Mortality in the Flowers, Fruits and Young Regeneration of Trees in the Knysna Forests ofSouth AfricaAuthor(s): John PhillipsReviewed work(s):Source: Ecology, Vol. 8, No. 4 (Oct., 1927), pp. 435-444Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1930151 .Accessed: 25/08/2012 18:36

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MORTALITY IN T.HE FLOWERS, FRUITS AND YOUNG REGENERATION OF TREES IN THE KNYSNA

FORESTS OF SOUTH AFRICA

JOHN PHILLIPS

Forest Research Station, Deepwalls, Knysna, South Africa

Introduction

Insufficient importance is attributed to mortality in studies of plant dis- tribution and succession. Indeed, as one ecologist has remarked in the course of correspondence with the writer, one is almost accused of having a morbid mind if one emphasizes the need for investigation of the factors responsible for mortality in plants. Some pass the matter lightly by, others do not even remember its existence. In South Africa attention has been directed to the subject, in passing, by flews ('20, p. 450) and Schonland ('24, p. 456), while in America Clements ('i6, pp. 58-6o) has kept it in mind. The work of Watt ('I9, 23) in Britain has been particularly valuable.

On reviewing the results of various ecological experiments in the in- digenous forests of the Knysna region, the writer has been forced to the con- clusion that much light is likely to be cast upon various problems in plant sociology by means of a thorough investigation of the agencies responsible for death, and of the amount and rate of death for which they are respon- sible. It is thought that a general account of the results of some studies being carried out by the writer may set forth certain points of interest and of importance.

The mortality is greatest in the flowers, fruits and young regeneration, and in this communication attention is confined to a review of the factors causing death in these stages of ten of the more important tree species in the Knysna forests. Such factors are the following:

( I ) Inherent low degree of fertility in the flowers and in the fruits. (2) Defeat in competition for pollination. (3) Irregular occurrence of flowering seasons: such seasons may be few and

far between, and the influence of a disease of the flower crop is there- fore potent.

(4) Poor capacity of seeds for lying dormant-seedlings often are produced at uncongenial periods climatically and edaphically. (On the other hand, seeds with good dormant capacity are subjected to the depreda- tions of various enemies, during their periods of dormacy.)

(5) Unsuitable germination and establishment conditions, aerial (light, temperature, humidity, air movements) and edaphic (depth, porosity, moisture-content, acidity, of the soil).

(6) Insects and fungi attacking flowers, fruits and regeneration. 435

436 JOHN PHILLIPS Ecology, Vol. VIII, No. 4

(7) Birds and mammals feeding on fruits and seeds. (8) Reactions of plant communities upon prime habitat factors, such as

light and soil-moisture content.

Individual Species

In the following account of the mortality factors, species by species, the more important points only, are discussed.

PODOCARPUS ELONGATA 1'Herit. (P. falcatus R.Br.)

This species is dioccious. Since exploitation of the giant trees, many female trees go unpollinated, owing to their isolated positions with respect to male trees: in some places too many male trees have been removed, in others too many females.

Weather conditions at times of flowering greatly influence the degree of effective pollination: windy, cool, and moderately humid conditions being favorable, but calm, warm, and dry weather being distinctly detrimental in that the pollen is not transported to the female trees and in addition becomes shrivelled.

Flowering seasons occur at intervals of 2 to 4 years, the density of the crop varying from a very few flowers to a superabundance. The mature fruit is not produced until 9 to 12 months after fertilization, during which lengthy period the developing fruit is subjected to various agencies of de- struction. Strong winds throw thousands, and the fruit bat (Rousettus collaris) knocks down thousands more, in its attempts to feed upon the green but succulent epimatium. Most of the ripe fruits that fall are immediately devoured by the wild pig (Potaniocliocrus chocropotamius), which voids a large proportion with the seed-shells broken and worthless.

Large numbers that escape the attention of the pig do not produce seed- lings because ere the seed-shells-which are hard and chitinous-are decayed sufficiently to allow the embryoes to develop, the latter have succumbed either from fungus or insect attack or from decay set up by penetration of moisture. Experiments show that even under full exposure to sun and wind, and after removal of the thick, succulent epimatium, 6 to 24 months are required for the rotting of the seed-shell. Under normal forest conditions germination is delayed even longer, from I2 to 48 months after fall. When the epi- matium is left in position the period is prolonged by 3 to 6 months.

