Prospective Culture of the Cortez Oyster Crassostrea corteziensis from

Northwestern Mexico: Growth, Gametogenic Activity, and Condition Index

Author(s): Jorge Chávez-Villalba, Andrés Hernández-Ibarra, María R. López-Tapia, and José M. Mazón-
Suástegui
Source: Journal of Shellfish Research, 27(4):711-720.
Published By: National Shellfisheries Association
DOI: http://dx.doi.org/10.2983/0730-8000(2008)27[711:PCOTCO]2.0.CO;2
URL: http://www.bioone.org/doi/full/10.2983/0730-8000%282008%2927%5B711%3APCOTCO
%5D2.0.CO%3B2

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and
environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published
by nonprofit societies, associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of
BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries
or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research
libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Shellfish Research, Vol. 27, No. 4, 711–720, 2008.

PROSPECTIVE CULTURE OF THE CORTEZ OYSTER CRASSOSTREA CORTEZIENSIS

FROM NORTHWESTERN MEXICO: GROWTH, GAMETOGENIC ACTIVITY,
AND CONDITION INDEX

JORGE CHÁVEZ-VILLALBA,1* ANDRÉS HERNÁNDEZ-IBARRA,1 MARÍA R. LÓPEZ-TAPIA1

AND JOSÉ M. MAZÓN-SUÁSTEGUI2
1
Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Unidad Sonora, Apdo. Postal 349,
Guaymas, Sonora 85454, Mexico; 2Centro de Investigaciones Biológicas del Noroeste (CIBNOR),
Mar Bermejo 195, Col. Playa de Santa Rita, La Paz, BCS 23090, Mexico

ABSTRACT This study examined growth, gametogenic activity, condition index, as well as the relationship of the life cycle to
environmental parameters of the Cortez oyster Crassostrea corteziensis, which was cultured for 25 mo in the lagoon of Las
Guásimas (Sonora, Mexico). We used oocyte diameter and cytological characteristics of the gonad to determine reproductive
stages in females and males. The condition index was used to describe the oyster’s physiological health. Temperature, salinity,
seston, and chlorophyll a, b, and c were recorded at the study site. The Cortez oyster had isometric shell growth, reaching 103.2 ±
1.82 mm height and 150.3 ± 4.98 g total weight. Data were adjusted to the von Bertalanffy growth equation (LN ¼ 132.2 mm and
K ¼ 1.08 y–1), and survival was about 70%. This native species exhibited a distinctive gametogenic cycle, with the beginning and
end of the cycle controlled by seawater temperature fluctuation (15–33°C), which once started, is continuous over a 9-mo period
(March to November). Elevated temperature (>25°C) produced high gametogenic activity, exhibiting primary, growing, and
mature oocytes, and partial spawning in April, September, and November. The peak spawning event occurred in August, when
seawater reached peak temperatures of 31°C to 33°C, which was followed by a significant reduction of the condition index. During
winter, storage of nutrients took place, and this appears to be used in the following season for gametogenesis. In general, the
condition index was high throughout the study period. Energy for growth and reproduction came from phytoplankton blooms in
summer and high concentration throughout the year of nonchlorophyll particulate organic matter. Observations show that this
oyster is a protandrous species. High survival, elevated yields, and a long, continuous gametogenic cycle indicate that
C. corteziensis has importance in aquaculture in Gulf of California.

KEY WORDS: Crassostrea corteziensis, oyster, growth, gametogenesis, oocyte size, condition index, von Bertalanffy

INTRODUCTION natural beds and near-disappearance of the species in north-

western Mexico. Most of the studies of this species have focused
Currently, bivalve aquaculture in northwestern Mexico is
on describing occurrence and seasonal variation of trace and
based on the cultivation of the introduced Pacific oyster
heavy metals and biochemical composition of oysters (Osuna-
Crassostrea gigas, with production of 2,900 tons in 2003
López et al. 1990, Páez-Osuna et al. 1993, Osuna-López et al.
(SAGARPA 2003). However, serious loses have been reported
1999, Rivero-Rodrı́guez et al. 2007). Given the problems
by producers at the culture sites in 1997. Massive die-offs have
occurring with the introduced species, C. gigas, there is
been recorded each year in several areas and time intervals,
increasing interest in the commercial potential of farming the
affecting spat, juveniles, and adults. Producers demand solu-
native species.
tions to this widespread problem or alternatives that use other
Natural spat collection of C. corteziensis is not possible;
bivalves. However, there is limited information on the causes of
therefore, hatchery production is the only feasible approach for
massive die-offs in this area and no measures or remedies have
supplying juveniles. Our center (CIBNOR) produces spat of the
emerged to reduce this serious loss. Concerning other bivalve
Cortez oyster under controlled conditions (Mazón-Suástegui
species, there is limited ecological and biological information,
et al. 2002). More recently, juvenile oysters were raised in an
but previous studies of the native oyster Crassostrea corteziensis
experimental culture area in the State of Sonora, using plastic
(Hertlein 1951) suggested that cultivation of this species in the
containers suspended from long-lines (Chávez-Villalba et al.
coastal lagoons had potential (Sevilla 1959, Stuardo et al. 1973,
2005). In this study, we report data of growth rates and survival
Stuardo & Martı́nez 1975). The native species may represent
of the Cortez oyster. However, information about the gameto-
an alternative to balance the losses of C. gigas farms, but more
genic cycle of the species is still limited. Whereas contributions
studies on the biology of C. corteziensis are essential for
to the study of reproduction have been made (Cuevas-Guévara
implementing aquaculture activities.
& Martı́nez-Guerrero 1979, Ruı́z-Durá 1980, Frı́as-Espericueta
Crassostrea corteziensis is distributed from the Gulf of
et al. 1997) to determine the aquaculture potential of C.
California to Peru (Fisher et al. 1995) and is usually associated
corteziensis, it is necessary to have a more complete under-
with the roots of red mangrove (Rhizophora mangle) (Páez-Osuna
standing of its reproductive biology and life history. Sustainable
et al. 1993). Extraction of the Cortez oyster peaked in 1970 on
aquaculture relies on the timing of gametogenic development
the Pacific coast of Mexico (Cuevas-Guévara & Martı́nez-
and spawning events so potential broodstock can be collected
Guerrero 1979). However, intensive exploitation and reduction
at the appropriate time (Aragón-Noriega et al. 2007). We need
of freshwater into lagoons resulted in severe reduction of
detailed knowledge of the reproduction process, condition
*Corresponding author. E-mail: jechavez04@cibnor.mx indices, growth rates, and basic environmental conditions.

