Breeding Habits of Twenty-two Species of Marine Mollusca.
[Read before Royal Society of New Zealand, Canterbury Branch, October, 2, 1940; received by the Editor, October 30, 1940; issued separately, September, 1941.]
The observations here recorded were made in the Manukau Harbour, Auckland, in 1926, and more especially at the Marine Fisheries Investigation Station, Portobello, during 1930–32. The difference in latitude, equivalent to some 700 miles, accounts not only for certain distributional differences among the species studied, but also for the later spawning season in the colder waters of Portobello in the south. The development was not studied in close detail, or beyond the earlier stages on account of the depositions of rust from the iron salt-water pipes which defeated development beyond the preliminary stages. The use of jars and dishes suspended in the tanks to avoid rust accumulation entailed an equally fatal stagnation with the encouragement of an infusorian fauna. The study is therefore one of habits rather than of embryology. The observations on the spawn and on the habits of the adult molluscs during breeding season are of significance in ecological and other field studies. Measurements of the sizes of the eggs were made with the aid of a micrometer eyepiece and stage micrometer; numerical estimates were made by fractional counting and by the Bayer method (Bayer, 1908). The nomenclature follows the check list by Powell (1937). Statements of the colour of the eggs under the microscope refer to transmitted light without the use of colour filters.
Haliotis iris Martyn. Paua.
An aquarium specimen (December 14, 1931) commenced to exude clouds of eggs at 7 a.m., and within 15 hours had, according to the Bayer method of counting, produced about a million eggs. In bulk, the eggs are whitish, but, under the microscope, greyish-blue. Captive specimens feed on the small brown flora at night, with a downward rasping movement of the lips and a simultaneous forward travelling movement, so that they clear a track before them as they go. During the day they remain secluded, returning always to the same spot. At Seal Point, Otago, they are abundant from October to March, but spend the winter in deeper water. That they possess a “homing instinct” in relation to this migration, as they do in their diurnal movements, was ascertained by marking the shells.
Maurea punctulata (Martyn).
An aquarium specimen spawned at Portobello (October 29, 1931); eggs in bunches of about 12, or in a single row in a floating ribbon; total at least 900, probably many more. Eggs 0·35 mm., adhesive, at first soft and pliable and variously shaped, but becoming spherical and relatively firm within an hour; colour, bright orange; outer plasma with minute reticulations, nucleus spherical and central in a film of clear fluid.
Spawning occurs strictly at the surface, the mollusc following any rise or fall in the water level and suspending the spawning operation till exactly at the surface. The water level is also preferred at other seasons, and a retreat to the floor of the tank after three months' captivity was found to be a prelude to death.
Benhamina obliquata (Sowby). plate 20, fig. 1.
Ribbons of eggs (plate 20, fig. 1) attached to rocks between tide marks, Quarry Point, Otago Harbour, December to January. Ribbons 37 to 103 mm. long; capsules 0·32 × 0·26 mm., ovoid, irregularly spaced but averaging 300 per mm.; eggs one per capsule, diameter 0·007 mm. Captive specimens did not spawn in the aquarium tanks.
Zeacumantus subcarinatus (Sowerby).
Spawning season November–December (Manukau Harbour), December to February (Otago Harbour). Spawn in intertidal pools, crevices, empty cockle shells, or Sertularians (Sertularia ramulosa); clumps of spawn small, though sometimes the product of more than one parent. Capsules exuded in captivity (February 2, 1930) at the rate of 20 per minute, 0·89 × 0·72 mm. to 0·63 × 0·52 mm.; eggs 0·25 mm., single, rarely two per capsule, transparent, yellow under microscope, in greenish gelatinous matrix.
Cabestana spengleri (Perry). Plate 20, fig. 2.
Spawning season October–November (Manukau Harbour; common Week's Island), December–January (Otago Harbour; common Pulling Point). Capsules in leathery baskets firmly attached to rocks below extreme low-water mark, frequently covered by the parent even after apparent completion. The tough imbricating membranes of the basket (plate 20, fig. 2) form a leathery cup with inturned margins, its inner surface densely packed with digitiform capsules, of which the oldest ones are in the base of the cup and pointing towards the aperture, the later ones deposited in a close spiral and approximately radial direction, the outermost row pointing across the aperture. The following measurements indicate the range of sizes:—
|Diameter.||Depth.||Base width.||Length.||Number of|
The number of eggs per capsule is equally variable, 600–2,600, diameter 0·45 mm., yellow granulated, embedded in gelatinous matrix. Aquarium specimens died in six weeks without spawning.
