Reproductive Strategies of the Eastern Oyster Crassostrea virginica (Gmelin 1791) in Tropical Lagoons of the Mexican Gulf of Mexico

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REPRODUCTIVE STRATEGIES OF THE EASTERN OYSTER CRASSOSTREA VIRGINICA

(GMELIN 1791) IN TROPICAL LAGOONS OF THE MEXICAN GULF OF MEXICO

DALILA ALDANA ARANDA,1* MARTHA ENRIQUEZ DIAZ,

1FABIOLA LANGO REYNOSO,

2

THIERRY BRULE,1JORGE MONTERO

1AND ERICK BAQUEIRO CARDENAS

1

1CINVESTAV IPNMerida, Biology and Aquaculture of Mollusks, Km 6 Antigua Carretera a Progreso,Merida, Yucatan, Mexico; 2Instituto Tecnologico de Boca del Rıo, Carretera Veracruz, Cordoba Km 12,Apdo. Postal 68, Boca del Rıo, Veracruz 94290, Mexico

ABSTRACT The oyster fishery is 1 of the most important coastal fisheries inMexico.Management is based on aminimum legal

size of 80 mm and several seasonal bans that vary along the coast of the Gulf ofMexico.We describe the gonad development cycle

of Crassostrea virginica (Gmelin 1791) along the Mexican coast of the Gulf of Mexico for 5 lagoons for the years 2000 and 2004,

between latitudes 21�41’16.75‘‘ N and 18�23’51.08’’ N. Significant differences in duration and intensity were observed among

reproductive stages associated with different environmental conditions. Gametogenesis and mature stages correlated positively

with temperature and total chlorophyll, respectively. Spawning correlated negatively with salinity in both years. Maturity

correlated positively with total chlorophyll levels. The reproductive stages varied from seasonal, a few months, to continuous

throughout the year. Recovery, expressed as the number of organisms in postspawning and resting stages, was fast for populations

that presented constant gametogenesis and spawning, with less than 50% of the population in postspawning and resting stages.

Environmental fluctuations in total chlorophyll are the regulating factors for gametogenic activity, rather than latitudinal

temperature variations. This makes monitoring environmental conditions in the lagoons or gonad development a necessity to

predict reproduction and recruitment for proper management of the oyster resource.

KEY WORDS: gonad development, eastern oyster, environmental temperature

INTRODUCTION

Crassostrea virginica (Gmelin 1791) is a resource from theGulf of Mexico coast of economic and social importance. In

Mexico, its production reached 40,768 tons in 2010; however,since the 1990s, catch volume has declined as a result ofoverexploitation. Production is based on natural beds, tradi-

tional farms, and enhanced beds. It is an important source ofsocial employment, with more than 5,169 fishers and 10,000shuckers employed, the latter of which consists mainly of

women. Management of the oyster fishery in Mexico is basedon a minimum legal size of 80 mm and temporal bans fromApril 15 to May 31, and from September 15 to October 31,based on population structure and abundance, along the coastal

states of the Gulf of Mexico.Walker and Heffernam (1994) demonstrated that tempera-

ture and salinity, associated with latitude, regulate the intensity

and duration of gametogenesis in Mercenaria mercenaria. Theeffect of environmental factors on the reproduction of Crassos-trea virginica has been determined by Loosanoff (1942), Durban

(1960), Shaw (1962), Kennedy and Battle (1964), Ropes (1965,1979)AU1 , Langton (1987)AU2 , Goulletquer et al. (1994), Kennedy et al.(199AU3 6), Baqueiro Cardenas and Aldana Aranda (2000), and

Aldana Aranda et al. (2003). These authors have shown that thereproductive cycles are determined by local environmentalconditions within the same latitude, particularly for specieswith a wide distribution range, such as C. virginica. Further-

more Cox and Mann (1992) explained differences in spawningand fecundity seasonality, intensity, and duration resultingfrom variations in size and parasitism. Therefore, species with

a wide distribution present a reproductive pattern with alter-ations imposed by environmental variables (Sastry 1979),

showing different reproductive tactics and variations in the

behavior of the reproductive cycle, given the prevailing envi-ronmental conditions, within a genetically defined reproductivestrategy (Wootton 1984).