711
712 CHÁVEZ-VILLALBA ET AL.
For instance, there are no reports concerning the variations of
the condition index through an annual cycle, with the exception
of a gonad index determined by Frı́as-Espericueta et al. (1999).
This study was designed to determine the aquaculture
potential of Crassostrea corteziensis in a coastal lagoon of
Sonora, Mexico by documenting growth and survival of the
Cortez oysters in a suspension system, measure gametogenic
activity and variations in its condition index, and determine how
environmental parameters affect growth and reproduction of
this oyster.
MATERIALS AND METHODS
Spat Production
A batch of 200 adult oysters (80–100 mm) was collected in
Bahı́a Ceuta, Sinaloa. The specimens were placed in thermal-
insulated containers and transported by airplane to facilities at
CIBNOR in La Paz, B.C.S. Broodstock management, spawn-
ing, larval culture, setting of eyed larvae, and nursery proce-
dures were performed following methods described in previous
studies (Mazón-Suástegui et al. 2002, Chávez-Villalba et al.
2005). When the spat reached an average length of 2–3 mm,
approximately two months after fertilization, about 5,000 spat
(height 2.66 ± 0.1 mm; n ¼ 30) was taken from the growing tanks
and transported from La Paz to Guaymas to initiate experi-
mental cultivation.
Culture
The cultivation experiment was carried out in a lagoon
(27°33#N, 110°38.5#W) adjacent to Bahı́a Guásimas, located
about 40 km southeast of Guaymas, Sonora (Fig. 1). The
experiment was performed with assistance of personnel at the
Palapas de Bélem Cooperative that cultures C. gigas. The same
practices and maintenance activities used for the Pacific oyster
were used for raising the Cortez oyster. The standard practice is
Figure 1. Cultivation site of the Cortez oyster Crassostrea corteziensis in the lagoon at Las Guásimas in Sonora, Mexico.
to place spat in 2-mm mesh plastic bags (;1,000 juveniles per
bag) on plastic trays attached to a long-line. Juveniles (30 mm
height) were placed directly on the plastic trays. Maintenance is
performed each month by cleaning or replacing trays and
reducing the density to 60–80 oysters per tray when they reach
;80 mm height. Empty shells were recovered and counted at
each sampling to estimate mortality.
Sampling
Samples of 30 oysters were taken each month throughout the
25-mo experiment, starting in July 2003 and ending in Septem-
ber 2005. No samples were collected in June and October 2004.
Specimens were transported to the laboratory for cleaning and
measuring height, length, width, and dry weight. Three princi-
pal dimension complexes of oyster valves (Carriker 1996);
height, distance between umbones, and posterior margins of
the valves; length, maximal distance between ventral and dorsal
margins parallel to the hinge axis; and width, maximal distance
between the outside surface of closed valves measured at right
angles to the plane of closure of the valves. Only height was
measured in July, the beginning of the experiment; all other
dimensions were recorded monthly from August 2003 to the
end of the study. After recording these data, the oysters were
opened. The tissues and shells of 10 specimens were used to
calculate the condition index (CI) described by Walne & Mann
(1975). The soft tissues were dried in an oven for 48 h at 80°C
and dry weight then determined. The CI was calculated as: CI ¼
(P1 3 1,000)/P2, where P1 is the dry weight of soft tissue (g)
and P2 is the dry weight of the shell (g). Measurements of total
weight and estimates of CI started in October 2003. Another 10
oysters were used for histological studies of their gonads.
Semi-Quantitative Histology
A 1-cm3 section of the visceral mass above the pericardium
was fixed in Davidson’s solution for 48 h (Howard & Smith
 PROSPECTIVE CULTURE OF CRASSOSTREA CORTEZIENSIS 713

1983). Samples were then placed in 70% alcohol where they
were stored. For dehydration, samples were passed through a
series of increasing ethanol concentrations, cleared in xylene,
and then embedded in paraffin, following standard histological
techniques (Howard and Smith, 1983). Sections (;5–6 mm)
were mounted on glass slides and stained with Harris hema-
toxylin and eosine Y/floxine B procedure. The histological
preparations were examined using an optical microscope (Zeiss)
connected to a digital camera (Canon PowerShot G5). For
female specimens, 5–10 photos were taken on a random basis to
record at least 100 oocytes from each specimen. Sigma Scan Pro
5.0 software was used for image analysis, and a calibration of
the program used a microruler of 1,000 mm mounted on a slide
before measuring the oocytes. After calibration, measuring
methods were established, based on the description by Lango-
Reynoso et al. (2000). The surface of each oocyte that presented
a well-defined germinal vesicle was measured by drawing its
perimeter on the computer screen to calculate an area (in pixels)
that was transformed into ap theoretical
ffiffiffiffiffiffiffiffiffiffiffi diameter (in mm), using
the relationship: Dtheoretical ¼ 4S=p (Lango-Reynoso et al. 2000).
To assess the reproductive phase of female Cortez oysters,
we used the classification used for C. gigas (Lango-Reynoso
et al. 2000), which is based on oocyte diameter and cytological
features of the gonad (Table 1). For males, we used the
classification of Chávez-Villalba et al. (2002), which is based
on the percentage of spermatids and sperm in the follicles (Table
2). Gonads in undifferentiated oysters were mostly connective
tissue without sexual cells.
Environmental Parameters
Seawater surface temperature and salinity were recorded at
each sampling event with a laboratory thermometer and
refractometer. At the same time, 4 L seawater was collected to
measure concentrations of chlorophyll a, b, and c, and seston.
The concentration of chlorophyll was determined by the
method described by Contreras-Espinosa (1984). In brief, one
liter of seawater was passed through A/E Gelman filters. The
filters were placed in conical tubes where they were crushed with
10-mL 90% acetone, the conical tubes were covered with
aluminum foil and stored in the dark at 4°C for 24 h; samples
were centrifuged at 1,300g for 10 min; spectrophotometric
readings were made at 630, 647, 664, and 750 nm. For seston
determinations, we used the technique described in Chávez-
Villalba et al. (2005). Two liters of seawater is passed through
4.7-cm diameter GF/C Whatman filters. The filters with
samples were placed in an oven at 80°C for 24 h, then weighed,
and then placed in a muffle furnace at 450°C for 4 h. The filters
were weighed again to obtain the organic seston as the
difference of the previous weight, so that the total seston was
the sum of the inorganic seston and the organic seston.
Data Analysis
Shell measurements (height, length, and width) and weight
of oysters were used to determine isometric and allometric
relationships among variables. For isometric relationships, we
used linear regression tests to obtain descriptive equations;
allometric growth was estimated using potential regression.
In both cases, goodness-of-fit was described by the r2 cor-
relation coefficient (Sokal & Rohlf 1969). The nonparametric
test of Kruskal-Wallis was used to determine differences
in the condition index. Statistical significance was set at P <
0.05.
Daily growth rate (height; in mm) was calculated as:
DWR ¼ ðt1  t0 Þ=d;
where t1 ¼ height at time 1, t0 ¼ height at time 0, and d ¼ day.
Growth was adjusted to the von Bertalanffy model, with height
as the variable (Pauly 1987):