Large numbers of podocarpia are destroyed by the larvae of Ceratitis capitata, while a heavy toll is taken by the larvae of a moth.

Germination and establishment are not good under normal conditions of canopy, Fusarium spp. killing many of the developing plants. Under ex- posure to strong insolation germination is better, but the formation of in- solation lesions at the collars of the seedlings results in the death of a large proportion.

October, 127 MORTALITY IN TREES IN KNYSNA FORESTS 437

While 50 to So per cent of the fruits are viable, it is seldom that more than 5 to IO per cent succeed in germinating; certainly less than 2 per cent produce plants that do not succumb before the age of I to 2 years.

Thus it is evident that there is an appreciable mortality to be considered in the instance of P. elonigata.: there is a constant struggle between it and the forces of annihilation.

PODOCARPUS THUNBERGII Hook. (P. latifolits R.Br.)

This species is often dioccious, hence the remarks concerning the influence of felling made under P. clongata apply to it as well.

Weather conditions at times of flowering (which takes place in alternate ears only) are even more important in their influence upon the fruit crop than in the instance of P. clonggata, for not only do they assist or hinder fertilization, but also control the activities of an important flower and fruit attacking fungus, Corynclia uberata Fries.

While exceptionally dry and warm conditions are unfavorable to fertiliza- tion, they definitely inhibit the development of the fungus, whereas exceed- inglv moist conditions are not only very favorable for the disease but in addition prevent efficient transport of the pollen.

Windy, cool, moderately humid conditions are the most congenial to fertilization, but the chances against the joint occurrence of these are really great.

Ouantitative studies show that in some years some trees bear scarcely a single podocarpium that is not diseased by Corynelia. Most of the diseased fruits fall prematurely, but some develop to their mature size, but produce non-viable " seeds." Fruits attacked when nearly mature show non-diseased but starved embryoes, which develop into poor plants.

Many fruits are attacked by Ceratitis capitata larvae, and their embryoes are completely destroyed.

Thousands of disease-free, immature fruits are wind-blown, while birds (chiefly Turacus corythaix and several species of dove), bats, and monkeys throw down large numbers in the course of their searches for food.

Considerable numbers of the mature and non-diseased fruits that reach the soil are devoured by wild pig, which passes many of these broken, and bluebuck (Cephaloplius inonticola) is responsible for the destruction of a fair quantity. Baboon and monkey, and in some localities, mice, may de- stroy almost every fruit upon the ground.

Germination takes place within 4 months of fall. Under normal forest conditions the ravages of Fusariurn spp. which " damp off " the young plants and of a cutworm (larvae of Euxoa sp.) are so great that go to ioo per cent of the first-stage seedlings may disappear within a few days. If these pests be absent, another factor responsible for much death is the occurrence of leaf litter and humus so deep that the radicles of the plants can find no hold, and, in time of drought, no moisture, and accordingly wilt and die.

29

438 JOHN PHILLIPS Ecology, Vol. VIII, No. 4

Seedlings appearing upon exposed ground suffer from insolation lesions and from foliage scorch, over 50 per cent of them dying within a few weeks of appearance.

Here again is an example of constant warfare waged between the tree and factors causing mortality. Were it not that P. Thunbergii produces an abundance of flowers it would long since have been ousted.

PLATYLOPHUS TRIFOLIATUS Don.

This endemic monotype has been described by Phillips ('25) in a recent paper. It presents many interesting points bearing on the subject of mor- tality.

The species blossoms regularly each year, and has disease-free flowers. Pollination is efficient. Many thousands of capsules are borne on almost ever tree, but these contain few viable seeds, the average germinative ca- pacity being 2 to 4 per cent. The seeds are delicate, short-lived, and are im- prisoned within the tough, membranous walls of the capsules. Unless the latter decay within 3 months so as to allow of the development of the seed, death follows.