Coastal lagoons in the Gulf of Mexico are subject tovariations in salinity and temperature, with changes in organicmatter and pollutant concentrations (Botello et al. 2004). These

factors are critical for total chlorophyll and gonad developmentin oysters (Kennedy et al. 1996). The reproductive cycle ofCrassostrea virginica has been studied throughout its range;however, most studies have been conducted along the north

Atlantic coast (Kennedy & Battle 1964, Barber 1996, Wilsonet al. 2005). The eastern oyster C. virginica has a latitudinalrange from 51�N, Saint Lawrence, Canada, to 1�Nof the coast

of Brazil, encompassing a wide range of biogeographical andecological conditions (Buroker 1983). However, few studieshave been carried out in tropical zones (Baqueiro Cardenas

et al. 2007, Arias De Leon et al. 2012). Bivalves living in tropicalregions generally show continuous and asynchronous repro-duction (Lubet & Mann 1987, Baqueiro Cardenas & AldanaAranda 2000). Maturation of the broodstock is controlled by

both endogenous and exogenous factors; among the latter,temperature and food are the most important (Mann 1979,Sastry 1979, Muranaka & Lannan 1984, Barber & Blake 2006).

Arcos et al. (2009) studied an enzyme-linked immunosorbentfor Crassostrea corteziensis to assess the degrees of gonadmaturity in relation to different diets and environmental

conditions. Galtsoff (1964) and Arias De Leon et al. (2012)demonstrated that Crassostrea virginica shows a conservativereproductive tactic, with the accumulation of reserves during

the cold season and its use in another season to supportgametogenesis. Arias De Leon et al. (2012) observed peaksin the gonadosomatic condition index that coincided withthe lowest salinity. The purpose of the current study was to

assess the reproductive tactics adopted by C. virginica and to*Corresponding author. E-mail: [email protected]

DOI: 10.2983/035.033.0100

Journal of Shellfish Research, Vol. 33, No. 1, 1–8, 2014.

1

determine its relationship with environmental parameters in thetropical lagoons along the Mexican Gulf coast of Mexico in two

separate years.

MATERIALS AND METHODS

FigureF1 1 shows the different lagoons where oyster beds were

studied. For the state of Veracruz, samples came from theTamiahua (21�41’16.75’’ N) and Vega de Alatorre lagoons. Forthe state of Tabasco, samples came from the Carmen,

Machona, and Mecoacan lagoons (18�23’51.08’’ N). Theselagoons were selected given their importance in regional oysterproduction. Although these lagoons are on the same coast, they

are subjected to different salinities and temperature rangesbecause of the differential freshwater runoff.

All analyses are based on histological sections of the visceralmass, which includes gonad tissue, the digestive gland, and

sections of the digestive tract. Thirty organisms were sampledfrom each site each month during the years 2000 and 2004 (n ¼3,600 oysters analyzed). Monthly samples were preferred given

the extent and distance between lagoons (1,500 km) and oysterbeds, favoring bank location over sampling frequency.

All organisms for the histological analysis measured 60–70

mm in shell length. Hematoxylin–eosin stain was used for allanalyses (Luna 1968). The reproductive cycle is based on thepractical scale of Lucas (1965), who divided gonad development

into five stages: I, resting, only germinal epithelium can bedetected among connective tissue; II, gametogenesis, cleardevelopment of gametes is seen with a dominance of immaturegametes; III, mature, dominance of mature gametes, ova, or

sperm fill the follicles, which appear anastomosed and compact;IV, spawning, follicles appear partially empty and broken; V,postspawning, follicles are empty and broken, and phagocytes

are abundant in the connective and gonadal tissues. Surfacetemperature, salinity, and total chlorophyll were recorded witha multiparameter probe (YSI 6600, Yellow Springs, OH) when

samples were collected. Univariate analysis of variance(ANOVA) was used to establish the significance in the observeddifferences of occurrence of the reproductive stages. Themedian differences between ranking factors (Lagoons) were

analyzed using the Kruskal–Wallis nonparametric statisticalranges test, which uses statistical distribution as the value of Hin the hypothesis test provides a robust test against the problems

of asymmetry, kurtosis, and heteroskedasticity, which affectparametric tests such as ANOVA AU4(Sokal & Rohlf 1995).

