Chapter XXX: The Viviparous Mangroves of Fiji (2)

_The means of dispersal of the genus Rhizophora_

My experiments and observations were for the most part made on the Asiatic and American species in Fiji; but I enjoyed the opportunity of confirming some important points on the coast of Ecuador. We can only look to the currents for the explanation of the capacity of the genus to cross tracts of ocean; but, given this capacity, there is much that is difficult to understand in the distribution of the genus and of a species like Rhizophora mangle; and it is probable that we shall have to look behind the means of dispersal to a distant age in the distribution of shore-plants of the mangrove type.

When Schimper published his work on the Indo-Malayan strand flora in 1891, but little was known of the duration of the floating capacity of Rhizophora seedlings (p. 166). In giving the results of my investigations I am merely describing the agencies of dispersal at present in operation. Such agencies have their limitations, and we may, perhaps, be thus able to explain why Rhizophora is restricted in the Pacific islands to the archipelagoes of the Western Pacific; but many serious objections would at once present themselves if we regarded the occurrence of the genus in America, as well as in Asia and Africa, as a matter depending on capacities and means of dispersal.

The fruits of Rhizophora, as they display themselves before the protrusion of the germinating seed, have no buoyancy, and the germinating fruits until the hypocotyl has protruded for some inches (6 inches in the case of R. mangle) also sink in sea-water. With a further increase in the length of the hypocotyl, the germinating fruit acquires buoyancy; and when the seedling, usually 10 or 11 inches in length, becomes detached from the fruit on the tree and falls into the sea, it floats readily in 95 per cent. of the cases. Such seedlings occur very commonly in the floating drift of the estuaries and out at sea both in Fiji and in Ecuador.

Out of five seedlings of the Asiatic species, Rhizophora mucronata, that had fallen naturally from the tree, three were afloat and healthy after eighty-seven days’ immersion in sea-water. Out of twenty seedlings of the American mangrove, Rhizophora mangle, sixteen floated after ninety days and four were afloat and healthy after one hundred and twenty days, the greater number sinking during the fourth month. These results indicate considerable powers of buoyancy, and go to show that extensive tracts of ocean could be traversed by the floating seedling.

It should, however, be observed that not all the full-sized seedlings float. With Rhizophora mangle about 5 per cent. sink in sea-water and from 20 to 50 per cent. sink in fresh-water; whilst with R. mucronata the proportion of non-buoyant seedlings is rather greater. There would thus appear to be a rather nice adjustment of the specific weight of the seedlings to the density of sea-water. Generally speaking, they may be seen floating vertically or steeply inclined in the fresh-water of estuaries and horizontally in the sea. With the buoyant seedlings of Rhizophora mucronata, as a rule, about 90 per cent. float horizontally in sea-water, and about 70 per cent. float vertically or steeply inclined in fresh-water. The same general rule applies to R. mangle, whether in the rivers and seas of Fiji or in those of Ecuador. In those cases where the seedling drops prematurely on account either of storms and floods or of the depredations of a grub that frequently attacks the fruit, this rule would not apply. One may frequently notice in Fiji after heavy weather that seedlings detached prematurely, and often carrying the fruit, are floating in numbers horizontally in the rivers. In a few days, as a rule, the fruit-case becomes detached and sinks.

It may be remarked that the horizontal position is much better adapted for the safety of the seedling in transport than the vertical position. In the last case the plumule, which protrudes above the water, would be unable, as indicated in my experiments, to withstand the scorching rays of the sun in a smooth sea; whereas in the horizontal position, which the seedlings assume in sea-water, the plumule is more or less completely submerged, and the risk of withering in the sun is very much less. The Rhizophora seedlings would certainly have little chance of crossing in safety a large tract of sea, if they floated, as they do in river-water, with the plumule exposed above the surface. It is not unlikely that the comparatively restricted area occupied by Rhizophora conjugata may be due to the attitude its seedlings assume when floating in sea-water.

The stranded seedlings of Rhizophora readily establish themselves for a while in very different situations; and it is by no means necessary that they should be washed ashore on a muddy coast. When half-buried amongst the heap of vegetable drift piled up on a sandy beach they are frequently to be found striking into the sand and showing their first leaves. Here they ultimately perish in the great majority of cases; but when protected long enough to reach the moist sand four or five inches below, they may give rise to a little mangrove colony. When caught in a fissure in the bare reef-flats these plantlets are sometimes able to establish themselves. Rhizophora seedlings would, however, require a coast prepared by them by the work of ages before they could form extensive swamps. It is, therefore, not surprising that Prof. Penzig found no evidence of mangrove-settlements on the shores of Krakatoa fourteen years after the eruption.

