Journal of Shellfish Research, Vol. 21, No. 2, 627–634, 2002.

REPRODUCTIVE CYCLE OF THE BIVALVE CLAMS SEMELE SOLIDA (GRAY, 1828)

(SEMELIDAE) AND GARI SOLIDA (GRAY, 1828) (PSAMMOBIIDAE) FROM CHILE

DONALD BROWN,1* BERNARDITA CAMPOS,2 AND H.-JÖRG URBAN3

1
Departamento de Biología, Instituto de Ciencias Biológicas y Químicas, Facultad de Ciencias,
Universidad de Valparaíso, casilla 5030, Valparaíso, Chile; 2Facultad de Ciencias del Mar,
Universidad de Valparaíso, casilla 13-D, Viña del Mar, Chile; 3Alfred-Wegener-Institute for Polar
and Marine Research, Section of Comparative Ecosystem Research, Columbusstr. 27568 Bremerhaven,
Germany

ABSTRACT Commercial clam landings reached an average of almost 91,000 tons annually in Chile over the last decade. In spite of
the high value of this resource, few efforts have been made to understand the basic biology of the exploited species, data that might
in the future be needed to aid in their protection or even artificial culture. This study is a contribution to the knowledge of the
reproductive cycles of two valuable species, Semele solida (Gray) and Gari solida (Gray). Representative samples of these species were
collected at two widely separated localities in Chile and examined histologically to determine their seasonal reproductive cycles. It was
found that the species were of separate sexes, and had annual gonadal cycles. In S. solida from northern Chile, the reproductive period
extended from June 1991 to February 1992. In G. solida from southern-central Chile, the reproductive period was relatively short, from
October 1991 to February 1992. In both species, most specimens have empty gonads by March. The data obtained are useful in
developing management plans related to their reproductive periods. Relevant to culture strategies, S. solida has the comparative
advantage of a lengthy reproductive period, wherein mature individuals may be frequently encountered in nature for spawning
inductions. G. solida, with its shorter annual reproductive cycle may have the advantage of being induced to mature in artificial
conditioning systems over relatively short periods of time.

KEY WORDS: clam reproduction, reproductive cycle, bivalves, Semele solida, Gari solida, Chile

INTRODUCTION
Chilean coastal waters host very productive and diverse clam
fisheries due to the rich coastal upwelling and favorable water
temperatures. The largest clam populations occur in the protected
bays and fjords of southern Chile. Over a number of years official
fisheries records in Chile (SERNAPESCA 1990–1999) considered
all clam species as one generic group (“clams”) among which were
included the venerids Protothaca thaca (Molina), Venus antiqua
(King and Broderip), Eurhomalea exalbida (Chemnitz), E. lenticu-
laris (Sowerby), E. rufa (Lamarck), and the mactrid Mulinia edu-
lis. Semele solida (Gray) and Gari solida (Gray) belonging to the
Semelidae and the Psammobiidae respectively, and objects of this
study are also included in this group. They are primarily exploited
in artisanal fisheries, and commercialized mostly in canned form.
G. solida is highly valued from the culinary standpoint. In 1994,
the first year of its listing as an individual species, 4613 tons of S.
solida were harvested, declining to 2071 tons by 1999; G. solida,
recorded separately beginning in 1990, was registered at 31,373
tons, which declined to 9931 tons by 1999 (SERNAPESCA 1990–
1999). The only regulation for the fishery of these clams is a
minimum size limit of 55 mm for S. solida and 60 mm for G.
solida (Subsecretaría de Pesca 1996).
Despite their great economic value, not much research has been
done on reproduction in Chilean clams, particularly in S. solida
and G. solida. One recent report (Jeréz et al. 1999) suggested that
G. solida in southern Chile had a continuous reproductive cycle
throughout the year, a pattern apparently common among the heav-
ily commercialized clams such as V. antiqua (Lozada & Bustos
1984) and P. thaca (Henríquez et al. 1981). This also was true for
E. lenticularis (Campos & Brown 1997, Campos et al. 1999) and
M. edulis (Jaramillo et al. 1998).
* Corresponding author. E-mail: donald.brown@uv.cl
Semele solida (Fig. 1A), locally termed “tumbao”, occurs par-
tially buried in sand and gravel bottoms from the intertidal (Osorio
et al. 1979) to the subtidal zone (Urban 1994). Its geographic
distribution ranges from 12°S to 47°S. (Viviani 1979). Gari solida
(Fig. 1B), locally termed “culengue”, occurs completely buried in
bottom sands and gravels, usually at greater depths than S. solida
from the intertidal to 15-m depth (Urban 1994). Its range of dis-
tribution along the Pacific Coast, as given by Viviani (1979) and
later by Guzmán et al. (1998), was between 12°S and 47°S.
Biologic data for species of economic importance is fundamen-
tal for proposing regulatory recommendations for sustainable har-
vest of these resources over time. The obvious declines in harvest
over the years enhances the need for more information on the
reproduction and survival of these species to support efforts di-
rected towards their artificial culture, repopulation, or management
as a renewable resource in over-exploited beds.
In this study, we describe the reproductive cycles of G. solida
and S. solida by means of histologic observations of gametogen-
esis during different seasons of the year. Patterns in reproductive
cycles, including gametogenesis and resting gonadal periods were
studied in a population of S. solida from northern Chile and in a G.
solida population from central-southern Chile, representing the
first study of this nature for these two clam species in their re-
spective regions.
MATERIALS AND METHODS
Adults of each species were obtained by diving at monthly
intervals from June 1991 to July 1992. S. solida was collected in
La Herradura Bay (29°58⬘S) and G. solida from Coliumo Bay
(36°32⬘S) (Fig. 2). Maximum anterior-posterior length of the shell
was measured on each specimen, to the nearest 0.1 mm. Matura-
tional status of the gonad was determined monthly on around 30
animals of each species. Tissue samples 5 mm in thick-

