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@ Spr[nger-Verlag 1990
Abstract
Reproduction of the commercial sea urchin Paracentrotus
lividus (Lamarck) from contrasting habitats on the west
coast of Ireland was examined from May 1986 through
August 1988. Urchins were collected intertidally from an
exposed rocky shore and subtidally from a protected bay.
Monthly measurements of the gonad index and histological
examination of the gonads demonstrated that P. lividus has
an annual reproductive cycle. Although the two populations
exhibited similar reproductive patterns over three breeding
seasons, there were inter-annual and inter-population differences in the amplitude of gonadal growth and in the time
when spawning started. The subtidal urchins had significantly larger gonads and exhibited a longer period of reproductive maturity compared with the intertidal urchins. This
difference was also evident in the histology of the ovaries at
the beginning of breeding, when most of the subtidal females
contained mature ovaries, whereas most of the intertidal
females contained premature ovaries. An inter-annual difference in the onset of spawning was observed, with the start
of gamete release differing by as much as four weeks between years. It appears that inter-annual differences in sea
temperature influence the temporal variation in spawning
by P. lividus and that increasing temperature may serve as
an exogenous cue for gamete release. The inter-annual variability in the onset of spawning suggests that photoperiod
does not cue gamete release. Gonadal growth, on the other
hand, occurs during the coldest months of the year and during the period of shortest days, suggesting that temperature
and photoperiod may both influence gonadal growth during
the winter. Oogenesis and spermatogenesis of P. lividus were
examined histologically. During the post-spawning recovery
and growth stages, the gonads gained weight through
growth of the nutritive phagocytes and the accumulation of
periodic acid Schiff (PAS)+ droplets by these cells. The
* Present address: School of Biological Sciences, Zoology AO8,
University of Sydney, Sydney, New South Wales 2006, Australia
PAS + material appears to play a nutritive role in gametogenesis. For the females, the frequencies of six ovarian maturity stages was assessed at approximately monthly intervals.
Small oocytes were present throughout the year and clusters
of early oocytes were most apparent during the spent and
recovery stages. With the onset of vitellogenesis and subsequent accumulation of ova, the nutritive phagocytes and
their PAS + droplets became depleted. The ovarian condition at the onset of breeding was variable, due to differences
in the number of vitellogenic oocytes, differences in the
number of ova in storage, and differences in the amount of
PAS + material. In general, the nutritive phagocyte tissue is
reduced by the onset of spawning and is exhausted by the
termination of breeding. A similar series of events occurs
during spermatogenesis. The relevance of this study for the
use of P. lividus as a brood-stock organism for mariculture
is discussed.
Introduction
The sea urchin Paracentrotus lividus (Lamarck) has a boreomediterranean distribution (Mortensen 1943, Southward
and Crisp 1954) inhabiting intertidal rock pools and shallow
subtidal habitats. In Europe, P. lividus has been an important source of gametes for embryological research since the
turn of the century (Czihak 1971) and it is also of commercial importance, with a high market demand for its roe,
particularly in France. Destructive harvesting methods employed in France caused the collapse of the P. lividus fishery
in the 1970's with a complete disappearance of urchins from
areas of former abundance (Allain 1975, Southward and
Southward 1975, R~gis et al. 1986). An Irish fishery for
P. lividus supplied the French market until recent times, but
now, after 20 yr intensive fishing, this fishery has largely
ceased due to the depletion of commercial stocks (own personal observation). The depletion of wild stocks of P. lividus
and the lucrative market for this urchin have generated
276
interest in the potential of P. lividus for mariculture (R6gis
1980, Birais and Le Gall 1986).
There are several studies on the pattern of gonadal
growth of Paracentrotus lividus. An annual cycle of gonadal
growth is documented for Mediterranean populations of
P. lividus, with two spawning periods each year (Fenaux
1968, R6gis 1979). A single and prolonged spawning period
is reported for P. lividus in Brittany (Dominique 1973). In
Ireland, both single and double spawning periods are reported for the species (Crapp and Willis 1975, Willis 1976).
Despite the economic importance of P. lividus, there is a
paucity of information on the cellular events of gonadal
development in this echinoid.
The aims of this investigation were to determine the
annual cycle of gonadal growth of Paracentrotus lividus
from contrasting habitats on the west coast of Ireland and
to document gametogenesis through histological examination of the gonads. Particular attention was paid to the
development of nutritive, non-gametogenic tissue of the gonads which is the major component of the gonads during the
fishing season. Three breeding seasons were studied to establish the regularity and amplitude of gonadal growth between years and between populations. The influence of environmental seasonality on reproduction of P. lividus was also
examined. This study is intended to constitute a guide to the
use of P. lividus as a brood-stock organism for mariculture.
