Gastropoda: Muricidae

New. Zealand Journal of Marine and Freshwater Research, 2002, Vol. 36: 321-332 0028-8330/02/3602-0321 $7.00 © The Royal Society of New Zealand 2002

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lnfluence of diet and temperature on physiological energetics of Chorus giganteus (Gastropoda: Muricidae) during reproductive conditioning J. M. NAVARRO* G. E. LEIVA Instituto de Biología Marina Dr Jürgen Winter Universidad Austral de Chile Valdivia, Chile email: [email protected] C. S. GALLARDO Instituto de Zoología Universidad Austral de Chile Valdivia, Chile C. VARELA Departamento de Acuicultura Universidad de Los Lagos Osorno, Chile Abstract The influence of two bivalve diets (Mytilus chilensis "chorito" and Tagelus dombeii "navajuela") at three temperatures (13,15,and 18ºC) was studied during the reproductive conditioning of Chorus giganteus (Lesson, 1829). Energy budgets were determined taking into account energy acquisition (ingestion and absorption) and energy expenditure (oxygen consumption, ammonia production, and energy placed into mucus production and egg laying). Relative physiological condition was assessed by calculating the scope for growth index (SFG). Diet and temperature both played key roles in the physiological energetic and reproductive conditioning of this snail. Tagelus was the preferred prey, probably because of its greater vulnerability to predatory attack by C. giganteus. The highest feeding rate was observed at 15ºC, coinciding with optimal growth. Absorption efficiency was similar with

*Author for correspondence. M01012 Received 24 January 2001; accepted 5 September 2001

both diets, despite the differential preference in prey. Temperature had no effect on oxygen uptake, but increased as the snails fed on Tagelus during the reproductive conditioning period. Diet was the main factor affecting SFG, and temperature, although significant, accounted for a lower percentage of variation in SFG. Highest growth rates were observed at 15ºC on a Tagelus diet. Reproductive effort, measured as the proportion of the total energy budget of an organism that is allocated to reproduction, was highest at 18ºC with a Tagelus diet. Energy would not be allocated for reproduction when the snails were fed with M. chilensis, as SFG was negative at all three temperatures. Keywords Chorus giganteus; Muricidae; physiological energetics; scope for growth; conditioning INTRODUCTION Chorus giganteus (Lesson, 1829), an endemic muricid gastropod known as "trumulco", inhabits shallow marine environments from Valdivia (39º56'S, 73º35'W) to Antofagasta (23º39'S, 70º24'W) (Osorio et al. 1979). Because of its commercial value as a food in Asian markets this snail has been exported over the last two decades resulting in over-exploitation of natural stocks. Preliminary observations suggest this is a suitable species for mass culture in controlled aquaculture systems, based on its reproductive attributes. These include the production of encapsulated embryos with lecithotrophic larvae which feed on nurse eggs and, under natural conditions, having a planktonic phase of only 2-5 days (Leiva et al. 1998; González & Gallardo 1999). This planktonic phase may be eliminated entirely as the larvae are competent for metamorphosis at hatching (Gallardo & Sánchez 2001). This reproductive mode allows mass propagation of juveniles for culture as newly settled individuals are capable of active feeding on juvenile bivalves (González 1997). High shell growth rates have also been observed for this species, reaching

