Observations on the Growth of Macrocystis in New Zealand.
With a description of a free-living form.
[Read before the Wellington Branch, September 23, 1942; received by the Editor. October 2, 1942; issued separately, March, 1943.]
Skottsberg (1907) figured diagrammatically the branching system of Macrocystis pyrifera (L.) Ag. Illustrations and descriptions published by Brandt (1923), Setchell and Gardner (1925), and Setchell (1932) all fit into Skottsberg's scheme, which they supplement by indicating which of the leaf blades have basal cysts or bladders. Setchell's photographs and very clear sketches (1932, Pl. 33, 34, 35) show that M. integrifolia Bory, though differing in the haptera and the flattened “rhizomes,” has the same general plan of branch and leaf arrangement.
In New Zealand M. integrifolia has not so far been observed, and M. pyrifera conforms so rigidly to the normal scheme of branching (Moore, 1941; Rapson, Moore and Elliott, 1942) that any departure seems noteworthy.
Brandt (loc. cit., p. 18) describes the life cycle of an individual long branch. “As the frond approaches the surface the rate of growth decreases, the terminal leaf gradually becomes smaller and less delicate, and fewer laterals split off, until finally no more are formed. … After division ceases the laterals (i.e., leaves) continue to grow in length and breadth.… The terminal leaf seldom attains the size of the laterals.” The sequence of changes at the end of the frond as it ages are not described further, but Figure 15 shows the kind of “young leaves at the tip of a nearly mature frond.”
This paper records how the growth of a long frond can be arrested, terminated, or modified in various ways.
Arrest of Growth.
(A) Breakdown of tissues in the most actively growing part of the terminal leaf.
This type of arrest was noted as common at D'Urville Island in January, 1941, at Port Adventure in February of the same year, and a month later, by Mr. Rapson, in several other beds at Stewart
Island. At Thorndon, Wellington, in the following October, out of 27 tips collected near the water surface in one area 11 showed breakdown of this kind. In another sample, comprising seven whole plants, the total number of tips was 52, of which probably more than half had not yet reached the surface. Of the 15 tips showing breakdown only three were on fronds less than 1.2 metres long, while of the 19 fronds over 1.2 metres long only one was actively growing. Near low tide mark this type of injury has been seen on young plants only a few decimetres long.
Breakdown seems to be caused by some agency acting near the surface and over a considerable area at once. Physical stresses, chemical changes (e.g., excess of fresh water or pollution by sewage) or pathological organisms might be responsible. Black rot, a bacterial disease recorded by Brandt, does not seem to be involved. The stipe and any partly swollen bladders attached to it may continue to grow for some time and persist after the leaf blades have fallen. Breakdown of this kind is to be regarded as an accident cutting across the normal development of the frond.
(B) Derangement or modification of the growing tissues.
(1) Incomplete Fission. The slit in the growing region of the terminal leaf is occasionally incomplete so that two bladders remain attached distally, though proximally they are distinct, and their two blades develop independently of one another. This kind of monstrosity has been seen on fronds that display no other abnormality. It does not involve any arrest of growth and is mentioned here only for completeness.
(2) Senescence. During the maturation of a leaf on a long frond, the stem connecting blade to stipe swells to form a gas-containing bladder that helps to buoy up the frond. When a swelling of this kind begins to develop in the growing region of the stipe within the terminal blade (Sprossspitze or Endfähnchen of Skottsberg) further growth is limited to the expansion and maturation of the organs already laid down. If the swelling is very near the end the result shows nothing but normal leaves, with one terminal (c.f. Brandt, loc. cit. Fig. 15). If, as frequently happens, the swelling of the immature stipe extends along below the bases of several developing leaves, there are various modifications of normal leaf and stem that may emerge. (Fig. 1. Plate 34.)
Where bladders in stipes occur at all they are usually fairly abundant—e.g., out of 86 tips that could be raked from one rock 41 had bladders of this kind. Amongst there, 12 were at an early stage of development, 10 of medium size, and 19 fully grown or wearing away. Early and late stages can be found on different fronds of a single plant. No correlation between length of frond and size of bladder in stipe was established, but amongst 46 fronds measured the distal leafy portion averaged in 14 with small stipe-bladders 1.3 metres, in 13 with medium-sized bladders 1.0 metres, and in 19 with large stipe bladders 0.6 metres.
