Relation of seasonal changes in the mass of the gonad and somatic tissues of the zebra ark shell Arca zebra to environmental factors.

ABSTRACT Over the period from June 2002 to June 2003, we examined the relationship of seasonal changes in the mass of the gonad and somatic tissues to environmental factors for four size groups of the zebra ark shell Arca zebra at Chacopata, in northeastern Venezuela. The gonads of A. zebra began to increase in size when individuals attained 18-20 mm in shell length, but maximum gonad mass relative to somatic mass was only attained at 55-60 mm in length. Large individuals (>50 mm) showed a distinct annual reproductive cycle with a marked increase in gonad mass from July to late September 2002, coinciding with the increase in temperatures related to stratification of the water column. A decrease in gonad size occurred during October 2002 through January 2003 and coincided with a temperature decline related to renewed upwelling. The mass of somatic tissues was highest between late August to late December 2002, coinciding with the reproductive period and elevated temperatures. Other environmental factors showed little seasonal variation, although chlorophyll a concentration was lowest during the major period of increase in the gonad and somatic tissues (July to late September 2002), suggesting that the animals were not limited by the abundance of phytoplankton food. A. zebra seemed to be well adapted to the high loads of inorganic seston found in the Chacopata region.

KEY WORDS: reproduction, bivalve Arca zebra, Venezuela, temperature

INTRODUCTION

Both environmental factors and endogenous processes control reproductive activities in marine bivalves (Bernard 1983, Griffiths and Griffiths 1987, Thompson and MacDonald 1991). Temperature, which affects rates of many physiological processes, is the environmental factor that is most often indicated to influence reproduction in marine invertebrates (Kinne 1970). In many species, particular gametogenetic phases are associated with specific temperature conditions, and temperature changes have been indicated to stimulate maturation and spawning (Giese & Pearse 1974, Roman et al., 2001). Another important environmental factor is food availability. Energetic costs for reproduction (which are usually high) depend on food ingested, or on reserves built up during periods of high food availability (Bayne & Newell 1983, Barber & Blake 1991). Many studies have examined how reproductive activities are related to food availability, stored reserves and various environmental factors (particularly temperature and salinity) in temperate bivalve species (Mackie 1984). However, we have a much poorer understanding of such relationships in tropical species because far fewer studies have been made of tropical species (Lodeiros & Himmelman 2000).

In this study we examine changes in the mass of the gonads and somatic tissues of the tropical zebra ark shell Arca zebra (Swainson, 1833) throughout a year and relate the changes to environmental factors. A. zebra, which commonly forms dense beds on rocky bottoms between 1 and 20 m in depth, is distributed along western shores of the Atlantic Ocean from North Carolina and Bermuda to Brazil (Lodeiros et al. 1999). A large natural bed of ark shells occurs in the region of Chacopata, on the Araya Peninsula, in northeastern Venezuela. This bed covers an area of 70-80 [Km.sup.2] and has been intensively harvested by local fishermen for over 25 y. About 40,000 tons are harvested per year and the income provided is second to that of the sardine in Venezuelan artisanal fisheries (Mendoza 1999, Lodeiros et al. 2005). A. zebra is a protandric hermaphrodite, with individuals measuring 30-65 mm (anterior-posterior axis) being predominately male, 65-80 mm individuals being male or female in equal numbers and >80 mm individuals being predominately female (Nakal 1979, Garcia 1987). The gonads are undeveloped in 20-30 mm individuals. Gametogenesis appears to be continuous, but there are peaks in July, October and March (Mora 1985, Alvarez 1992, Saint-Aubyn et al. 1992). Relationships between the reproductive cycle and environmental changes have not been previously examined. Knowledge of such relationships is needed to develop methods for producing ark shells in a hatchery. Further, an understanding of seasonal cycles in somatic and gonad tissues is required to develop a rational strategy for the management of the arc shell fishery.

MATERIAL AND METHODS

At monthly intervals from June 2002 to July 2003, we collected samples of ark shells A. zebra from 3-4 m in depth from the natural bed at Chacopata (longitude between 63046' and 63054' and latitude between 10[degrees]42' and 10[degrees]46'). Each sample was transported (for a period of 40-60 min) in insulated boxes (at 5[degrees]C to 8[degrees]C to prevent spawning) to the Centro de Investigaciones Ecologicas de Guayacan (Universidad de Oriente) where the animals were dissected.

