Description of Female, Male and Larval Forms of a Tiny
Stalked Barnacle, Ibla idiotica n.sp.
[Read before the Otago Branch, June 12, 1945; received by the Editor, June 6, 1945; issued separately, December, 1945.]
During the course of a study of the barnacle Pollicipes spinosus, the writer found attached to occasional specimens a tiny new cirripede belonging to the genus Ibla. Subsequent searching provided more extensive material, and a description of the species is now presented.
Material and Methods: Different specimens were examined alive, dissected in alcohol, mounted in glycerine-formalin, stained in acid carmine, or serially sectioned. Whereas more than 100 females were dissected, only about 5 or 6 specimens of each form (male, female, nauplius and cypris) were sectioned. These were chiefly cut at 10 microns and stained with Mallory.
Smaller females would sometimes stay alive in dishes of sea-water for several days, but no attempt was made to rear the various forms under observation. Drawings were made with the aid of a camera lucida, for the loan of which the Otago University Zoology Department is thanked.
Description of Species.
Ibla idiotica n.sp.
A small unisexual species.
Female with peduncle irregularly scattered with chitinous spines; terga and scuta with several strong transverse ridges; penis and other male organs lacking; caudal appendages less than half as long as the pedicels of the sixth cirri; simple digestive glands at the junction of oesophagus and stomach.
Male minute, triangular; with two large fronto-lateral horns; lacking peduncle, mantle and valves. Cirri almost if not entirely absent. Trophi absent. Antennules, in mature specimens, deeply withdrawn inside the body.
Nauplii with antennae and mandibles reduced.
Type Locality: Karitane Peninsula, Otago.
Type Specimens: Otago Museum.
Habitat and Distribution.
Although first discovered attached to the peduncles of Pollicipes spinosus Q. and G., this curious little species has subsequently been found much more frequently on the allied Scalpellum villosum Leach (= Calantica villosa). Isolated or more exposed individuals
of either of these pedunculates have in no case been found carrying Ibla. But where a number of specimens of S. villosum are growing in a close colony on the dark, wet, underhung surface of a large rock at low tide, I. idiotica not infrequently occurs. It is usually on the villous peduncle of Scalpellum, sometimes on the valves, and occasionally on the sessile barnacle Tetraclita purpurascens Darwin when this latter was attached to S. villosum. To what depth this species of Ibla occurs has not been ascertained. Its upper limit is not much above low tide-mark, continuous moisture externally being probably essential.
Ibla idiotica has been found in the vicinity of Dunedin on the Karitane Peninsula, at Long Beach, and at Bruce's Rocks. Limited examining of S. villosum colonies around Wellington and Stewart Island failed to reveal it. The writer has not searched for it in other parts of New Zealand.
The female has a thick chitinous covering which lacks calcification. Its colour is a uniform, translucent, dull yellow all over. Live individuals are very active, the muscular peduncle of a young specimen being able to swing the capitulum rapidly through a rightangle. When placed in a dish of sea-water these barnacles will usually extrude and withdraw their cirri at frequent intervals—a contrast to the sluggish behaviour shown by the allied Pollicipes spinosus and Scalpellum villosum. Young females are fairly transparent, and one older one stayed alive for several hours after removal of the body from the mantle. In such specimens, numerous rapid peristaltic waves can be seen passing along the oesophagus. The rectum also frequently contracts, and the minute caudal appendages show considerable movement.
As in other species of Ibla, the only valves present are a pair of scuta and a pair of terga (Figs. 1, 2, 8 and 9). The tips of the terga characteristically are turned in towards the cirri, and under high magnification show a honeycomb-like structure unlike the rest of the valve. But occasionally they are worn down almost to the level of the scuta, giving such individuals an atypical appearance. The peduncle is usually approximately as wide as it is long. But sometimes it may become considerably elongated.
The total length of mature females is from 2 to 3.5 mms. In young specimens the greatest width is at the base of the scutum (Fig. 1). But older ones, with many young in their mantle-cavities, may show a considerably expanded peduncle (Fig. 2). In such specimens the mantle cavity may be very extensive, dipping deeply into the peduncle. In fact, perhaps the most remarkable feature of the females is their astounding fecundity (Fig. 10).