TABLE 1.
Reproductive classification used for Crassostrea gigas to describe the reproductive stages of C. corteziensis. Females were classified by
oocyte diameter (Lango-Reynoso et al. 2000) and males by cytologic characteristics of the gonad (Chávez-Villalba et al. 2002).

Stage Interval
Female Stages (mm) Histological Description
Early gametogenesis 3.0–12.0 Follicles are elongated and often isolated in abundant connective tissue
with walls consisting of primary oocytes of homogeneous size.
Growing 12.1–30.0 Start of oocyte growth. Large range in oocyte size at all gametogenic stages
can be observed, including some free oocytes. Interfollicular connective
tissue disappears.
Mature 30.1–41.0 Follicles of relatively homogeneous size completely filled with mature oocytes
with distinct nucleus.
Degenerating 41.1–60.0 Follicles containing degenerating oocytes, often elongated in shape, sometimes
broken. Obvious redevelopment indicated by increased number
of primary oocytes.
Male stages
Early gametogenesis Abundant connective tissue containing elongated follicles with walls consisting
of germinal epithelium with some spermatogonia and spermatocytes
Growing Connective tissue is reduced and follicles become larger; normal sequences of
spermatogenesis are observable with spermatocytes I and II, spermatids and
some spermatozoids are organized in the lumen
Mature Connective tissue almost disappeared. Follicles filled with packages of
spermatozoids oriented with tails toward the follicle lumen
Undifferentiated oysters Abundant connective tissue with no follicles. Follicles, when present, small and
isolated with no detectable presence of sexual cells.
714 CHÁVEZ-VILLALBA ET AL.

TABLE 2.
Isometric and allometric growth relationships of Crassostrea corteziensis.

Relationship Equation n CC* R2 F-Ratio P-Value

Height – Length y ¼ 0.6048x + 7.1121 666 0.940 88.39 5056.98 0.0000
Height – Width y ¼ 0.3558x – 4.1851 666 0.891 79.38 2557.54 0.0000
Length – Width y ¼ 1.4205x + 20.2131 666 0.882 77.77 2323.21 0.0000
Weight – Height y ¼ 0.00007(x3.0953) 606 0.921 84.77 3697.18 0.0000
Weight – Length y ¼ 0.004(x2.3473) 606 0.758 57.48 897.73 0.0000
Weight – Width y ¼ 1.9561(x–1.0212) 606 0.721 51.97 718.47 0.0000

* Correlation coefficient.

n o
RESULTS
Ht ¼ H‘  1  e½K ðtt0 Þ ;
Environmental Parameters

where HN is the asymptotic height (mm), K is the growth
constant per year, t is the age (in years) and t0 is the age at zero
height. The parameters of the model were calculated using the
FAO-ICLARM Stock Assessment Tools software (FiSAT;
Gayanilo et al. 1995).
Similar patterns were observed in the concentrations of
chlorophyll a, b, and c (Fig. 2). In 2005, peaks occurred (in mg
L–1) in July (a ¼ 28.8, b ¼ 47.5, and c ¼ 55.1) and August (a ¼
21.3, b ¼ 35.3, and c ¼ 40.9). Low concentrations occurred in
spring 2004 and 2005, but also in July 2003 and March, June,