Pearson�s correlation was performed on the five reproductivestages with temperature, salinity, and total chlorophyll. Corre-lations among reproductive stages and the environmentalparameters were carried out using a redundancy analysis (Van

den Wollenberg 1977). Dissimilarity of reproductive stagesamong lagoons was evaluated with PERMANOVA, a non-parametric variance analysis, represented by nonmetric dimen-

sional scaling, using 999 permutations (Anderson 2001). Theresults from this analysis were compared graphically with thedaily effect of temperature through a generalized additivemodel

using a quasi-Poisson distribution. This was achieved by usingthe vegan package (Okasanen et al. 2012) for R statisticalsoftware (R Development Core Team 2012).

RESULTS

Mean maximum and minimum values of temperature,

salinity, and chlorophyll for the lagoons are presented in T1Table 1.Mean monthly temperatures are shown, obtained from dailyrecords for the 5 lagoons during 2000 and 2004. Temperature was

lower during 2000 than in 2004 for all 5 lagoons. Mean tempera-tures fluctuated between 25.14�Cand 25.47�C in 2000, and between26.40�C and 26.44�C for 2004. Mean salinities fluctuated from

24.3–33.3 PSU.Environmental conditions for theVeracruz lagoonsare similar in mean temperature and salinity. The environmentalconditions for the Tabasco lagoons differ from the Veracruzlagoons and Vega de Alatorre lagoon, and had the highest total

chlorophyll level (chlorophyll varied from 12.6–85.0 mg/m3/h).

Reproductive Cycle

The reproductive cycles for oysters from the Tamiahua,Vega de Alatorre, Carmen, Machona, and Mecoacan lagoonsare shown in F2Figure 2 for the year 2000, and in F3Figure 3 for 2004.

Resting

The resting stage during 2000 and 2004 varied from a min-imum of 5% of the sampled population at Tamiahua lagoonduring January 2000 to a maximum of 80% for the Carmen and

Machona lagoons, with peaks during March and April andNovember and December for both years. In contrast, this stagewas constant and intense for the Tabasco lagoons, and almost

nonexistent for the Veracruz lagoons (Figs. 2A and 3A).

Gametogenesis

Two different types of behavior were identified duringgametogenesis. Oysters from the Veracruz lagoons showed

similar behavior during both years, presenting constant game-togenic activity, with two peaks of up to 40% in January andAugust for Tamiahua lagoon, and July and September for Vega

Alatorre lagoon. Well-defined, seasonal gametogenic activitywas seen from February to June by up to 50% of the sampledoyster populations from the Tabasco lagoons, except for oystersfrom Mecoacan lagoon during 2000, when gametogenesis was

constant in a high percentage of the population throughout thewhole year (Figs. 2B and 3B).

Maturity

The presence of the mature stage varied from constant andintense in the Veracruz lagoons to minimal and seasonal in the

Figure 1. Coastal lagoons of the Gulf of Mexico for the reproductive

studies of Crassostrea virginica included in this analysis. 1, Tamiahua

lagoon; 2, Vega de Alatorre lagoon, Veracruz; 3, Carmen lagoon; 4,

Machona lagoon; 5, Mecoacan lagoon, Tabasco.

ALDANA ARANDA ET AL.2

Tabasco lagoons. For the latter, intensity varied between years,from a high percentage (up to 50%) for 6 mo during 2000between June and November, to just less than 30% fromMarchto May 2004 (Figs. 2C and 3C).

Spawning

Spawning was observed throughout the year for the twolagoons of Veracruz, with higher frequency peaks during

March, June, September, and November, and with a lowerpercentage for Mecoacan lagoon. Spawning was seasonal forthe sampled population from the lagoons of Carmen andMachona, extending from June to November both years (Figs.

2D and 3D).

Postspawning

Postspawning was registered throughout the year in oysters

from both the lagoons in Veracruz and from Mecoacan,Tabasco. The intensity and duration were similar for both yearsin organisms from the Veracruz lagoons, but was much more

intense during 2004 in theMecoacan lagoon. For the lagoons ofCarmen and Machona, postspawning was seasonal, with anaverage of 26% of the organisms during 2000 from June toDecember, and more than 50% during 2004, extending from

July to November (Figs. 2E and 3E).

Nonparametric statistical analysis

Figures F44 and F55 show the results of the Kruskal-Wallis testbetween the median number of the reproductive stages amongsites during 2000 and 2004 (n¼ 1,800 individuals for each year).

For both years, the resting andmature stages showed significantdifferences (P < 0.0001), whereas spawning (H ¼ 10.60, P ¼0.025) and postspawning (H ¼ 4.69, P < 0.30) did not.