627
628 BROWN
Figure 1. Species under study. A: Semele solida, 78 mm total length
(maximum anterior-posterior shell dimension); B: Gari solida, 89 mm
total length.
ness were obtained and fixed 24 h in Bouin’s fluid and prepared by
routine histologic procedures as follows: dehydration with graded
series of ethanol, clearing in xylol and embedding in Paraplast.
Five micrometers histologic sections obtained from three levels of
each gonad separated 500 ␮m, were stained with hematoxylin and
yellowish eosin, dehydrated in graded series of ethanol, cleared in
xylol and permanently mounted with Canadian balsam (Gabe
1968).
The gametogenic cycles of the two clams were followed by
describing the histologic appearance of the gonadal sections and
classifying them into different stages of maturity using a modifi-
cation of the scale proposed by Lucas (1965). Each individual was
assigned to one of the following stages based on the degree of
morphologic development of its germ cells: (d1) ⳱ initial devel-
opment or maturation; (d2) ⳱ advanced development or matura-
tion; (d3) ⳱ complete development or maturation; (r1) ⳱ initial
regression or evacuation; and (r2) ⳱ total regression or evacua-
tion. The results were expressed as percentage frequency histo-
grams of: (1) males in each gonadal stage; (2) females in each
gonadal stage; and (3) males plus females in each stage, separately
for S. solida and G. solida during the sampling period from June
1991 through July 1992.
ET AL.
Figure 2. Location of collection sites for A: S. solida and B: G. Solida
on the Chilean coast.
RESULTS
Semele solida specimens measured from 38.9 to 86.0 mm and
Gari solida from 41.4 to 88.0 mm. The two clam species were of
separate sexes, with no hermaphroditism and no sexual dimor-
phism evident. Histologic analysis of the gonad in both species
showed a multilobulate organization of the acini connected to
evacuation tubes covered by simple ciliated epithelium similar to
that observed in other bivalves (Sastry1979). The acini consisted
of a basal lamina of variable thickness depending on the stage of
gonadal maturity. Its relative thickness was greatest in specimens
initiating gametogenesis, and in those that had spawned. In these
specimens an intra-acinar reticulum consisting of vesicular so-
matic cells and an intra-acinar space containing groups of ame-
bocytes may be found (Figs. 3A and 4F).
The cells of the male germinal line that characterize spermato-
genesis may be restricted to two zones of the gonadal acinus: (1)
a basal region representing the early germinal line that includes
spermatogonia and spermatocytes that form a band of circular
voluminous nuclei, and recently formed round spermatids that also
form a band of small circular nuclei (Figs. 3A, 3B and 4A, 4B),
that is evident in G. solida; and (2) a lumen region, representing an
advanced germinal line with spermatids undergoing cytodifferen-
tiation with heavy stained elongated nuclei, gathered by their heads
in double columns, giving a “feathered” appearance (Figs. 3B, 3C
and 4B, 4C).
 REPRODUCTIVE CYCLE OF CHILEAN CLAMS 629

