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Rawson, M. V. 1973. The development and seasonal abundance of the parasites of striped mullet,
Mugil cephalus L., and mummichogs, Fundulus heteroc/itus (L,). Ph.D. Dissertation, Univ. of
Georgia. 100 pp.
Roberts, L. S. 1970. Ergasilus (Copepoda: Cyclopoida): revision and key to species in North America.
Trans. Amer. Microsc. Soc. 89: 134-161.
Siegel, S. 1956. Nonparametric statistics for the behavioral sciences. McGraw-Hill Book Co., New
York. 312 pp.
Skinner, R. 1975, Parasites of the striped mullet, Mugil cephalus, from Biscayne Bay, Florida, with
descriptions of a new genus and three new species of trematodes. Bull. Mar. Sci. 25: 318-345.
White, H. C. 1940. "Sea lice" (Lepeophtheirus) and death of salmon. J. Fish. Res. Bd. Can. 5: 172175.
Wilson, C. B. 1936. Parasitic copepods from the Dry Tortugas. Pap. Tort. Lab. 29: 327-347.
DATEACCEPTED: February 12,1986.
ADDRESS: Department of Zoology, University of Florida, Gainesville, Florida 32611. PRESENTADDRESS:South Carolina Marine Resource Research Institute, P.O. Box 12559, Charleston, South Carolina, 29412.
BULLETIN
OFMARINESCIENCE,
40(2):382-387,1987
FECUNDITY VARIATION IN RELATION TO INTERMITTENT OR
CHRONIC SPAWNING IN THE CUTTLEFISH, SEPIA OFFlelNALIS L.
(MOLLUSCA, CEPHALOPODA)
Sigurd v. Boletzky
The reproductive biology of the common cuttlefish of the eastern Atlantic and
Mediterranean Sea, Sepia officinalis Linnaeus, 1758, is now known in considerable detail (Boletzky, 1983, review), but we do not yet have quantitative data
on individual fecundity. Traditionally, fecundity of cephalopod females is estimated from the number of fully mature ova contained within the ovary of an
individual; rarely is it estimated from the number of eggs an individual is actually
observed to lay (Voss, 1983). From a study of the natural population of S. officinalis
in the Catalonian Sea, Mangold-Wirz (1963) provided precise numbers of mature
and immature ovarian eggs for various adult sizes and concluded that a single
female may lay from about 200 to 550 eggs depending on its size, which may
vary from about 110 to about 250 mm in dorsal mantle length (ML). Richard
(1971) indicated similar numbers (150 to 500) for the cuttlefish population of the
English Channel. A much higher number was reported by Boletzky (1975) from
a large-sized wild female that spawned during nearly 4 months in the aquarium.
The estimated total of eggs produced by the animal was one order of magnitude
higher than hitherto known numbers. Although this estimate may have been
somewhat high, it is clear that cuttlefish can lay considerably greater numbers of
eggs than counts of mature ovarian eggs would suggest, provided that the female
survives sufficiently long to allow full maturation of ova that were immature at
the outset of spawning.
383
NOTES
ML
mm
100
/
°C
+
.•.
+
n;Il~:.:t:"""""i:....,.....+
20
"
.
,,'
.
........ .'
............... ............ .
.
15
1
a
11182
11183
I
a
.
500
d.y.
Figure I. Growth of Sepia officinalis reared under normal daylight and small rations to the age of 7
months, thereafter (sub-sample of 10 individuals) at constant dim light and higher food rations to the
age of 12 months, and finally (3 surviving individuals) under constant bright light until natural death
(crosses). Broken lines indicate growth of males, double solid line growth of single female. The arrow
marks onset of spawning. Dotted line marks temperature in 0c. ML = dorsal mantle length.
This is the first detailed account of prolonged spawning in Sepia, primarily
based on observation of a small-sized female reared from hatching. The observed
body size corresponds to the minimum size of sexually mature females in natural
populations of S. officinalis, and to average adult size of other species such as S.
orbignyana.