Argobuccinum tumidum (Dunker). Plate 21, fig. 4.
Capsules are laid in irregular rounded clusters; on rocks at low tide mark, Goat Island (September 15, 1931), and Quarantine Island (August 3, 1931), Otago Harbour. Another trawled in 19 fathoms off Otago Heads was attached to weed, sponge and worm tubes. The capsules at the base are more densely packed and more firmly attached than at the surface, where the brims are free (plate 21, fig. 4). As shown by the following measurements, the trawled specimen, which measured 185 × 75 mm. and contained 385 capsules, contained larger
and more capsules, and more eggs per capsule and per cluster, than the harbour specimen:—
[The section below cannot be correctly rendered as it contains complex formatting. See the image of the page for a more accurate rendering.]
|Specimen from 19 fathoms.||Intertidal, Goat Island.|
|Length of capsule||12–14 mm.||8–9 mm.|
|Width at brim, major axis||6–9 mm.||5–7 mm.|
|Width at brim, minor axis||4-4-5 mm.||3–4 mm.|
|Diameter of egg||0–28 mm.||0–26 mm.|
|No. of capsules||385||333|
|Eggs per capsule, average||2,700||2,100|
|No. of eggs||1,040,000||700,000|
During copulation in the aquarium, the male was carried for five hours on the back of the female, but spawning did not occur.
Cominella maculosa (Martyn). Plate 21, fig. 3.
In the Manukau Harbour from October to December the usual muddy habitat is forsaken and the egg capsules are deposited on the surface or undersurfaces of rocks at about half-tide level, or on shells and even crabs (Paramithrax minor) in the same situations. The capsules are in clusters of 40 or 50, often compound, sometimes loosely pendulous. The capsules are horny, tapering at each end, base with an expanded attachment disc, apex truncate or bluntly pointed; height 7 mm., major width 5 mm., maximum width of minor axis 2 mm., eggs creamy to yellow, in gelatinous matrix, average number 300, diameter 0·18 mm. Found boring into and eating Saxostrea glomerata (Gould) and Chione stutchburyi (Gray), Manukau Harbour.
Cominella glandiformis (Reeve).
Capsules taken (November 26, 1926) in Manukau Harbour on rocks and Serpulid colonies (Serpula zeylandica), in clusters to which one or more parents may contribute. Capsules yellow to light brown, height 3 mm., base 2–5 mm., brim 1 mm.
Zeatrophon ambiguus (Philippi). Plate 22, fig. 7.
Specimens dredged February 23, 1931, off Otago Heads were in the act of spawning on empty shells of Struthiolaria papulosa, up to 35 capsules per shell, and continued to deposit capsules after transfer to the aquarium, both on shells of the species mentioned, on the side of glass jar, and on aquarium walls. Five capsules deposited in captivity in four hours; height of capsule 2 mm., diameter 10 mm., with a brim exit 1 mm. in diameter; of soft material; base hard and chitinoid.
Neothais scalaris (Menke). Plate 22, fig. 8.
In Manukau Harbour spawning commences in October, numerous specimens congregating on rocks in muddy localities to spawn; captive specimens in Otago spawned November 23, 1931, one producing 92 capsules in four days and another 186 in three days. Capsules in clusters, those at the outer surface with overlapping edges but looser than those at the base. Average height of capsules 9 mm., brim oval or diamond-shaped, 6·5 × 4·5 mm., exit at least 1 mm.
Lepsia haustrum (Martyn). Plate 22, fig. 5.
From December capsules are deposited singly or usually in groups on a common basal membrane attached to rocks left high and dry at low tide and frequently in muddy localities. Capsules circular unless crowded, at first cream-coloured but change to purple. Base 6 mm., exit on brim 1 mm.
Lepsiella scobina (Quoy and Gaimard). Plate 22, fig. 6.
Spawning in Manukau November 26, 1926, capsules scattered on rocks or in dense clusters, latter with a common basal membrane; capsules horny, thin, globate, creamy-white changing to purple as development proceeds; height 3 mm., base 3 mm., brim 1·5 mm., exit 1 mm. or less. This mollusc was observed drilling circular holes about a sixteenth of an inch in diameter on rock oysters in the Manukau Harbour. Time taken to drill a single hole, about four hours.
Lepsithais lacunosa (Bruguière). Plate 23, fig. 10.