Figure 3. A–E: Light photomicrographs of different histological stages of male and F–J: female gonadal acini of S. solida collected in La
Herradura Bay from June 1991 to July 1992. A–E bar = 100 µm; F–J bar = 200 µm; A and F = initial development of maturation (d1); B and
G = advanced development of maturation (d2); C and H = total development or maturation (d3); D and I = initial regression or evacuation (r1);
E and J = total regression or evacuation (r2).
630 BROWN ET AL.

Figure 4. A–E: Light photomicrographs of different histological stages of male and F–J: female gonadal acini of G. solida collected in Coliumo
Bay from June 1991 to July 1992. A–E bar = 100 µm; F–J bar = 200 µm; A and F = initial development or maturation (d1); B and G = advanced
development or maturation (d2); C and H = total development or maturation (d3); D and I = initial regression or evacuation (r1); E and J =
total regression or evacuation (r2).
 REPRODUCTIVE CYCLE
The cells of the female germinal line in the basal region are
represented by oogonia, previtellogenic and adhered vitellogenic
oocytes. In the lumen region they are represented by pedunculate
vitellogenic oocytes as well as free oocytes (Figs. 3G, 3H, and 4G,
4H). The histologic stages of the gonads of S. solida and G. solida
females are shown in Figures 3F–3J and 4F–4J, respectively.
The three sampled areas of the gonad from both species all
showed the same degree of gametogenic activity or development
of the germinal line, indicating synchronic maturation throughout
the gonad.
Semele solida
The distribution of percentage frequencies of the different his-
tologic stages in male gonads, female gonads, and in the popula-
tion as a whole for S. solida are given in Figures 5A, 5B and 5C,
respectively. This species presented a seasonal pattern of gonadal
development in both sexes. Males and females with developed or
mature gonads (d3 stage) as well as in initial regression (r1) (Figs.
3D and 3I) were predominant from June 1991 to February 1992. In
contrast, from March to June 1992, there was a greater frequency
of individuals in total regression (r2) (Figs. 3E and 3J). Although
in both sexes the frequency of samples with gonads in initial stages
of development (d1) (Figs. 3A and 3F) was observed between
April and July 1992, the number of females in this stage was
greater, and predominated over those in total regression (Fig. 5A
vs. Figure 5B). However, during the first period, there was a small
percentage of males in total regression (r2) and in initial develop-
ment (d1) (Fig. 5A), which was a condition more apparent in
females (r2-d1; Figure 5B). Some observations not included in the
figures suggested that individuals technically considered to be in
regression could show a new wave of initial maturation beginning
at the germinal line in the gonadal acini.
The second period was characterized by the total regression
stage (r2), where all individuals had gonads with depleted acini in
March 1992 (Figs. 5A, 5B). The percentage frequency distribution
of the different gonadal stages for the population sample (Fig. 5C)
shows this tendency in both males and females.
It is of interest to point out the difference in gonadal conditions
between specimens sampled in June to July 1991 compared with
those from the same period in 1992. In 1991 a high frequency of
both sexes contained elevated numbers of specimens with gonads
in advanced and total development (d2–d3), whereas in 1992 this
condition was different, with specimens containing gonadal acini
in total regression (r2) or without advanced germinal line (Fig. 5).
Gari solida
In this species the distribution of percentage frequencies of the
different histologic stages in males, females, and the entire popu-
lation are given in Figures 6A, 6B, and 6C, respectively. There is
a periodicity in both sexes with the same general tendency.
There is a well-marked period in which advanced and totally
developed gonads (d2-d3) are observed, as well as those in initial
regression (r1) (Figs. 4D and 4I) from October 1991 to February
1992. In females this period is much shorter (November 1991 to
January 1992). This condition persisted in some males until April
1992. Some observations not included in the figures showed indi-
viduals in regression during this period, which had a new wave of
initial maturation beginning at the germinal line, as observed in S.