In the laboratory, we divided the bivalves into four groups, based on shell length (anterior-posterior axis); 10-30 mm, 30-50 mm, 50-70 mm and 70-90 mm. We analyzed 20 individuals for each size group. For each ark shell, we first removed the byssus and secondly removed epibionts and detritus from the shells. We then dissected the bivalve into three components, shell, gonad and somatic tissues. The gonad and somatic tissues were dried at 60[degrees]C for 72 h prior to recording their dry mass. The mass of the gonad as a percentage of the mass of the somatic tissues was calculated as a gonad index.

At weekly intervals, we also took three water samples just above the beds (at 3-4 m depth) with a 5-1 Niskin bottle. From each sample we first took subsamples for determinations of the oxygen concentration (Winkler method) and salinity (induction method). Then the sample was passed through a 280-[micro]m filter to remove macroplankton. Finally, samples were taken for determinations of the chlorophyll a concentration (using the spectrophotometric method, Strickland & Parsons 1972) and of the mass of organic and inorganic materials in the seston (gravimetric method). A Sealog thermograph (Vemco Ltd., Halifax, Canada) was placed on the bottom and set to record the temperature at 10-min intervals. As the thermograph only functioned from July to December 2002, we also obtained estimates of surface temperatures from satellite images that were available from the Institute of Marine Remote Sensing of the University of South Florida, USA (http:// imars.usf.edu/sst/index_rm.html). We calculated mean temperatures for intervals of three days (including night and day images, but excluding cloudy period). These images were obtained with advanced very high resolution radiometer (AVHRR) sensors on a NOAA satellite.

From these images, sea surface temperature was extracted using the closest pixel to our study site. A time series of sea surface temperature was created, which was low pass filtered using of moving average with a window of three. When a cloud covered the pixel corresponding to our study site, we used the average of two pixels upstream and two downstream from our site (the mean current goes from east to west) and when this approach wasn't suitable, a gap was left. Finally, we fitted all data using the MATLAB cubic splineinterpolation function (a commercial package produced by Mathsoft; www.mathsoft.com).

For the mass of the gonad and somatic tissues of each of the four size groups we first applied a 1-way ANOVA to test for variations in size over time, and then followed with a posteriori Duncan tests to identify the periods when significant (P < 0.05) changes occurred.

RESULTS

Each of the four size groups of ark shells A. zebra showed changes in somatic tissue mass and gonad mass over time (one factor ANOVAs, P < 0.05). The seasonal changes in somatic tissue mass were greatest for the two larger size groups that measured 50-70 mm and 70-90 mm in shell length, respectively (Fig. 1). The mass increased from late June through September 2002, decreased sharply in October 2002 (ANOVA, Duncan test, P < 0.05), increased in over the next 2-3 mo and then decreased again during January to February 2003. After this decrease values remained low until the last month of our study (late May to late June 2003) when another increase occurred. The somatic tissue mass of 30-50 mm individuals often showed a different pattern. For example, there was a significant decrease during the first month of the study and no decrease in the last month (Duncan test, P < 0.05, P > 0.05, respectively). However, a decrease did occur during January 2003 (Duncan test, P < 0.05), which coincided with the decrease in the largest size groups. Finally, the smallest group, individuals measuring 10-30 mm, showed much less variation in tissue mass than the larger individuals.

[FIGURE 1 OMITTED]

The gonad mass of the two largest groups of ark shells, measuring 50-70 mm and 70-90 mm in shell length, respectively, increased rapidly during the first months of the study to a peak in late September 2002, and then a major decrease occurred during October 2002 through January 2003 (Fig. 2). After this decrease, the gonads remained small until the last month (June 2003) when renewed growth occurred. Surprisingly, the gonad mass was similar for 50-70 mm and 70-90 mm individuals (ANOVA, P > 0.05) on most sampling dates. As a result, relative gonad mass to somatic tissue mass (the gonad index) was usually greater for 5070 mm individuals than for 70-90 mm individuals (Fig. 2, ANOVA, Duncan test, P < 0.05), especially in the period of major reproductive activity. Gonad mass of the two smallest groups of ark shells, measuring 10-30 mm and 30-50 mm, respectively, was always small (Fig. 2). Nevertheless, the relative gonad mass of 30-50-mm individuals showed seasonal variations, and the values during the last three months of our study were similar to those of larger (>50 mm) individuals. The gonad index of 10-30 mm individuals was negligible until February 2003, but then the values increased and followed a pattern similar to that in larger animals (with a marked increase during the last two months, May and June 2003).