Normal breeding season October to December. After a two-hour copulation (October 7, 1930) aquarium specimen deposited capsules four days later, at nights only, total about 125 capsules each in six nights. Capsules attached to one another and to a common basal membrane on rocks; colour light to dark brown; upper surface nearly flat with well-defined rim, circular or polygonal of crowded capsules; height 2·4 mm., distal width 4·4 to 5 mm. exit on brim average 1 mm.
Alcithoe arabica (Martyn). Plate 23, figs. 9a, 9b.
Ovicapsules common at all depths to 23 fathoms in and around Otago Harbour on bottoms of sand or mud, occasionally on stone, weed, sunken wood, but chiefly on the shells of the following species in order of preference: Maoricolpus roseus, Tawera spissa, Paphies australis, Chione stutchburyi, Tanea zelandica, Mactra ovata, Maorimactra ordinaria. One ovicapsule per shell, rarely two; two to three embryos per ovicapsule. Ovicapsules 12 to 14 mm. high, diameter 10 to 17 mm. Obtainable from August to February, whitish or yellowish at first, usually brown to black after December; protective covering double, outer layer calcareous, strong, smooth, thickness 0·2 mm., with microscopic pores 0·12 mm. apart; inner membrane tough, smooth, horny. Ovicapsule subglobose above attachment disc, which is usually less than the maximum diameter, but may be expanded asymmetrically, especially if on shell of Maoricolpus roseus. The development period is lengthy. In 1930 ovicapsules were taken January 8, February 18, and October 25, and although the embryos were already well advanced, hatching required a further 6 to 8 weeks. The embryos moved freely in the unbroken egg till within two days of hatching, and then became quiescent as though eating through the envelope; after emergence they persistently left the water and crawled out of the aquarium jar. Length of shell at hatching 5 mm., width 4 mm.; protoconch blunt, almost flat, tegument usually attached thereto, operculum distinct, length 1·5 mm.; shells at first cinereous, with or without a few brown zig-zag radial stripes, shells wholly brown on the eighth day, length 7·5 mm. Outer lip sharp, fragile. One ovicapsule collected October 25, 1930, contained three embryos;
outer shell much broken, inner membrane complete; embryos hatched as usual. Captive parents fed freely on opened shellfish meat. One adult was seen to open and devour a live Tawera spissa.
Pleurobranchaea novaezelandiae Cheeseman. Plate 24, figs. 11, 12.
Spawn common in Blueskin Bay and down to 23 fathoms, September to November at least. On the night of October 9, 1931, after five weeks in captivity a specimen commenced to spawn on the weed Ulva latissima and in eleven hours deposited an irregularly coiled mass of spawn of a total length of about 70 cm. (fig. 12); in this the capsules were regularly spaced in a close spiral with about two turns per mm. and about 280 capsules per turn, eggs 6 to 30 per capsule, total fully 4,000,000 eggs. The next day, within an hour of adding a newly-captured specimen, the two commenced an 18-hour copulation, and in 20 days both spawned, coils about 20 cm. long, width about 30 mm. or twice as much as before, but with the turns of the spiral more distant and the capsules scattered (fig. 11). A close-up observation of the spawning of this tectibranch showed that as the spawn first extruded from the oviduct, the egg mass was without any semblance of a circular shape, but as it passed through the hollow made by the mantle and foot and coming in contact with the water, it coagulated into a comparatively firm structure filling out into a circular coil, the edge nearest the foot adhering to the weed.
Archidoris wellingtonensis Abraham. Plate 24, fig. 13.
Spawning season December to March. These large slugs are common at Seal Point, Otago, in a steep rocky channel where the surf is especially rough at high tide. Copulation is reciprocal; specimens in captivity crawled round one another before commencing a four-hour copulation, both spawning four days later. A large specimen 240 mm. in length collected mid-February at Quarantine Island crawled restlessly in the aquarium over green and brown weed and hydroids without feeding, until in three weeks it had shrunk to half the original size; when a piece of violet-coloured sponge was added, the slug crawled on to it at once and fed steadily until in four days it was almost buried in the remains of the sponge; it then moved to a large smooth rock and in 12½ hours deposited a mass of salmon-pink spawn, weighing 440 grms. in the form of a spiral of ten turns, length 2·7 metres, width of ribbon 56 mm. Eggs 0·05 mm., capsules 0·65 mm., average 50 eggs per capsule. Latter in transverse rows, 2 per mm., 148 capsules per row, total number of eggs 40,000,000. The number in the specimen figured is about 300,000. Young (1924, p. 189) records the spawning of this nudibranch in October at Portobello… “Ribbon one inch wide, eleven inches long and eggs about as large as a small pin head, so that the total number of eggs must have run into many thousands.… All attempts to hatch the eggs failed.”