On first appearance the seedlings are exceptionally delicate, and a large proportion of them succumbs within a day or two, owing to unsuitable con- ditions in the germination-bed-excessive depth of humus, absence of mois- ture, or its superabundance, and acidity of the upper humus and soil, being all-important factors. Plants appearing under full exposure to insolation are lesioned off as soon as the surface soil heats up; the young foliage is sensitive to scorching. Except in the most congenial sites, and under certain trees more commonly producing seed of greater fertility, regeneration is ex- ceedingly rare.

What is the tendency ?-Is Platylophus being worsted in the contest for existence, or is it slowly but steadily asserting its capacity to live? A fea- ture of the greatest interest is the almost entire absence of disease, mortality being the outcome of inherent non-fertility.

CUNONIA CAPENSIS L.

Cunonia flowers fairly regularly year after year, and always produces extraordinarily large crops of small fruit-capsules. Each capsule contains from 30 to 50 minute, flimsy, winged seeds. Of these 95 to 98 per cent are non-viable, owing to poor development of the embryoes.

Owing to the enormous amounts of seed produced (the average amount per tree being 3,ooo,ooo to 6,ooo,ooo, according to size and age of the in- dividual), however, there are sufficient viable seeds to produce many millions of seedlings. Large numbers of the viable seeds lodge upon stones, tree trunks, and other uncongenial sites, and fail to produce seedlings. The seedlings resulting from seed reaching the ground, in many instances num-

October, 1927 MORTALITY IN TREES IN KNYSNA FORESTS 439

ber 5,00o to io,ooo per square-meter; they are minute and delicate. Owing to their vast numbers the mortality is great, due not only to biotic enemies (principally Fzisariitm spp.) but also to competition for 'space-sometimes a dozen plants occurring upon less than a square centimeter. Large numbers are trampled to death by wild animals, while insect-seeking birds in the course of their searches for prey, pull many millions from the soil. Dry periods result in the death of millions from drought, while very moist periods are equally detrimental in that root and stem rots carry off the greater portion of the crop. On account of their minute size and delicate nature the plants appearing on exposed ground are immediately lesioned and scorched to death. A large proportion of the plants that do succeed in attaining the height of several inches, is killed by a defoliating Geometrid larva.

OCO TEA BULLATA E. Mey.

The peculiar flowering behavior of this species has been described else- where by Phillips ('24).

The tree bears male, female and hermaphrodite flowers on the same in- florescence's, as well as forms connecting these, and as insects and birds do not pollinate the flowers, the degree of effective self-pollination depends largely upon the proportion of hermaphrodite flowers. Inflorescences having a high proportion of hermaphrodite flowers show a higher degree of fertiliza- tion than those with male and female flowers more abundant than hermaphro- dites. Thus the chance arrangement of the sexes is one of the factors that determines the nature of the fruit crop.

A further potent factor to be considered is a fungus, Pestalozzia sp. nov., attacking the stigma and style of female and hermaphrodite flowers; flowers infected on first appearance cannot be fertilized; flowers infected after fer- tilization, develop drupes that are infected with the fungus. Such fruits fail to develop, or else develop to a certain point and then decay.

Drupes that have escaped fungus destruction are often infected with the larvae of Ceratitis capitata and of a moth, which destroy the embryoes in most instances. Naturally some drupes are attacked by both the fungus and the larvae.

Immature drupes, infected and non-infected, are knocked from the branches in very large numbers, by the fruit bat and by turacus and doves. These drupes are attacked on the ground by Fusarium spp. and moulds.

Mature drupes free from disease are very rarely found on the tree, and the larger proportion of these on falling to the ground are destroyed by fungi, insects, and wild pig. Those removed from the tree or from the ground by birds (especially by turacus and Aminydrus vzorio), on being voided, produce seedlings in most instances.

The germination conditions required are often wanting, and the delicate seedlings succumb in fairly large numbers. A small proportion of those that

440 JOHN PHILLIPS Ecology, Vol. VIII, No. 4

attain an age of from 2 to 3 years are weakened and killed by the stem-at- tacking Morenoella Phillipsii Dge., and by one of the Trichopeltaceae at- tacking the foliage. Exposed seedlings are readily lesioned.

Plants over 3 years are attacked by a pith and wood destroying Ceram- bycid larva, which causes either death or periodic " die-back."