This species, like others of the genus, shows the first pair of cirri placed close to the trophi, their bases being far removed from the remaining legs and their rami short (Fig. 10). The number of segments per ramus for the cirri varies a little among different individuals. An example is as follows: Cirrus, 1; outer ramus, 4;
inner, 4; C.II, 6, 4; C.III, 7, 7; C.IV, 7, 7; CV, 7, 7; C.VI, 8, 8. The caudal appendanges are extremely minute (Fig. 7). Each is unsegmented and carries two setae.
The internal anatomy shows the peculiar feature whereby Ibla stands apart from other adult barnacles—namely, the oesophagus running right round the outside of the adductor muscle anteriorly before joining the stomach (Fig. 6). At the point of junction (and at both sides of the brain) lie a pair of digestive glands. Each is a single hollow bag, lined with large cubical epithelium cells and containing a grey secretion. The ventral nerve-cord is very stout relative to the size of the body, in this respect resembling that of extremely young specimens of other pedunculates. The large sub-oesophageal ganglion is succeeded by 4 others. The adductor muscle is stout, its fibres unstriated. Cirri, trophi and body-wall are supplied with various muscles whose detailed arrangement and nerve-supply were not worked out.
The peduncle is supplied with numerous longitudinal muscle fibres (Fig. 6), which give it externally a faintly lined appearance. The ovaries are relatively compact bodies in its upper half. The cement glands in the connective tissue below them are not clearly defined, but their two ducts, running down the antennules, could readily be seen. In sections stained with Mallory's the light-brown granular cement at the base contrasted sharply with the thick blue-stained chitinous covering of the peduncle.
Contents of Mantle Cavity of Female.
Most of the females carry in their mantle-cavities a diverse assortment of individuals. Not only are males present, of all shapes and appearances. Embryos, nauplii and cypris larvae may also occur in varying numbers.
To obtain a clearer picture of the course of events, 50 females were each measured with an eyepiece micrometer and then opened under a microscope. Their sizes and contents are shown in Table I.
Assuming that the length roughly corresonds to the age of the female, the following conclusions may be drawn:—
The youngest females (less than 1.6 mms. long) carry no males or young.
The slightly larger forms show various stages in the develoment of males.
Females less than 2 mms. long almost invariably lack other young, whereas those over 2.3 mms. almost invariably contain them.
As the females grow in size both the number of males and number of young tend to increase.
The tendency of the crosses in the 6 columns of males to move from the upper left to lower right, when considered together with anatomical evidence, suggests that the course of development of the male is: cypris; pre-male enclosed in cypris carapace; pre-male (i.e. form with cypris antennules still protruding); opaque male; transparent male with well-developed testes; dead male.
The 50 females just considered were all collected from the same locality in February. Other females have been collected in smaller
[The section below cannot be correctly rendered as it contains complex formatting. See the image of the page for a more accurate rendering.]
|Length in mms.||Cypris only.||Pre-male in cypris.||Pre-male.||Opaque male.||Transparent male with testes.||Empty male||Total males||Embryos.||Nauplil.||Cypris larvae.||Total young.|
|2.59||[ unclear: ]||5||7||1||8|
|*2.70||[ unclear: ]||3||—|
|2.76||+||[ unclear: ]||3||7||3 1||11|
|2.86||[ unclear: ]||[ unclear: ]||5||2||6||8|
|2.92||[ unclear: ]||2||15||12||27|
|2.97||[ unclear: ]||2||20||8||28|
|3.07||[ unclear: ]||+||4||19||9||28|
|3.45||+||[ unclear: ]||+||4||16||4||5||25|
[Footnote] * This specimen had an elongated peduncle. Its eapitulum was relatively smaller.
Fig. 1.—Ibla idiotica: lateral view of young female. X 15.
Fig. 2.—Ventral (anterior) view of older female. X 15. Adductor muscle and median eye visible by transpareney between seuta.