Gametogenesis was significantly different during 2000 (H ¼15.75, P < 0.0028) but not during 2004 (H ¼ 5.16, P < 0.242).The mature and resting stages were significantly differentbetween oysters from the northern lagoons compared with

those from the southern lagoons for both years. Pearson�s

TABLE 1.

Mean, maximum (max), and minimum (min) temperatures (n$ 24), salinities (n$ 24), and total chlorophyll (n$ 24) measured forthe different tropical lagoons of the Gulf of Mexico, Mexico, for 2000 and 2004AU15 .

Lagoon

2000 2004

Temperature (�C) Salinity (UPS)

Chlorophyll

(mg/m3/h) Temperature (�C) Salinity (UPS)

Chlorophyll

(mg/m3/h)

Min Max Mean Min Max Mean Min Max Mean Min Max Mean Min Max Mean Min Max Mean

Tamiahua 16.29 33.29 23.98 20.3 31.5 24.9 25.3 25.3 25.3 22.87 31.88 24.44 20.4 36.2 26.6 24.8 28.1 25.2

Vega Alatorre 15.50 32.65 24.00 7.0 32.2 27.1 25.7 60.5 36.5 15.30 31.59 24.65 — 33.0 31.4 30.0 85.0 44.8

Carmen 17.55 32.84 25.14 31.1 31.1 31.1 18.8 18.8 18.8 26.10 29.90 26.40 27.2 35.0 31.1 18.8 25.4 22.1

Machona 18.00 32.00 25.10 30.0 39.0 33.2 15.4 15.4 15.4 24.00 31.00 26.70 30.0 39.0 33.3 4.7 22.8 15.4

Mecoacan 19.85 32.34 26.44 7.0 36.0 25.5 15.4 15.4 15.4 26.20 29.00 25.47 7.0 38.0 24.3 6.7 21.4 15.4

Figure 2. Comparative reproductive tactics of Crassostrea virginica in

2000, from 5 Mexican lagoons of the Gulf of Mexico, obtained by

histological sampling. (A) Tamiahua. (B) Vega Alatorre. (C) Carmen. (D)

Machona. (E) Mecoacan.

Figure 3. Comparative reproductive tactics of Crassostrea virginica in

2004, from 5 Mexican lagoons of the Gulf of Mexico, obtained by

histological sampling. (A) Tamiahua. (B) Vega Alatorre. (C) Carmen. (D)

Machona. (E) Mecoacan.

REPRODUCTION OF EASTERN OYSTER IN TROPICAL LAGOONS 3

correlation showed a positive correlation between gametogen-esis and temperature for oysters in 2000, but not for 2004(TableT2 2).

Redundancy Analysis

FigureF6 6 presents the results of the redundancy analysisbetween the frequency of the reproductive stages for Crassos-

trea virginica and monthly environmental parameters (n ¼ 360,corresponding to 120 values for each environmental parameter)for the 5 lagoons during 2000 and 2004. Oysters from the

Mecoacan, Carmen, and Machona lagoons presented differentreproductive tactics from those in the Tamiahua and Vega deAlatorre lagoons. During 2000, a test of significance of the firstcanonical axis resulted in an eigenvalue of 0.227, an F ratio of

14.385, and a P value of 0.002. The best predictor for thereproductive stagesmature and spawning was total chlorophyll,which accounted for 90.2%of the total inertia notedAU5 (F¼ 8.201,

P ¼ 0.01). Total chlorophyll was also associated with oystersfrom the Tamiahua and Vega Alatorre lagoons. Oysters fromthe Carmen, Machona, and Mecoacan lagoons showed a re-

productive tactic in which the resting stage was dominant.Correlations between the original variables and canonicaldiscriminant axes were as follows: resting, 0.60; gametogenesis,

0.28; mature, 0.39; spawning, 0.51; and postspawning, 0.50. Thecumulative percentage variance was 89.6%, confirming the

variation present among lagoons along theMexican Gulf coast.During 2004, the values for the first canonical axis were an

eigenvalue of 0.347, an F ratio of 17.891, and a P value of

0.0001. The best predictor for the reproductive stages matureand spawning was total chlorophyll for oysters from theTamiahua and Vega Alatorre lagoons, which accounted for

49.7% of the total inertia noted AU6(F ¼ 2.56, P ¼ 0.041). Incontrast, Carmen, Machona, and Mecoacan oysters presentedbehavior contrary to those located in the north, where theresting stage was dominant. The correlations between the

original variables and canonical discriminant axes were asfollows: resting, 0.51; gametogenesis, 0.96; mature, 0.71; spawn-ing, 0.99; and postspawning, 0.85. The cumulative percentage

variance was 90.5%, confirming the variation among lagoons.