Immediate environment seems to be more effective than season. At Worser Bay, in two places 45 metres apart, all accessible tips were taken on two occasions. The ratio of total number of tips to those with stipe bladders was, in September, for the outer place 65:6, for the inner place 74:12. Corresponding figures for the same places in the following February were 49:1. and 86:41. In a third locality some six kilometres away, from a patch cleared in October, 19 surface tips taken a year later included 6 with bladders in stipes. This kind of tip has also been collected in Wellington in July, and in March, 1941, Mr Rapson found that at Ruapuke Island, Foveaux Strait, 14 out of 38 tips collected were of this kind. Here, and at Ocean Beach, Stewart Island, where he reported this same sort of “moribund tip,” the kelp is growing in quite deep water in off-shore beds.
Brandt (loc. cit., p. 19) says: “When the water is too warm for vigorous growth, some leaves next the tip do not develop.”
The temperature affecting the growth of the frond tip is that within a few decimetres of the surface at any given time, not the average or mean temperature. Surface temperatures, taken at weekly intervals at 9 a.m. over a year at Worser Bay, very near to Macrocystis beds, are recorded by Oliver (1923). They range from 9.1° C. to 17° C. A surface temperature of 20° C. at Island Bay is said to be exceptionally high. Greater temperatures are recorded in the Macrocystis beds of the North American west coast, where Brandt associates high temperatures with poor yields. His Figure 12 shows that at 13.45° C. the number of hundreds of tons of wet kelp per square mile of area harvested was 21, at 16.75° C. 17, and at 20.65° C. only 8.
The development of a bladder within the stipe may be a normal occurrence in the maturation of every healthy frond that has attained the limit of growth permitted by its particular environment. The number present in any bed would then depend on its past history (e.g., time of cutting or removal of fronds by storm, etc.) and on the age and rate of growth of the fronds. They are found on short, young stems in plants attached near low tide mark, and therefore are probably in some way correlated with surface conditions, of which temperature may be important. Whereas an actively growing tip droops well under water, with the development of a stipe bladder it is raised up to the surface, where it is exposed to more severe conditions.
Whatever the stimulus that causes these stipe bladders to form, they restrict further elongation of the fronds affected, and when present in large numbers indicate that the bed concerned in the process of temporary deterioration.
Brandt, in describing the development of a long frond, states that the stem of about the third lateral (leaf) from the base rounds out and becomes a hollow cyst or float, and all subsequent laterals develop cysts.
Figure 1 shows that, in conjunction with the swelling of the terminal part of the stipe, leaf blades lacking their own basal bladders may be produced. Several cases can be recorded where bladderless leaves occur near the tip of a long frond beyond the usual bladdered leaves without any concomitant swelling of the stipe. This phenomenon, which may be called rejuvenation, may follow when the Endfähnchen, after a relatively inactive period, begins to divide again, and, like the basal leaves, forms at the first few divisions bladderless blades.
Types of Branching of Long Frond.
Amongst the leaves at the base of a plant it seems to be a fairly general rule that any blade not provided with a bladder is capable, sooner or later, of dividing unequally to give one or more bladderless leaves like itself, together with the initial of a new long frond. The formation of bladderless leaves near the tip of a frond introduces the possibility of the production of a second order long frond, branching off from the normally un-branched long frond, which Setchell (loc. cit.) designates as of the final order.
Specimen X, Figure 2, if the second interpretation is correct, is an example of this sort of thing, as it might develop on a frond whose growth was already limited by the production of a stipe bladder. Other specimens figured show earlier stages in the development of such a branch a little further removed from the frond tip.
Specimens secured from Paterson Inlet, Stewart Island, illustrate branching of long fronds very fully, both in early and late stages and in some variety of form (Figure 4, Plate 35). The type of branching already described, where a bladderless blade on a long frond divides heterosotomically (Setchell, 1932, p. 453), is well represented.