Yet suited as Rhizophora seedlings are for crossing tracts of sea, I regard them as quite unfitted for being transported by the currents unharmed across an ocean. The plumular bud is insufficiently protected for such a long voyage of many months, and perhaps of years. Though the horizontal position of the seedling would secure the plumule against being scorched in the sun, it increases considerably the risk of injury from direct impact.

As bearing on their capacity for dispersal in other fashions, it may be remarked that Rhizophora seedlings can withstand long drying. Five which had been kept dry for nine weeks, after having been found stranded on a beach, were planted in the mud of a mangrove-swamp. In a fortnight two of them were developing the first leaves and throwing out roots. As long as they are protected by a covering of vegetable _débris_ and sand, the stranded seedlings might retain their vitality for months.

BRUGUIERA RHEEDII (Blume)

This species is reduced in Hooker’s _Flora of British India_ to Bruguiera gymnorhiza (Lam.), and thus viewed it has a very wide range in the Old World, corresponding very much to that of Rhizophora mucronata, namely, tropical East Africa, tropical East Asia to the Liukiu Islands, the Indian Archipelago, New Guinea, tropical Australia, and Western Polynesia, as in New Caledonia, Fiji, Tonga, and Samoa. There are four or five species of the genus, but all are confined to the Eastern Hemisphere, none occurring in America.

As with the species of Rhizophora, this plant is indebted for its present dispersal to the floating seedling, which, however, often falls from the tree whilst still attached to the fruit, but is generally freed in a day or two. The seedlings float for a long time in sea-water. I kept one of them afloat for 117 days, when it was quite sound and healthy. They appear to be better fitted than the species of Rhizophora for the “rough-and-tumble” of ocean transport, since the plumule is much less prominent, projecting only one line (2·5 mm.) or less, whilst with the two Fijian species of Rhizophora the plumule measures from seven to twelve lines (18 to 30 mm.). In the latter part of the year they are to be found in abundance in the floating drift of rivers, and there they readily develop the first leaves and roots. They are also frequent in the sea off the coasts, and they are stranded in large numbers on the beaches, where they readily strike into the sand when partially buried amongst the vegetable drift.

The empty flowers and the germinated fruits containing the cotyledons are very common in floating drift. They look much alike, but the flowers are much smaller and possess the long style, whilst the fruits contain the cotyledons at the bottom of the seed-cavity.

As with Rhizophora, there is a rather curious adjustment of the buoyancy of the seedling to the density of sea-water. About 75 per cent. of those afloat in the fresh-water of rivers assume the vertical position, the plumular end protruding between two and five lines (5 to 12 mm.) above the surface, while the remainder float horizontally or nearly so. In sea-water about 50 per cent. float either vertically or steeply inclined, and the other half float horizontally.

With regard to the times of flowering and fruiting, it may be remarked that the trees are mostly in flower during the hot months from November to February, and that the fruiting is in active operation in the latter half of March. The floating seedlings occur in abundance in the river-drift at the end of the year, a circumstance which corresponds with the fact that a period of six months passes between the fertilisation of the ovule and the fall of the seedling into the water.

Fertilisation, or, more correctly speaking, the discharge of the pollen, takes place after the opening of the flower, and not before, as in the case of the species of Rhizophora. The flower-bud is at first erect, but subsequently it begins to bend downwards, and ultimately it hangs more or less vertically. The provision to secure fertilisation under these circumstances is rather curious. Without some such contrivance as is below described, the pollen would merely fall out of the flower. Each petal has its sides rolled or folded inwards so as to completely inclose two stamens. In the bud the folded petals are white and flexible, but as the flower expands they redden and become dry and elastic, and are only prevented from flying open with a spring by the interlocking of the hairy tips of their lobes. Whilst the folded petals are becoming stiff and elastic during the opening of the flower, the inclosed stamens are at the same time preparing themselves for their function. The anthers are dehiscing and the filaments are acquiring elasticity. All is now ready, and a slight shake or a touch puts the mechanism into action. The petals unfold themselves with a spring, and the stamens thus suddenly exposed and released fly forward, and a little shower of pollen is thrown towards the centre of the flower. This process is accomplished in ordinary fine weather during the first twenty-four or thirty-six hours after the expansion of the flower. When the opening occurs in the early morning, half of the stamens will be found released in the evening and the rest on the following day. During the next day or two the petals and the stamens fall out of the flower. In wet weather, the petals never acquire elasticity, and in consequence do not unfold. In this case pollenisation is never effected, and the folded petals soon fall to the ground, carrying the stamens within them. Cross-fertilisation would be much more likely to occur with species of Bruguiera (if, as is probable, the same process of pollenisation is usually followed) than with species of Rhizophora, since the stamens are securely inclosed in the petals for some hours after the expansion of the flower.

