THE BREEDING SEASON OF THE BRACHIOPOD,

LINGULA UNGUIS (L.)

S. H. CHUANG
University of Malaya in Singapore, Singapore
Yatsu (1902) believed that the breeding season of Lingula unguis lasted from
mid-July to the end of August in Misaki, Japan, since he could not find the larvae
at any other time of the year. Kurne (1956) confirmed Yatsu's observation, and
also found that the peak of breeding occurred during the first half of August.
Sewell (1912) found several larvae in December and February in the plankton off
the south coast of Burma. He attributed this (p. 90) to either a local peculiarity
or possibly to the existence of two breeding seasons during the year, one in the
summer months July and August, and a second from December to February.
Ashworth (1915) obtained larvae in the southern part of the Red Sea in June
and October, and in the Indian Ocean in October. He also found a larva in
Annandale's plankton sample obtained in the Strait of Bab-el-Mandeb in March.
This led him to believe that in the southern part of the Red Sea a succession of
spawnings extended at least over the period from the beginning of March to the
early part of September.
Yatsu (1902) observed the spawning of Lingula unguis in captivity on several
occasions in July and August. He noted that spermatozoa and ova were dis
charged forcibly through the median setal tube. Kume (1956) observed that in
L. unguis spawning in the laboratory occurred twice daily, at sunrise and after
sunset.
In the present study plankton samples were collected to determine the occur
rence of the larvae of Lingula. The spawning behavior of adult female specimens
in the laboratory was also studied.
MATERIALS AND METHODS
The plankton hauls were made with a fine tow-net at a depth one foot below the
surface off the north coast of Singapore Island. On each occasion 4-10 hauls of
10 minutes each were made, more hauls being made under favorable weather con
ditions. The Lingula larvae from the plankton samples were isolated and classified
according to the number of pairs of cirri. In this study a larva with n pairs of
cirri and a pair of buds, the length of each of which has equalled the diameter of
the base of the median tentacle, is assigned to the stage of n + 1pairs of cirri
(abbreviated to n + 1 p.c. stage). Although the hauls were made 12miles from
a good bed of Lingula unguis, it was not possible to assign the larvae to this Species
with certainty.
Specimens of Lingula unguis for the laboratory study of spawning behavior were
obtained from the north coast of Singapore Island. A plot of muddy sand with
the greatest concentration of burrows was chosen, and from it all the available
202
BREEDING SEASON OF LINGULA UNGUIS 203
specimens were dug out with a shovel during ebb-tide. The area worked roughly
amounted to 515square meters per trip. In the laboratory every 25 specimet1@
were laid on their dorsal or ventral side in a rectangular tray, 30 cm. by 45 cn1.@
under 4 cm. of natural sea water renewed once a day. These trays were stacked
on shelves in a darkened room maintained at a temperature of 1820 C. Every
morning they were examined with the light of a lamp for spawned ova. Specimens
that had spawned were transferred into marked petri dishes, 920cm. in diameter
and with a capacity of 50400cc. They were maintained in these dishes with
daily renewal of water during the rest of the experimental period for easier estima
tion of the ova spawned.
Frequent attempts were also made to find the time of settlement of the larvae
by searching for the young postlarvae at the Lingula beds along the north and east
coasts of Singapore Island.
RESULTS
I. Occunnence of planktonic lanvae
The larvae of Lingula obtained from plankton hauls during the period July.
1952June, 1953 are tabulated according to the number of paired cirri. Dead
larvae with disintegrating cirri are assigned to the column of unclassifiable specimens
(Table I).
Inspection of Table I shows that (1) the larvae appeared in practically every
month of the year, suggesting a continuous breeding throughout the year. This fits
in with Orton's rule (1920, p. 353), that in those parts of the sea where temperature
conditions are constant or nearly constant, and where biological conditions do not
vary much, that marine animals will breed continuously. (2) On most occasions
the free-swimming larvae were at different stages of development. This suggests
that the larvae of each catch were not the products of any single (lay's spawning.
(3) Older larvae of 8 and 9 p.c. stages were rare. (4) Young larvae of 2 and
3 p.c. stages appeared in July, August, September, October and November of 1952
and in January, February and June of 1953. (5) The young larvae of 2 and 3 p.c.
stages were captured two or three times at intervals of 57days in August and
September. Their occurrences did not bear any relationship to the phases of
the moon.