A second type of branching, of which an early stage is suggested by a specimen from Worser Bay, is even more common. In this case it is the blade of a bladdered leaf, apparently normally produced in the ordinary sequence, that divides heterosotomically to give rise to a branch long frond, with, in nearly every case, at least two bladderless proximal leaves. This contrasts with the statements of Skottsberg (1907, p. 91), Brandt (1923, p. 12) and Setchell (1932, p. 454) that there seems to be no evidence that a blade which has developed (or started to develop) a bladder ever proceeds to a longer-branch production.
A third type of branching differs from the second in that the initial heterosotomic division extends right down to the stipe, its products being one bladdered leaf, attached to the stipe at the point of origin of the new branch, and one bladderless stalked leaf, from which, by continued heterosotomic division of the ordinary kind, the new frond develops.
The figures show how these types of branching are associated on individual specimens, and that branches can be counted to the fourth order.
Provenance of Branched Specimens.
Although several Wellington specimens show aberrant leaves that apparently could give rise to branches on long fronds, actual branching of this kind has been seen only in specimens from Paterson Inlet, Stewart Island, grown under very special conditions.
Mr Roy Traill, of Leask's Bay, informed the present writer during the kelp survey of February, 1941, that, in addition to the beds of kelp growing on the outer coast, with conspicuous floating parts covering wide areas of the sea surface, there were, within Paterson Inlet, considerable areas of quiet bays where a similar kelp grew, completely submerged and close to the mud-sand bottom, from which it was often lifted in quantities on boats' anchors.
One of these areas near Kaipipi Point was visited in Mr Traill's launch, and a single specimen was secured in exactly the type of place previously described. There was not time to explore further, but a month later, in another but quite similar place, Ryan's Creek, suggested by Mr Traill, Mr Rapson collected more specimens, that, like the first, possess a number of features that distinguish them from open-water Macrocystis.
Characteristics of Submerged Macrocystis.
Branching.—All specimens show branching of the long fronds of the types described above and illustrated in Figures 3 and 4.
Texture.—All leaf blades, though not abnormally small for inshore plants, are of very delicate texture, completely flaccid when out of water, and entirely lacking that coriaceousness that enables a leaf on a floating stipe to flick out of the water and wave like a flag in high wind. (Leaves from a two-metre-long attached juvenile hauled up from 9 metres depth at Maori Kelp, Stewart Island, were similarly delicate.) When lifted into a boat with anchor or fishing line the long, clinging weed has an investing layer of slimy mud, possibly partly bacterial, which makes it particularly objectionable to handle.
Bladders.—Bladders are narrow and not fully distended as they are in floating fronds. Stipes are slender and internodes short.
Reproduction.—No fertile leaves were seen. Fronds are no doubt divided by the decay of older parts of stipes.
Growing tips.—Endfähnchen, though unusually delicate, are healthy and actively dividing.
Attachment.—Holdfasts are completely absent from all specimens examined. The oldest part of each is a ragged length of stipe, more or less decayed at its lower end.
Habitat of Submerged Macrocystis.
Paterson Inlet is a wide arm of the sea, open to the east and running approximately westwards across Stewart Island. Tides and winds cause considerable, sometimes violent, water movements in the
central and deeper stretches of the Inlet, and here floating fronds of attached Macrocystis fringe projecting points. There are many sheltered, almost land-locked bays seldom disturbed by currents or waves where muddy bottom deposits can accumulate. It is in such places, in comparatively shallow water (2 metres) that the submerged Macrocystis was collected, and that extensive beds of it are said to occur. The tide range in the Inlet, calculated from data given in the Nautical Almanac, is from 1.6m. at neap tides to 3m. at spring tides.
“Loose-lying Formations” of Algae.
These beds of submerged Macrocystis would appear to be equivalent to the “loose-lying formations” of the Baltic (Rosenvinge, 1898, Svedelius, 1901) which are analogous to the “Migrations-formation” described by Schiller (1909) from the Adriatic Sea. An account of the former (Baker and Bohling, 1916, p. 339) is quoted for comparison.
“All the loose-lying formations occur within the sublittoral region. They are composed of different forms derived from the attached species of the littoral region, which, when torn loose by the waves and carried by the currents into still places, collect together in great masses on the floor of the sea. Here they continue to grow, reproducing themselves by vegetative means, often over a mobile bottom, otherwise destitute of vegetation; but they never become embedded or fixed to the substratum. The dwarf Fuci are dominant forms in the uppermost of the two chief loose-lying formations of the Baltic; the formation characteristic of deeper waters is dominated by Phyllophora brodiaei f. elongata. The loose-lying Fucus formation occurs, in general, at a little depth, varying from 8–10 metres: but occasionally the formation may extend up to the lower limits of the littoral zone.”
