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PHYSIOLOGY OF THE CARIBBEAN SCALLOPS ARGOPECTEN NUCLEUS AND ... physiological rates for the two species were similar except for oxygen ...
Journal of Shellfish Research, Vol. 25, No. 3, 823–831, 2006.

EFFECT OF MICROALGAL CONCENTRATION AND WATER TEMPERATURE ON THE PHYSIOLOGY OF THE CARIBBEAN SCALLOPS ARGOPECTEN NUCLEUS AND NODIPECTEN NODOSUS L. A. VELASCO* Instituto de Investigaciones Tropicales (INTROPIC), Universidad del Magdalena, Carrera 2 No 18-27, Taganga, Santa Marta, Colombia ABSTRACT Argopecten nucleus and Nodipecten nodosus are two Caribbean scallops occurring in Colombia, which have recently been selected for artificial culture based on their high commercial value. As part of an effort to develop culture technology for these species, we studied the effects of food concentration and temperature on feeding rates (filtration, ingestion, and absorption), oxygen consumption, ammonium excretion and scope for growth in adults of the two scallop species. We tested the effects of four concentrations of the microalga Isochrysis galbana (10, 20, 40 and 60 cells ␮L−1) at three water temperatures (20, 25 and 28°C), at a constant salinity of 36‰. The results showed that increases in food concentration induced increases in feeding rate, oxygen consumption and growth potential, but at values of 60 cells ␮L−1 these variables decreased, indicating saturation of the digestive tract. The excretion rate increased at low food concentrations, particularly at the middle (25°C) and/or at the highest temperature tested (28°C). This suggested utilization of endogenous proteins as a supplementary energy source under these conditions. The increase in temperature had no significant effect on the feeding variables or on the scope for growth of A. nucleus, but raised the N. nodosus ones. All the physiological rates for the two species were similar except for oxygen consumption, which was greater in N. nodosus than in A. nucleus. Using values obtained for the algae concentrations, which produced the greatest growth potential, the optimal value for I. galbana for both the scallops was 40 cells ␮L−1, whereas the optimal temperature for N. nodosus was 25°C. There was no single optimal temperature for A. nucleus, which functioned equally well at between 20°C and 28°C. KEY WORDS: scallop physiology, scallop culture, Argopecten nucleus, Nodipecten nodosus, Colombia, Caribbean.

INTRODUCTION

Temperature and concentration of particulate food are two of the main factors that affect bivalve filter feeders in relation to their growth (Wilson 1987), survival (Paul 1980), gonadal conditioning (Martinez et al. 2000, Martínez & Pérez, 2003) and physiology (Bricelj, et al. 1987, Navarro & Iglesias 1995, Navarro et al. 2000). Studies carried out on the physiology of bivalve filter feeders in response to broad ranges of microalgal concentrations (Griffiths & King 1979, Bacon et al. 1998, MacDonald et al. 1998, Velasco & Navarro 2002, 2003) and/or water temperature (Alí 1970, Winter 1970, Bougrier et al. 1995, Sicard et al. 1999, Laing 2000) have shown that the filtration rates, ingestion, absorption, oxygen consumption and/or excretion become modified with changes in these parameters, and allow maintenance of high values in scope for growth within given ranges of the parameters depending on the species observed. Argopecten nucleus (Born, 1780) and Nodipecten nodosus (Linné, 1758) are two scallops of commercial importance from the Caribbean coast of Colombia. These species are epibenthic filter feeders and may coexist on sandy bottoms from 10–100 m depth. A. nucleus is a moderately-sized, unattached species (length ⳱ 50 mm), whereas N. nodosus is a larger (length ⳱ 150 mm) species, which remains attached to hard substrates. No naturally occurring beds of these scallops have been encountered in the sea off Colombia; population aggregates have been maintained in artificial cultures, produced from the capture of (scarce) naturally occurring seed obtained in spat collectors (maximal of 6–77 spats collector−1) (Urban, 1999). These two scallop species have shown high growth rates in suspended cultures, reaching commercial sizes within 11 mo (Urban 1999, INVEMAR 2003). It is known that growth and survival of N. nodosus is negatively affected by ex-

*E-mail: [email protected]

treme temperatures (29°C), low salinities ( 0.9784, P < 0.0001), whereas no association was noted between the oxygen consumption rates (r ⳱ −0.08, P ⳱ 0.3579). Correlation of the scope for growth with excretion rates was negative (r ⳱ −0.2422, P ⳱ 0.005). The factorial analysis of variance showed that the growth potentials of the two scallops was significantly influenced

Figure 2. Argopecten nucleus and Nodipecten nodosus. Absorption efficiencies under different concentrations of Isochrysis galbana and water temperatures.

