Chapter XXX: The Viviparous Mangroves of Fiji (1)

RHIZOPHORA AND BRUGUIERA

_Rhizophora._—Represented by Rhizophora mucronata, Rhizophora
mangle, and the Selala, a seedless intermediate form.—Their
mode of association and characters.—The relation of the
Selala.—Polyembryony.—The history of the plant between the
fertilisation of the ovule and the detachment of the seedling.—Absence
of a rest period.—Mode of detachment of the seedling. Capacity
for dispersal by the currents.—_Bruguiera._—The mode of
dispersal.—Peculiar method of fertilisation.—Length of period between
fertilisation and the detachment of the seedling.—Mode of detachment
of the seedling.—Summary.

BETWEEN 1897 and 1899 I made numerous observations on the Fijian species of Rhizophora and Bruguiera (mostly around the coasts of Vanua Levu and in the Rewa delta); and these were supplemented in the early part of 1904 by observations on the first-named genus in Ecuador. I did not make any collections in Fiji until Prof. Schimper asked me to obtain specimens; and a fair-sized collection containing specimens dried, and preserved in spirit, was sent to him. His illness and death shortly followed, and I lost the advantage of his great experience in these matters. In a letter written to me in 1898 he expressed the hope that I would publish my notes on the mangroves of Fiji. Years have since passed by, and as I read again his words of encouragement I take up once more the interrupted task.

RHIZOPHORA

Of the three species of this genus, two of them, Rhizophora mucronata and R. conjugata, are Asiatic and are unknown in America; whilst the third, R. mangle, was until recently regarded as peculiar to the American and West African regions.

When Mr. Hemsley wrote the Report on the Botany of the Challenger Expedition he remarked (iii, 149) that the American Rhizophora (R. mangle) appeared to be restricted to that region, and he questioned its existence in the Pacific Islands as indicated by Jouan for New Caledonia. The same view was taken by Prof. Schimper in his work on the Indo-Malayan strand-flora published in 1891. There was, in fact, much to support this view, since Dr. Seemann, one of the most accomplished botanists who have explored the Pacific, describes only the Asiatic Rhizophora (R. mucronata) in Fiji, and nothing is said of any other species collected by the United States Exploring Expedition under Wilkes in Fiji and Samoa.

However, in a paper on the flora of Tonga, read before the Linnean Society in 1893, Mr. Hemsley includes the American mangrove, Rhizophora mangle, amongst the collections made there by Mr. Lister; and he refers to its occurrence also in Stewart Island (I suppose in the Solomon Group), but he suggests that it was accidentally introduced with ballast in both these localities. In 1897 I found a species of Rhizophora, to all appearances identical with the American species, in great abundance in the Rewa delta in Fiji. Subsequently the same mangrove came under my notice as the prevailing species in Vanua Levu in the same group; and on sending photographs of a branchlet in flower and fruit and of the germinating fruit to Prof. Schimper he expressed the opinion that they belonged to the typical Rhizophora mangle.

There are four typical mangroves in Fiji, namely (1) Bruguiera rheedii, the “Dongo” proper of the natives; (2) Rhizophora mangle, usually known as “Tiri-wai,” that is to say, the Tiri of the river, or rather of the estuary; (3) Rhizophora mucronata, the “Tiri-tambua” of the Fijian, signifying the Whale’s Tooth Tiri in allusion to the form of its fruit; and (4) a seedless form intermediate between the two species of Rhizophora, which the Fijians designate “Selala,” a name signifying “the tree with empty flowers.”

Bruguiera rheedii and Rhizophora mucronata were alone recorded by Dr. Seemann and his predecessors; but he significantly refers to the natives speaking of four mangroves. Mr. Horne, who spent twelve months in the group some years later, also overlooked the American Rhizophora; but it is apparent that both these botanists were naturally more interested in the vegetation of the inland regions than of the coast swamps, and we have before observed that they failed to record Scirpodendron costatum, a giant-sedge very common and conspicuous in the swamps. It is not easy to understand Dr. Seemann’s remark that “mangroves are restricted to but few parts of the larger islands.” Horne, who was in the islands eighteen years afterwards, makes frequent allusion to them. The natives whom I questioned closely on this subject scouted the idea that any of the four mangroves above named were recent arrivals. The coasts, as they said, had always been extensively fringed by mangroves; and the reader has only to refer to my remarks in the second chapter of my volume on the geology of Vanua Levu to convince himself that mangrove swamps of considerable extent existed in the time of Commodore Wilkes (1840).

_The Relative Abundance and Mode of Association of the three Fijian
forms of Rhizophora._

Stated in their order of frequency, we have first Rhizophora mangle, the American species, then Rhizophora mucronata, the Asiatic species, and lastly the Selala. The first is equally at home at the sea-border and on the banks of brackish estuaries. The second is, as a rule, more exclusively at home on the sea-coasts; and the same may be said for the Selala. Usually all three kinds occur in the lower part of an estuary; but as we ascend the river and the water freshens, the Asiatic Rhizophora and the Selala disappear, and the American plant is alone found in the higher reaches, where the density of the water ranges according to the state of the tide between 1·000 and 1·010. I examined the distribution of these three forms of Rhizophora in numerous estuaries of Vanua Levu, as well as in the Rewa estuary in Viti Levu; and it was ascertained that in all cases they followed the rule above indicated. When the estuary receives but few streams and the water is mostly salt, the three Rhizophoras may extend miles inland; but when it contains a large body of fresh-water, Rhizophora mangle may be the only form observed from the mouth of the river to the head of the estuary, and it may monopolise the adjacent coasts. On the other hand, Rhizophora mucronata may occupy almost exclusively a long extent of coast; or the Selala may prevail in certain localities, as on parts of the Mathuata coast of Vanua Levu.