[FIGURE 2 OMITTED]

The relation of gonad mass and the gonad index (gonad mass as a percentage of somatic tissue mass) to shell length for all individuals collected during our study provided information on the size at sexual maturity (Fig. 3). Although gonad mass was consistently low in ark shells up to a shell length of about 50 mm, the gonad index increased at 18-20 mm in shell length (up to 32%), indicating the onset of gonad production. Nevertheless, full maturity was not attained until a much larger size. For example, numerous individuals up to 37-mm in shell length had indices near 0%. Individuals measuring greater than 50-55 mm in length appeared to be fully mature, because what they had was wide spread in indices with few individuals with low indices.

[FIGURE 3 OMITTED]

Although the thermograph we placed on the ark shell bed only functioned from July to December 2002, the record was sufficient to show that the temperature record from the NOAA satellite provided a good approximation of temperatures at our study site (Fig. 4). (The satellite data were also similar to values recorded by a thermograph at Turpialito, in the Golfo de Cariaco, 10[degrees]26'56" N; 64[degrees]02'00"; Urbano et al. 2005). Temperatures showed a progressive increase from about 24[degrees]C in July 2002 to a peak near 27[degrees]C in October and November 2002 and this corresponded to the period of stratification of the water column. Then temperatures declined to about 23[degrees]C, indicating renewed coastal upwelling, and the lowest temperature (21.3[degrees]C) was recorded in mid March 2003. After the lowest temperature was recorded, temperatures showed an upward trend until June 2003, although with considerable fluctuations indicating irregular upwelling events.

We did not observe seasonal changes in salinity. Values were generally near the yearly mean (36.7[per thousand]), although increases by up to 1[per thousand] were recorded on a few dates (Fig. 4). Oxygen concentrations were generally high, 3 and 5 mg/L, and the only indication of a seasonal pattern was the slight decrease in oxygen levels between August and December 2002 (Fig. 4).

[FIGURE 4 OMITTED]

The mass of total seston varied from 20-40 mg/L over the study period and showed no distinct seasonal pattern (Fig. 5). An increased variation in values during the last four months of the study coincided with the increased temperature variations during the same period. The mass of organic seston also showed no seasonal pattern, and values only ranged from 5-8 mg/L. The proportion of inorganic seston to total seston was high, generally >70%. The concentration of chlorophyll a (Fig. 5) was usually in the vicinity of 1 [micro]g/L, although sporadic increases to 2.5-5.0 [micro]g/L were recorded. The consistently low values recorded between late July and early November 2002, coincided with the period of high temperatures associated with the stratification of the water column.

[FIGURE 5 OMITTED]

DISCUSSION

The relation of the gonad index to shell length for the A. zebra showed that although the gonads begin to develop at 18-20 mm in shell length, full sexual maturity was only attained at 50-55 mm. The observations of seasonal changes in gonad indices for the four different size groups of ark shells further showed that 10-30 mm individuals had negligible reproductive output, and that 30-50 mm individuals had substantially less output than larger individuals. Individuals measuring 50-70 mm had high reproductive output, because gonad mass was similar to that of 70-90 mm individuals, and relative gonad mass was greater than that of 70-90 mm individuals.

The marked increase in gonad mass of fully mature arc shells (>50 mm) between July and late September 2002 suggested a major period of reproductive activity. This agrees with the reports of Nakal (1980) and Alvarez (1992) that the gonads of both male and female arc shells are in advanced gametogenesic stages during these months. In contrast, Saint-Aubyn et al. (1992) observed that maximum gonad mass of A. zebra during 1991 was in July. Such variations likely reflect interanual differences in environmental factors, particularly factors associated with coastal upwelling, which is driven by the trade winds (Okuda et al. 1978, Lodeiros & Himmelman 2000).