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Figure 3. Argopecten nucleus and Nodipecten nodosus. A. Oxygen consumption rates and B. Ammonia excretion rates under different concentrations of Isochrysis galbana and water temperatures.

by the microalgal concentration (df ⳱ 3, P < 0.0001), whereas the water temperature affected N. nodosus (df ⳱ 2, F ⳱ 16.01, P ⳱ 0.0001) and not A. nucleus (df ⳱ 2, F ⳱ 0.86, P ⳱ 0.4289). The scope for growth increased together with food concentration up to 40 cells ␮L and thereafter decreased at 60 cells ␮L−1, except in N. nodosus at the low temperature (20°C), at which the scope for growth continued to increase. Temperature affected the scope for growth of N. nodosus only at the intermediate food concentrations of 20 y 40 cells ␮L−1 (df ⳱ 3, P < 0.0277), with an increase in scope for growth stimulated at 25°C. The analysis of covariance showed that the scope for growth of the two scallops was statistically similar (df ⳱ 1, F ⳱ 3.2, P ⳱ 0.0761). DISCUSSION

Feeding Rates

The highest rates of filtration, ingestion, and absorption recorded for the two scallop species in this study were obtained at intermediate concentrations of microalgae offered as food. These results were in agreement with results of previous studies on the feeding of bivalves exposed to broad ranges of algal concentration

as in the case of Mytilus chilensis (Velasco & Navarro 2002, 2003). The decrease in feeding rates at high concentrations of microalgae has not been noted in other studies, such as those of Aulacomya ater (Griffiths & King 1979), Mytilus chilensis (Navarro & Winter 1982), Placopecten magellanicus (Bacon et al. 1998) and Musculista senhousia (Inoue & Yamamuro 2000). Alternatively, stabilization of feeding rates may occur at high food concentrations, as shown for Tapes philippinarum (Coutteau et al. 1994); Mya arenaria (Bacon et al. 1998) and Mulinia edulis (Velasco & Navarro 2002, 2003). It may be that the latter two results were because of the narrow range of microalgal concentrations tested. The reduced feeding rates of the bivalves at low food concentrations has been explained as the direct, and uncontrolled scarcity of food, whereas at high concentrations it may represent a reduction in the pumping of water, and to the increase in production of pseudofeces, which allows the bivalve to regulate the ingestion rate and avoid saturation of the alimentary system (Iglesias et al. 1996, Velasco & Navarro 2002). The concentration of Isochrysis galbana at which the ingestion rate of Argopecten nucleus and Nodipecten nodosus was at a maximum, inducing regulation, or lowering of ingestion (“saturation concentration”), was at 40 cells ␮L−1 (8 mg L−1); this value coincided with that observed in other bivalves fed on microalgal diets including Meretrix meretriz

Figure 4. Argopecten nucleus and Nodipecten nodosus. Scope for growth under different concentrations of Isochrysis galbana and water temperatures.