The manner of association of these three Rhizophoras is of interest in connection with the origin of the seedless Selala. They very rarely occur mingled together, but grow gregariously in contiguous colonies; and not uncommonly all three may occur on the same line of coast within a distance of a few hundred yards. The colonies pass into each other without a break, and there is no fixed rule of association. Whilst on the south side of Vanua Levu the Selala is generally associated with the American Rhizophora, on the north side it is usually in touch with the Asiatic species. In other localities all three occur in contiguous colonies. The Selala colony may be exposed on the line of a river-bank or along the sea-coast, or it may lie in the heart of an extensive mangrove tract. The most extensive mangrove region in Fiji, that of the Rewa delta, is in great part occupied by Rhizophora mangle; but all three forms grow together in the eastern part of the delta; and here, strangely enough, as at Daku, the Selala may grow sporadically, and all three may grow mixed together with their branches intercrossing.

_The Characters of the Selala or Seedless Rhizophora compared with those
of the American Mangrove (R. mangle) and the Asiatic Mangrove (R.
mucronata)._

The three kinds of Rhizophora, when seen at the same time along a tract of coast, may be readily distinguished by the different shades of green of their foliage, that of Selala being dark green, that of Rhizophora mucronata light green, and that of Rhizophora mangle intermediate in shade. The Selala is usually the tallest of the three, and attains a height of from 20 to 30 feet or even 40 feet and over, the aerial roots dropped from the higher branches giving it a characteristic aspect. Rhizophora mangle is generally the shortest, and at the coast is from 10 to 12 feet high; but where the mangrove vegetation is most luxuriant, as in the great swamps in the interior of the Rewa delta, it forms tall trees as much as 40 feet in height, displaying the aerial roots hanging from the higher branches. Rhizophora mucronata is, as a rule, intermediate in height, and is distinguished by its stout, reddish trunk and reddish aërial roots.

The trunks of Selala are often in an inclined position and supported entirely by the trestle-like aërial roots, the lower end raised some 5 or 6 feet above the ground with the rest of the trunk inclined upwards. They then look like gigantic walking-stick insects. The same habit may be sometimes observed with the larger trees of Rhizophora mucronata, and in fact all three may present at times the same habit of growth. The taller trees of Rhizophora mangle may resemble the Selala in habit, and the smaller trees of the Selala may approach the habit of Rhizophora mangle.

The distinctive characters of the Selala are given in the table opposite. It will be there seen that this form is intermediate between the other two species as regards the form and size of the petioles and peduncles; the size of the bracts and bracteoles; the colour, form, and size of the flowers; and in the length of the style. Its leaves are smaller than in the case of the other two species, but pointed and semi-aristate like those of Rhizophora mucronata. There are, however, two varieties of the Selala, both with larger foliage than that belonging to the prevailing type of the tree, and from 10 to 15 feet in height. In one the flowers are more numerous, each flowering stem branching four or five times and bearing at least twenty-four flowers, the first branch being trichotomous and the rest dichotomous. In the other, which is the prevailing form on the Mathuata coast, there is a nearer approach to Rhizophora mucronata in the rounding of the peduncles and in the length of the style. Then, again, there are divergent varieties of Rhizophora mangle which in the larger bracts and bracteoles and in the greater size, form, and paler hue of the flowers come nearer to the Selala. Taking all the characters together, the Selala, though intermediate between the Asiatic and the American species, comes in the most critical diagnostic points, as in the inflorescence, in the individual flowers, and in the form of the apex of the leaf, nearest to Rhizophora mucronata, the Asiatic species.

The seedless character of the Selala is well known to most Fijians of the coast districts, the native name signifying empty (lala) flowers (se). Now and then they aver that it produces fruit, but the numerous offers of rewards in money never resulted in their bringing me the fruits. During my residence of two years in the group I examined the Selala trees in a great number of localities and never succeeded in finding them in fruit.

With all three kinds the anthers burst in the bud before it begins to open, and we may ask why the process of self-fertilisation, which is effectual with the other two kinds, produces no result with the Selala. In all three cases the flower-buds and expanded flowers hang downwards, and the expanded flowers retain their parts for the first twenty-four hours, the pollen being caught in quantity on the hairy edges of the petals. During the next day the withering stamens fall out, and on the following day the petals fall too. With the Selala, the style soon begins to blacken and wither, and in a few days the flower becomes detached and drops off. With Rhizophora mucronata and Rhizophora mangle, the style preserves its healthy condition, and shortly evidences of fertilisation appear in the altered shape of the ovary. It is apparent, therefore, that in the case of the Selala fertilisation has not occurred, although the mechanical processes connected with it have been carried out. The cause of this is not far to seek.

