretaceae. In: Taxonomy, Phyto-

geography and Evolwtion (Ed. by D. H. Valentine), p. 307. Academic Press, London and New York. HOFMEYER, J. (I9zi). A note on the germination of the seed of Elephantorrhiza burchellii Benth. S. Afr. J7.

Nat. Hist., 3, 215. IVENS, G. W. (I967). In the report of U.N.D.P. and F.A.O. on Savanna Development, Khartoum, p. 150. JACKSON, G. (I968). The vegetation of Malawi. II. The Brachystegia woodlands. Soc. MalawiJ., 21, i2. JACKSON, G. (I968). Notes on West African vegetation. III. The seedling morphology of Butvrospermum

paradoxum (Gaertn. f.) Hepper. J. W. Afr. Sci. Ass., 13, 215. JACKSON, G. (1970). Vegetation around the city and nearby villages of Zaria. In: Zaria and its region (Ed.

by M. J. Mortimore), p. 6i. Occasional Paper No. 4 of the Department of Geography, Ahmadu Bello University, Zaria, Nigeria.

SCHLISING, R. A. (I969). Seedling morphology in Marah (Cucurbitaceae) related to the California Medi- terranean climate. Am. J. Bot., 56, 552.

TRAPNELL, C. G. (1959). Ecological results of woodland burning experiments in Northern Rhodesia. J. Ecol., 47, 129.



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