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(8 mg L−1, Zhuang & Wang 2004) and P. magellanicus (7 mg L−1, Bacon et al. 1998). The lack of influence of the temperature on the feeding rates of Argopecten nucleus showed that this species had a high capacity for rapid acclimation within the temperature range tested. Similar results had previously been presented for Argopecten purpuratus exposed to 16°C and 20°C for three weeks (Navarro et al. 2000). The increase in feeding rates in Nodipecten nodosus with increase in temperature and its decrease at temperatures as high as 28°C, indicated that this species did not become acclimated to different temperatures in a short time (15 h). This result coincided with the responses described for other bivalves, including Argopecten ventricosus (Sicard et al. 1999) and Pecten maximus (Laing 2000). Other studies only described increases in feeding rates with increases in temperature, as with Arctica islandica, Modiolus modiolus (Winter 1970), Venerupis decussata, Mercenaria mercenaria (Walne 1972), Ostrea edulis (Beiras et al. 1995) and Pecten fumatus (Heasman et al. 1996) possibly because of the fact that the cited authors worked within a narrower temperature range. The presently described effect of temperature on the feeding rates of N. nodosus was observed only at intermediate food concentrations (20 and 40 cells ␮L−1). Extreme concentrations apparently produce a limiting effect, which annulled the positive effect obtained at intermediate temperature (25°C). The similarity between feeding rates in Argopecten nucleus and Nodipecten nodosus contrast with the higher capacity for retaining particulate in the bigger branchial area per unit dry weight of N. nodosus (Velasco, in press). It suggests that A. nucleus has higher pump activity than N. nodosus. Other studies, which have compared interspecific feeding rates have demonstrated greater particle retention and feeding rates in species having greater branchial surface areas (Foster-Smith 1976, Hawkins et al. 1990, Velasco & Navarro 2002). Absorption Efficiency

Absorption efficiency generally decreases when the concentration of microalgae increases, as in the cases of Mytilus edulis (Widdows 1978), Aulacomya ater (Griffiths & King 1979), Mytilus chilensis (Navarro & Winter 1982), Argopecten purpuratus (Fernández-Reiriz et al. 2005) and Hiatella arctica (Sejr et al. 2004). This has been attributed to the decrease in residence time of the food in the stomach when the ingestion rate is high (Bayne et al. 1989). The absorption efficiencies of Argopecten nucleus and Nodipecten nodosus were relatively high, and its variation showed no relation with the concentration of microalgae, nor with the ingestion rate, in agreement with the results obtained with Mya arenaria, Placopecten magellanicus (MacDonald et al. 1998) and in Meretrix meretriz (Zhuang & Wang 2004). The maintenance of high absorption efficiencies in A. nucleus and N. nodosus at the highest food concentration tested could be related to the strong regulation of the ingestion rate, which avoids oversaturation of the digestive tract and affects the efficiency of the digestive process. The lack of influence of temperature on the absorption efficiency of Nodipecten nodosus coincides with that found for Argopecten purpuratus after an acclimation period (Navarro et al. 2000), indicating a high degree of plasticity in this variable with regard to temperature changes. In Argopecten nucleus the increase in temperature from 20°C to 25°C produced an increase in the absorption efficiency as noted for Ostrea edulis (Beiras et al. 1995) and Meretrix meretriz (Zhuang & Wang 2004). Low temperatures

produce a decrease in kinetic energy of molecules, and a decrease in the probability that they will react upon colliding (Eckert et al. 1990), which should retard hydrolysis of different substrates and reduce the efficiency of their digestion. The similarity of the absorption efficiencies of Argopecten nucleus and Nodipecten nodosus agree with results obtained in comparisons of absorption efficiencies among bivalve species, including Mulinia edulis and Mytilus chilensis (Velasco & Navarro 2003, 2005) and Mya arenaria and Placopecten magellanicus (MacDonald et al. 1998). This indirectly suggests a similarity in the composition and/or activity of the digestive enzymes of the two species, possibly induced by being exposed to similar environmental conditions. It was demonstrated in M. edulis and M. chilensis that although the composition and activity of the digestive enzymes in their digestive glands and crystalline styles were different (Labarta et al. 2002), they had comparable absorption efficiencies (Navarro et al. 2003, Velasco & Navarro 2003). Oxygen Consumption