Plants that escape the ravages of disease but do not experience congenial light and moisture conditions, die after several years of non-assertive ex- istence, or remain stunted individuals that never produce flowers.

Thus from start to finish, Ocotca has to pass through the fire of various unfriendly influences. The existence of the species at all can be accounted for only on the grounds of its producing fast-growing coppice, and of its production of fairly large amounts of fruits at very short intervals. A non-coppicing species experiencing the same mortality as Ocotea, but flower- ing at longer intervals, would probably become either rare or extinct within a few centuries.

OLINIA CYMOSA Thunb.

Interesting features in the biology of this tree were described recently by Phillips ('26).

Flowers are produced very irregularly. Some trees bear every year, others every second, third, or fourth year, but full fruit-crops occur every third or fourth year only. The degree of effective pollination is low (6 to 20 per cent of the flowers being fertilized), largely owing to the crowding of the flowers, and to a widespread aphid disease causing marked hypertrophy of the flower-parts.

The pseudo-drupes take IO to 14 months to mature (and some remain on the tree for 2 to io months after maturity), during which lengthy period they are knocked off by wind, by turacus, doves, amydrus, bats, monkeys, and baboon, a large proportion of the total crop never attaining maturity.

The germinative capacity of the seeds is 8 to I2 per cent only, and ger- mination is delayed for about I2 to 40 months according to site factors. The embryo is minute and is enclosed in a chamber in a chitinous endocarp, which in turn is encased in a succulent, I/IO inch thick, pericarp. It is delayed in development on account of the non-rupture of the imprisoning walls.

While 8 to I2 per cent of the seeds produce viable embryoes, only about i per cent of them actually produce plants, owing to death of the embryoes ere liberation from the pseudo-drupes. Further, Ceratitis capitata larvae destroy some of the seeds. Fallen mature fruits are much destroyed by wild pig and by mice.

On first appearance, the seedlings are exceedingly delicate, and generally fail to establish themselves on account of absence of congenial light, moisture, and soil-texture conditions; they are markedly insolation-tender in early youth. To add to their troubles a Capnodiunt sp. and Asterina reticulate Klch. & Cke. together with a Fusariumn sp., at times take a heavy toll. Oc- casionally a coccid malady appears, doing much local damage.

October, 1927 MORTALITY IN TREES IN KNYSNA FORESTS 44I

FAUREA MCNAUGHTONII Phill.

Phillips ('27) has described aspects of the biology of this interesting tree elsewhere.

Flowers are borne annually and in large numbers (5o,ooo to So,ooo per tree), and are fertilized to the extent of 4I to So per cent. Owing to in- herent non-development of the ovules, however, but I 2 to I per cent only, of the nuts are viable.

Of the viable nuts large numbers fall prematurely, owing, to their being insecurely seated upon the spikes. From quadrat studies it seems that not more than 40 per cent of the viable nuts actually succeed in establishing seedlings, but were it not for the absence of biotic foes it is evident that the degree of establishment would not be so high.

Regeneration of the first-stage is often exceedingly abundant under large parent-trees, as many as 50 to ioo plants being found per square-meter.

Owing to the depth of litter and of the humus, many plants fail to find proper root-hold, and, during times of drought, readily wilt. Others that succeed in fixing their roots in the upper surface of the soil proper, die in time from lack of moisture, the result of strong competition between the numerous seedlings. On the whole the mortality is high-within 3 or 4 years but 2 or 3 of the 50 to ioo plants remain.

Did Faurea not fruit so regularly and so lavishly, its poor germinative capacity and the post-germination mortality, would have a most serious ef- fect upon the regeneration stages. As it is, the peculiar distribution and local occurrence of the plant is better understood in the light of its regenerat- ing capacity.

MYRSINE MIELANOPHLEOS R. Br.

Abundant flowers appear every second year, and produce mature fruits w-ithin 2 to 3 months of fertilization. The proportion of flowers that is pollinated effectively is medium-2I to 40 per cent of the total produced.