Fig. 3.—Mandible. X 85. FIG. 4.—Maxillule, X 85. FIG. 5.—Maxilla. X 85.
Fig. 6.—Longitudinal section of young female. X 90. al., antennule; ad., adductor muscle; br., brain; cI. base of 1st cirrus; c.d., cement duct; cem., cement; d., digestive gland; e., median eye; l.m., longitudinal muscles of peduncle; m., mouth; n.c., nerve cord; od., part of oviduct; oes., oesophagus; ov., ovary rudiment; st., stomach.
Fig. 7.—Pedicels of cirri VI, with caudal appendages (c.ap.) between them, X 140.
Fig. 8.—Terga, X 38. FIG. 9.—Scuta, X 38.
Fig. 10.—Female with side of mantle and peduncle removed, showing two males, six nauplii and thirteen embryos in mantle-cavity. Reconstruction, X 24.
Figs 11–13.—Stages from late embryo to lare nauplius. Lateral view, X 100.
Fig. 14.—Ventral reconstruction, late nauplius, X 100. f.h., frontal horns.
Fig. 16.—L.S. late nauplius, X 100. i., intestine; oes., oesophagus; st., stomach.
Fig. 17.—Tip of eypris antennule, X 450.
Fig. 18.—Lateral view of cypris, X 100. cem., cement gland.
Fig. 19.—Young pre-male, still within cypris carapace, X 45.
Fig. 20.—Pre-male, lateral view, X 45.
Fig. 21.—Pre-male, ventral view, X 45.
Fig. 22.—Opaque male, with pair of humps. Dorsal view, X 45.
Fig. 23.—Opaque male, lateral view, X 45. (Flagellum of antennule still protruding.)
Fig. 24.—Fully developed male, ventral view, X 45.
a1. antennule; c.l., cypris limbs; l.e., lateral (cypris) eye; c., median eye; mn., mandible; mxu., maxillule; mxa., maxilla.
Fig. 25—Male. ventral view, X 170.
Fig. 26.—T.S. cypris, through adductor muscle, X 100.
Fig. 27.—T.S. pre-male inside cypris carapace, X 110.
Fig. 28.—L.S. opaque male, X 150.
Fig. 29.—Cypris, lateral reconstruction, X 160.
a1., antennule; abd., “abdomen” of cypris; add., cypris adductor muscle; br., brain; e.d., cement duct, c.l., cypris limbs; c.l.m., cypris limb muscles; e., median eye; int., intestine; l.e., lateral eye; m.c., mantle cavity; n., nerve mass; n.c., nerve cord; [ unclear: ] ., sperm opening; oes., oesophagus; st., stomach; s.v., seminal vesicle; t. testis; y., yolk.
numbers in the months of January, March, June, August and November. In each instance, the larger females have contained both males and young. Hence, if any cessation occurs in breeding, it must be for a relatively brief period of the year.
A number of other females were dissected without being measured. The maximum number of dwarf males found in a female was six. Amongst fairly small specimens, several were found containing a single cypris, a pre-male in cypris carapace, or a pre-male. Only one, however, was found containing a nauplius but no male. Its length was 2.27 mms. And altogether but a single specimen has been opened with embryos and no male—the specimen in Table I of 1.94 mms. in length. Both of these specimens are above the minimum size at which a fertile male may be present. The significance of these points will be discussed subsequently.
The fully-developed male is shown in Fig. 25. It is about 0.4 mms. long, transparent, and nearly motionless; muscle fibres being almost absent.
The most conspicuous organs are the two large testes, in which the live sperms may be seen by transparency actively swirling around. Each testis narrows posteriorly into a short duct, the two soon fusing to expand into a median seminal vesicle. This latter varies considerably in size, being sometimes so packed with sperms that it is as large as a testis (Fig. 24). The seminal vesicle opens ventrally near the posterior end by a median longitudinal slit. No penis is present. Slight twitching movements have been observed in this region, which possibly assist in the exit of sperms.