Generalized Additive Model

Figure F77 shows the results of a generalized additive modelusing the daily effect of temperature (n ¼ 3,650, correspondingto corresponding to daily temperature for 365 days for 5 sites

Figure 5. The Kruskal-Wallis test results for the median number of the

different reproductive stages of Crassostrea virginica for 2004 among the

sampled sites. (A) Resting stage. (B) Gametogenesis. (C) Mature. (D)

Spawning. (E) Postspawning. 1, Tamiahua; 2, Vega Alatorre; 3, Carmen;

4, Machona; 5, Mecoacan. *Significant difference among treatments.

Figure 4. The Kruskal-Wallis test results for the median number of the

different reproductive stages of Crassostrea virginica for 2000 among the

sampled sites. (A) Resting stage. (B) Gametogenesis. (C) Mature. (D)

Spawning. (E) Postspawning. 1, Tamiahua; 2, Vega Alatorre; 3, Carmen;

4, Machona; 5, Mecoacan. *Significant difference among locations.

ALDANA ARANDA ET AL.4

and for the 2 y studied) through the stages of the reproductivecycle of oysters from 5 lagoons in the year 2000 (Fig. 7A) and2004 (Fig. 7B). The lagoons present differences in the compo-sition and frequencies of the reproductive stages. For the year

2000, (df ¼4.43, F ¼ 6.975, P ¼ 0.001) and for 2004 (df ¼ 4.41,F ¼ 7.0494, P ¼ 0.001), the differences among reproductivestages are explained by temperature. For the year 2000, r2 was

35.8% (P¼ 0.02); for the year 2004, r2 was 61.1% (P < 0.0001).For the 2 y studied, it was observed that sites that had warmer

temperatures, including the Carmen and Mecoacan lagoons,were associated with the resting stage. In contrast, the VegaAlatorre and Tamiahua lagoons had colder temperatures andwere associated with the maturity stage.

DISCUSSION

The duration of each stage—in particular, the postspawning,

resting, and gametogenesis stages—and the percentage of thepopulation in each are indicators of the regeneration capabil-ities of the population. A greater percentage of organisms at

these stages for a longer period of time are the result of low totalchlorophyll, taking the population longer to recover froma previous spawning. Gametogenesis lasting for a short timein a small percentage of the population, preceding intense

maturity and/or spawning, in a greater percentage of the pop-ulation indicates rapid gonad recovery (Baqueiro Cardenas &Aldana Aranda 2000, Aldana Aranda et al. 2003). Bayne

et al. (1976) classified molluscs depending on the energy sourcefor reproduction. ‘‘Conservatives’’ are those that store energy intheir tissues and use it for reproductive processes, independent

of food availability in the environment; ‘‘opportunistic’’ arethose that take advantage of food availability for reproductiveprocesses, with little impact on body reserves. Glycogen plays

TABLE 2.

Pearson correlation between average of environmental pa-rameters and rest, gametogenesis, maturity, spawn, and

postspawn stages for oysters in 2000 and 2004.

Year Variable

Temperature Salinity Productivity

r P value r P value r P value

2000 Gametogenesis 0.79 0.11 0.75 0.14 –0.43 0.47

Mature 0.23 0.71 –0.28 0.65 0.85 0.07

Spawn –0.79 0.11 –0.63 0.25 0.16 0.80

2004 Gametogenesis 0.32 0.61 –0.62 0.27 –0.55 0.34

Mature –0.10 0.88 –0.45 0.45 0.62 0.26

Spawn –0.40 0.51 –0.74 0.15 0.17 0.78

Figure 6. (A, B) Redundancy analysis between frequency of reproductive

stages of Crassostrea virginica and environmental parameters for the 5

tropical lagoons of the Gulf ofMexico for oysters sampled in 2000 (A) and

2004 (B). I, resting stage; II, gametogenesis stage; III, mature stage; IV,

spawning stage; V, postspawning stage.