Reproduction of Paracentrotus lividus (Lamarck) was examined from May 1986 through August 1988 at two sites on the
west coast of Ireland. At Ballynahown (93 I'W; 5313.4'N),
urchins were collected from two adjacent mid-shore tide
pools. At the second site near Glinsk Pier (950.7'W;
5322.4'N), urchins were collected from depths of 3 to 5 m
with the aid of SCUBA. The two study areas are separated
by 30 km and represent contrasting habitats. Ballynahown
is an exposed rocky shore and the tide goes out beyond the
urchin pools most days of the year. The pools were devoid
of macroalgae and had a pink colour due to a crust of
coralline algae lining the substratum. At this site, the urchins
fed on drift sea weed and covered themselves with ensnared
pieces of Fucus and Laminaria spp. In contrast, Glinsk lies
in a sheltered part of Bertraghbouy Bay and the urchins
were only exposed during the lowest spring tides, two to
three weeks a year. At this site the urchins were located in
a kelp bed under and around Laminaria-covered boulders.
Thirty Paracentrotus lividus were collected from each site
at 4 to 6 wk intervals from May 1986 through December
1987 and from February 1988 through August 1988. Their
reproductive cycle was monitored by the gonad index method and by histological examination of the ovaries. Sex determinations were made on freshly dissected specimens by examining the gonads for extruded gametes. From each
urchin, four gonads were dried and the fifth was preserved
in Bouin's fluid. The viscera and test were also dried. After
drying to constant weight, the gonads and the body were
Results
277
Temperature (C):
before
after initial
spawning spawning
before
after initial
spawning spawning
11
10 i
9
8
121
<
.....
BALLYNAHOWN
GLINSK
,di
6
5
4
3
Ballynahown
19 June 1986
1 May 1987
16 May 1988
Glinsk
20 June 1986
9 June 1987
1 June 1988
13.0
11.5
12.4
15.0
13.4
16.0
1027
950
955
942
996
1015
a
20
18
13.0
13.4
14.5
15.0
15.5
16.0
1027
996
1001
942
1016
1015
16
,11
14
e
12
10
8
Females
Males
Combined
Ballynahown
22 May 1986
1 May 1987
16 May 1988
7.3 (0.65)
8.8 (0.36)
7.7 (0.42)
7.2 (0.48)
9.3 (0.53)
7.7 (0.50)
7.2 (0.30)
8.3 (0.29)
7.6 (0.31)
Glinsk
20 June 1986
10 May 1987
1 June 1988
10.9 (0.52)
9.0 (0.55)
10.7 (0.75)
11.1 (0.97)
8.6 (0.47)
9.3 (0.51)
11.0 (0.46)
8.5 (0.33)
10.0 (0.45)
6
4
M.'J.'J.'A.'S.'O:N.'D.'J.'F.M.
A:M: J. J. A. S: O . N . D . J . F . M . A . M . J . J . A . S . O .
IOO0
2g
I"
900
800
700
600
500
400
M.' J.' J.' A: S.'O: N.' D.' J.'F.'M.' A:M: J.' J. ' A.' S.' O: N.' D.' J.' F.'M.' A~M.' J.' J.'A.' S.' O.
278
logical condition of the gonads (Fig. 2f, g, 30. For 1987,
histological examination of the ovaries revealed that gamete
release started in June. Spawning in the subtidal was
also episodic over the summer. The minimum GI of the
subtidal urchins ranged from 3.3 to 4.6 and was similar
between years. The maximum GI ranged from 8.6 to 11, and
the peak value obtained for 1987 (8.6) was significantly
lower compared with the peak indices of 1986 and 1988 (11,
p=0.0001, 10, p=0.08, respectively). Comparisons of the
GI of female and male urchins from the subtidal indicated
that the GI maxima of the two sexes did not differ (Table 2).
The dates when spawning was first detected show that
the two populations started gamete release around the same
time in 1986 and 1988, but in 1987 the intertidal urchins
spawned a month earlier than the subtidal conspecifics
(Table 1). In general, gamete release terminated in late August or early September, although some of the subtidal
urchins continued to spawn through September, with the
minimum GI recorded in October, 1986 (Fig. I a).
The maximum GI of the subtidal urchins was significantly higher than that of their subtidal conspecifics in 1986
and 1988 (p = 0.0001, p = 0.002, respectively). This difference
was most apparent in the 1987/1988 period of gonadal
growth (October-March). In 1987 there was no difference in
the maximum GI of the two populations, but the GI of the
subtidal urchins remained significantly higher for the duration of the breeding period (p = 0.002).