In Paterson Inlet, as far as is known, the “loose-lying formation” is composed of only one form, derived probably in an exactly comparable way from portions torn off by storms from the attached species of the sublittoral and deposited in these quiet waters, where, without becoming fixed, they continue to make apical growth, but not quite typically.
It has not been possible to consult the original accounts of the Baltic and Adriatic formations, but it seems that loose-lying Fuci have been recorded much more commonly than loose-lying laminarians. Frye (1914, p. 65) records that Nereocystis plants, torn loose and then tied to other plants, continue to grow; he illustrates by a photograph (Plate XXIII) continued growth in the holdfast of unattached Nereocystis.
For Macrocystis a comparable record is that of Skottsberg (1907, p. 93, Fig. 102), who describes and figures an abnormal bladderless form, found within Carenage Creek, Berkeley Sound, East Falkland Island. The depth was one metre, the bottom sand with shells, the water “bedeutend versüsst,” and the place very sheltered. He adds (1941, p. 32): “We should expect the creek where the
stream empties to be brackish, and the salinity is probably low, but Berkeley Sound is wide and open, and there is quite some movement in the water outside, in Port Louis, so that conditions must be more favourable than expected.” The specimen came from what is recorded as a “mixed Codium-Rhodymenia Association” with Codium fragile, Ahnfeltia plicata, and Rhodymenia palmatiformis abundant.
Of the specimen collected he says: “Haftorgane kamen leider nicht mit. Das wunderliche Aussehen rührt daher, dass die Kurzsprosse, als die Blasenbildung ganz ausblieb, die Fähigkeit der Verzweigung nicht verloren, die zuerst Lessonia-artig geschah und später zur Bildung von Langzweigen führte. Dieselben erreichen natürlich niemals den Wasserspiegel, denn der schwache Stamm vermag sie nicht emporzuheben. … Die allermeisten Blätter, die in normalen Fällen sich niemals teilen würden, haben hier kleine Spalten.”
The Stewart Island specimens, except for the possession of bladders, often ill-developed, match this quite well, and the habitat is strikingly similar.
It seems probable that a “loose-lying formation” dominated by Macrocystis is present in Paterson Inlet and possibly also in the arms of Berkeley Sound.
The specimens examined show the features typical of limicola forms in general—viz., vegetative reproduction, dwarf habit (in more delicate texture as well as in smaller size), excessive branching, and absence of attachment disc; but, like the Baltic loose-lying Fuci, they lack the tendency to spirality shown in the marsh forms. Marsh-inhabiting brown algae, comparable to those of Blakeney Point (Baker, 1912), Clare Island (Cotton, 1912) and other parts of European and American coasts, have not been recognised in New Zealand, nor have free-living types intermediate between marsh and submerged (Naylor, 1928) been noted here.
From analogy with other records of free-growing algae, and from the incipient branching observed in Wellington, usually in situations rather atypical for the species, it may be concluded that the branching form in Paterson Inlet has been developed directly from the attached plants of the outer coast, and therefore is a habitat form or ecad of M. pyrifera.
The material on which this discussion is based was acquired partly thanks to Mr Roy Traill's extensive and accurate knowledge of Paterson Inlet, partly through the help of the Biologist of the Marine Department, Mr. A. M. Rapson, who, at my request, kindly brought back specimens from Stewart Island, partly by the use of a boat very generously lent by the Wellington Harbour Board. All this assistance is most gratefully acknowledged.
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*Rosenvinge, L. K., 1898. Algenvegetation ved Grönland Kyster. Medd. om Gronland, vol. 22.
*Schiller, J., 1909. Uber Algentransport und Migrationsformationen im Meere. Internat. Revue Hydrob. u. Hydrogr., vol. 2, pp. 62–98.
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*Svedelius, N., 1901. Studier ofver Ostersjons Hafsalgflora, Uppsala.
[Footnote] * Not seen.