Oxygen consumption by Argopecten nucleus and Nodipecten nodosus increased with the increase in microalgae concentration, and at the highest concentration tested, this rate decreased, demonstrating a similar response to that of the feeding rate. This showed that the costs of feeding activities, digestion and absorption were variable and depended on the food concentration. Similar results have been described for other bivalves such as Donax vittatus (Ansell 1973), Aulacomya ater (Griffiths & King 1979), Mytilus edulis (Thompson & Bayne 1972, Bayne et al. 1984,1989), Mya arenaria (MacDonald et al. 1998), Musculista senhousia (Inoue & Yamamuro 2000), Mulinia edulis, Mytilus chilensis (Velasco & Navarro 2003), Cerastoderma edule (Navarro et al. 1992, 1994) and Hiatella arctica (Sejr et al. 2004). It is in contrast, however, with the finding that there was no influence of food concentration on oxygen consumption in M. arenaria and Placopecten magellanicus (Mac Donald et al. 1998). The increase in oxygen consumption by Argopecten nucleus and Nodipecten nodosus with increase in water temperature is explained by the positive effect of increase in temperature on the speeds of metabolic reactions (Eckert et al. 1990) and is in agreement with results from other bivalves such as Ostrea edulis (Beiras et al. 1995) Crassostrea gigas (Bougrier et al. 1995) and Argopecten ventricosus (Sicard et al. 1999). This behavior differs from that found for O. edulis (Beiras et al. 1995) and Argopecten purpuratus (Navarro et al. 2000) after being experimentally held at a different temperature for a relatively long period (3 wk); under these conditions the oxygen consumption did not vary with temperature, showing an acclimation of the organisms to manipulation of this parameter. According to Eckert et al. (1990), acclimation of tissues and organisms to different temperatures could occur because of the modification of sensitivity of enzymatic activity, changes in molecular structure of one or more enzymes, or to changes in the quantities of enzymes. In spite of the similarities among feeding rates of the scallops, Nodipecten nodosus had greater oxygen consumption than Argopecten nucleus, suggesting that the latter species was more efficient than the former in utilization of this resource in carrying on its metabolic functions. In studies comparing oxygen consumption among bivalve species (Mac Donald et al. 1998, Velasco & Navarro 2003), it was noted that the existence of interspecific differences in oxygen consumption coincided with parallel differences in feeding rates.

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Excretion Rate

The decrease in excretion rate in Argopecten nucleus and Nodipecten nodosus with increases in food concentration contrasts with most comparable studies, as the more typical response has been a positive relation between these variables (Mulinia edulis, Mytilus chilensis, Velasco & Navarro 2003, Hiatella arcaica, Sejr et al. 2004), or even no relation at all (Mya arenaria and Placopecten magellanicus, MacDonald et al. 1998). It is known that bivalves use proteins stored in body tissues as energy sources when the food supply is incapable of satisfying metabolic requirements, resulting in an increase in the excretion rate (Bayne & Newell 1983). Therefore the lower ranges of food concentration tested in this study (10 and 20 cells ␮L−1) may have been insufficient to supply the energetic demands of the two scallop species, which then had to rely on the catabolism of endogenous proteins. The reduced excretion rates of Argopecten nucleus and Nodipecten nodosus at low water temperatures, particularly when the food concentration was 20 cells ␮L−1 or less, could be explained by a decrease in metabolism under these conditions, which could in turn, lower the metabolic demands of the organisms to a point at which they were not required to resort to the use of stored proteins. The same tendency has been observed in other bivalves such as Ostrea edulis (Beiras et al. 1995). The excretion rate of Argopecten nucleus was similar to that of Nodipecten nodosus, similar to findings in interspecific comparisons under the same conditions in Mya arenaria and Placopecten magellanicus (MacDonald et al. 1998) and Mulinia edulis and Mytilus chilensis (Velasco & Navarro 2003). The similarity in excretion rates of the bivalves, together with the similarities between absorption rates, suggested that the utilization of proteins in the two species comparisons were quite similar. Scope for Growth

The positive high correlation between scope for growth and feeding rates, and the low values of oxygen consumption and excretion indicated that the energy acquisition by feeding was more important than the energy output in determining the values of scope for growth. Because values for ingestion and absorption depend on the filtration rate, it can be assumed that the filtration rate is the main determinant of physiological condition in Argopecten nucleus and Nodipecten nodosus under the conditions tested in the present study. Similar conclusions have been derived for Argopecten purpuratus (Navarro et al. 2000), Mya arenaria and Placopecten magellanicus (Bacon et al. 1998, MacDonald et al. 1998), and Mulinia edulis and Mytilus chilensis (Velasco & Navarro 2002; 2003). Nevertheless, in species such as Ostrea edulis (Ansell & Sivadas 1973) and M. edulis (Velasco & Navarro 2002), under certain conditions the oxygen consumption may constitute an important portion of the energy absorbed, and may have an important effect on the growth potential. The high growth potentials of Argopecten nucleus and Nodipecten nodosus when fed intermediate microalgal concentrations (40 cel ␮L−1), as well as the low values obtained at the extremes of the algal concentration (10 and 60 cel ␮L−1), are in accord with results obtained for Aulacomya ater (Griffiths & King 1979), and Mytilus chilensis (Velasco & Navarro, 2003). They differ, however, with findings from other studies, where scope for growth and algae concentration showed an inverse relation, as in M. chilensis (Navarro & Winter 1982), or a direct relation as in Cerastoderma edule, Tapes decussatus (Navarro & Iglesias, 1995), Mulinia edu-