II. Laboratory spawning of the females in Lingula unguis
Many specimens brought into the laboratory in every month of the year were
found on dissection to have ripe ova. Observations of laboratory spawning are
summarized in Table II, which shows that (1) spawning occurred 514days after
collection among specimens collected on every occasion. (2) Observation on the
duration of spawning of each batch was completed only for the batch collected on
July 29, 1952. Observations on other batches were discontinued after various
periods. (3) The smallest specimen that spawned had a ventral-valve length of
22.6 mm. and the largest. 46.0 mm. Presumably, the females become sexually
mature in this locality when they attain the former size approximately, and continue
to spawn thereafter at intervals. The presence of ripe ova in many specimens
exceeding 50 mm. in length seems to indicate that the spawning power is retained in
old age.
Date of collectionNumber
of larvae with the following pairs of cirri
Uncles
2 3 4 5 6 7 8 9 sifiableTotal14.
7.1952
22. 7.1952
13.8.1952
19. 8.1952
24. 8.1952
31. 8.1952
7. 9.1952
14. 9.1952
21. 9.1952
28. 9.1952
6.10.1952
26.10.1952
2.11.1952
9.11.1952
16.11.1952
6.12.1952
15.12.1952
3. 1.1953
2. 2.1953
26. 3.1953
15. 4.1953
20. 5.1953
27.5.1953
12. 6.1953
29. 6.195310
20
4
3
9
8028
5
31
4
59
14
38
10
15
4
22
3
81
2
21
39
2
69
1
1
1
1
1
61
1
6
1
4
4
593
1
6
2
115
43
12
81 11
2
1
12

3
6
2
2531
1
20
51
99
0
0
2
85
29
0
55
0
0
49
0
5
110
10
2
0
7
8
219
13Total126210156207613123252796TABLE
II
Laboratoryspawning of Lingula unguis from the north coast of Singapore IslandDate
of collectionOnset
of
spawning
(days after
collection)Total
spawn
ing days.
when expt. is
discontinuedNumber
of
males and
females
collectedNumber
of
spawning
femalesVentral-valve
length of
spawning females (mm.)MinimumMaximum30.
5.1952
28. 6.1952
14. 7.1952
29. 7.1952
28. 8.1952
13. 9.1952
6.10.1952
5.11.1952
30.11.1952
31.12.1952
27. 2.19536
8
5
5
14
12
6
11
1074
95
188
78
52
82
80
59
29159
134
293
275
93
59
65
316A
few
55
6
57
28
11
11
9
9
10
Afew23.9
30.3
22.6
23.4
27.5
27.0
27.5
26.7
32.441.0
39.1
46.0
43.2
37.1
42.3
38.3
39.0
43.4
204 S. H. CHUANG
TABLE I
Number of Lingula larvae from plankton samples obtained off the
north coast of Singapore Island
30
205
BREEDING SEASON OF LINGULA UNGUIS
Further data on the batch collected on July 29, 1952 are summarized in Figure 1,
which shows that (1) during a period of 6 months or so, there were some specimens
spawning each week. (2) The most intensive spawning occurred between the
seventh and thirteenth week of captivity when from 109135cases of spawning per
week were observed. (3) Cases of intensive spawning when several thousand ova
were extruded by a female per day occurred during the first half of the observational
period. -
OF CAPTIVITY
FIGURE 1. Lingula unguis. Number of cases of laboratory spawning per week during
captivity. These cases were compiled from daily records of fifty-seven spawning females
collected on July 29, 1952 from the north coast of Singapore Island.
The spawning behavior of 5 females from among the more consistent spawners
of the July 29, 1952 batch reveals that (1) all the ova of an individual were not
extruded at once. (2) Spawning in a female occurred in a series of bursts sepa
rated by rest intervals. (3) The first burst was usually the most intensive and
consisted of 123days of spawning. (4) Other bursts of lower intensity followed
at irregular intervals over a period of 23months. (5) The laboratory spawning
did not have any relationship to the phases of the moon or the tides.
Spawning occurred both day and night. The ova were forcibly squirted out
of the central exhalant setal tube, as Yatsu (1902) had previously observed. On
20 25
O <oo Ova perday
11111 00-200 I11 II
@ 200-1000 ii I, IS
>1000 p II II
340
(D 320
300
LI) 80
0 60
(I)
ILl 40
(r,
0 20
WEEKS
206 S. H. CHUANG
a few occasions these came out in the accessory exhalant currents found midway
along the lateral gape of the animal. In 24 hours a spawning female produced
from half a dozen to about 3000 ova. When only a few ova were spawned, these
were found singly in the dish. However, when a few hundred or more ova were
extruded, they were coated liberally with mucus which enabled them to stick
together and form big sheets or clumps, as Yatsu ( 1902) had noted.