Figure 7. (A, B) A generalized additive model using the daily effect of

temperature through the stages of the reproductive cycle of Crassostrea

virginica from 5 locations in the year 2000 (A) and 2004 (B). I, resting

stage; II, gametogenesis stage; III, mature stage; IV, spawning stage; V,

postspawning stage.

REPRODUCTION OF EASTERN OYSTER IN TROPICAL LAGOONS 5

a central role in energetic and metabolic supply of gametogen-esis in many bivalves (Gabbott 1975, Bayne et al. 1982, Ruiz

et al. 1992, Mathieu & Lubet 1993).It is generally accepted that the gametogenic cycle in bivalves

is linked closely to the seasonal cycle of storage and use ofglycogen reserves. Several authors have reported maximum

glycogen content immediately preceding and during gameteproliferation (Ansell 1972, Ansell et al. 1980, Barber & Blake1985, Chavez-Villalba et al. 2003). Our results show that

reproductive tactics of Crassostrea virginica were dependenton prevailing environmental conditions. A well-defined matu-rity stage in a large percentage of organisms represents an

accumulation of mature gametes, which frequently precedesa massive, synchronized spawning event. On the other hand,this stage may not be evident, which generally coincides withprolonged spawning in a small percentage of the population.

These 2 types of behavior are associated with the environmentalfactors that induce spawning, and are highly correlated withrecruitment processes (Lucas 1965). Ruiz et al. (1992) studied

the effect of temperature, salinity, and total chlorophyll onthe condition, reproductive activity, and biochemical com-position of Crassostrea gigas. Their results showed 2 spawn-

ing periods—the first coinciding with the predicted time ofmaturation (June to July) and a second that occurred witha major phytoplankton bloom. They observed glycogen

accumulation followed by a period of gametogenesis andrelated lipid biosynthesis during vitellogenesis with glycogenbreakdown. They also observed high variation in carbohy-drate levels during storage and gametogenic development,

suggesting that carbohydrates were the main respiratorysubstrate. In contrast, proteins and lipids were importantfor supporting energetic requirements during winter when

food was scarce.Didri et al. (2007) observed seasonal variations in the

biochemical composition of Crassostrea gigas in the Bizert

lagoon, Tunisia, in relation to environmental conditions andthe reproductive cycle, with a clear cycle of energy storage anduse during which lipid and glycogen concentrations in thegonad–visceral mass were inversely related. The increase in

total fatty acid values appeared to be related to an increase inthe chlorophyll concentrations and high protein levels, whichcorresponded to oocyte maturation and then decreased with

spawning, at the expense of the available food in autumn. Thisstudy demonstrated that variations in reproductive tactics aredependent on environmental conditions, rather than being

a species characteristic.Differences in gametogenic activity may be attributed to

variations in environmental factors among lagoons. A shorter

gametogenic period in a greater percentage of the populationleads to a clear maturity stage, as a consequence of higher totalchlorophyll. From the patterns of reproductive tactics forCrassostrea virginica, it is demonstrated that this species varies

from seasonally synchronous in Long Island Sound to contin-uous in Florida, as reported by Loosanoff (1968) and Walkerand Heffernam (1994) forMercenaria mercenaria. Sastry (1970)

showed a latitudinal effect on the reproductive physiology ofthe scallop Aequipecten irradians. Chavez-Villalba et al. (2002)reported that the duration of the gametogenic cycle in Crassos-

trea gigas and, in particular, the duration of the spawningperiod are influenced directly by geographical latitude, affectingthe temperature of the area.

According to Laruelle et al. (1994) and Fabioux et al. (2005),temperature has a positive effect on gametogenesis in Ruditapes

decussatus, which may affect the metabolic rate of the animaldirectly, or affect the availability of food indirectly, because themaximum rate of increase in weight occurs during the spring,when both the water temperature and chlorophyll a increase

rapidly. We identified two general tactics in spawning behavior:(1) seasonal and synchronous, and (2) continuous and asyn-chronous. The results from this study show that temperature

correlates highly with gametogenesis, and salinity fluctuationspresent a low correlation with different stages of the reproduc-tive cycle. Cherkasov et al. (2007) studied the combined effects

of temperature and exposure to the toxic metal cadmium onhemolymph in relation to immune defense and metal transportin Crassostrea virginica. They observed a significant increase inthe percentage of apoptotic hemocytes with elevated tempera-

ture (28�C), supporting the idea that 28�C is stressful physio-logically for this species. They also reported strong effects ofenvironmental temperature on hemocyte viability and metal

transport capability. Pollutants are a factor that was not takeninto consideration for the current study, and might play animportant role in the reproductive tactics identified in the

lagoons studied, resulting from different concentrations ofpollutants (Botello et al. 2004, Villanueva & Botello 1998).