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2.5 cm during the first year (Urrutia & Navarro unpubl. data). In contrast to other species of muricids inhabiting intertidal rocky shores, C. giganteus lives buried in subtidal soft bottom between 8 and 12 cm depth and feeds mainly on its natural prey, the bivalve Tagelus dombeii. Temperature and diet have been shown to be environmental factors playing an important role in determining the scope for growth (SFG) and reproduction of marine organisms (MacDonald & Thompson 1986; Bayne & Hawkins 1990; Navarro & Torrijos 1995). SFG (Bayne & Newell 1983; Stickle 1985) is a physiological index which reflects the fitness of individuals to adapt to environmental factors, particularly temperature and diet. When SFG is positive, energy is available for growth and/or reproduction, but when this index is negative for a prolonged period of time the organism must catabolise tissues, and ultimately may die. SFG and reproduction are positively correlated in the bivalve Mytilus edulis (Bayne et al. 1978) and diet and temperature are key factors influencing potential for production and gametogenesis in the scallop Argopecten purpuratus (Navarro et al. 2000). According to Robinson (1992), these variables also play an important role regarding the quality of the eggs, survivorship of the larvae, and growth of spat. The present work represents the first attempt to elucidate the interactive effects of diet and temperature on the physiological energetic of a Chilean gastropod during reproductive conditioning, using the SFG as a physiological/ condition index. MATERIALS AND METHODS Experimental design Individuals of C. giganteus were collected from Chaihuín, Valdivia (39º56'S, 73º35W), one of the largest populations of this species. The experimental organisms were selected by size ranging between 10 and 12.5 cm in shell length (mean = 11.4 cm), with a dry tissue weight range between 11.3 and 15.4 g (.mean = 13.7 g). These individuals were transferred to the Metri Experimental Laboratory at Puerto Montt (41º36'S, 72º42W), where they were divided into groups of 18 individuals and placed in experimental aquaria with a constant flow of sea water of 1 litre/min to avoid any reduction in oxygen concentration between inflow and outflow. Two different diets, its natural prey the bivalve T. dombeii (4-6 cm shell length) and the mussel M. chilensis (3-5 cm shell length), were supplied ad libitum at 13, 15, and 18ºC,

temperatures selected according to the natural range observed in its natural environment (1116ºC). To make comparisons between different experimental conditions, all physiological rates were standardised to the average dry tissue weight of the experimental snails (13.7 g), by allometric relationships between the dependent variable (e.g., IR = ingestion rate) and dry tissue weight (W) (i.e., IR = aWb) Ingestion rate Consumed prey mass was measured every 3 days by collecting all the empty shells and the remaining tissue in the bivalves. The length of the empty shells was measured and the unconsumed soft tissues dried to constant weight. To evaluate the daily ingested ration, regressions between shell length of 80 individuals of each prey (L = cm) versus dry tissue weight (W = g) were carried out using the allometric equation W = aLb. Ingestion rate was converted to energy units using the conversion factors 1 g dry tissue weight of T. dombeii = 18 870 J (Urrutia et al. in press) and 1 g dry tissue weight of M. chilensis = 21 180 J (Navarro & Winter 1982). Net absorption efficiency Absorption efficiency was estimated by the ratio method of Conover (1966), measuring the organic content of food and faeces. Representative samples (five replicates) of each diet were dried (80ºC) to constant weight and ashed for 16 h at 450ºC to determine the organic content. The foot of T. dombeii and the mantle border and adductor muscle of M. chilensis were not included in the analysis considering that these parts of the body were not consumed by C. giganteus. Samples of faeces were taken from the experimental tanks using Pasteur pipettes and filtered by vacuum onto pre-combusted (450ºC), tared glass fibre filters. Filters were rinsed with isotonic ammonium formate (3%), dried to a constant weight (80ºC), weighed, ashed at 450ºC for 3 h, and weighed again to estimate the organic fraction of the faeces. Absorption rate was calculated as the product of the organic ingestion rate (mg h-1) and absorption efficiency (%). Oxygen uptake Oxygen uptake was measured individually at each diet-temperature combination at monthly intervals during the reproductive conditioning period (August-November 1998). Before any oxygen uptake measurement, the snails were fed ad libitum with the aim of representing a condition close to the routine metabolism. Measurements were done on