+-----------------+--------------------------------------------------------+ | | FIJI | | CHARACTERS +------------------+------------------+------------------+ | | RHIZOPHORA | SELALA (a | RHIZOPHORA | | | MUCRONATA. | seedless form). | MANGLE. | +-----------------+------------------+------------------+------------------+ |Height of tree | | | | | in feet | 12-20. | 20-40. | 9-12. | | | | | | |Colour of foliage|Pale green. |Dark green. |Intermediate | | | | |shade. | | | | | | |Base of leaf |Tapering. |Sub-rounded. |Tapering. | | | | | | |Apex of leaf |Acute, and |Acute, and |Very obtuse, | | |terminating |terminating in |with no | | |in a twisted |a twisted point |twisted point. | | |point a line |less than a line | | | |(2·5 mm.) long. |(2·5 mm.) long. | | | | | | | |Leaf-stalk |Rounded, 1 - |Rather flattened |Length as in | | (petiole) |1-2/10 inch, |horizontally, |Selala, but | | |(25-30 mm.) long, |5-8/10th inch |flattening | | |about as long as |(12-20mm.) long, |very marked. | | |the peduncle. |shorter than the | | | | |peduncle. | | | | | | | |Inflorescence |Branching |Branching usually |Usually branching | | |(dichotomous) two |twice, but |only once | | |or three times |sometimes three |(trichotomous) and| | |with four to eight|times; first |bearing only three| | |flowers. |branching |flowers; but | | | |trichotomous, rest|sometimes | | | |dichotomous; six |branching again | | | |to twelve flowers;|(dichotomous) and | | | |in one variety, |bearing then six | | | |flowers as many as|flowers. | | | |twenty-four. | | | | | | | |Peduncle (lowest}|Rounded. |Flattened above. |{Flattening more | | flower-stalk) }| | |{marked than with | | | | |{Selala. | | | | | | |Pedicels |As stout as the |More slender than |As in Selala. | | |peduncle, and |the peduncle, and | | | |rounded. |angular. | | | | | | | |Bracts and |Large, 1-1/2 line |Small, 2/3 line |Very small or | | bracteoles |(4 mm.). |(2 mm.). |absent. | | | | | | |Calyx |Very pale yellow, |As in R. |Pale or bright | | |or dirty white, |mucronata. |green, angular at | | |rounded at base | |base in the bud, | | |in the bud, lobes | |lobes 3-1/2 lines | | |4-1/2 - 5 lines | |(8 mm.). | | |(11-12 mm.). | | | | | | | | |Length of style |1-1/2 lines |1 line (2·5 mm.). |1/2 line | | |(4 mm.). | |(1·5 mm.). | | | | | | |Fruit |Ovoid and usually |No fruits |Conical, somewhat | | |symmetrical, with |produced. |curved, and thus | | |large persistent | |not symmetrical; | | |bracteoles at | |bracteoles at base| | |base. | |very small or | | |(Hypocotyl 16 | |absent. | | |inches.) | |(Hypocotyl 9 or | | | | |10 inches.) | | | | | | |Colour of trunk, | | | | | rootstock and | | | | | roots |Reddish. | — | — | +-----------------+------------------+------------------+------------------+

+-----------------+-------------------------------------+ | | ECUADOR. | | CHARACTERS. +------------------+------------------+ | |RHIZOPHORA MANGLE |RHIZOPHORA MANGLE | | | (Mangle chico). | (Mangle grande). | +-----------------+------------------+------------------+ |Height of tree in| 10-15. | 50-80 and more. | | feet | | | | | | | |Colour of foliage|Pale green. |Dark green. | | | | | |Base of leaf |Tapering or |Tapering. | | |sub-rounded. | | | | | | |Apex of leaf |Very obtuse, with |Very obtuse, with | | |no twisted point. |no twisted point. | | | | | |Leaf-stalk |Flattened above |Flat above with a | | (petiole) |and below, with no|median groove, | | |median groove, |1 inch (25 mm.) | | |1/2 inch (12 mm.) |long, two-thirds | | |long; not half as |the length of the | | |long as the |peduncle. | | |peduncle. | | | | | | |Inflorescence |As described under|Branching at least| | |R. mangle of Fiji.|three times, | | | |sometimes four or | | | |five times, | | | |trichotomous or | | | |dichotomous, | | | |twelve to | | | |forty-eight | | | |flowers. | | | | | |Peduncle (lowest}| | | | flower-stalk) }|}Sub-angular. |Rounded. | | | | | |Pedicels |More slender than |More slender than | | |the peduncle, and |the peduncle, and | | |rounded. |angular. | | | | | |Bracts and |Scarcely |Well developed, | | bracteoles |developed, 1/2 |1 line (2·5 mm.). | | |line (1 mm.). | | | | | | |Calyx |As with R. mangle |As with R. | | |of Fiji. |mucronata and | | | |Selala of Fiji, | | | |but lobes 4 lines | | | |(10 mm.). | | | | | |Length of style |Less than a line |1-1/2 lines | | |(2·5 mm.). |(4 mm.). | | | | | |Fruit |As in R. mangle of|Conical, not | | |Fiji. |symmetrical, and | | |(Hypocotyl 9 or |somewhat curved; | | |10 inches.) |large persistent | | | |bracteoles at base| | | |as in R. | | | |mucronata. | | | |(Hypocotyl 12 to | | | |15 inches.) | | | | | |Colour of trunk, | | | | rootstock and | | | | roots | — | — | +-----------------+------------------+------------------+

Although the ovaries of the Selala contain four ovules, which in size and appearance do not differ from those of Rhizophora mangle and R. mucronata, its pollen when compared with that of the other two forms presents a remarkable difference. The pollen of these three mangroves was examined in five localities far apart from each other, and in all the same results were obtained. The pollen-grains of the Selala are much smaller than those of the other two, and differ much from them in form. They are irregularly oval in outline, and have a shrunken look beside the spherical symmetrical grains of the two species with which they are compared. They are from one-fourth to one-third the size of those of Rhizophora mucronata, and from one-third to one-half the size of those of Rhizophora mangle.

There is much to support the view that the Selala is a cross between the other two species, its intermediate characters and its seedless condition being especially indicative of such a derivation; but there are several difficulties in accepting this explanation.

(1) The circumstance of the anthers bursting in the flower-bud would considerably lessen the chances of cross-fertilisation; but this objection is not insurmountable, since numerous insects, such as flies, ants, and small coleoptera, visit the newly opened flowers, and they might sometimes produce a result. When I made this suggestion to Prof. Schimper he replied that insect-pollination was quite possible after the expansion of the flowers.