The external appearance of the male is highly bizarre, largely owing to the extreme development of the two spinous horns. These structures are not, as might be expected, embedded in the lining of the female's mantle cavity, the male being quite free. So to what extent they assist in holding it in position is not clear. Posteriorly the body terminates in two protrusions, each carrying one or two setae. Just anteriorly to them lie a couple of protuberances, each with from one to three setae. No trace of mouthparts has been discerned.
Deeply embedded in the body between the testes lie two chitinous structures, which, when dissected out, prove to be typical cypris antennules, complete with setae. They are now empty of muscles, however, and communicate with the exterior only by a minute pore on the median anterior margin.
The alimentary canal is present in a reduced form. An oesophagus is lacking. A small, globular stomach whose lumen contains amorphous contents is placed between the posterior margins of the testes, immediately behind the antennules. From it a slender intestine passes down posteriorly. The presence of a lumen in this was doubtful, and serial sections indicate that it ends blindly with no arms.
A black median eye is a conspicuous feature. From behind it a minute solid “brain” and nerve-cord runs backwards for a short
distance. Associated with the lack of an oesophagus is an absence of a circumoesophageal commissure.
Other organs include a pair of round cellular structures placed at each side of the seminal vesicle but not connected with it; and several irregularly-scattered small refrigent bodies. The functions of these are not known.
The space surrounding the organs is empty of tissue except for occasional strands running from the testes to the ectoderm. Some more densely-staining fibres, running from the bases of the antennules to the dorsal surface, are probably the vestiges of the muscles running from the cypris antennules.
A minority of the males show an extra pair of humps placed on the middle of the dorsal surface (Fig. 22). A single specimen was found with only one testis, but this contained motile sperms.
Only a relatively small proportion of the males show the appearance indicated in Fig. 25. Some are opaque, others empty. Some show short horns, and the antennules may protrude to a greater or less extant. A correlation of these various types with the size of the female and a consideration of their anatomy gives the following picture of the course of their development:—
The male cypris sheds its lateral eyes and its six pairs of limbs, the body contracting into a dense, opaque mass inside the carapace (Fig. 19). Sections show, embedded in this mass, testis rudiments in the form of two large, densely-nucleated bodies (Fig. 27, t), with between them a stomach and solid intestines. The cypris oesophagus having been lost, the double ventral nerve-cord expands anteriorly directly into a “brain.” Ventrolaterally lies a pair of yolk-masses—potential female cement glands, which probably provide a food reserve for the male. Cement ducts are also present, but could not be traced actually entering the non-functionless antennules. From these latter, conspicuous muscle fibres pass back to the dorsal surface. The pair of protrusions in which the body ends posteriorly lie above the end limbs and “abdomen” of the cypris (Fig. 19). Whether they represent the caudal appendages of the normal cirripede, or whether (together with the setae just anterior to them) they are all that remains of the cirri of other Ibla males is difficult to say.
When the cypris carapace is shed there results what has been termed for convenience a “pre-male” (Figs. 20, 21, 28). The lateral horns are more conspicuous but still short; the non-motile antennules protrude anteriorly; and the whole body is densely opaque.
Then the antennules are withdrawn into the body. For a while the long flagellion of each continues to protrude (Fig. 23), but finally it also is withdrawn. Externally the body still looks opaque, but internally the testes are becoming differentiated, and sections show developed sperms in their centres. Such a male, although still heavily yolked and opaque in appearance, is presumably able to fertilise eggs. For it will be noted in Table I that females with these opaque males may also contain embryos and sometimes even nauplii.
Successive stages are seen in the loss of the oily-looking globules, as a result of which the males become transparent. The testes, instead
of showing a few sperms in the middle of a cell mass, now are largely filled with spermatozoa. Simultaneously the horns are elongating and becoming spinous. Thus do we arrive at the fully-developed male, such as was initially described.
Presumably the only supply of food for the male is that already stored in the body. The regular appearance of contents in the stomach suggests that it may have some function in the process of its absorption and utilisation. Finally, however, this supply is exhausted. Then the testes and seminal vesicle become empty of sperms, and the remaining chitinous shell crumples up and dies. That the male has a shorter life than the female is obvious, but just how much shorter it is not known.