Navarro et al.-Energetics of growth and reproduction in Chorus giganteus four animals selected randomly from the tank populations. Individual snails were left for 1 h in sealed plastic chambers of 2.5 litre volume, while a second chamber without snails was used as a control. Water samples were taken from each experimental chamber and from the control and analysed using the Winkler method, modified by Ohle (1953). The oxygen consumed by each individual was estimated by the difference between the oxygen contained in the control and that contained in the experimental chambers over time periods of 60 min. Values of oxygen uptake ( ml O2 h-1) were transformed to energy equivalents (1 ml O2 consumed = 19.9 J (Elliot & Davison 1975)). Ammonia excretion Ammonia excretion was measured monthly using snails selected randomly from each experimental tank. Four animals per condition were placed individually in plastic vessels containing 2.0 litre of filtered (0.45µm) sea water. One additional container with no snails served as a control. After an incubation period of 1 h, samples from water containing the snails and from the control were analysed for ammonia according to Solorzano (1969), expressed as µg NH4-N h-l and converted to energy units using the factor 1µg NH4-N = 0.025 J (Elliot & Davison 1975). Mucus production Mucus production was estimated on animals selected randomly from the experimental tanks. Individual snails were placed in glass beakers of 2.0 litre of filtered (0.45 µm) sea water. Specimens were removed after 24 h and the internal surfaces of the beakers were scraped and rinsed with filtered sea water. This material was filtered onto pre-weighed and combusted glass fibre filters, dried at 80ºC to constant weight, and ashed again for 3 h at 450ºC. Values for mucus production were expressed as mg h-l and transformed to energy equivalents (1 mg dry mucus = 6.90 J (González et al. 1990)). Scope for growth This physiological index of energy balance to estimate production (growth + reproduction) was calculated after converting all the physiological rates to energy equivalents (J h-1). SFG = A - (R + U + M) where A = energy absorbed (J h-1); R = oxygen uptake (ml O2 h-1) x 19.9 J; U = ammonia excretion rate (µg NH4-N h-1) x 0.025 J; M = mucus production (mg h-1) x 6.90 J.

Fig. 1 Chorus giganteus. Food consumption at three different temperatures and two diets during reproductive conditioning. Values are means ± SE.

Cost of reproduction As no spawns were obtained in the experimental tanks, energy content of egg masses was determined on spawns obtained from other snails maintained

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under similar laboratory conditions. To calculate the energy contained, embryos and capsule walls were separated and dried at 60ºC to constant weight and analysed by calorimetry using an adiabatic pump. Statistical analyses A two-way analysis of variance was performed to test the interaction of diet and temperature on the variation of the physiological variables at each time point of the study. Logarithmic transformation was done on data not normally distributed and with no homogeneous variances Differences were considered significant when P < 0.05. RESULTS Physiological rates Diet was the main variable affecting the ingestion rate at each month of the experimental period. A significant effect of temperature was observes only during some months. The interaction diet*temperature did not significantly affect this physiological variable. Food consumed was greater (P < 0.05) when C. giganteus was fed with the bivalve T. dombeii than M. chilensis at each of the three experimental temperatures 13, 15, and 18ºC (Fig. l). Ingestion rate of Tagelus ranged between

9.6 mg h-1 ind.-1 (July at 13ºC) and 24.6 mg h-l ind.-1 (June at 150C). Much lower values of ingestion were obtained with the M. chilensis diet, ranging between 0.17 mg h-l ind.-1 (August at 18ºC) and 3.32 mg h-l ind.-1 (June at 15ºC), no food consumption was detected on two occasions (November at 13ºC and October at 18ºC). Snails ranging between 10 and 12.5 cm length (average = 13.7 g dry tissue weight) consumed between 5.3 and 7.3 Tagelus of 4-6 cm shell length per month at 18 and 15ºC, respectively (Table l). Consumption rates were lower with Mytilus, ranging between 0.77 and