(2) If, as seems highly probable, the pollen of Selala is impotent and the ovules fertilisable, then its seedless condition implies not only an incapacity for self-fertilisation, but also for cross-fertilisation; and if Selala with its impotent pollen does not admit of cross-fertilisation, this would still less be expected of Rhizophora mucronata and R. mangle where the pollen is potent and where fertilisation takes place in the bud. I endeavoured to fertilise the Selala flowers with the pollen of the two other species; but there were no results, the flowers falling off in a few days. It may here be remarked that on one Selala tree I found a solitary flower with an enlarged ovary, as if through fertilisation.

(3) It is not easy to explain the gregarious growth of the Selala if it is a seedless hybrid. The colonies could not be renovated by mere intercrossing, especially in places where, as on the north coast of Vanua Levu, the dense belt of mangrove is for many miles composed in mass of Selala trees, with a few trees of the Asiatic and American Rhizophoras growing on the outskirts.

It is obvious that in order to clear the way for considering this problem the means of renovating the Selala colonies should be inquired into. In the first place, whilst seedlings occur in numbers under the trees of the other two Rhizophoras they are never to be found under the Selala trees. The mode of reproduction of the Selala is evidently vegetative, and the question arises as to what mode of vegetative reproduction occurs. The Selala trunks, as already observed, are often inclined, the trunks being supported on trestle-like aërial roots. These trunks send out branches which in their turn drop aërial roots; and when the decay of the parent trunk takes place, the branches are able to live independently. The primary branches in due time send out secondary branches which also let fall aërial roots; and thus the process is repeated indefinitely, the result being a maze of semi-prone trunks, branches, and aërial roots. The first stage of the process ends with the death of the parent trunk, and the primary branch, supported by its own aërial roots, is often all that the observer can distinguish in the centre of a colony. This is evidently the mode by which the Selala colonies are renovated in their interior. One sometimes observes in the midst of one of these colonies extensive bare mud-flats 100 to 500 yards across from which apparently the trees have died off _en masse_. The natives assert that when part of a Selala tract is cleared the trees never grow again.

But _pari passu_ with this process of vegetative reproduction of the Selala, by which the mass of the colony is preserved and renovated, there is evidently some other process of reproduction in operation amongst the trees of Rhizophora mangle and R. mucronata at the edge of the colony, as a result of which Selala seedlings are produced. Whilst no seedlings are to be observed striking into the mud under the Selala trees, numbers occur, as before observed, under the trees of the other two species. Those under the trees of R. mangle possess in nearly all the cases the distinctive leaf-characters of that mangrove, and would be recognised at once as belonging to that species. On the other hand, those beneath the trees of R. mucronata are of two kinds, some of them being readily recognised by their foliage as of the Selala type others, again, being typical seedlings of R. mucronata. Only those seedlings, or “keimlings” as we might term them, were noted that had dropped plumb from the branches above.

Such were the results of my investigations on Vanua Levu. My field of inquiry was then shifted to the Rewa delta, where, with the assistance of the Daku natives, who, like most Fijians, display a keen interest in matters relating to their plants, I spent a few days in investigating the origin of the Selala trees that grow sporadically in that locality. On pulling up some of the young trees we found that the original radicular or hypocotyledonary portion of the keimling could be still distinguished. My zealous native friends also pointed out to me that though the leaves in form and colour were those of the Selala, the rootstock was reddish like that of R. mucronata, and not white as with R. mangle. The natives averred that the Selala trees are produced in the first place from fruits of R. mucronata. When young, they said, they are Tiri-tambuas (R. mucronata), but when old, Selalas. Yet although R. mucronata may be now regarded as the source of the Selala trees, and my Vanua Levu observations pointed unmistakably in this direction, it could not be definitely settled whether this was the result of a cross with the male element of R. mangle or whether the Tiri-tambua (R. mucronata), in producing two types of seedlings, one fertile with the parent characters and the other seedless of the Selala type, brought about the same end. On the whole I am inclined to the view that the Asiatic Rhizophora presents us in the dimorphism of its seedlings the true explanation.

This inference is supported by the behaviour of Rhizophora mangle on the coast of Ecuador, a subject which is discussed in Chapter XXXII, and I have given the results of my observations on the Ecuadorian Rhizophoras side by side with those on the Fijian trees in the table before given. There are two very distinct forms of the American Rhizophora (R. mangle) in the swamps of Ecuador. There is the low coast tree, the “Mangle chico” of the Ecuadorians, ten to fifteen feet in average height, which grows on the sea-front of the swamps and has all the general appearance and the more conspicuous characters of the American Rhizophora in Fiji. There is also a tall tree, 60, 80, or even 100 feet high, that forms the great mass of the mangrove swamps. In its inflorescence, in the dark green colour of its foliage, and in other characters, it comes near the Fijian Selala; but it differs in fruiting abundantly. This is locally termed the “Mangle grande,” and its true relation to the Fijian Selala appears to be as follows. Whilst both as regards the flowers approach the Asiatic Rhizophora (R. mucronata), the Fijian Selala resembles the Asiatic tree also in its foliage, whilst the “Mangle grande” or the Ecuadorian Selala more resembles the typical American tree (R. mangle) in its leaves and also in its seedlings. Here in the Ecuadorian swamps there can be no question of crossing, since both, according to Baron von Eggers, belong to one species. Therefore I am inclined to the opinion that whilst the Asiatic Rhizophora displays dimorphism in Fiji, the American Rhizophora displays dimorphism in Ecuador. The reversion on the part of the “Mangle grande” of Ecuador to some of the characters of the Asiatic plant is remarkable, and points to the greater antiquity of the Asiatic R. mucronata as compared with the American R. mangle.