Nearly eight weeks pass between the date of fertilisation and the commencement of germination. This is somewhat similar to the period given for Rhizophora mangle, namely, nine weeks, and it obviously leaves little or no time for any stage of quiescence or dormant vitality in the case of the seed. The changes which the fruit undergoes in this interval are a considerable increase in girth and a thickening of the calycine walls, together with a contraction of the mouth of the tube. However, I found no method sufficiently accurate for recording the rate of increase of the fruit.

It is known that germination is in progress when the end of the hypocotyl begins to lift up the lining membrane at the bottom of the calycine tube (see Figs. 21 to 26). The floor of the tube begins to bulge up, but since this cannot be well seen at first, a better index is afforded in the elevation of the style which accompanies it. The top of the style preserves previous to this time a constant level with regard to the tips of the calycine teeth. But this does not indicate the actual beginning of germination. As shown in Fig. 21, the seed lies about two and a half lines (6 mm.) below the floor of the calycine tube, and the tip of the hypocotyl has to penetrate the intervening tissues before it can push up the lining membrane and raise the style. Judging from the subsequent rate of growth, seven or eight days at least, and perhaps as much as two weeks, are requisite for this purpose. It is not necessary to give further details here, and it may be at once stated that the average of numerous observations on the length of the interval between fertilisation and the elevation of the style was sixty-four days, the range being fifty-nine to sixty-nine. After deducting ten days for the time occupied for the radicle in reaching the floor of the calycine tube (see Figs. 22 and 23), we obtain, as already remarked, nearly eight weeks as the time elapsing between fertilisation and germination.

The radicle or hypocotyl, therefore, in the first stage of germination pierces the tissues above it and reaches the floor of the calycine tube. It does not, however, pierce the lining membrane of the tube but pushes it upward until it ruptures about 4 millimetres below the base of the style which is carried up with it. Thus a kind of cap is formed, as shown in Fig. 24, which does not fall off from the end of the hypocotyl until it has protruded rather more than an inch. The hypocotyl attains a length varying between 5 and 11 inches, the average being about 8 inches.

The whole period may be thus divided up:—

(1) Period between fertilisation and germination 7-1/2
weeks.

(2) Period between the beginning of germination and the 1-1/2 protrusion of the point of the hypocotyl at the floor of the weeks. calycine tube

(3) Period occupied in the growth of the hypocotyl 8 inches 18 weeks. outside the fruit and terminating in the fall of the seedling

——

Total 27 weeks.

The total period of twenty-seven weeks between fertilisation and the fall of the seedling is thus six weeks shorter than that estimated for Rhizophora mangle. On comparing the two tables it will be seen that the difference mainly lies in the length of the second period, namely, that between the commencement of germination and the protrusion of the hypocotyl from the fruit. With Rhizophora mangle the fruit grows considerably in length during this period of the germinating process. On the other hand with Bruguiera rheedii there is, during this period, practically no increase in the length of the fruit, and the radicle has only to penetrate the tissues, 2-1/2 lines in thickness, between the seed and the floor of the calycine tube.

In the mode of separation of the seedling there are very marked differences between this species of Bruguiera and the species of Rhizophora. With Bruguiera rheedii the four small cotyledons, which are united at the base, are, however, left behind at the bottom of the seed-cavity, when the seedling is detached. But there is no expulsion of the seedling, the connection being ultimately severed at the contracted base of the cotyledons inside the fruit. When the seedling is full-sized the nutritive supply begins to fail, and in consequence the pressure of the sides of the fruit on the inclosed plumular end of the seedling becomes slacker, the union with the cotyledons becomes weaker, and the connection of the fruit with its peduncle at the basal joint becomes slighter. Usually the fruit falls before the seedling is ready to drop out, and the connection is severed after a few days’ flotation in the water; but sometimes the union between the seedling and fruit is weaker than that between the fruit and its peduncle, and in that case the seedling falls and leaves the fruit containing the cotyledons on the tree. The whole process of separation is much simpler than with species of Rhizophora. Here it is mainly a matter of the failure of the nutritive supply, whilst with Rhizophora it is almost a process of parturition.