Figure 2. Concentration of chlorophylls a, b, and c, particulate organic material (POM), and particulate inorganic material (PIM) in relation to
temperature and salinity measurements during the study period.
 PROSPECTIVE CULTURE OF CRASSOSTREA CORTEZIENSIS
and September 2005; concentrations in these months were lower
than 0.3 mg L–1. Particulate inorganic material (PIM) was
higher than particulate organic material (POM) at most sam-
plings and both followed a similar changing pattern at different
scales; varying slightly at a low concentration prior to February
2004 and present at a high concentration after July 2004, except
in March, April, and May 2004 when PIM was lower than POM
(Fig. 2). Highest concentration of PIM (298 mg L–1) and POM
(62 mg L–1) occurred in July 2004 and the lowest PIM occurred
in April 2004 (0.5 mg L–1) and the lowest POM in December
2003 (7 mg L–1). Temperature patterns were similar on an
annual basis, with highest temperature in July 2003 (33°C),
August 2004 (33°C), and August 2005 (30.5°C) and the lowest in
December 2003 (15°C) and December 2004 (16°C) (Fig. 2). A
clear pattern in salinity was not evident, with highest salinity of
42 in December 2004 and April to May 2004 and lowest salinity
of 33 in September 2004 (Fig. 2).
Growth
Growth of oysters after 25 mo of cultivation was: height ¼
103.2 ± 1.82 mm, length ¼ 63.4 ± 0.74 mm, width ¼ 31.9 ± 0.78
mm and 150.3 ± 4.98 g total weight (Fig. 3). Isometric and
allometric growth relationships are shown in Table 2. The daily
growth rate (height) was 0.218 mm during the first year and
0.127 mm over the entire experiment. Analysis of height used
von Bertalanffy growth model. The results for the model were;
HN ¼ 132.2 mm (height); K ¼ 1.08 y–1, and t0 ¼ –0.18. The
growth model, using height (H), is H ¼ 132.2 { 1 – e[–1.08 (t+0.18)]}.
Finally, survival at the end of the experiment averaged more
than 70% and no massive die-offs occurred during the study period.
Reproduction
From histological preparations, we confirmed the four
reproductive stages (early gametogenesis, growing, mature,
and degenerating) (Fig. 4A, B, C, and D) for female oysters
described by Lango-Reynoso et al. (2000) and found cytological
features of hermaphrodite oysters (Fig. 4E). We confirmed the
three stages (early gametogenesis, growing, and mature) for
male oysters (Fig. 4F, G, and H) described by Chávez-Villalba
et al. (2002).
Assessment of reproductive activity started in October 2003
on very young oysters (6 mo old). The annual gametogenic cycle
began in March 2004 and April 2005 with high activity until
Figure 3. Monthly average of height, length, width, and weight (%SE)
of the Cortez oyster Crassostrea corteziensis cultivated in the lagoon at
Las Guásimas in Sonora, Mexico.
715
November in both years (Fig. 5). Elevated proportions of
vitellogenic oocytes (70–83.2%) were detected from May
through November 2004 and from July through September
2005 (62.5–77.2%). Maximum reproductive activity (seasonal
peaks, defined by percent of mature oocytes) occurred in
October 2003 (66%), April 2004 (66%), and June 2005
(61.3%). Although degenerating oocytes were uncommon in
the histological slides, these provided evidence of partial spawn-
ing in November 2003 and April, August, and September 2004.
Higher proportions of mature males were observed from March
through December 2004, reaching 100% of the examined speci-
mens in July and August 2004 (Fig. 5). In 2005, high proportions
of males in the growing stage occurred from March through May
and September with a peak of mature oysters (75%) in July.
By measuring oocyte diameter, gametogenesis began in
March 2004 and April 2005 with growing oocytes measuring
24.9 ± 8.5 mm and 20.6 ± 11.4 mm, respectively (Fig. 6). Growing
stage prevailed from May to November 2004 and May to
September 2005. Significant declines in oocyte diameter from
October to November in 2003 and from April to May in 2004
and 2005 indicated the presence of spawning events. The end of
the gametogenesis cycle was clearly identified by oocytes in
early gametogenesis in December 2004 and no females in
December 2005. Although linear regression analysis showed
R2 ¼ 0.39, oocyte diameter was related (P < 0.05) to seawater
temperature. During the study, oocytes ranged from 2.5–46.1 mm.
Condition Index
Values derived from the Walne-Mann condition index (CI)
are shown as three curves with higher values in December 2003
(66.7%), April 2004 (69.4%), and June 2005 (72%) (Fig. 6).
Significant reduction (P < 0.05) of CI occurred from July
through August in 2004 and 2005 and lowest CI occurred in
September, evidence of a major spawning event. Nevertheless,
the other spawning periods, detected by histological observa-
tions, did not reflect significant changes in CI.
Sex Ratio Related to Size
Of the oysters specimens we observed histologically, 50.9%
were females, 35% were males, 12.7% were undifferentiated,
and 1.4% were hermaphrodites. Frequency distribution based
on size classes of females, males, hermaphrodites, and undif-
ferentiated oysters showed that females were most abundant
(67.5–90.5%) in the middle size classes (70–80 mm) and less
abundant in the small and large size classes (Fig. 7). Males were
present in higher proportions in the small (70%) and largest size
classes (50%) and less in the middle size class (9.5%; 70–75
mm). When oysters grew larger than 95 mm in height, their
sexual ratio became close to equal. No oysters were found to
determine sex ratio in the 85–90 mm size class. Mature males
were found in oysters six months old (45–50 mm), indicating
that gonads became functional in young, small specimens.
DISCUSSION
Environmental Parameters
Research has demonstrated that growth in bivalves is
influenced by variations in the quantity of the seston (Toro
716 CHÁVEZ-VILLALBA ET AL.

Figure 4. Cytological characteristics, seen under light microscopy, of female, hermaphrodite, and male gonads of the Cortez oyster Crassostrea
corteziensis at different reproductive stages. Females: A$ early gametogenesis, B$ growing, C$ mature, and D$ degenerating. Hermaphrodites$ E.
Males: F$ early gametogenesis, G$ growing, and H$ mature. Ct$ connective tissue, Fo$ follicle, Do$ degenerating oocyte, Go$ growing oocyte,
Mo $ mature oocyte, O $ oocytes, Po $ primary oocyte, Sp $ spermatozoids. Bars $ 50 mm.