This accords with the opinion expressed by Schimper in his work on the Indo-Malayan strand flora that the American Rhizophora is either a degenerated descendant of the Asiatic R. mucronata or a sister form derived from a common ancestor. America, as we have seen, possesses only one of the three species of Rhizophora, and this is the only representative that it owns of the four Asiatic genera (Rhizophora, Kandelia, Ceriops, Bruguiera) that constitute the tribe Rhizophoreæ. The rule prevailing with current-dispersed plants that America is a distributor and not a recipient evidently does not apply to the Rhizophoreæ; and to explain their distribution we must go back to some epoch very remote from the present. That Fiji derived its representatives of Rhizophora mangle from America by the agency of the currents I do not for a moment admit. The restriction of the species and indeed also of the genus to the Western Pacific is very significant. It is far more likely that, as I have pointed out in the case of Lindenia (see page 396), the American Rhizophora was once widely distributed over the tropics of the Old and New Worlds, and that it is now on the “down grade” towards extinction. Its survival in the Western Pacific could thus be explained without our being obliged to suppose that the seedlings or keimlings have been carried uninjured across the Pacific Ocean, an ocean voyage for which, as shown in a later page, they are not well fitted.

_The Occasional Occurrence of more than one Seed in the Fruits of
Rhizophora mucronata and Rhizophora mangle (Polyembryony)._

The bilocular ovary contains four ovules, one of which only as a rule becomes a seed. But it is incorrect to say that the fruits are always one-seeded, since two or even three seeds are occasionally produced, and they may all germinate. In November, 1897, I noted eight hundred fruits of Rhizophora mangle germinating on the trees in one of the creeks of the Rewa delta. Out of this number eight fruits had two germinating seeds and one had three, the protruding radicles being in all stages of growth. Just two years afterwards I counted eight hundred more fruits in the same locality, and then observed seven with two germinating seeds and none with three, the radicles protruding in all cases. On another occasion at Wailevu in Savu-Savu Bay I counted four hundred, and none had more than a single radicle protruding. The results appear to vary with the locality, but in the Rewa creek the proportion of fruits in which more than one seed germinated was fairly constant at dates two years apart, namely, about one per cent. Occasionally, however, in particular localities a greater proportion may be noticed. Thus near Daku in the Rewa delta I found that the proportion was between two and three per cent. for the same species (R. mangle), those with three germinating seeds being about half per cent.

The case of more than one seed germinating in the fruits of Rhizophora mucronata never came under my observation; but in one locality, where I examined a considerable number of fruits near the stage of germination, between ten and fifteen per cent. showed two seeds approaching maturity.

Warming thoroughly investigated the polyembryony of Rhizophora more than twenty years ago, seemingly from materials brought to him from the West Indies (Engler’s _Botanische Jahrbücher_, band iv., 1883). With the usual German thoroughness he deals with the work of earlier observers, and goes back to Piso in the middle of the 17th century. Of the four ovules, he remarks, three usually abort, and only in rare cases are two seeds developed. He quotes Baron von Eggers to the effect that only in three per thousand cases was more than one seedling observed protruding from a germinating fruit. These remarks evidently all apply to the American species. I do not find any reference in my notes to polyembryony in Ecuador, and evidently its occurrence is not so frequent there as in Fiji.

It is frequently apparent in the cases where more than one seed germinates in a fruit that on account of the difference in the length of the protruding seedlings germination does not always begin at the same time. Thus in Fiji the difference in the length varied between one and three inches, an amount representing at least from ten to twenty days’ growth, as will be subsequently pointed out. Warming in one of his figures gives a fruit where an interval of some months seems to be indicated, since one of the seedlings has fallen out and the other is protruding less than an inch. By cutting across a fruit containing two seeds one may sometimes observe one seed quiescent and the other beginning to germinate. The significance of this occasional interval between the germination of seeds in the same fruit will be referred to in a later page.

_The Seasons of Flowering and Fruiting of the Species of Rhizophora in
Fiji._

The Selala flowers all the year. With the two American and Asiatic species there are considerable variations between different localities. Generally speaking, they flower and fruit all the year through; but the flowers are usually less abundant in the warm season from December to February, and the germinating fruits which are to be observed on the trees every month of the year are more numerous in that season.

_The History of the Reproductive Process in Rhizophora from the
Fertilisation of the Ovule to the Falling of the Plantlet or Seedling
from the Tree._

I devoted great attention to this subject in the instance of Rhizophora mangle, being desirous of determining two points, in the first place as to whether there was any period of rest between the maturation and germination of the seed, and in the second place as to the period that elapsed between the commencement of germination and the fall of the seedling.

The principal change in the ovary for the first three or four weeks after fertilisation is shown in its increased breadth. The increase in height is but slight during this period; and in fact after thirty days the ovary only added 2 millimetres to its original height of 3 millimetres. After this the growth of the fruit proceeds until the tip of the radicle pierces its summit, the fruit being then about eleven lines (2·8 cm.) long. _From the date of fertilisation to the time the radicle pierces the top of the fruit a period of about fifteen weeks elapses._ (The fruit, it should be here remarked, continues to grow in length and breadth after the radicle has protruded, attaining a length of thirteen or fourteen lines [3·5 cm.] when the seedling or “keimling” is ready to fall.)

By referring to the table below it will be observed that there is no period of rest in the growth of the fruit up to the date of the protrusion of the radicle. It will now be shown that there is normally no pause between the epoch of the maturation of the seed and the beginning of germination, or, in other words, that from the time of the fertilisation of the ovule to the onset of germination there is no cessation in the process of growth of the embryo. That period of dormant vitality which almost all seeds pass through forms no normal feature in the life-history of this species of Rhizophora.

RHIZOPHORA MANGLE AND R. MUCRONATA.