The drupes contain a single i-seeded endocarp, 40 to 6o per cent of the seeds being fertile under normal conditions. It often happens, however, that the drupes when still young, are attacked severely by the fungus Cory- nelia fructicola v. Hohnel., with the result that only I to 5 per cent of the seed-crop of a tree is viable. On other occasions the larvae of Ceratitis capitata attacks the coat of the young fruit and renders the development of the drupe impossible.

The drupes are not firmly set upon the trees, and therefore are thrown in large numbers, ere maturity, by wind and visiting birds, bats, monkeys and baboon. Mature drupes are destroyed by wild pig to a considerable degree, but the losses due to mice and bats, which break open the endocarps, are infinitely greater.

Owing to the large numbers of fruits produced, so many fruits ag- gregate under large parent-trees that even after the various biotic foes have

442 JOHN PHILLIPS Ecology, Vol. VIII, No. 4

been satisfied, as many as I,500 to 3,ooo drupes may be found per square meter.

Germination takes place within 2 to 4 months, the young plants being vigorous from first appearance. As many as i,ooo to i,500 plants I inch to 2 inches high have been enumerated per square meter. The mortality among these crowded individuals is very great, owing to exhaustion of moisture con- tained in the upper humus and soil layers, and to the parasitic Rhizoctonia sp. and Fusariuom spp. which attack the roots and stems respectively. After a year or two, areas bearing originally many thousands of plants bear but sev- eral dozen.

Larger stage seedlings are much browsed by blue buck. Thus despite an abundance of fruits produced every other year, the re-

generation of Myrsine never becomes superabundant, except very locally. Mortality is sufficient to keep it in check.

APODYTES DIMIDIATA E. Mey.

Fruit-crops of any importance are spaced by 3 to 4 years owing to a Psyllid disease of the flowers, this pest destroying the entire flower-crops. At the same time it is necessary to record that non-diseased flower-crops sometimes produce absolutely no fruits despite the presence of myriads of Apis mellifica, the most efficient pollinator; apparently fertilization does not take place, but the reasons for this are not at all clear.

The fruits mature 6 to 8 months after fertilization, but most of them fall prematurely, due to the action of wind. (The trees are seldom visited by birds and mammals.)

The germinative capacity of the drupes of normal trees is sometimes 50 to 70 per cent, but more usually the fertility is of the order IO to 20 per cent only. Mould fungi and the larvae of a fruit fly being responsible for many non-viable germules.

Germination takes place within I I/2 to 3 months, the crown-influence- zones of large fruiting trees bearing many thousands of first-stage plants. Within a few days parasitic fungi, principally Pestalozzia sp. (much re- sembling in its work P. Hartigi Tbf.), thin out the communities-a work they continue until but a few plants remain. Mice and blue buck are much attracted to the seedlings, and destroy a very large proportion of those that escape the ravages of the Pestalozzia and other fungi.

On open sites the first-stage plants are lesioned immediately, and die from sun-scorch in very large numbers.

On account of the long periods separating efficient seed-years, the stock- ing of Apodytes regeneration at times becomes very low. Later-stage plants are destroyed by bush buck (Tragelaphus sylvaticus), which relishes the foliage and bark.

Apodytes dimtidiata, therefore, holds its place only after experiencing severe losses in the attempt to assert itself.

October, I927 MORTALITY IN TREES IN KNYSNA FORESTS 443

GONIOMA KAMASSI E. Mey.

This small but valuable tree produces full flower-crops at 3 to 4 year intervals. Even in " full" years, the flowers are by no means numerous.

Full flower-crops by no means indicate full fruit-crops, since the degree of effective pollination is very low-i to 5 per cent only, of the total being fertilized. This is to be accounted for by the fact that the honey-bee does not visit the long-tubed flowers, the pollinators being Nectariniidae which are comparatively rare in the darker portions of the forests (Gonioma is a sub- story tree experiencing strong shade) Anthophora and Xylocarpa species and several species of Lepidoptera, which are by no means abundant.

The follicles take 6 to 8 weeks to mature, but, not being firmly seated, are thrown by strong wind prematurely. The numerous, large-winged, flat seeds are 30 to 40 per cent fertile, but are much destroyed by small Curculionidae.

On falling to the soil the seeds are attacked by mould fungi and various insects, and but a few of the viable germules ever succeed in germinating.