solida (see earlier). In a second, more extensive period, the gonads
were characterized by the occurrence of total regression and initial
OF CHILEAN CLAMS 631
development (r2–d1) (Figs. 4E and 4A, respectively) in males
from June to September 1991, and from March to July 1992 (Fig.
6A). In females the r2–d1 period (Figs. 4J and 4F, respectively)
extended notably until October 1991, and from February to March
1992 (Fig. 6B).
Figure 6C shows the general frequency of the gonadal stages
for the general population, with a similar pattern to that presented
separately for males and females. From June to August 1991,
February 1991, and April to July 1992 the number of specimens in
each population sample exceeded the males and females together
because included were specimens whose total regression stage was
such that there were no cells on the germinal line differentiated
enough to permit sex determination. In comparing the gonadal
stages of specimens obtained in June to July 1991 with those of the
same period in 1992, stages were observed that were near total
regression and initial development showing an inverse fluctuation
where regression predominated in 1991 and initial development in
1992.
Finally, it was apparent in both species that the stages of ad-
vanced or total maturity were observed in water having higher
relative temperature, whereas initial stages of development were
related to water of relatively low temperature, although our tem-
perature measurements were not extensive (Figs. 5C and 6C).
DISCUSSION
The reproductive cycle is characterized by a series of events
that in annual species comprises a reproductive period involving
the gametogenic and spawning phases and a resting period in
which there is not gametogenic activity.
Present results have shown similar values between the annual
reproductive cycles of S. solida and G. solida, where both showed
seasonal gametogenesis and spawning, followed by a resting pe-
riod without production of gametes.
The reproductive period of S. solida, from June 1991 to Feb-
ruary 1992 was longer than that of G. solida. Most of the speci-
mens showed gametogenic activity and signs of having spawned.
The majority of spawning occurred in February, and in March all
specimens had empty gonads. This point marked the initiation of
the resting period, indicated by a completely regressive condition
in the gonad, which was more marked in G. solida than in S.
solida.
We are cautious to consider the possibility of a second spawn-
ing phase during the reproductive period of S. solida because of the
low number of animals (4) sampled and examined in October,
notwithstanding that all of them were in advanced development
(D2).
In G. solida the reproductive period was relatively short, from
October 1991 to February 1992; the spawning phase mostly occurs
in February. A majority of the specimens had empty gonads in
March 1992; then the spawning phase mostly occurs in February.
The presence of specimens with gonads in the initial state of de-
velopment in this period may indicate possible activity in gonial
multiplication and generation of cytes without gametogenic activ-
ity that leads to massive production of differentiated gametes. The
results showed that low temperatures favored the proliferative ac-
tivity of the early germinal line, while high temperatures aided
cytodifferentiation of the advanced germinal line. This condition
was most notable in the reproductive cycle of G. solida from
Coliumo Bay, a more southerly location. These events occurred
632 BROWN ET AL.

Figure 5. Distribution of different gonadal stages in A. males; B. females; and C. males + females of S. solida colleced in La Herradura Bay from
June 1991 to July 1992, with sea surface temperature added. The length of each area represents the percentage frequency of specimens in each
histologic stage of the gonadal acini. N = number of specimens examined.

simultaneously in both males and females showing (expected) syn- from the majority of the specimens, a phenomenon more pro-
chrony of the reproductive cycles. nounced in S. solida. There was a predominance of advanced
Every monthly sampling during the reproductive period stages of gonadal maturity, and also those with complete regres-
showed a few individuals having gonadal conditions differing sion as an evidence that spawning had occurred. These observa-
 REPRODUCTIVE CYCLE OF CHILEAN CLAMS 633