+-------------------------------------------+ | RHIZOPHORA MANGLE. | +-------------------------------------------+ | _Growth of fruit in height._ | +---------------------+---------------------+ | Lines or tenths of | Number of days | |an inch (millimetres | since | | in brackets). | fertilisation. | +---------------------+---------------------+ | | | | 2 (5) | 30 | | 3 (7·5) | 42 | | 4 (10) | 50 | | 5 (12·5) | 61 | | 6 (15) | 67 | | 7 (17·5) | 74 | | 8 (20) | 83 | | 9 (22·5) | 92 | | 10 (25) | 100 | | 11 (28) | 105 | | | { Protrusion| | | 107{ of the | | | { hypocotyl | | | | _Growth of the protruding hypocotyl._ | | | | 10 (25) | 127 | | 20 (50·5) | 141 | | 30 (76) | 151 | | 40 (101·5) | 160 | | 50 (127) | 167 | | 60 (152) | 175 | | 70 (177·5) | 185 | | 80 (203) | 202 | | 90 (228) | 222 | | | {Fall of | | | 229{the | | | {seedling | +---------------------+---------------------+

_Explanation of the Table._

We have here shown the period between fertilisation and the fall of the seedling from the tree.

This period divides itself into two parts, the first being concerned with the continuous growth of the fruit and of the inclosed embryo until the tip of the hypocotyl appears through the apex of the fruit, the second being indicated by the growth of the protruding hypocotyl until the fall of the seedling.

The height of the fruit is measured from the base of the calyx-lobes, and the length of the hypocotyl at first from the apex of the fruit and afterwards from the edge of the protruding neck of the cotyledonary body. The height of the ovary at the time of fertilisation is about 3 millimetres; and from that time onward it is to be regarded as a fruit.

[_To face page 452._

FIGURES ILLUSTRATING THE DEVELOPMENT OF
THE SEED AND THE GERMINATING PROCESS
OF RHIZOPHORA AND BRUGUIERA

(Natural size. Drawn for convenience of description in the erect
position.)

1. Rhizophora mucronata Fruit 3-1/3 lines (8-9 mm.) high, six to
seven weeks after fertilisation. The
micropyle is but slightly dilated, and is
occupied by a small plug of endosperm.

2. Rhizophora mucronata Seed of fruit represented in Fig. 1.

3. Rhizophora mucronata Fruit 5 lines (12 mm.) high, eight to nine
weeks after fertilisation. Germination is
about to begin. A large plug of endosperm now
protrudes through the dilated micropyle, but
still covers the lengthening hypocotyl.

{Seed of fruit represented in Fig. 3. In
4.} Rhizophora mucronata {Fig. 4 the plug of endosperm is shown on the
5.} {upper end of the seed; whilst in Fig. 5 it
{has been removed, exposing the tip of the
{hypocotyl.

6. Rhizophora mucronata Fruit 7-1/2 lines (18 mm.) high, eleven to
twelve weeks after fertilisation.

7. Rhizophora mucronata Fruit, seventeen or eighteen weeks after
fertilisation.

8. Rhizophora mucronata Full-grown fruit with upper portion of
seedling just before detachment from the
tree. The long tapering plumule is here
inclosed in the cotyledonary body. The *
indicates the point of detachment of the
seedling.

9. Rhizophora mucronata The cotyledonary body of Fig. 8.

9A.} {Illustrating different stages in the 9B.}Rhizophora mucronata {development of the plumule and of the neck of 9C.} {the cotyledonary body resulting finally in 9D.} {the expulsion of the plumular end of the {seedling from the fruit cavity as in Fig. 8. {(See page 458.)

10. Rhizophora mucronata Fruit with two seeds.

FIGURES ILLUSTRATING THE DEVELOPMENT OF
THE SEED AND THE GERMINATING PROCESS
OF RHIZOPHORA AND BRUGUIERA—(_continued_)

(Natural size. Drawn for convenience of description in the erect
position.)

11. Rhizophora mangle Fruit, six weeks after fertilisation.

12. Rhizophora mangle Seed with plug of endosperm, as shown in Fig. 11.

13. Rhizophora mangle Fruit, eight weeks after fertilisation. The tip of
the hypocotyl is now piercing the plug.

14. Rhizophora mangle Embryo (enlarged) shown in Fig. 13.

15. Rhizophora mangle Fruit, ten weeks after fertilisation. The growing
hypocotyl has now pierced the plug.

16. Rhizophora mangle Embryo shown in Fig. 15.

17. Rhizophora mangle Fruit, nearly sixteen weeks after fertilisation.

18. Rhizophora mangle Full-grown fruit, just before the detachment of the
seedling from the tree. The long tapering plumule
is inclosed in the tube of the cotyledonary body.
The point of detachment of the seedling is
indicated by *.

19. Rhizophora mangle The cotyledonary body of Fig. 18.

20. Rhizophora mangle Fruit with two seedlings in different stages of
growth (given in the first plate).

21. Bruguiera Rheedii Fruit, about four weeks after fertilisation. (The
shaded portion is the calyx-tube or cup, in the
midst of which rises the style.)

22. Bruguiera Rheedii Germinating seed.

23. Bruguiera Rheedii Germinating fruit, about eight weeks after
fertilisation.

24. Bruguiera Rheedii Germinating fruit, about ten weeks after
fertilisation. Here the growing hypocotyl,
carrying the style with it, has pushed upwards the
lining membrane of the floor of the calyx-tube,
which has ruptured and forms a cap on its extremity.

25. Bruguiera Rheedii Germinating fruit, thirteen or fourteen weeks after
fertilisation.

26. Bruguiera Rheedii Fruit with full-grown seedling just before its
detachment from the tree.

[_To face page_ 453.

RHIZOPHORA MUCRONATA.