280
ent in the oviduct. Partly spawned ovaries are variable in
appearance. Some ovaries (Fig. 2 g) contain oocytes at all
stages of development, as described for Stage III, whereas
other ovaries (Fig. 2 f) contain a large store of ova, as decribed for Stage IV. Thus, at the beginning of the breeding
season, it appears that females with Stage III and Stage IV
ovaries both commence spawning.
Partly spawned ovaries with the Stage III condition
(Fig. 2 g), have a small number of ova at the onset of spawning and primary oocytes replace ova as they are shed; In
these ovaries, vitellogenesis continues during the early part
of the breeding season, with vitellogenic oocytes surrounded
by nutritive phagocytes. There is a progressive decrease in
the PAS + material in the phagocytes as oocyte growth continues. The oocytes mature successively and spawned ova
are replaced as long as there are large primary oocytes remaining in the ovary. By the end of spawning, most of the
fully-grown oocytes have undergone maturation and the
nutritive phagocytes are reduced or absent.
By contrast, ovaries that progress from Stage IV to Stage
V have a large store of ova at the onset of spawning and
there are few or no primary oocytes to replace them as they
are shed (Fig. 2f). In these ovaries, vitellogenesis is mostly
finished and the nutritive phagocytes are reduced or absent.
281
Fig. 3. Paracentrotus lividus. Histology of testes. (a) Stage I: crosssection through ascinus of recovering testis containing relict spermatozoa (R) and nutritive phagocytes (NP) which form an
eosinophilic meshwork. (b) Stage I: primary spermatocytes along
ascinal wall (arrowheads). (c) Stage II: columns of spermatocytes
project centrally (arrowheads) in growing testes, nutritive phagocytes fill ascini. (d) Stage III: premature testis with spermatozoa (S)
282
(I) Recovering
] Premature
(111)
[]
[]
(11)Growing
(IV) Mature
[]
(Vl) Spent
BALLYNAHOWN
100
LU
50
q:::
' M.' J, ' J. ' A,' S.' O.' N.' D.' J.' F.' M.' A.' M.' J. ' J. ' A.' S.' O.' N.' D.' J. ' F.' M.' A." M.' J.
1986
1987
1988
GLINSK
100
LU
=o
50
1111!111!i
A.'
. A.
GI
Temperature (C)
Oct. Mar.
max.
Oct.
Mar.
min.
Gross appearance of dissected urchins
Ballynahown
1986-1987
1987-1988
4.0
3.2
7.1
6.1
8.3
7.6
12.0
13.8
6.8
7.8
5.5
6.0
Glinsk
1986-1987
1987-1988
4.4
5.4
7.6
9.8
8.6
10.0
12.0
10.7
6.6
8.3
5.5
6.0
283
Oocyte size-frequencies
Examination of the oocyte size-frequency distributions reveals that small oocytes were present throughout the year
284
BALLYNAHOWN
2O%
120,
100-
100
80"
80
6O
4O
40
r3
2o
May
1986
Jun
20
July
Aug
Dec
Oct
May
1986
too
E.lO0
~ 60
~ so
JUly/
Jun
Aug
Oct
Sept
Nov
F-
~< 60
o
40
40
~ 29
~ 20
0
0
Jan
1987
Mar
1i
si
May
Jun
July
Apr
Feb
1987
Sept
May
Jun
July
Sept
100
80
60
401
40
20
Mar
1988
May
Jun
Aug
Mar May
1988
Jun
Aug
Fig. 6. Paracentrotus lividus. Oocyte size-frequencydistributions of females from Ballynahown and Glinsk
recorded in August, whereas in 1988 the maximum sea temperature, 17.5 C, was recorded in June. Temperature minima of 5.5 and 6.0 C were recorded in February and December 1987, respectively. It should be noted, however, that
compared with the subtidal urchins, the rock pool urchins at
Ballynahown experienced a fluctuating temperature regime
due to their intertidal location. On several occasions the
rock pools were noted to have a higher temperature than the
sea in the summer and a lower temperature in the winter
(Fig. 1 b).
The GI shows that maximum gonadal growth occurred
between October and March (Table 3). This period coincides with the shorter days of the year (day length _< 12 h;
Fig. 1 c; Table 3). It also coincides with the period of decreasing sea temperatures, and gonadal growth exhibits an
inverse relationship with temperature (Fig. 2 a, b; 7). By the
period of minimum sea temperatures in February 1987, the
gonad indices for Ballynahown and Glinsk were 7.3 and 7.5,
respectively, approximately double the GI minima and close
to the GI maxima for 1987 - 8.3 and 8.6, respectively.