The seedlings on first appearance are very delicate, and readily die unless suitable establishment conditions are available. They are rare within the forests. Fortunately the species forms natural " layers " and thus propagates itself vegetatively.

Discussion Much additional evidence of the same kind could be adduced, but suf-

ficient data have been brought forward to exemplify the nature and the in- fluence of the mortality in the life of the Knsyna forests.

It is clear from the foregoing accounts that each of the species dealt with has a definite struggle with various physiological disabilities, biotic foes, and habitat conditions. In addition, it is seen from a study of plant succession that each of the species loses many germules and many seedlings through the influences of other species, particularly those of species forming dense layers in the forests (e.g. Hemitelia capensis, tree fern, in moist forest, and Trichocladus crinitus, in medium-moist and dry forests) and those of fast- growing, weedy species (e.g. Helichrysum petiolaturn, Plectranthus fruti- cosus, and Cyperaceae) in exploited forest. Low light-intensity, insufficiency of soil-moisture, or excessive soil-moisture, with accompanying high acidity, and mechanical pressure, are some of the more important reactions of these communities. Either singly or combined, these factors have much to do with the poverty of flower-crops, the germination of seeds, and the disappearance of regeneration.

Obviously, mortality is but the potent implement of natural selection- the survivors on being tried by the fire are found worthy of existence, and are entrusted with the transmission of the germ of life of their respective species.

The biology of the various forest species, together with the more pro- found biology of the forest community, cannot adequately be investigated or

444 JOHN PHILLIPS Ecology, Vol. VIII, No. 4

explained unless the role of agencies of discomfort, of disease, and of death, be given study and consideration.

It is natural that agencies of mortality should definitely influence the general distribution of a species-perhaps favoring one species in as much as it hinders the spread of a second and competing species, perhaps prevent- ing spread of a third species, perhaps killing out a fourth.

Again in the process of succession, the dominance, the subjugation, or disappearance of a species, in a community or region, may be traceable to a niortality-factor-complex, powerful in action but undetectable except by study of the life-histories of the species of the region and of the communities they form.

Furthermore, it is not going beyond facts to contemplate the evolutionary importance of mortality in stimulating variation in plant forms.

Finally, the nature of the relationships of the factors responsible for mortality, species by species, is of fundamental importance in the practice of forestry.

Summary

I. Attention is directed to the importance of the study of the causes of mortality in plant communities.

2. The factors mainly responsible for mortality in flowers, fruits, and young regeneration, are listed.

,. The more important factors responsible for death in flowers, fruits and young regeneration of Podocarpus elongate L'Herit., P. Thunbergii Hook., Platylophus trifoliatus Don., Cunonia capensis L., Ocotea bullata E. Mey., Olinia cymosa Thunb., Faurea McNaughtonii Phill., Myrsine mela- nophleos R. Br., Apodytes dimidiata E. Mey., and Goniorna Kamnassi E. Mey., important trees of the Knysna forests, are briefly discussed.

4. The general importance of mortality is stressed.

LITERATURE CITED

Bews, J. W. 1920. The Plant Ecology of the Coast Belt of Natal. Annals Natal Museum, IV (2).

Clements, F. E. 1916. Plant Succession. Pub. 242, Carnegie Inst., Washington. Phillips, John. I924. Biology, ecology, and sylviculture of " Stinkwood " (Ocotea

bullata E. Mey.). South African Jour. Sci. XXI. . 1925. Platylophus trifoliatus Don: A Contribution to its Ecology. South

African Jour. Sci. XXII. 1926. Biology of the flowers, fruits, and young regeneration of Olinia cymosa Thunb. (" Hard Pear "). ECOLOGY, 7: 388-350. I927. Faurca McNaughtonii Phill. (" Terblanz ") A Note on Its ecology and distribution. (Read before Royal Society of South Africa, Oct. 20, 1926.)

Schonland, S. 1924. On the theory of age and area, Ann. Bot., Vol. 38, No. 151. Watt, A. S., 1919. On the causes of failure of natural regeneration in British

oakwoods. Jour. of ECOL. 7: 173-203. 1923. On the ecology of British beechwoods. Jour of ECOL. 11: 1-48.