et al. 1999). The concentration of POM was relatively constant
throughout the experiment, but seston was less concentrated
from July 2003 to April 2004, compared with May 2004 to the
end of the study in 2005. Changes in seston load were not related
to significant variations in shell growth. However, a significant
increase in total weight was detected during the change from
low to high concentrations of seston in May 2004. Paterson
et al. (2003) demonstrated that POM is a controlling factor in
the growth of the Sydney rock oyster Saccostrea glomerata. The
oysters in our study were cultivated in parallel with other batch
of oysters in a different lagoon (Chávez-Villalba et al. 2005). In
the lagoon at Las Guásimas, weight gain after cultivation for 13
 PROSPECTIVE CULTURE OF CRASSOSTREA CORTEZIENSIS
Figure 5. Percentage of females and males in the several reproductive
phases of the Cortez oyster Crassostrea corteziensis during the study
period.
mo reached 59.9 g under average POM concentrations of 31 mg
l–1; weight gain at the other location was 30.1 g under average
POM concentrations of 9.7 mg l–1. This suggests that the con-
centration of POM influences weight gain, but ecophysiological
experiments are needed to confirm this. We believe that Cortez
Figure 6. Box and whisker plots of oocyte diameter (– $ median, box$
50% of data, vertical lines$ range, *$ values between the inner and outer
fences, s $ outlier values), and average values (%SE) of the condition
index of Crassostrea corteziensis during the study period.
717
Figure 7. Percentage of females, males, hermaphrodites, and undifferen-
tiated Cortez oysters Crassostrea corteziensis in relation to shell height.
oysters adjust their feeding behavior to different food condi-
tions and exploit POM under great variations in PIM.
In coastal habitats, POM consists of bacteria, detritus,
nanozooplankton, but phytoplankton is the main source of
nutrition for bivalve filter feeders (Dame 1996). Phytoplankton
biomass at Las Guásimas, expressed as chlorophyll a concen-
tration, increased during spring and the highest values occurred
during the summers of 2003, 2004, and 2005. The range
observed in this study coincided with the annual cycle of
chlorophyll reported by Arreola-Lizárraga (2003) for this same
coastal lagoon. Normally, seasonal abundance of phytoplank-
ton (chlorophyll a) is strongly related to temperature (Toro
1996). This was the case in Las Guásimas, where phytoplankton
blooms occurred during the summer and low concentrations
of microalgae were associated with low temperatures during
winter. Moreover, high chlorophyll levels in summer seem to
be fueled by additional nutrients coming from freshwater run-
off from summer rainstorms and shrimp farming activities
within the lagoon. More nutrients from phytoplankton and
algae have been associated with aquaculture activities (Toro
et al. 1999). Similarly, Castillo-Durán (2007) found a significant
increase of nutrients during farm operations from April to
October. In terms of potentialities for oyster aquaculture in this
coastal lagoon, the author reported a succession of phytoplank-
ton communities during summer and winter associated with
changes in the water masses; for example, summer was charac-
terized by 68% diatoms (Coscinodiscus concinnus, Lioloma
delicatulum, and Paralia sulfata) with a diversity index of H# ¼
6356 bits cell–1 and winter by 44% diatoms (Actinocyclus
curvatulus, Paralia sulfata, and Thalassionema nitzschioides
nitzschiodes) with a diversity index of H# ¼ 1,686 bits cell–1.
Growth and Mortality
The oyster industry in northwestern Mexico is based on the
production of Crassostrea gigas. Some experimental cultivation
has been done with C. corteziensis, but the results are not
available and information comes from personal communica-
tions. Recently, agencies within the State of Sonora supported
studies of growth of the native oyster in different locations in
the state. Unfortunately, the results of these experiments are not
published, but we collected information from reports to com-
pare our results with these findings. These unpublished reports
showed daily growth from 0.222–0.253 mm over a period of 7–10
718 CHÁVEZ-VILLALBA ET AL.
mo of cultivation in lagoons with typical marine conditions.
Higher growth rates were detected (0.304 mm) in experiments
carried out in discharge channels of shrimp farms with hyposa-
line water of ;25. Growth rates in marine locations were similar
to results obtained here, when adjusting for the length of time
(0.251 mm for 10 mo). In general, growth rates of the Cortez
oyster are lower than for the Pacific oyster at marketable size
(>80 mm or >60 g) in 7–10 mo of cultivation. Geographically,
growth rate of C. gigas diminishes in southern locations
(Ramı́rez-Filippini et al. 1990) and has slower growth than
specimens described in our study. The authors obtained growth
curves of suspension and bottom cultures of C. gigas oysters
using von Bertalanffy-growth-function with values of LN (60.7
and 78.9, respectively) and K (0.0078 and 0.0057, respectively),
which were lower than values we obtained with the Cortez
oyster: LN ¼ 132.25 mm and K ¼ 1.08 y–1. In a previous study,
we reported the data derived from the von Bertalanffy equation
(LN ¼ 114 mm and K ¼ 1.1 y–1) obtained from 13 mo of
cultivation of C. corteziensis at Laguna El Soldado (Chávez-
Villalba et al. 2005). Growth values at Las Guásimas fitted the
model we proposed earlier; we obtained a similar value for K,
but the calculated LN was higher because the data came from a
two-year experiment, where Lmax ¼ 135 mm. We believe the model
is useful for oystermen in predicting growth of Cortez oysters.
Since 1998, massive die-offs of C. gigas have regularly
occurred around the end of October, March, and April at
farms in northwestern Mexico. No massive die-offs occurred at
Las Guásimas during the study period. Over the course of this
study, survival was ;70% and was similar to survival rates