Ctenodoris flabellifera (Cheeseman). Plate 25, fig. 14.
Common in Otago and Manukau Harbours; spawning from December to March. After a 3½ hours copulation one of the two captive specimens deposited the spawn shown in fig. 14 four days later, finishing in 5½ hours; length of ribbon 420 mm., width 7 mm., 16 rows per cm., 150 capsules per row, 3 to 15 eggs per capsule, total roughly
1,000,000 eggs. The other specimen two days later deposited a ribbon 350 mm. long and 17 mm. wide; twice this length was deposited by a third animal in captivity.
Aphelodoris luctuosa (Cheeseman). Plate 25, fig. 15.
Spawning season November to January (Manukau Harbour). The sample figured was deposited on the weed Cystophora in an aquarium, February 2, 1930; length 700 mm., width of ribbon 25 mm., capsules irregularly scattered, diameter 0·29 mm., eggs 3,000,000, diameter 0·06 mm., eggs 6 to 16 per capsule.
Dendrodoris citrina (Cheeseman). Plate 26, fig. 17.
Spawning season October to December (Otago Harbour), ribbons deposited chiefly on Ulva lactuca. That shown, from a captive specimen 37 mm. in length, was deposited on sponge in 7 hours; length 180 mm. (unusually small), width 10 mm., colour orange, eggs salmon-pink; thickness of ribbon at base 2 mm., and mid-width 4 mm., distal margin acute. Capsules 0·07 mm., eggs 0·008 mm., total eggs 24,000.
Siphonaria zelandica Quoy and Gaimard. Plate 26, fig. 16.
Spawn common. December to January (Otago Harbour), between tide levels; on rocks, especially soft rock free from weed, or on shells of the same species of or chitons (Eudoxochiton nobilis, rarely Sypharochiton sinclairi); at first pale yellow, changing to cloudy white. Spawn semi-circular, crescentic, or pot-hook shaped, length 10 to 25 mm.; capsules 400 to 600, diameter 0·18 × 0·12 or 0·15 × 0·15 mm. spherical, each with 3 to 10 eggs; diameter of eggs 0·05 mm. The gelatinous matrix retains its original sticky nature, instead of coagulating as in the case of most species, and so collects small fragments of debris. Mestayer (1920, p. 171) records Kerguelenia obliquata (Benhamina obliquata) spawning at Island Bay in April.
Cryptoconchus porosus Burrow.
A captive specimen from 9 p.m. till midnight February 1, 1930, liberated an almost continuous stream of capsules which, after a period of suspension, settled down and almost covered the parent; in open water dispersal would presumably occur during this interval. Diameter of capsule 0·24 mm., each with several eggs, diameter 0·07 mm.
Amaurochiton glaucus (Gray).
Spawns freely in captivity. December 15, 1931, a specimen which had commenced to spawn at midnight covered itself as well as the adjacent tank floor with greyish powdery eggs, diameter 0·12 mm., approximate total (Bayer's method) 4,000,000. Captive specimens remain under ledges during daylight, grazing on plant growth on the floor of the tank; marked specimens returned to self same spot after nocturnal rambles.
Summary and Conclusions.
1. Eggs of Haliotis iris, Cryptoconchus porosus and Amaurochiton glaucus are liberated in great numbers and are slowly dermersal; in open waters settling would presumably be delayed and dispersal would occur.
2. Eggs of Benhamina obliquata, Pleurobranchaea novaezelandiae, Archidoris wellingtonensis, Ctenodoris flabellifera, Aphelodoris luctuosa, Dendrodoris citrina and Siphonaria zelandica are deposited in gelatinous ribbons attached to rocks or sessile organisms. These species include the nudibranchs and limpet-like pulmonate in the series studied. Eggs of Zeacumantus subcarinatus are embedded in clumps of gelatinous matrix, not drawn out into a ribbon.
3. Eggs of Cabestana, spengleri, Argobuccinum tumidum, Cominella maculosa, C. glandiformis, Zeatrophon ambiguus, Neothais scalaris, Lepsia haustrum, Lepsiella scobina, Lepsithais lacunosa and Alcithoe arabica are deposited in capsules attached to rocks or sessile organisms. The capsules of Lepsia haustrum, Lepsiella scobina, Lepsithais lacunosa and Alcithoe arabica, which are carnivorous gastropods, are deposited on a basal membrane, which in the case of Cabestana spengleri extends upwards to form an open globose cup or basket containing the capsules.