_Growth of the first seven inches of the hypocotyl after it protrudes
from the fruit._

10 lines (25 mm.) after 26 days 20 lines (50·5 mm.) after 41 days 30 lines (76 mm.) after 51 days 40 lines (101·5 mm.) after 61 days 50 lines (127 mm.) after 70 days 60 lines (152 mm.) after 78 days 70 lines (177·5 mm.) after 86 days

In my description of the germinating process of Rhizophora mangle from this particular standpoint I adopt the general views of Prof. Schimper, the observations being my own, the phraseology employed being his. It would be out of place here to deal with the biological significance of a process to which observers like Warming, Goebel, Karsten, Schimper and Haberlandt have applied their greater talents as well as their greater experience. I investigated the subject carefully from my own standpoint of inquiry, and whilst the reader will find in my rough sketches of the various stages of the process a little aid in following the argument, he is referred for detailed treatment of the subject to the memoirs of the above-named botanists as well as to those of yet more recent investigators.

After fertilisation, according to Prof. Schimper (_Ind. Mal. Strandflora_), the embryo-sac is filled with endosperm, which subsequently protrudes and forms a plug completely closing the micropyle (see my figures). As my observations showed, the seed during the first eight weeks after fertilisation increases continuously in size, and the plug of endosperm, at first inconspicuous, becomes of considerable size, the seed attaining a length of seven millimetres. The embryo meanwhile grows rapidly, and at the end of this period of eight weeks the radicular tip or the point of the hypocotyl begins to protrude from the micopyle, still covered by the plug of endosperm, the fruit being between four and five lines (10-12 mm.) in length (figures 11-14). In another week, when the fruit has grown another line in length, the tip of the radicle is on the eve of piercing the plug, and this may be termed _the commencement of germination, nine weeks after the act of fertilisation_. The next stage, after an interval of one and a half weeks, is illustrated in figure 15; and _after a period of about fifteen weeks from the date of fertilisation the tip of the radicle pierces the top of the fruit_. As shown in the figures, the fruit grows in length throughout the process.

The question as to whether the matured seed passes through a stage of quiescence before it germinates finds its answer in the statement that only nine weeks elapse between fertilisation and germination. It may, however, be urged that the maturation of the seed could be accomplished in a few weeks, and that after this a period of dormant vitality might follow. This objection can be at once disposed of and the whole matter placed beyond reasonable doubt by making, as I did, a large number of vertical sections of the fruit in all its stages. It will then be perceived that there is a fairly constant relation in all stages of growth between the seed and the fruit, whether maturating or germinating. Since the growth of the fruit is continuous (see Table) up to the time of the protrusion of the tip of the hypocotyl through its coats, it follows that there can be no appreciable pause between the completion of maturation and the commencement of germination of the seed. In other words, both fruit and seed preserve the same relation during the process, and the absence of any period of rest is to be inferred from the uninterrupted growth of the fruit.

We will take, to illustrate this point, a fruit between four and five lines long in the stage that immediately precedes germination (see figure 11). The fruit proceeds with its growth, and the seed, we will suppose, remains quiescent for a month. At the end of that time (see Table) the fruit would be eight lines long, and the seed, of course, would be unchanged. This condition of things never presented itself to me. Fruits eight lines long were always far advanced in germination (see figure 15). If the seed passes through an interval of rest before germination, it must be of a very short duration and practically _nil_.

This absence of any period of rest between the final maturation of the seed and its fertilisation had already been assumed by Prof. Schimper. Writing to me on July 14, 1898, when my observations were in progress, he says:—“I am ready to assume, according to my own experience, that there is continuous development until the falling off of the embryo. More accurate observations on the subject would be interesting, and would not present any great difficulties.” At the end of the same month he wrote the preface to his great work on Plant-Geography; and he expresses himself decidedly on this point. Speaking of Rhizophora mucronata (English edition, p. 396), he says that “the fruit ... soon after the completion of its growth is pierced at its summit by the green hypocotyl, as the embryo does not undergo any period of rest, but continues to develop without interruption.”

Though the rest-period is normally non-existent with the seeds of Rhizophora, it has already been observed that it is indicated in rare cases and under exceptional conditions. Thus I have already remarked that in Fiji about one per cent. of the germinating fruits of the American species exhibit more than one seed. These seeds usually begin to germinate about the same time, but in a few cases, say, one in ten, a marked difference in the length of the protruding hypocotyls points to the fact that one of the seeds began to germinate some weeks after the other. We at times also meet with fruits which when cut across display two seeds, of which only one is beginning to germinate. Such cases indicative of a pause between the maturation of the seed and the beginning of germination would be very rare. With Rhizophora mangle, probably one in a thousand fruits would be a generous estimate.

In passing it may be remarked that the same stages occur with Rhizophora mucronata in the development of the seed and in the subsequent germinating process. When the fruit is three lines long the micropyle is but slightly dilated (see figures 1 and 2). When it is four lines long the endosperm begins to escape from the gaping micropyle and forms a projecting plug. The growth of the embryo now becomes rapid, the endosperm escapes in greater quantity, and by the time the fruit is five lines long the tip of the radicle is on a level with the micropyle, although still covered by the plug (see figures 4, 5). After this, germination begins; and when the fruit is six lines in length the radicle is in the act of penetrating the plug. Ultimately the tip of the radicle pierces the top of the fruit when this last is nine or ten lines long. As shown in the figures there is continuous growth of the fruit during the maturation and germination of the seed, until, in fact, the plantlet drops into the water. With reference to the stage when germination begins, it should be remarked that the formation of the large plug of endosperm outside the micropyle does not necessarily indicate the beginning of germination. Germination is in progress only when the hypocotyl or radicle begins to lengthen and is on the point of piercing the plug of endosperm that fills up the gaping micropyle. This is well shown in this species in the case of fruits with two seeds. Both seeds may have large plugs of endosperm, and yet only one may show indications of germination in the lengthening hypocotyl.