The maturity and spawning stages correlated to total

chlorophyll levels. The shorter and seasonal spawning at Vegade Alatorre lagoon is associated with changes in salinity.Environmental fluctuation in total chlorophyll is the regulatingfactor for gametogenic activity, rather than latitudinal temper-

ature variations. Rodrıguez Jaramillo et al. (2008) AU7founda negative correlation between chlorophyll a content and gonadcoverage area inmale and femaleCrassostrea corteziensis. Daily

and seasonal fluctuations in temperature imply a physiologicalstress in membrane adaptations (Lannig et al. 2006, Pernet et al.2007). Arias De Leon et al. (2012) AU8reported differential re-

productive activity in oysters for the lagoons of Tamiahua andVega de Alatorre, and among beds within the lagoons de-termined by temperature.

Baqueiro Cardenas and Aldana Aranda (2000) reported

reproductive tactics for different bivalves along the Pacific andGulf of Mexico coasts, showing that environmental conditionsdetermine the duration and intensity of each reproductive stage.

Food availability is a major determining factor for gonadrecovery and maturation (Soniat & Ray 1985, ContrerasEspinosa et al. 1994). Jouaux et al. (2013) observed that food

deprivation during preconditioning in Crassostrea gigas led toreduced gonial proliferation as a result of lower proliferatingcell nuclear antigen (PCNA) expression, leading to a significant

reduction in reproductive effort Franco et al. (2010) reportedthe expression of PCNA associated with the proliferation ofreproductive cells in the gonadal area of oysters, and confirmedthat gonial mitosis increases under high food conditions,

accompanied by total depletion of storage tissue. These resultsconfirmed the close relationship between energy reserves andgametogenesis (reinitiation, timing, and reproductive effort)

and demonstrated the presence of a regulated balance betweenstorage and reproductive pathways. In the current study,oysters from lagoons with low total chlorophyll levels exhibited

a slow recovery of gonads and a minimum maturity stage.For those lagoons in which conditions are stable throughout

time, gonad recovery was slow, with a minimummaturity stage,

ALDANA ARANDA ET AL.6

and associated with low total chlorophyll levels. Faster gonadrecovery was found for sites with a greater nutrient content, as

shown by beds from Tamiahua lagoon. Haunert (2005) de-scribed the effect of water quality on oyster reproduction.Synchronous spawning was detected where wide fluctuationsin salinity were recorded. O�Beirn et al. (1998) and Gullian and

Aguirre Macedo (2009) demonstrated that Crassostrea virginicaexposed to fluctuating environmental conditions experience greatergametogenic variations, implying different reproductive tactics

within the same bed at different tidal levels. Therefore,C. virginicaalong the Gulf coast of Mexico behaves as both conservative andopportunistic. When conditions are homogeneous and food

availability is regular, oyster populations assume the conservativetactic, but when conditions change throughout the year or foodavailability is irregular, they adopt the opportunistic tactic.

It is interesting to note that the reproductive behavior for

oyster populations from the Tamiahua and Vega de Alatorrelagoons from Veracruz, and Mecoacan, Tabasco, was similar

despite being located far apart, emphasizing the effect ofprevailing environmental conditions on the reproductive tactic

adopted. This makes monitoring environmental conditions inthe lagoons or gonad development a necessity to predictreproduction and recruitment for a proper management of theresource.

ACKNOWLEDGMENTS

This study was supported by projectsM0034-2008-02/109498‘‘Diagnostico biologico-pesquero y sistema de informaciongeografico del recurso ostion de las lagunas de Veracruz para

su uso, ordenamiento y manejo sustentable’’ and COSNET1252.01 (Consejo del Sistema Nacional de Educacion Tecno-logica of Mexico). Thanks to Teresa Colas and Irma Perez forsupport in histological processing, and Gemma Franklin,

a native English speaker, for reviewing this manuscript. Thanksto anonymous reviewers.

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