obtained in the study of C. corteziensis at El Soldado, where a
massive die-off occurred (Chávez-Villalba et al. 2005). Survival
of the Cortez oyster at Las Guásimas was similar to reports of
experimental cultures of the Pacific oyster (Ochoa-Araiza &
Fimbres-Peña 1984, Ramı́rez-Filippini et al. 1990). However, it
is essential to estimate survival rates of the native Cortez oyster
at larger scales to anticipate the impacts on commercial operations.
Reproduction
Gametogenesis of the Cortez oyster involves a cycle that
begins in March-April and ends in November, with temperature
as the major factor affecting reproduction. Initiation and extent
of gametogenesis were related to the high annual temperature
variations of 15°C to 33°C. Wide seasonal fluctuations in these
coastal lagoons is from water masses from the lower Gulf
province (Arreola-Lizárraga 2003). The rapid change from low
to high temperature activates gametogenesis and induces
oocytes to pass rapidly from the early stage to the growth and
maturity phase at the beginning of the cycle. This same pattern
was observed at the start of reproduction of C. gigas in other
coastal lagoon in this region (Chávez-Villalba et al. 2007). The
presence of different oocyte phases at the same time indicated
a polymodal oocyte distribution in the Pacific oyster during
periods when conditions for spawning are favorable (Lango-
Reynoso et al. 2006). This pattern was present during the entire
gametogenic cycle of the Cortez oyster under the influence of
long-term high temperatures of 25°C. This situation produced
high oocyte growth rates and generated continuous production
of primary oocytes, rapid oocyte growth, and accumulation of
ripe oocyte before spawning. Evidence of partial spawning in
the histological slides was detected in April, August, September,
and November 2004, which coincides with other reports of
partial spawning in C. corteziensis (Cuevas-Guévara &
Martı́nez-Guerrero 1979, Ruı́z-Durá 1980). The significant
reduction of the condition index from July to August in 2004
and 2005 suggests that massive spawning occurs when temper-
ature reached a peak. Temperature started to fall in September,
but growing, mature, and reabsorbed oocytes were still present
until November in 2003 and 2004. No oocyte in these phases
occurred with minimum temperatures from December, which
indicated the end of the gametogenic cycle, characterized by a
short and rapid process of gamete reabsorption inside the gonad.
Temperature and food supply are the most influential factors
on initiation and duration of the reproduction cycles of bivalves
(Dinamani 1987, Ruiz et al. 1992), so gametogenesis in many
tropical bivalves is normally continuous because temperature
and food supply vary little during the year (Urban 2000).
Among temperate species, where temperature and seston vary
seasonally, gametogenesis is a cyclic pattern (Fabioux et al.
2005). The cycle in C. corteziensis is as a combination of these
two patterns; the beginning and the end of the cycle is related to
increasing and decreasing temperatures, and once initiated, it is
continuous over nine months with several spawning periods.
The timing and amplitude of the cycle correlates with seawater
temperature, with annual variations based on the quality and
quantity of the food supply. Energy required for gametogenesis
comes from two sources, phytoplankton and nonchlorophyll-
related seston. No correlation between POM and chlorophyll a
suggests that when phytoplankton is low, POM is composed of
other constituents (protozoa, bacteria, zooplankton, detritus,
etc.). Oysters use the organic components of these constituents.
Concentrations of POM in winter were sufficient for oysters
to increase energy reserves. In the absence of sexual activity
during the winter of 2003 and 2004, the condition index
indicates accumulation of energy and specific nutrients that
will be used for initiation of the gametogenic cycle. These results
indicate that nutrient accumulation over the winter is as
important in the reproduction of the Cortez oyster as in other
species (Ren et al. 2003). Berthelin et al. (2000) found that
reserves in C. gigas accumulate during the autumn-winter and
are used later for gametogenesis. Also, Chávez-Villalba et al.
(2007) found the same pattern of reproduction in this same
species in other coastal lagoons in this region. In general, the
Cortez oyster maintained high CI throughout the study; with
the exception of February and March, CI averaged 10% higher
than the CI of the Pacific oyster during one year of cultivation at
Laguna El Soldado (Chávez-Villalba et al. 2007). This is relevant
information for future commercialization of this species.
Gamete development in terms of oocyte diameters con-
firmed the significant relationship of gametogenesis with tem-
perature; large oocytes were found during periods of rising
temperatures, whereas primary cells were associated with low
temperatures. Ren et al. (2003) found that oocyte diameter in
C. gigas was directly related to surface seawater temperature.
The size of oocytes have been used to describe reproduction of
C. corteziensis, but the method was based on two categories,
small (maturing) or large (>50 mm.) spawning oocytes (Ruiz-
Durá 1980). The maximum diameter in our Cortez oysters was
46 mm; we suspect that differences in cell size are related to the
methods used to assess phases of gametogenesis. Nevertheless,
oocyte diameter is a good quantitative descriptor of reproduc-
tive development in females.
 PROSPECTIVE CULTURE OF CRASSOSTREA CORTEZIENSIS
The sex of any individual within a population is partly a
function of size, which in most cases is linked to age (Deslous-
Paoli & Héral 1988). In the Cortez oyster, males predominated
until the oysters reached 50–55 mm height, which corresponds
to an age of six month; after which, females are more abundant.
Small numbers of hermaphrodites were observed before the