MATERIALS AND METHODS
Cuttlefish hatched in the laboratory on 23 and 24 October 198 I (Fig. I) from a late summer/autumn
spawn were reared under natural daylight conditions in an open circuit sea water aquarium using
standard techniques (Boletzky and Hanlon, 1983). To obtain sexual maturity at minimum adult size
(Boletzky, 1979), food rations comprising mysid, palaemonid and crangonid shrimp were kept to a
minimum for the young animals. At age 7 months, a batch of 10 individuals measuring between 32
and 43 mm ML was transferred to a room with constant, very feeble, dim light to promote sexual
maturation (Richard, 197 I). The animals were kept in individual compartments of large tanks and
were fed daily (under a torch light) one palaemonid shrimp. Due to high mortality probably caused
by poor water quality during the summer months, only three individuals survived. At age 12 months,
when the animals were considered sexually mature, they were transferred to individual 50-liter tanks
constantly lit from above by fluorescent tubes (PHILIPS TLS 40 W / 33 "Blanc Industrie") to promote
spawning. Two of these individuals were males (87 and 90 mm ML), one was a female (80 mm ML).
They were now fed larger rations of shrimp and small crab to ensure optimal feeding conditions.
During the following months, one of the males was at different intervals mated with the female.
After copulation, which generally started immediately, the animals were separated to avoid uncontrolled interaction that could stress the female under these confined conditions. A small batch of eggs
was placed in the tank of the female to provide a visual stimulus for spawning. After the onset of egglaying, mating was permitted at intervals varying from about 1 week to about 1 month (Fig. 2). Eggs
were counted regularly and the bulk oflarge batches was removed and placed in a separate tank where
embryonic development proceeded. A small batch of eggs was always left with the female as a visual
stimulus.
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BULLETIN OF MARINE SCIENCE, VOL. 40, NO.2,
I
1987
m
n
eggs
laid
50
25
o
t
o
I
t
I
t
50
t
t
I
100
days
Figure 2. Numbers of newly laid eggs from the female of Figure 1, recorded at daily control (black
columns) or at the end of a period of several days (white columns). Roman numbers indicate months;
arrows in the lower part of the figure indicate the days at which the female copulated with one of the
males of Figure 1.
RESULTS
Spawning Sequence. - The first batch of eggs was observed on 3 January 1983,
one day after mating. It contained 25 eggs with normally arranged nidamental
envelopes and one egg incompletely wrapped. Measurement ofthis ovum showed
a normal size of 6.0 x 4.8 mm. Later measurements of newly laid eggs revealed
virtually identical sizes, with only a slight decrease to ovum diameters 5.8 x 4.6
mm in late March.
Figure 2 shows the irregular intervals of spawning events and the highly variable
numbers of'eggs produced between the (generally daily) observations. The cumulative curve of egg release (Fig. 3) demonstrates, however, that these irregular
episodes oscillate around a mean rate of 4 eggs released daily during the first 2
months of chronic spawning. This linear increase then changed to an exponential
rate that was maintained until the end. The last large batch comprising 27 normal
eggs was laid on 26 April, and was accompanied by two empty egg cases. On the
following day, only 10 normal eggs were laid, and about 20 empty egg cases, some
of which were unpigmented. On 29 April, the animal was found dead.
Ovarian Egg Population. -Dissection of the dead animal showed that the ovary,
which had a volume of about 15 ml, was depleted of mature ova. However, there
were 85 full-sized ova still enclosed in their follicles (recognizable by the reticular
pattern of folds). Maturing eggs of smaller sizes were present in the following
numbers: 58 (4-5 mm), 128 (3-4 mm), 134 (2-3 mm), 191 (1-2 mm), and about
400 (0.25-1.0 mm). They totaled roughly 1,000 eggs (Fig. 4).
385
NOTES
total no.
of eggs
maturing
ova
(hypothetical
rate)
,,+
.....
E
1000
-
+,C
.
••
~ •
500
•
••
•
.•+'
0'"
-
-
_
A+B
-
••
-
•
.•
•
•
•
•
100 -
•
-
•
•
50
•
•
••
I
I
II
o
III
IV
100
50
v
150
days
Figure 3. Cumulative curve giving total number of eggs laid over the whole period of spawning. The
inset shows the ovarian eggs recorded post mortem (size categories A to E according to Figure 4)
arranged by extrapolation of the final rate of egg laying (see text).
Effective Fecundity. - Except for the last two batches of eggs laid, all previous ones
were normal and contained no empty egg cases. Embryonic development proceeded normally and resulted in healthy young animals that measured 6 to 8 mm
ML at hatching. The total effective fecundity of this small-sized female thus
amounts to nearly 640 viable eggs.