Haberlandt, in the memoir before quoted, describes quite a different mode of detachment in the case of Bruguiera eriopetala. Here the seedling falls normally whilst still attached to the fruit, and the separation is subsequently effected by the expansion of the mouth of the calyx-tube due to the swelling of the “endosperm-neck” from the entrance of water.

_Summary_

(1) There are four typical mangroves of the Rhizophoraceæ in Fiji, Bruguiera rheedii, Rhizophora mucronata (the Asiatic species), Rhizophora mangle (the American species), and the Selala, a seedless form intermediate between the two species of Rhizophora just named, but nearest to the Asiatic species.

(2) It is shown that the sterility of the Selala is connected with the impotent character of the pollen; and since the ovules appear capable of fertilisation this is held to indicate that cross fertilisation has not been in operation in producing the barren form.

(3) Good reasons are given for the belief that the Asiatic species of Rhizophora is the parent of the Selala, not as the result of a cross between the Asiatic and American species, but as connected with dimorphism, the Asiatic species producing two kinds of offspring, one of them with impotent pollen.

(4) In support of this view it is pointed out that there are two forms of Rhizophora mangle in Ecuador, one of which comes near the Fijian Selala, though producing seed. There could thus be no question of crossing, since but one species occurs there.

(5) The Selala reproduces itself in a vegetative fashion when growing, as it often does, in an inclined position. The parent trunk dies and the primary branches supported by the aërial roots, remain alive and in their turn give rise to secondary branches similarly supported.

(6) Although, as a rule, only one of the four ovules of Rhizophora becomes a seed, occasionally a fruit contains more than one seed. With R. mangle in Fiji about one per cent. of the germinating fruits displayed more than one hypocotyl.

(7) As a result of a protracted series of observations in Fiji, it was established that in the case of a seedling of average length of Rhizophora mangle a period of thirty-three weeks elapsed between the date of fertilisation of the ovule and the detachment of the seedling from the tree. In the instance of R. mucronata it was placed at forty-two weeks. A period of thirty-eight weeks, or nine to ten months, is regarded as typical for the genus.

(8) It is established that normally there is no rest-period for the seed in the case of Rhizophora, the seed at once beginning to germinate on reaching maturity. In those exceptional instances, however, where there is more than one seed, it is shown that in some cases the seeds do not begin to germinate together, and that a rest-period of at least some weeks can be at times postulated for one of the seeds.

(9) An analogy exists between the process of expulsion ending in the detachment of the seedling of Rhizophora from the fruit and the process of parturition.

(10) Experiments show that Rhizophora seedlings can float unharmed in sea-water for a period of at least three or four months. Though nine-tenths or more float in sea-water, as much as a fourth or a half sink in fresh-water. As a rule they float vertically in fresh-water and horizontally in sea-water, the horizontal position safe-guarding the plumule against the risk of being withered up by the sun in a calm sea.

(11) It is shown that in the case of Bruguiera rheedii the seedlings when detached from the tree can float unharmed in sea-water for months. In their specific weight they display a similar fine adjustment to the density of sea-water, as is above described in the case of Rhizophora.

(12) With this species of Bruguiera, fertilisation takes place not in the unopened flower, as in Rhizophora, but after the flower’s expansion; and a very singular mechanism is here described which secures the completion of the process.

(13) A period of twenty-seven weeks elapses between the fecundation of the ovule and the detachment of the seedling from the tree in the case of Bruguiera rheedii; and it is shown that there is normally little or no room for any rest-period, and that, as with Rhizophora, the seed on reaching maturity begins to germinate.

(14) Though the seedlings of Rhizophora and Bruguiera could be transported in safety a few hundred miles across the sea, it is held that they could never cross the Pacific and reproduce the plant. That the American species of Rhizophora has reached the Western Pacific from the New World is not accepted. Rather is its present distribution regarded as representing its original wide range over much of the tropical zone.