The newly spawned ovum was spherical in shape. The mean of 62 ova was
95.55 /L4.60 @. Each was enclosed in a prominent vitelline membrane 3 @&in
thickness. The nucleus was visible in the living ovum. After some time the
unfertilized ovum degenerated. It gradually enlarged, presumably on imbibing
water, became irregular in shape and finally disintegrated after 12days in sea
water.
When a transparent specimen was examined under a binocular microscope
during its spawning period, the ova were found circulating in the coelomic fluid in
the visceral cavity. They were also found in the coelomic fluid in the longitudinal
pallial sinuses. On one occasion the pedicle of a spawning female accidentally
snapped; the coelomic fluid that oozed out contained not only the usual coelomic
corpuscles but also some ova.
Analysis of further data of the July 29, 1952 batch reveals that (1) large
specimens produced more ova than small ones. For instance, 6 females of 4146
mm. ventral-valve length averaged 17,250 ova per specimen during the entire
observation period; 9 females, 30-40 mm. long, averaged 13,000 ova with a maxi
mum of 17,800 ova; 3 others, all below 30 mm., averaged 4000 ova with a maximum
of 7500 ova. (2) During the entire observation period of 188 days the largest
specimen, 46.0 mm. long, spawned 28,600 ova in 104 days; the second largest, 43.5
mm. long, spawned 22,350 ova in 76 days. (3) A specimen, 39.8 mm. long,
spawned on 125 days out of 188 days. (4) The females dissected at the end of the
spawning period usually had spent ovaries.
The production of a large number of ova is presumably necessary to counteract
the following possible wastages: (1) wastage of ova through fertilization taking
place outside the body, when the germ cells are shed into the sea; (2) wastage of
larvae due to the long pelagic larval period, which, according to Yatsu (1902),
lasted 1% months.
Observations on the laboratory spawning of female specimens suggest that the
long breeding season of Lingula in the tropics may be due to the following: (1)
all the ova were not shed at once but intermittently over a long period of time; (2)
the staggering of the peaks of individual spawning in a large population; (3) the
presumable tendency of the postlarvae from the different spawnings to reach spawn
ing age at different times of the year.
The female specimens in L. unguis continued to spawn in the laboratory in
complete isolation from the males, contrary to the hypothesis of Yatsu (1902, p. 4)
that Until the sperm is discharged the eggs even when well ripened seem to be
retained within the body.
The females, even when reared singly in separate petri dishes, continued to
spawn in the laboratory for several months. Crowding therefore was not necessary
for the females to continue spawning, contrary to the observation of Kume (1956,
p. 223) that the frequency of shedding was greatly reduced in the vessel in which
only a small number of individuals were cultured.
BREEDING SEASON OF LINGULA UNGUIS 207
III. Occurrence of young postlarvae
Attempts to collect the young postlarvae were unsuccessful in the muddy
Lingula beds along the north coast of Singapore Island. Along the east coast the
beds are sandy. Here some young postlarvae with the following minimum ventral
valve lengths were obtained on the following dates: April 16, 1952, 6.5 mm.;
September 24, 1952, 2.7 mm.; October 22, 1952, 3.7 mm.; November 3, 1952, 5.8
mm.; and July 3, 1953, 1.4 mm. Presumably it was only when the spatfall was
considerable that the young postlarvae could be found.
SUMMARY AND CONCLUSIONS
1. The planktonic larvae of Lingula were found in almost every month of the
year,suggestingcontinuousbreedingoffSingapore Island.
2. Several heavy spatfalls were observed in 1952, indicating several peaks of
spawning during the year.
3. The spawning behavior of the female in Lingula unguis was described and
its bearing on the continuous breeding in the tropics was suggested.
4. It was suggested that a female spawned a large quantity of ova to counteract
the possible wastage of ova accompanying external fertilization and the wastage
of larvae during the long pelagic larval period.
LITERATURE CITED
ASHWORTH, J. H., 1915. On larvae of Linqula and Pelagodiscus (Discinisca). Trans. Roy.
Soc. Edinb., 51: 4569.
KUME, M., 1956. The spawning of Lingula. Nat. Sci. Rept. of Ochanotnizu Univ., Tokyo,
6: 215223.
ORTON, J. H., 1920. Sea-temperature, breeding and distribution in marine animals. J. Mar.
Biol. Assoc., 12: 339366.
SEWELL, R. B. S., 1912. Note on the development of the larva of Lingula. Rec. Indian Mus..
7: 8890.
YATSU, N., 1902. On the development of Lingula anatina. J. Coil. Sci.. Tokyo, 17: 1112.