peak in females, which occurred at 70–75 mm, but also were
present in two larger size classes (75–80 and 95–100 mm). These
results are similar to the proportion of each sex at each growth
interval as in the Pacific oyster, where juveniles usually mature
as males and change into females later in life (Baghurst &
Mitchell 2002). Hermaphrodites represent an intermediate
stage from male to female in the Pacific oyster (Lango-Reynoso
et al. 2006); the proportions at that stage (0.35% to 1.7%)
(Mann 1979, Paniagua-Chávez & Acosta Ruiz 1995, Steele
1998) are similar to our results (1.5%). These observations
suggest that the Cortez oyster is a protandric, dioecious species
with functional hermaphroditism.
CONCLUSION
Experiments in cultivation of the native Cortez oyster were
characterized by high survival and similar or better weight gain
LITERATURE CITED
Aragón-Noriega, E. A., J. Chávez-Villalba, P. E. Gribben, E. Alcántara-
Razo, A. Maeda-Martı́nez, E. Arambula-Pujol, A. Garcı́a-Juárez &
R. Maldonado-Amparo. 2007. Morphometric relationships, game-
togenic development and spawning of the geoduck clam Panopea
globosa (Bivalvia: Hiatellidae) in the central Gulf of California.
J. Shellfish Res. 26:423–431.
Arreola-Lizárraga, J. A. 2003. Bases de manejo costero: Patrones
ecológicos en la laguna costera Las Guásimas, Territorio Yaqui,
México. Doctoral Thesis Centro de Investigaciones Biológicas del
Noroeste, La Paz, B.C.S., Mexico. 61. pp.
Baghurst, B. C. & J. G. Mitchell. 2002. Sex-specific growth and
condition of the Pacific oyster (Crassostrea gigas Thunberg). Aquac.
Res. 33:1253–1263.
Berthelin, C., K. Kellner & M. Mathieu. 2000. Storage metabolism in
the Pacific oyster (Crassostrea gigas) in relation to summer mortal-
ities and reproductive cycle (west coast of France). Comp. Biochem.
Physiol. 125B:359–369.
Carriker, M. R. 1996. The shell and ligament. In: V. S. Kennedy, R. G.
Newell & A. F. Eble, editors. The eastern oyster Crassostrea
virginica. Maryland: University of Maryland, College Park. 104 pp.
Castillo-Durán, J. A. 2007. Influencia de la variabilidad ambiental de
una laguna costera semiárida subtropical en el desarrollo de los
ostiones, Crassostrea gigas (Thunberg, 1793) y Crassostrea corte-
ziensis (Hertlein, 1951), bajo condiciones de cultivo. Master’s Thesis.
Universidad de Sonora, Hermosillo, Mexico. 51. pp.
Chávez-Villalba, J., J. Barret, C. Mingant, J. C. Cochard & M. Le
Pennec. 2002. Autumn conditioning of the oyster Crassostrea gigas:
A new approach. Aquaculture 210:171–186.
Chávez-Villalba, J., M. R. López-Tapia, J. M. Mazón-Suástegui & M.
Robles-Mungaray. 2005. Growth of the oyster Crassostrea corte-
ziensis (Hertlein, 1951) in Sonora, Mexico. Aquac. Res. 36:1337–
1344.
Chávez-Villalba, J., F. Villelas-Ávila & C. Cáceres-Martı́nez. 2007.
Reproduction, condition and mortality of the Pacific oyster Cras-
sostrea gigas (Thunberg) along coastal Sonora, Mexico. Aquac. Res.
38:268–278.
Contreras-Espinosa, F. 1984. Manual de Técnicas Hidrobiológicas.
Mexico: Universidad Autónoma Metropolitana-Iztapalapa. 141 pp.
719
than the Pacific oyster. Growth rates indicated that marketable
size could be reached in 18 mo, which would necessitate new
cultivation programs for the native species. Resistance to
massive die-off events would compensate for longer grow-out.
The duration of gametogenesis activity determines the
availability of spat during the year, an essential factor for the
success of a developing aquaculture (Urban 2000). With a
continuous gametogenic cycle over nine months, hatchery
production of larvae and spat would probably occur for most
of the year. However, better yields of early stages would be
anticipated for August and September. This study demon-
strated that the native Cortez oyster is an excellent alternative
for diversifying and improving aquaculture activities in parts of
the Gulf of California.
ACKNOWLEDGMENTS
The authors thank CIBNOR technicians David Urias, and
Edgar Alcántara for laboratory and field assistance. This
research was supported by the International Foundation for
Science, Stockholm, Sweden with a grant to Jorge Chávez-
Villalba and by SAGARPA-CONACYT 2003/002-061 and
CIBNOR AC 4.1 projects.
Cuevas-Guévara, C. A. & A. Martı́nez-Guerrero. 1979. Estudio goná-
dico de. Crassostrea corteziensis Hertlein, C. palmula Carpenter y C.
iridescens Hanley, de San Blas, Nayarit, México (Bivalvia: Ostrei-
dae). An. Centro Cien. del Mar y Limnol. 6:81–98.
Dame, R. F. 1996. Ecology of Marine Bivalves. An Ecosystem
Approach. New York, NY: CRC Press. 254 pp.
Deslous-Paoli, J. M. & M. Héral. 1988. Biochemical composition and
energy value of Crassostrea gigas (Thunberg) cultured in the bay of
Marennes-Oléron. Aquat. Living Res. 1:239–249.
Dinamani, P. 1987. Gametogenic patterns in populations of Pacific
oyster, Crassostrea gigas, in Northland, New Zealand. Aquaculture
64:65–76.
Fabioux, C., A. Huvet, P. Le Souchu, M. Le Pennec & S. Pouvreau.
2005. Temperature and photoperiod drive Crassostrea gigas repro-
ductive internal clock. Aquaculture 250:458–470.
Fisher, W., F. Krupp, W. Schneider, C. Sommer, K. E. Carpenter & V.
H. Niem. 1995. Guı́a FAO para la identificación de especies para los
fines de pesca. Pacı́fico Centro-Oriental. Plantas e Invertebrados
(Vol. 1). Rome: FAO. 646 pp.
Frı́as-Espericueta, M. G., F. Páez-Osuna & J. I. Osuna-López. 1997.
Seasonal changes in the gonadal state of the oysters Crassostrea
iridescens and Crassostrea corteziensis (Filibranchia: Ostreidae)
in the Northwest coast of México. Rev. Biol. Trop. 45:1061
1065.
Frı́as-Espericueta, M. G., J. I. Osuna-López & F. Páez-Osuna. 1999.
Gonadal maturation and trace metals in the mangrove oyster
Crassostrea corteziensis: seasonal variation. Sci. Total Environ.
231:115–123.
Gayanilo, F. C., Jr., P. Sparre & D. Pauly. 1995. The FAO-ICLARM
stock assessment tools (FiSAT) User’s guide. Rome: FAO Com-
puterized information series (Fisheries - 8).