4. Alcithoe arabica forms relatively enormous but correspondingly few capsules, attached singly (rarely in twos) to the bottom debris, with the reduction in the number of contained eggs to two, rarely three per capsule; the larvae are active and relatively large benthic animals when liberated.
5. No surface-floating molluscan eggs were recognised, for those of the first group above would appear but transiently if at all in the plankton; presumably the larvae of the second and third groups would appear in the neritic plankton, except that Alcithoe arabica has no planktonic stages, and apart from minor agencies such as the occasional deposition of a capsule on a gastropod shell tenanted by a Pagurid, is dependent on its own motility for dispersal.
6. A slight upward movement prior to oviposition occurs in the case of Cominella maculosa, whose forsaking of the normal muddy habitat in favour of rocks is presumably a prophylactic recourse against smothering of the eggs by silt. Also the nudibranchs usually spawn on weed or vertical rocky channels, possibly to escape silt and sand or benthic enemies, or to ensure optimum supplies of oxygen. But Alcithoe arabica spawns on debris on the sandy bottom of its normal habitat.
7. Apart from these slight upward movements, no spawning migrations have been detected, but Haliotis iris has a non-reproductive winter migration into deeper water. As shown by marked shells, this species and Amaurochiton glaucus have a “homing” tendency in that they return accurately to the same spot after a night foraging expedition, and in neither can this be interpreted, as has been claimed in the case of limpets, as a return to a spot where the irregularities of the rock surface are accurately matched by those of the shell margin. In the case of Lepsithais lacunosa, Archidoris wellingtonensis, and Ctenodoris flabellifera copulation is reciprocal; among the nudibranchs in general, copulation is a protracted process which occupies several hours.
8. In order to study further such phenomena as the transient appearance of opercula and shells in embryonic nudibranchs, the absorption of the nutritive material of the majority of encapsulated
ova by a surviving minority of embryos, and other problems of embryology and ecology, it is essential to have a supply of circulating sea water free from infusoria and other micro-organisms and from the rust of iron reticulating pipes.
9. Much more detailed studies are necessary before a critical estimate can be attempted of the sufficiency of ocean currents to account for distributional phenomena, such as the occurrence in New Zealand waters of Australian species, which Finlay (1924, p. 334) interprets in terms of the Notonectian Current. Kelp-frequenting chitons, limpets, and mussels, as well as pelagic larvae, come into question in this connection.
The writer is indebted to Dr. E. W. Bennett for helpful criticism and assistance during the compilation of this paper; to Mr. S. Broadley, for his help in timing the spawning and copulation of some of the species in the aquarium; to Miss Thelma Kent, A.R.P.S., for prints of the writer's negatives.
Bayer, H. von, 1908. A Method of Measuring Fish Eggs. Bulletin of the Bureau of Fisheries, U.S.A., vol. 28, pp. 1009–1014.
Burkenroad, M. D., 1931. Notes on the Louisiana Conch, Thais haemastoma Linn. in its relation to the oyster, Ostrea virginica. Bureau of Research. Dept. of Conservation of Louisiana. Vol. xii, Ecology, pp. 656–664.
Cooke, A. H., 1913. Molluscs. The Cambridge Nat. History, London, p. 129.
Finlay, H. J., 1924. List of Recorded Relationships between Australian and New Zealand Mollusca. Reports Australian Association Advancement Science, vol. 16, pp. 332–343.
Mestayer, M. K., 1920a. A note on Pleurobranchaea novaezelandiae, New Zealand Journ. Sci. and Tech., vol. iii, no. 3, pp. 171–2.
—— 1920b. Notes on the Spawn Coils of Kerguelenia obliquata, New Zealand Journ. Sci. and Tech., vol. iii, no. 3, p. 172.
Suter, H., 1918. Biological notes on Alcithoe arabica. Proc. Mal. Soc., vol. xiii, pp. 73–74.
Tattersall, W. M., 1920. Notes on the Breeding Habits of the Periwinkle. Fisheries Branch, Dept. Agri. and Tech., Dublin, Ireland.
Woodward, B. B., 1913. The Life of the Mollusc. London.
Young, M., 1924. Notes on the Spawning of Doris wellingtonensis. New Zealand Jour. Sci. and Tech., vol. vii, p. 189.