Figure 6. Distribution of different gonadal stages in A. males; B. Females and C. males + females of G. solida collected in Coliumo Bay from
June 1991 to July 1992, with sea surface temperature added. The length of each area represents the percentage frequency of specimens in each
histological stage of the gonadal acini. N = number of specimens examined.

tions suggest intrapopulation asynchrony of gametogenic activity, firmed this asynchrony and strengthened the hypothesis of con-
with partial evacuations of gametes over a longer period. The fact tinuous gametogenesis with various cycles of gametogenic activity
that the specimens showing signs of having spawned showed a and spawning by each individual during the reproductive period.
new wave of maturation in the germinal layer of their acini, con- A difference was observed in the degree of maturity of the
634 BROWN
population samples of S. solida between June and July 1991 where
advanced and complete maturity were well represented; in the
same period of 1992, on the contrary, maturity was just beginning.
This difference may be explained by normal adaptation to envi-
ronmental conditions such as temperature and food availability,
which may vary within a limited range from year to year.
Although Urban and Campos (1994) suggested that the repro-
ductive cycles of S. solida and G. solida were influenced by tem-
perature, Jeréz et al. (1999) working on a G. solida population
from the south of Chile found the annual reproductive cycle to be
continuous without a marked resting period. Further studies are
required to evaluate seasonal variations in gonadal cycles of these
species with latitude, as they are distributed over a broad latitudi-
nal range from Callao, Peru (12°S) to Chile’s Chonos Archipelago
(44°S). The hypothesis here is that the reproductive cycles of these
clams become shorter in populations the farther south they occur
on their distributional gradient. Some data available on other clam
species with extensive distributions support this hypothesis. Popu-
lations of Protothaca thaca (Henríquez et al. 1981), Tagelus
dombeii (Acuña et al. 1994) and Eurhomalea lenticularis (Campos
& Brown 1997) from central and north-central Chile exhibit con-
tinuous gonadal activity with various important spawning peaks
throughout the year. Nevertheless, T. dombeii from south-central
Chile showed a period of gonadal regression in the fall (Jaramillo
et al. 1998). This phenomenon is not clear across other clam spe-
cies inhabiting the south-central zone of Chile, such as Venus
antiqua, Tawera gayi, Mulinia edulis and Ensis macha that show
continuous reproductive cycles without resting periods (Lozada &
Bustos 1984, Jeréz et al. 1999).
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Acuña, E., Ch. Guisado & M. Berríos. 1994. Ciclo reproductivo de Tagelus
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Campos, B. & D. Brown. 1997. Aspectos reproductivos de la almeja Eu-
rhomalea lenticularis (Sowerby) proveniente de la rada El Algarrobo
(V Región). Informe Final Proyecto DIPUV 20–95, Universidad de
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ET AL.
From the practical point of view, regulation of harvesting these
clams should be based on considerations of their reproduc-
tive cycles by limiting their harvest during the major spawning
season. Consideration of the reproductive cycles is also important
in obtaining broodstock for aquaculture. Experimental studies
should prove this a feasible alternative for production or protect-
ion of the resource. In studying resource management of these
clams, S. solida shows a comparative advantage in having a
more extensive reproductive period, as mature individuals may be
encountered over an extended period. This implies that mature
broodstock would be available in nature for artificially induced
spawning (e.g., in aquaculture experimentation) over compara-
tively long periods. Although G. solida, in contrast, has a more
restricted reproductive period, it may be a species amenable to
artificial conditioning in aquaculture systems, given that its gonads
almost always contain high numbers of immature gametogenic
cells.
ACKNOWLEDGMENTS
The authors thank Ms. T. Jerí for sampling G. solida at
Coliumo Bay, and Ms. G. Bellolio (U. Católica del Norte at the
time) for providing S. solida from Herradura Bay. We also thank
Dr. R. Guerra for her supervision of the histologic processing at
the U. de Valparaíso, and Mr. C. Olivares for assistance in histo-
logic analyses. Corrections and comments by anonymous review-
ers helped to improve the manuscript. The work was financed by
FONDECYT Grant 91-502 to B. Campos.
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