Howard, D. W. & C. S. Smith. 1983. Histological techniques for marine
bivalve molluscs. USA: NOAA technical memorandum NMFS-F/
NEC-25. 97 pp.
Lango-Reynoso, F., J. Chávez-Villalba, J. C. Cochard & M. Le Pennec.
2000. Oocyte size, a means to evaluate the gametogenic development
of the Pacific oyster, Crassostrea gigas (Thunberg). Aquaculture
190:183–199.
720 CHÁVEZ-VILLALBA ET AL.
Lango-Reynoso, F., J. Chávez-Villaba & M. Le Pennec. 2006. Repro-
ductive patterns of the Pacific oyster Crassostrea gigas in France.
Invert. Reprod. Develop. 49:41–50.
Mann, R. 1979. Some biochemical and physiological aspects of growth
and gametogenesis in Crassostrea gigas and Ostrea edulis grown at
sustained elevated temperatures. J. Mar. Biol. Ass. UK 59:95–110.
Mazón-Suástegui, J. M., M. Robles-Mungaray, F. Flores-Higuera & A.
Avilés-Quevedo. 2002. Experiencias en la producción de semilla de
ostión de placer Crassostrea corteziensis en el laboratorio. IV
Simposio Nacional de Acuicultura y Pesca (Book of Abstracts).
Guatemala: Antigua. pp. 16–18.
Ochoa-Araiza, G. & M. T. Fimbres-Peña. 1984. Evaluación de temper-
atura, salinidad y crecimiento del ostión japonés (Crassostrea gigas)
en una laguna costera del estado de Sonora, México. Cienc. Mar.
10:7–16.
Osuna-López, J. I., H. M. Zazueta-Padilla, A. Rodrı́guez-Higuera & F.
Páez-Osuna. 1990. Trace metal concentrations in mangrove oyster
(Crassostrea corteziensis) from tropical lagoon environments, Mex-
ico. Mar. Pollut. Bull. 21:486–488.
Osuna-López, J. I., M. G. Frı́as-Espericueta, H. M. Zazueta-Padilla &
G. López-López. 1999. Heavy metals in the drowned oyster,
Crassostrea corteziensis, from lagoon system Ensenada del Pabellon,
Sinaloa, Mexico. Oceanides 14:113–119.
Páez-Osuna, F., H. M. Zazueta-Padilla & J. I. Osuna-López. 1993.
Biochemical composition of the oysters Crassostrea iridescens and
Crassostrea corteziensis in the northwest coast of México: seasonal
changes. J. Exp. Mar. Biol. Ecol. 170:1–9.
Paniagua-Chávez, C. G. & M. J. Acosta-Ruı́z. 1995. Desarrollo gonadal
de Crassostrea gigas en Bahı́a San Quintı́n, Baja California, México.
Cienc. Mar. 20:225–242.
Paterson, K. J., M. J. Schreider & K. D. Zimmerman. 2003. Anthro-
pogenic effects of seston quality and quantity and the growth and
survival of Sydney rock oysters (Saccostrea glomerata) in two
estuaries in NSW, Australia. Aquaculture 221:407–426.
Pauly, D. 1987. A review of the ELEFAN system for the analysis of
length frequency data in fish and aquatic invertebrates. ICLARM
Conference Proceedings 13: 7–34.
Ramı́rez-Filippini, D., J. Chávez-Villalba & C. Cáceres-Martı́nez. 1990.
Cultivo de ostión en costales sobre estantes en la zona intermareal en
la Bahı́a de La Paz, B.C.S.: Estudio comparativo de crecimiento y
resistencia, con el cultivo en suspensión. In: G. de la Lanza-Espino &
J. L. Arredondo-Figueroa, editors. La Acuicultura en México: De
los conceptos a la Producción. Mexico: Instituto de Biologı́a,
Universidad Autónoma de México. pp. 152–161.
Ren, J. S., I. D. Marsden, A. H. Ross & D. R. Schiel. 2003. Seasonal
variation in the reproductive activity and biochemical composition
of the Pacific oyster (Crassostrea gigas) from the Marlborough
Sounds, New Zealand. New Zeal. J. Mar. Fresh. 37:171–182.
Rivero-Rodrı́guez, S., A. R. Beaumont & M. C. Lora-Vilchis. 2007. The
effect of microalgal diets on growth, biochemical composition, and
fatty acid profile of Crassostrea corteziensis (Hertlein) juveniles.
Aquaculture 263:199–210.
Ruı́z, C., M. Abad, F. Sedano, L. Garcı́a-Martı́n & J. Sánchez-López.
1992. Influence of seasonal environmental changes on the gamete
production and biochemical composition of Crassostrea gigas
(Thunberg) in suspended culture in El Grove, Galicia, Spain.
J. Exp. Mar. Biol. Ecol. 155:249–262.
Ruı́z-Durá, M. F. 1980. Ciclo gonádico de Ostrea corteziensis (Hertlein,
1951). Memorias del 2do Simposio Latinoamericano de Acuacul-
tura (Vol. II). México: Departamento de Pesca. pp. 1232–
1250.
SAGARPA. 2003. Anuario Estadı́stico de Pesca, 2003. Mexico: Secretarı́a
de Agricultura, Ganaderı́a, Desarrollo Rural, Pesca y Alimentación.
Sevilla, M. L. 1959. Datos biológicos para el cultivo de ostión en
Guaymas, Sonora. Mexico: Secretarı́a de Industria y Comercio.
Dirección General de Pesca.
Sokal, R. & J. Rohlf. 1969. Biometry. San Francisco, CA: W. H.
Freeman and Company. 887 pp.
Steele, S. 1998. The reproductive biology of the Pacific oysters. Doctoral
thesis. University of Cork, Cork, Ireland. 138 pp.
Stuardo, J., A. Martı́nez & F. Escobar de la Llata. 1973. Informe final de
la segunda etapa de los estudios de la influencia de los cambios
hidrológicos del Rı́o Santiago en la biologı́a del ostión y medidas
para la rehabilitación de los bancos de dicha especie. Informe final.
Contrato de estudio No. EI-71-41, Clave LL-3. Mexico: Instituto de
Biologı́a, Universidad Nacional Autónoma de México y Secretarı́a
de Recursos Hidráulicos.
Stuardo, J. & A. Martı́nez. 1975. Relaciones entre algunos factores
ecológicos y la biologı́a de poblaciones de Crassostrea corteziensis
Hertlein, 1951, de San Blas, Nayarit, México. An. Centro Cienc. del
Mar y Limnol. 2:89–130.
Toro, J. E. 1996. Phenotypic response of a cohort of Ostrea chilensis
(Philippi 1845) to differing environmental conditions in three oyster
farms in Southern Chile. Aquac. Res. 27:1–7.
Toro, J., P. Paredes, D. Villagra & C. Senn. 1999. Seasonal variation in
the phytoplanktonic community, seston and environmental varia-
bles during a 2-year period and oyster growth at two mariculture
sites, Southern Chile. Mar. Ecol. 20:63–89.
Urban, H. J. 2000. Culture potential of the pearl oyster (Pinctada
imbricata) from the Caribbean. I. Gametogenic activity, growth,
mortality and production of a natural population. Aquaculture
189:361–373.
Walne, P. R. & R. Mann. 1975. Growth and biochemical composition in
Ostrea edulis and Crassostrea gigas. In: H. Barnes, editor. 9 th
European marine biology symposium. Scotland. Aberdeen Univer-
sity Press. pp. 587–607.