DISCUSSION
These results are meaningful in demonstrating the possibilities of fecundity
variation as a function of adult survival. They are complementary to earlier
observations (Boletzky, 1975; 1979) in that they represent a combination of (a)
386
BULLETIN OF MARINE SCIENCE, VOL. 40, NO.2,
no. maturing
1987
ova
500
o
o
E
o
2
C
3
4
5
6mm
size of maturing
ova
Figure 4. Size classes of maturing ova recorded in the ovary, from nearly mature eggs (A) to small
immature stages (E). The highest column of the histogram represents the smallest oogenetic stages
(0.25 to 1.0 mm) not considered in the inset of Figure 3.
spawning length similar to that reported in 1975 from a large-sized wild-caught
animal and (b) adult size similar to that of the laboratory-reared animal observed
to spawn massively during the first weeks of egg-laying (Boletzky, 1979: sub-batch
F').
Spawning Sequence. -Personal laboratory observations have shown a wide variety ranging from intermittent spawning with periods of inactivity as long as I
month, to virtually continuous chronic spawning over many weeks. The factors
responsible for the length of pauses occurring in egg maturation and spawning
are not yet known.
The cumulative curve of egg-laying observed here is fairly smooth, with an
early linear phase followed by an exponential phase. The former coincides with
the final phase of slow body growth ofthe female. Indeed mantle-length increased
by about 10% during the first 2 months of spawning (Fig. 1). This may have been
accompanied by an increase of the overall volume of the ovary, possibly coupled
with an increase in the rate of egg maturation.
Ovarian Egg Population. - The size distribution of ovarian eggs recorded post
mortem (Fig. 4) shows clear similarity with the size distribution of ovarian eggs
recorded in wild females by Mangold- Wirz (1963) and by Najai (in press). The
latter author includes very small maturing eggs measuring < 1 mm and thus
arrives at higher total numbers than Mangold-Wirz. Among the remaining ova
represented in Figure 4, those ranging from 1 to 6 mm (i.e., including the nearly
mature stages) amount to about 600. One can hypothesize that if the animal had
lived and continued to lay eggs at a rate similar to the exponential phase observed,
these 600 eggs would have been laid within about 40 days (inset of Fig. 3). Although
this extrapolation may be unrealistic for a small-sized individual already exhausted by prolonged spawning, it appears conceivable for animals of slightly
larger size.
Definitely egg counts from the ovary of a mature female captured from the sea
do not reveal whether the individual under consideration has already laid some
eggs before it was captured-as
they do not reveal how many of the immature
ovarian eggs would have reached full maturity if the animal had continued to live
and spawn. Once full maturity is reached, individual fecundity becomes a matter
of "refilling" ovarian space made available by spawning, in a race against predation
NOTES
387
or senescence. Considering, in the example described here, that more than 600
ova with a total volume of roughly 60 cm3 have been produced by an ovary that
has a capacity of only about 15 cm3, it is clear that the last eggs laid must have
been very small developing ova when spawning started.
Intermittent spawning characterized by long pauses is based on the same principle. As an example, a small wild-caught female which for several months had
been kept under conditions similar to those of the above-mentioned animals,
except for considerably higher water temperature, started spawning when it reached
a size of about 100 mm ML and within two days laid about 230 eggs. Exactly 26
days later, it laid about 320 eggs. Although the ova were small in this individual
(4.7 x 3.6 mm), the large batch of eggs released first must have occupied a large
part of the ovary. Consequently the following eggs grew from very small sizes to
full maturity in less than one month.
Effective Fecundity. - The effective fecundity represented by more than 600 viable
eggs in an individual measuring ca. 115 mm ML is about four times the extant
number of mature ova found in wild females of corresponding size (MangoldWirz, 1963; Najai, 1985). In the light of this observation, effective fecundities
between 1,000 and 2,000 are perfectly conceivable for large-sized individuals of
S. officinalis measuring over 200 mm ML. Whether in nature a female survives
to spawn over a period of time sufficiently long to allow complete maturation of
all the potentially available ova depends on various factors, including the availability of appropriate food to counteract exhaustion, and, conversely, the presence
of large predators dangerous to the cuttlefish.