We must now return to the subject of the growth of the hanging seedling of Rhizophora mangle. We have already remarked that, as shown in the Table, about fifteen weeks (107 days) is the average time elapsing between the fertilisation of the ovule and the protrusion of the tip of the radicle through the top of the fruit. A further period of seventeen and a half weeks (122 days) is occupied by the growth of the seedling on the tree, at the end of which period it drops into the water or mud according to the state of the tide. This gives a total period of nearly thirty-three weeks (229 days) as the duration of the time between fertilisation and the fall of the seedling. This may be divided, as has been already implied, in the following manner:—

(1) Period between fertilisation and germination. 9 weeks.

(2) Period between the commencement of germination 6-1/2
and the protrusion of the tip of the radicle weeks.
through the top of the fruit.

(3) Period occupied by the growth of the hypocotyl 17-1/2
outside the fruit, and terminating in the fall weeks.
of the seedling from the tree.

——

Total 33 weeks.

This represents the average of numerous observations, the deviations being from two to three weeks on either side. In the latter part of its growth, the lower end of the hypocotyl becomes thickened or club-like, and during the last week or ten days the increase in length is arrested altogether.

My observations on the growth of the seedling on the tree of Rhizophora mucronata were comparatively few; but, as shown in the Table on page 453 they give nearly the same rate of growth. Taking the average length attained by the hypocotyl on the tree at sixteen inches, and employing as well the data supplied by Rhizophora mangle, a period of 26-1/2 weeks would elapse from the time the hypocotyl pierces the top of the fruit until the plantlet falls from the tree. If we then add, as in the case of the other species, 15-1/2 weeks for the preceding period between fertilisation and the protrusion of the hypocotyl, we get a total of 42 weeks for the whole period from fertilisation to the fall of the seedling. In the extreme cases where a length of almost two feet is attained on the tree, the period would somewhat exceed twelve months; and in those rare instances in other regions, when, according to Schimper, the seedling is a metre in length, probably eighteen months would be required. The period for Rhizophora mucronata is thus considerably longer than for R. mangle, which is sufficiently indicated by the difference in the average length of their hypocotyls on the tree in Fiji, that for R. mucronata being sixteen inches, and that for R. mangle nine or ten inches.

The only other observations that have come under my notice relating to this subject are those made by Jacquin on Rhizophora mangle in the West Indies in the middle of the eighteenth century. The results are literally quoted by Warming; but I have referred to the original account in the work of Jacquin, entitled _Selectarum Stirpium Americanarum Historia_, Vindobonæ, 1763. According to this observer the seedling falls from the tree in the twelfth month from the fecundation of the flower. This happened in my observations on the same species in Fiji in the eighth or ninth month. Jacquin states that the tip of the radicle protrudes from the fruit in the third month, whilst my results give it as taking place in the fourth month. The difference in the length of the total period, it may be remarked, would be to a great extent determined by the varying length acquired by the seedling before it drops from the tree. In ordinary conditions it averages about ten or eleven inches, and the hypocotyl itself attains a length of nine or ten inches on the tree, both in Fiji and Ecuador; but in sheltered localities it may attain a length half as long again. I have already pointed out in the case of the fruits of Rhizophora mucronata that a year and more would be sometimes required, and the same remark would apply to unusually long fruits of R. mangle. Local conditions would often produce varying results, both in the rate of growth of the hanging seedling and in the duration of the period of its attachment to the tree; but it is probable that nine or ten months would represent for the genus the average length of the period between fertilisation of the ovule and the detachment of the seedling from the parent tree.

_The mode of separation of the seedlings of Rhizophora mangle and
Rhizophora mucronata_

This is a process of expulsion almost akin to parturition, and is brought about by the outward growth of the neck of the cotyledonary body. There is much that is of great interest in this subject; and I may add that Haberlandt, in a memoir published in the _Annales du Jardin Botanique de Buitenzorg_ for 1894, gives the results of an elaborate study of the viviparous process in this and other genera of mangroves. The same analogy seems also to have presented itself to him, but only in connection with the means employed in some of the genera, as with Bruguiera, for conveying nourishment to the growing embryo. He remarks that he was involuntarily reminded by these structures of the chorion-tufts and lobes in the placenta of mammals, and that such structures in the mammal are functionally nothing more than true _haustoria_ as found in the viviparous mangroves.

When studying the germination of the American and Asiatic Rhizophoras in Fiji, I observed that the neck of the cotyledonary body did not begin to form, nor the inclosed plumular bud to show signs of differentiation, until the hypocotyl had protruded about 4-1/2 inches with R. mangle, and between 6 and 7 inches with R. mucronata. The neck of the cotyledonary body then proceeds to grow in length, pushing before it the plumular end of the embryo-seedling, which it surrounds as a sheath. This operation continues until the hypocotyl has acquired a length of about seven inches with R. mangle, and about nine inches with R. mucronata, when the neck begins to protrude outside the fruit. The cotyledonary neck proceeds with its growth, and by the time the seedling is ready to fall from the tree it protrudes about an inch from the fruit-shell, having carried the growing plumular bud with it. The plumular end of the seedling has been now more or less expelled from the fruit-cavity, and the connection between the suspended seedling and the fruit now alone depends on a slight bond between the base of the plumule and the inner margin of the cotyledonary neck, as indicated by a cross in the figures given in the plate. The union is soon broken and the seedling falls.

Whether there is anything more than an analogy between the expulsion of a Rhizophora seedling and the birth of a mammal seems most unlikely; but the process is at all events a very remarkable one.