Although the adult females are only some 2–3 mms. long, their embryos, of about 1/3 mm. in diameter, are larger than those of most cirripedes (Groom, 1894, p. 130). They are unpigmented, whitish, and are not bound together into the usual pair of ovarian lamellae. There are indications also that different embryos in one female were not all at exactly the same stage of development. Conceivably, size limitations would prevent a female, herself 3 mms. long, from forming in her ovary up to 20 eggs at once.
The embryos are heavily yolked, and by the time of hatching show but little tissue differentiation. The large antennules are directed backwards (Fig. 11). Behind them on the ventral surface is a protruding cell-mass, which subsequently develops into the cypris limbs. Antennae and mandibles are represented, if at all, by slight swellings.
Nauplius and Cypris.
The nauplii, which are retained in the mantle-cavity, are highly modified. The large biramous antennae and mandibles, associated with the first free-swimming phase of most cirripedes, are absent as such. The carapace, instead of being flattened and triangular, is hemispherical. The cypris legs are precociously developed, originating in the late embryo as a solid mass of cells which in the nauplius splits into six pairs of separate biramous limbs (Figs. 11–13, 15).
The nauplii when alive are whitish, opaque, and almost motionless, nothing more than a slight twitching of parts of the ventral surface having been observed. This is explained by an examination of their internal anatomy, for muscle cells do not become fully differentiated until the cypris phase is reached. The main mass of the body is filled by “yolk” in the form of opaque, oily-looking globules. Dorsally and laterally it is bounded for the most part by a single thin layer of ectoderm cells; though a pair of multicellular bands are present which subsequently become muscles running to the antennules. Ventrally, and running into the appendages, is a dense zone of tissue, later to become the muscles and nerve-cord of the cypris.
Embedded in the yolk-mass is a thin-walled globular stomach with amorphous contents. A narrow oesophagus runs down to the
mouth; while posteriorly a slender solid cord of cells in the late nauplius represents the intestine (Fig. 16).
A typical labral gland is present. A pair of pyriform bodies, each consisting of a solid mass of cells, probably represents in reduced form the frontal horns and glands of most cirripede nauplii (Figs. 13, 14).
In the late nauplii (or metanauplii, though a fast line between this and the nauplius is hard to draw in this species), three pairs of appendages can clearly be recognised between the antennules and the cypris legs—probably the homologues of mandibles, maxillules and maxillae in the adult (Figs. 13, 14). In the final stages, large dark paired eyes can dimly be seen in the rather opaque body, and the striated carapace that characterises the cypris becomes secreted.
The change from nauplius to cypris is not nearly as marked as with more typical cirripedes; there is no folding-up of the carapace, as this is already largely folded, and there is no resorption of large biramous nauplius limbs, as these were not developed. The chief characteristic is the rapid differentiation of tissue which occurs after the cypris form has been acquired, giving the change from the opaque, immobile nauplius to the clear, active cypris.
The nauplius of Ibla idiotica is strikingly dissimilar from those of other cirripedes. Each of its characteristics—the reduced antennae and mandibles, the lack of tissue differentiation, and the large store of yolk—would appear, however, to be directly related to the absence of the free-swimming habit.
The cypris, by contrast, is almost surprisingly normal—a typical cirripede cypris (Figs. 17, 18, 26, 29). In comparing it, for instance, with the cypris of Pollicipes spinosus, the differences are relatively minor (Batham, 1945). In Ibla idiotica the carapace is usually more pointed anteriorly (though both species are variable in this respect), and its striations are further apart; pigmentation is lacking, except in the eyes; the cement glands are more compact; and the adductor muscle, which likewise radiates from a median endosternite, is not nearly so stout or well developed (cf. Fig. 26 with Figs. 35 and 49 in previous paper). Perhaps this latter feature is related to the metamorphosis from the nauplius; for whereas in P. spinosus the contracting of the adductor appears a major cause in the closing of the flat nauplius carapace, in Ibla idiotica the carapace of the nauplius is already more or less closed. Detailed relations of the alimentary canal to the yolk mass in the I. idiotica cypris were not worked out, as successive stages of known ages were not available. It appears, however, that here the food canal is continuous above the yolk mass (Fig. 29), instead of subsequently joining after the lateral subdivision of the yolk, as in P. spinosus. It is of interest to note that in the cypris larvae of both these species the relation of adductor and oesophagus is the same as it is in the adult of Ibla. but the reverse of the condition found in other adult cirripedes. In both species, however, whereas the cypris adductor consists of fibres radiating from a medium endosternite, that of the adult is formed of parallel fibres.