In each year, spawning commenced before the sea-temperature maxima and around the shortest days of the year.
The sea temperatures recorded at GI maxima and after the
onset of spawning are listed in Table 1. Over the three breeding seasons studied, spawning was bracketed on one side by
temperatures of 11.5 to 14.5 C measured before spawning
started, and on the other by temperatures of 13.4 to 16.0 C
measured one month later when spawning was first recorded. If gamete release is influenced by temperature, then tern-
BALLYNAHOWN
11
10
.
~
8<> I
oO
,.
tl
. . . . . . . .
y=-,416X+9.131; R2=.377
4
3
2
1
. . . .
.
8
.
9
Temperature
10
11
.
12
13
14
15
GLINSK
16 .
14 t
'2t
"~clO
y=-.507x+11.148;
R2=.191
J
,
6
t0
11
12
13
14
Temperature C
Discussion
285
demonstrated for Evechinus chloroticus where there is an
inverse relationship between density and gonad size in the
presence of equivalent food (Andrew 1986). For Paracentrotus lividus, high densities resulted in suboptimal growth in
culture, despite the enhanced availability of preferred food
(O'Sullivan 1988). The population densities of P. lividus
were not measured, because the urchin stocks at Glinsk were
harvested by divers during the investigation. For the intertidal and subtidal populations of P. lividus, it appears that
differences in food availability, wave action and density
probably influence the inter-site differences in gonadal
growth and reproduction. The influence of these factors
needs to be examined through a replicate study of several
populations that experience differences in exposure and
food availability.
Aspects of oogenesis differed in the two populations of
Paracentrotus lividus. Most of the subtidal females started to
accumulate ova in March and attained the Stage IV condition with a large store of ova a month prior to spawning.
The intertidal females lagged behind their subtidal conspecifics and, during the early portion of the breeding period, were characterized by continuous vitellogenesis and
oocyte maturation. This difference in the histological state
of the ovaries suggests that the subtidal urchins may have
accumulated a comparatively higher store of reserves during
the recovery and growth stages which promoted vitellogenesis of a large number of oocytes. Once initiated, vitellogenesis of P. lividus may be completed within a month, as reported for Strongylocentrotus purpuratus (Gonor 1973 a).
The within-sample difference in the state of gonadal maturity of Paracentrotus lividus is largely due to an intrapopulation variability in the development of the nutritive,
nongametogenic tissue. This variability was evident at the
onset of the ovarian cycle when some females had ovaries
that appeared empty, while others had ovaries containing a
well-developed layer of nutritive tissue and relict oocytes.
Relict oocytes appear to be recycled by the nutritive phagocytes and serve as a source of nutrients for the next vitellogenic cycle (Walker 1982). The variability in the amount of
reserves present in the ovaries in Stages VI and I and in the
amount of PAS + material accumulated during the growth
stage, undoubtedly influences the gonadal condition at the
onset of breeding. A within-population variability in the
gonadal condition is also reported for other populations of
P. lividus (Allain 1975, Crapp and Willis 1975) and for several echinoid species (Fuji 1960b, Pearse 1969, Chiu 1988).
As noted for other echinoids (Giese and Pearse 1974),
the gonad index method in conjunction with histology provided a good estimate of the reproductive cycle of Paraeentrotus lividus. The ovarian maturity method utilizes convenient, morphological criteria to assess gonadal development
and revealed the within-sample variability in gonadal condition. Ovarian development of P. lividus is an integrated sequence of events and many females had ovaries in a transitional state, particularly before and during breeding when
vitellogenesis, oocyte maturation and spawning are events
along a continuum. Post-spawning growth in P. lividus gonads occurs rapidly, as it does in Strongylocentrotusfrancis-
286
canus (Bernard 1977), but not as reported for other echinoids where a quiescent period of minimal gonadal growth
follows spawning (Fuji 1960b, Gonor 1973a).
The accumulation and storage of eosinophilic-PAS +
droplets by the nutritive phagocytes before and during
gametogenesis, the depletion of these droplets with oocyte
growth, and the phagocytosis of unspawned oocytes, are
characteristic features of echinoid reproduction (Walker
1982, Pearse and Cameron in press). Several immunocytochemical and ultrastructural studies show evidence that the
PAS + material plays a nutritive role in gametogenesis
(Walker 1982). Since the oocytes of several echinoids are
PAS + , it is inferred that the PAS + material stored by the
nutritive phagocytes is taken up by vitellogenic oocytes
(Holland 1967, Chatlynne 1969, Tyler and Gage 1984).