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lis (Velasco & Navarro 2003), Mya arenaria and Placopecten magellanicus (MacDonald et al. 1998). These differences in the responses of the scope for growth to food concentration may be caused by the utilization of more narrow ranges of food concentration in the laboratory than those to which the test organisms are accustomed in their natural habitats. The scope for growth of A. nucleus was not influenced by temperature, showing that this species had great plasticity of physiological rates in relation to this factor. On the other hand, the scope for growth of N nodosus was greater at the intermediate temperature in our study (25°C), where there was a high degree of sensitivity of the feeding rates in relation to temperature. The lowering of scope for growth at lower temperature was probably related to decrease in metabolic rate, and at high temperatures to the denaturation of related enzymes (Eckert et al. 1990). The direct relation between scope for growth and temperature coincide with that observed in other species such as Cerastoderma edule, Tapes decussatus (Navarro & Iglesias 1995), Argopecten purpuratus (Navarro et al. 2000) and Pecten maximus (Laing 2000). At extremes of food concentration, the scope for growth of Nodipecten nodosus was low, and independent of temperature, therefore under these conditions the negative effects of either the absence, or excess of food on the physiological condition of the organism nullified the positive effect of providing an optimal temperature of 25°C. Navarro and Iglesias (1995) found that at very low concentrations of food that the scope for growth of Cerastoderma edule and Tapes decussatus became negative and decreased with increase in temperature. In this study, the food concentrations were not so extreme as to produce negative scope for growth at which we might have observed a similar phenomenon. It has been found that the optimal food concentration increases with the water temperature for Arctica islandica, Modiolus modiolus (Winter 1970) and Pecten maximus (Laing 2000). This relation was not observed in this study with either scallop species. In Argopecten nucleus the optimal food concentration was independent of temperature, because the optimal food concentration was found to be the same (40 cel ␮L−1) at all the temperatures tested. Conversely, in Nodipecten nodosus the optimal food concentration increased with decrease in temperature. This response was probably because saturation of the alimentary system did not occur under low temperature conditions and high food concentrations, thus permitting continuance of high ingestion and absorption rates. Similarities between the scope for growth in Argopecten nucleus and Nodipecten nodosus indicate that the two species may compete with equal efficiency under the same conditions of food concentration and temperature, based on the environmental conditions occurring in each of their natural habitats. Studies that have compared scope for growth between species with differing habitats (epifaunal and infaunal) have found interspecific similarities under certain shared feeding conditions, which may not occur under other conditions in which interspecific differences become manifest (MacDonald et al. 1998, Velasco & Navarro 2002, Savina & Pouvreau 2004). In conclusion, this study found that: (1) the scope for growth and the feeding rates of Argopecten nucleus and Nodipecten nodosus increased with increased food concentration but decreased at higher and lower extremes of food concentration; (2) the scope for growth and feeding rates of A. nucleus were not affected by temperature, with the reverse true for N. nodosus, increasing at 25°C and decreasing at higher temperature (28°C); (3) A. nucleus and N. nodosus showed similar responses and values in all their physi-

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ological rates, except for oxygen consumption, where A. nucleus displayed lower rates. ACKNOWLEDGMENTS

The author gratefully acknowledges W. Barbosa, J. Barros and the staff of the Moluscos y Microalgas Laboratory of the Univer-

sidad del Magdalena for their help during the experiments and also thanks ASOPLAM and INVEMAR for providing the experimental animals. This study was supported by a research project CONCIENCIAS-SENA-UNIVERSIDAD DEL MAGDALENA 111709-12394 and the grant International Foundation for Science (IFS) A/3363-1.

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