The annual gonad cycle of A. zebra at Chacopata coincided with the seasonal changes in temperature. Both the major gonad increase from July to late September in 2002, and the beginning of a second increase during June 2003, coincided with periods of warming. Also, the decline in gonad mass from October 2002 through January 2003, likely indicating gamete release and decreased gonad production, occurred during declining temperatures. The period of minimal gonad size from February to May coincided with low temperatures. A similar positive association between reproductive activities and temperature is found in two other bivalves in northeastern Venezuela, Perna perna (Velez & Lodeiros 1990) and Lima scabra (Lodeiros & Himmelman 1999). In contrast, in the same region, a negative relationship between reproductive activities and temperature is found in the scallop Euvola ziczac (Lodeiros & Himmelman 2000) and the pen shell Pinna carnea (Narvaez et al. 2000), and there seems to be no association between reproduction and temperature in the bivalves Pinctada imbricata (Jimenez et al., 2000), Nodipecten nodosus (Velez et al., 1987) and Pteria colymbus (Marquez et al., 2000). Such variable relationships between reproductive activities and the annual temperature cycle in same region indicate that the different species have adopted different cues for coordinating gametogenetic events and spawning and likely contrasting strategies for providing energy for reproduction. We predict that a similar diversity of reproductive strategies exists within other invertebrate groups in the region.

The clearly annual reproductive cycle A. zebra was not correlated with other environmental factors, which generally showed little seasonal variation. For example, salinities and oxygen concentrations varied around the annual mean during most of the year. Also, the cycle in the mass of gonad and somatic tissues showed no relationship with food availability. In fact, the major increase in the gonad and somatic tissues in September 2002 coincided with the period of lowest chlorophyll a concentrations and below average levels of organic seston. These observations suggest that A. zebra in the Chacopata region is not limited by food availability. The inorganic content of the seston was always high in the Chacopata region (>70% of total dry seston mass) and a contributing factor could be the resuspension of materials caused by the extensive bivalve harvesting activities using drags (40,000 tons are harvested per year). Inorganic particles are often reported to be detrimental to the feeding of bivalves, because useful food particles can be strongly diluted by nonuseful particles (Riisgard 1988). However, the massive size of the arc shell population in the region, suggests that A. zebra is well adapted to the high levels of inorganic particles. This may be because of its ability to markedly increase its organic intake (by 31%) by selecting food particles, as reported by Ward and MacDonald (1996).

We show that the annual pattern of reproductive activity in A. zebra is positively associated with the temperature cycle, with the increased activity during August to December, which coincides with increased temperatures caused by stratification of the water column. This indicates that control of temperature will be an important in developing methods for producing spat in a hatchery. As the present rules controlling the arc shell fishery only limit harvesting during May to August (Novoa et al. 1998), the stocks are being harvested during the reproductive period. This strategy clearly provides greater tissue mass to the fishery, but it may also limit the production of new individuals. Surprising, an extremely high biomass of arc shells has been taken from the Chacopata bed for more than 25 y. Studies are required to provide insights into the mechanisms permitting this unusually high productivity and sustainability.

ACKNOWLEDGMENTS

The authors thank S. Darriba for critical comments on the manuscript and to N. Velazquez for aid with the sampling and analysis of the bivalves. The study was supported by funding from the Consejo de Investigacion de la Universidad de Oriente and the Fondo Nacional de Ciencia, Innovacion y Tecnologia de Venezuela (FONACIT).

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MARIA LISTA, (1) CESAR LODEIROS, (1) * ANTULIO PRIETO, (2) JOHN H. HIMMELMAN, (3) JULIAN CASTANEDA, (1) NATIVIDAD GACIA (4) AND CARLOS VELAZQUEZ (4)

(1) Instituto Oceanografico de Venezuela, Nucleo Sucre, Universidad de Oriente, Cumana 6101, Venezuela; (2) Dpto. Biologia, Escuela de Ciencias, Nucleo Sucre, Universidad de Oriente, Cumana 6101, Venezuela; (3) Departement de biologie, Universite Laval, Quebec City, Canada GIK 7P4; (4) Centro de Investigaciones Ecologicas Guayacan, Vicerrectorado Academico, Universidad de Oriente, Guayacanm Peninsula de Araya, Edo. Sucre, Venezuela

* Corresponding author. E-mail: [e-mail]