Moreover, recent biochemical investigations demonstrate
that vitellogenin is present in the nutritive phagocytes, where
in the females it provides a source of yolk precursors for
oogenesis (Ozaki et al. 1986, Shyu et al. 1986) and in the
males it appears to support spermatogenesis (R. Raft personal communication). Although it is likely that the PAS +
material in the nutritive tissue is also taken up by Paracentrotus lividus oocytes, the vitellogenic oocytes and ova did
not exhibit a PAS + tinctoral response.
The oocyte size-frequency data demonstrated that small,
previtellogenic oocytes were present throughout the year in
Paracentrotus lividus ovaries and that they were the most
abundant oocytes, even in mature ovaries, as reported for
Stylocidaris affinis (Holland 1967). This contrasts with the
oocyte size-frequency data of Strongylocentrotus purpuratus,
where mature ovaries contain a dominant class of large
oocytes (Gonor 1973b).
There are several reports of hermaphroditic individuals
in populations of normally dioecious echinoids (Boolootian
and Moore 1956, Lawrence 1987, Pearse and Cameron in
press) and, as noted for Paracentrotus lividus (Drzewina and
Bohn 1924), the incidence of hermaphroditism was low.
Most reports of hermaphroditic urchins note the presence of
ovaries and testes in the same animal (Boolootian and
Moore 1956). By contrast, the hermaphroditic P. lividus described here possessed ovotestes and, as for hermaphroditic
Strongylocentrotus purpuratus, the gonads were predominantly female (Gonor 1973 c). As noted by Gonor (1973 c),
ovotestes can be detected only through histological examination of the mosaic portion of the gonad, and may be a
more common expression of hermaphroditism in echinoids
than previously thought.
The seasonality of gametogenesis in several echinoid species raises questions about the role that seasonal environmental events play in controlling reproduction (Pearse 1981,
Pearse and Cameron in press). For Paracentrotus lividus, the
maximal period of gonadal growth coincides with decreasing sea temperatures and a day length of less than 12 h. This
suggests that temperature and photoperiod may both influence gonadal development. A relationship between decreasing temperature and gonadal growth has been noted for
Mediterranean populations of P. lividus and for Strongylocentrotus droebachiensis (R6gis 1979, Himmelman 1975). By
287
and growing stages of gonadal growth, when nutritive material is being elaborated and stored. During this period, the
gonads are filled with nutritive phagocytes and there are few
or no ripe gametes in the gonads. The urchin harvest declines in April and terminates in May, coinciding with the
period when the nutritive tissue is being converted into
gametes. Gonads at an advanced stage of sexual maturity
are not acceptable due to their soft texture.
The depletion of commercial stocks of Paracentrotus
lividus in European waters and the continued demand for
urchin roe has stimulated interest in the potential of this
urchin for mariculture (R6gis 1980, Birais and Le Gall
1986). It is clear from this investigation that the large subtidal urchins would be a superior source of gametes for
brood-stock purposes, compared with their intertidal conspecifics. The subtidal females possessed a larger store of
ova, and mature gametes were available in the subtidal population for at least five months of the year. By contrast, the
rock pool urchins were seldom fully mature at their GI
maximum and their ovaries contained an abundance of immature late vitellogenic oocytes. It is unfortunate that the
populations of P. lividus which appear to be the best source
of brood stock for mariculture have been depleted. The
temporal variability in the breeding period of P. lividus and
the possibility that sea temperature serves as an exogenous
cue for the induction of spawning have relevance for the use
of this urchin for brood stock. For the mariculturist, both
sea temperature and gonadal condition should be monitored
closely to assess the availability of mature gametes, particularly at the approach of the breeding season.
Acknowledgements. This work was supported by a postdoctoral
fellowship from the Department of Education, Dublin. I thank
Professor P. O. C6idigh and Dr. B. F. Keegan for support and use
of facilities. Thanks to Dr. D. McGrath for introducing me so
promptly to Ballynahown. The suggestions of Dr. V. Morris and
Dr. N. Andrew improved the manuscript. Thanks to Mr. A. Lawless, Mr. J. Galvin and Ms. E. Moylan for technical assistance and
to Mr. D. Burke, skipper of the R. V. "Ona 3". Mr. M. Ricketts and
Mrs. J. Jeffrey also provided technicaI assistance. The Dunsink
Observatory, Dublin, provided day-length information. This paper
is Contribution No. 316 from the University College Galway School
of Marine Sciences.
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Date of final manuscript acceptance: November 3, 1989.
Communicated by G. F. Humphrey, Sydney