CONCLUSION
The spawning mode observed in S. officinalis is not unique within the cephalopods. It is probably more widely represented than the extreme situations marking
the opposite ends of a continuum of reproductive modes or "strategies" evolved
in the cephalopods. At the one end, there are the clearly semelparous "big bang"
spawners, e.g., Loligo opalescens. Although these are quite generally considered
typical of cephalopod reproduction, examples of protracted terminal reproduction
in both decapods and octopods have been known for some time (Boletzky, 1981).
At the opposite, there may exist definitely iteroparous forms not yet recognized.
At least the example of Octopus chierchiae (Rodaniche, 1984) now provides clear
evidence that repeated spawning is compatible with the octopodan mode of spawning and brooding, refuting the widely held belief that the female octopus "invariably dies shortly after the eggs hatch" (Wodinsky, 1977). Whether to call this
situation iteroparity or intermittent spawning is largely a matter of taste, unless
we reserve the former term to repeated seasonal reproduction. What is important
at the population level is the tendency to "break" the limitation in holding capacity
of the gonad by prolonged ovary functioning with successive egg maturations.
According to the theory of reproductive strategies (MacArthur and Wilson, 1967;
Pianka, 1970), this tendency responds to selection within rather stable populations
subject to density-dependent mortality, called K-selection by the above authors.
Field studies focused on rates of mortality throughout the life cycle of Sepia
officinalis are necessary now to define the pattern of pre-reproductive mortality
in relation to fecundity.
ACKNOWLEDGMENTS
I am indebted to several colleagues who took care of the reared animals for short periods, and
especially to Dr. S. Shepherd who kindly took over the culture work for a whole month. Communication
388
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VOL.40, NO.2, 1987
of unpublished results by Dr. S. Ezzedine-Najai is also gratefully acknowledged. I thank Dr. K. Mangold
and Mr. R. Tait for their critical reading of the manuscript.
LITERATURE
CITED
Boletzky, S. v. 1975. The reproductive cycle of Sepiolidae (Mollusca, Cephalopoda). Pubbl. Staz.
Zoo!. Napoli 39(suppl.): 84-95.
---.
1979. Growth and life-span of Sepia o./ficina/is under artificial conditions (Mollusca, Cephalopoda). Rapp. Comm. Int. Mer Medit. 25/26(10): 159-168.
---.
1981. Reflexions sur les strategies de reproduction chez les Cephalopodes. Bull. Soc. Zool.
Fr. 106: 293-304.
--.
1983. Sepia officina/is. Pages 31-52 in P. R. Boyle, ed. Cephalopod life cycles. Vol. I.
Academic Press, London.
--and R. T. Hanlon. 1983. A review of the laboratory maintenance, rearing and culture of
cephalopod molluscs. Mem. Natl. Mus. Victoria 44: 147-187.
MacArthur, R. H. and E. O. Wilson. 1967. The theory of island biogeography. Princeton University
Press, Princeton, N.J. 203 pp.
Mangold-Wirz, K. 1963. Biologie des Cephalopodes benthiques et nectoniques de ]a mer Catalane.
Vie Milieu, 13(suppl.): 1-285.
Najai, S. 1985. Fecundity of the cuttlefish, Sepia officina/is L. (Mollusca, Cephalopoda) from the
gulf of Tunis. Vie Milieu 35: 283-284.
Pianka, E. R. 1970. On r- and K-selection. Am. Nat. 104: 592-597.
Richard, A. 1971. Contribution a l'etude experimentale de la croissance et de la maturation sexuelle
de Sepia officina/is L. (Mollusque Cephalopode). Doctoral Dissertation (These d'Etat), Univ. Lille
(nr. 243). Lille, France. 264 pp.
Rodaniche, A. F. 1984. Iteroparity in the lesser Pacific striped octopus Octopus chierchiae (Jatta,
1889). Bull. Mar. Sci. 35: 99-104.
Voss, G. L. 1983. A review of cephalopod fisheries biology. Mem. Natl. Mus. Victoria 44: 229-241.
Wodinsky, J. 1977. Hormonal inhibition of feeding and death in Octopus: control by optic gland
secretion. Science 198: 948-951.
DATEACCEPTED: April 8, 1986.
ADDRESS: C.N.R.S., Laboratoire Arago, F-66650 Banyuls-sur-Mer
(France).