|Embryos.||Nauplii.||Cypris Larvae.||Males.||Females With Young.|
|Average length in mms.||1.34||0.36||0.61||0.41||2.76|
This cirripede shows the various features that characterise the genus Ibla. In the large form the only valves present are paired scuta and terga. The oesophagus runs round anteriorly outside the adductor muscle. The first pair of cirri is reduced and placed far from the second pair. The mandibles show the typical dentition. Chitinous spines occur on the peduncle, into which the mantle cavity extends. Males are present. The nauplii do not swim freely in the sea. In each of these features, I. idiotica agrees with the other members of the genus.
From previously described species, however, several points distinguish it. In the size of the large form and the structure of its male, I. idiotica stands sharply distinct from I. cumingii and the hermaphrodite I. quadrivalvis. It is of much the same dimensions as Ibla segmentata (= I. pygmaea), which has been dredged not far from New Zealand (Broch, 1921, p. 262). This latter species differs from I. idiotica, however, in possessing a penis, in its long, jointed caudal appendages, and in the unequal rami of the first pair of cirri.
The question arises, how is the sex determined in this species? And where does a female's first male come from?
A hypothesis which suggested itself was that the first egg produced by a young female developed parthenogenetically in her mantle-cavity into the first male. This would be able to fertilise subsequent eggs, but any that missed fertilisation would develop into later males. If such a hypothesis were correct, one would expect to find some of the smallest females (about 1.5 to 1.6 mms. long) with single embryos or single nauplii in their mantle-cavities. In actuality, however, whereas a single eypris was found at least five times in a small female, no instance was discovered of embryos or nauplii in females less than 1.94 mms. long in the absence of a male (Table I). So it seems that a more feasible hypothesis is that a cypris from another adult crawls into the mantle cavity of a young female and there metamorphoses into a male. The two specimens found with young but no males at first seem contradictory to this idea. But when one considers the lengths of these two (1.94 and 2.27 mms.) in relation to others in Table I, it looks not improbable that they have already had males which have been lost.
That the male develops from a larva which entered the mantle-cavity from outside was postulated for Ibla cumingii by Darwin (1851, p. 202). It is also in agreement with the conclusions of Callan (1941, p. 258), in considering sex-determination in Scalpellum
scalpellum. In this species he found that the number of chromosomes was 32 in both hermaphrodite and complemental, no sex chromosomes being recognisable; and he gives additional evidence suggesting that sex is here environmentally determined.
Hence it is tentatively suggested that in Ibla idiotica a cypris which for some reason crawls into the mantle-cavity of another female (or perhaps is retained in its mother's mantle-cavity) becomes a male; but that one which attaches itself outside to another species of barnacle becomes a female. It is hoped some day to put the matter to test.
Broch, H., 1921. Studies in Pacific Cirripedes. Papers from Dr. Th. Mortensen's Pacific Expedition, 1914–16. X.
Batham, E. J., 1946. Pollicipes spinosus, II: Embryonic and Larval Development. Trans. N.Z. Roy. Soc., vol. 75, part 4.
Callan, H. G., 1941. Determination of Sex in Scalpellum. Nature, vol. 148, no. 3748, p. 258.
Darwin, C., 1851. A Monograph of the Sub-Class Cirripedia. Ray Society, London.
Groom, T. T., 1894. On the Early Development of Cirripedia. Phil. Trans. B., pp. 119–232.
Gruvel, A., 1905. Monographie des Cirrhipèdes ou Thecostracés. Paris. Masson et Cie.