Navarro et al.-Energetics of growth and reproduction in Chorus giganteus

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1.32 bivalves of 3-5 cm shell length per month over the range of temperatures tested (Table l). Thus, the number of prey ingested depended on the diet offered (P < 0.05), and was not affected by temperature alone (P > 0.05). The faeces produced by C. giganteus were difficult to recognise, and production was reduced at high temperature (18ºC) and also with a diet of M. chilensis. Therefore, absorption efficiency was measured only on a few occasions (n = 10). Similar values were obtained with both diets at 13 and 15ºC (Fig. 2) and significant differences (P < 0.05) were observed at 18ºC, where values of 74.7% were reached with the diet of Mytilus and 47.5% with Tagelus. A significant effect of diet on the oxygen consumption of C. giganteus was observed during the experimental period, being highest when the snails were fed with T. dombeii (Fig. 3). Temperature had a significant effect (P < 0.05) only when the snails were fed with the diet of Tagelus, heing highest at 13ºC than at 15ºC and 18ºC. No significant differences were observed at all the other temperature combinations, independent of diet. Oxygen consumption of C. giganteus was highly related with the reproductive conditioning period (from August to November) at 15ºC with the diet of Tagelus, increasing from 0.72 ml h-l ind. -1 to c. 3.0 mg h-l ind.-1 (Fig. 3). Ammonia excretion was characterised by large fluctuations during the study, without a clear pattern related to diet or temperature (Fig. 4). The analysis of variance showed a significant effect (P < 0.05) of diet on this physiological process at each month. Temperature had a significant effect (P < 0.05) only when the snails were fed with the diet of Tagelus, being highest at 13ºC in September and October. No significant differences P > 0.05 were observed at all the other temperature combinations, independent of diet and month tested. Diet plays a significant role (P < 0.05) in the total and organic mucus production of C. giganteus, being higher with Tagelus than with Mytilus at 13 and 18ºC (Fig. 5). Mucus production of snails fed with Tagelus appeared independent of temperature, whereas snails fed with Mytilus produced the largest (P < 0.05) amounts of mucus at 15ºC (Fig. 5). Fig. 6 Chorus giganteus. Scope for growth (SFG) estimated at three different temperatures and two diets during reproductive conditioning.

Scope for growth (SFG) Chorus giganteus fed T. dombeii always had positive SFG values, with the highest scope for growth (average = 140.6 J h-1) at 15ºC for a standard specimen of 13.7 g dry tissue weight (Fig. 6, 7A). The SFG was always negative when C. giganteus was fed with M. chilensis, with the lowest value at 18ºC (-17.7 J h-1) (Fig. 6, 7B). Thus, significant differences in SFG were obtained at each temperature when comparing Tagelus versus Mytilus diets. Differences in SFG were mainly associated with diet (P < 0.001) at each sampling month, with the association observed with temperature at a lower level of significance (P < 0.023). The interaction of both diet and temperature also showed a significant effect (P < 0.024) on SFG. A more integrated view of the

effect of diet and temperature on the energy balance is presented in Fig. 7A,B. Energy allocated to growth and/or reproduction (75.8%) was greater for snails fed with Tagelus at 15ºC. The largest amount of energy utilised (18.9%) was allocated to oxygen uptake (R) with smaller fractions of available energy spent in excretion (E) and mucus production (M). Similar results were obtained at 13 and 18ºC. SFG was significantly reduced when Mytilus was used as prey. The energy absorbed at 15ºC (10.6 J W-1) was highly reduced; the metabolic demand increased to 23.1 J h-1, representing 217.9% of the energy absorbed. Under these conditions there was no energy available for growth and/or reproduction, resulting in a negative SFG of -17.4 J h-1. Similar results were obtained at 13 and 18ºC (Fig. 6, 7B).

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New Zealand Journal of Marine and Freshwater Research, 2002, Vol. 36 Table 2 Chorus giganteus. Scope for growth (SFG) and energy allocation compared with reproductive and somatic production at different combinations of diet and temperature.

Cost of reproduction The energetic content of recently laid capsules of 17.95 ± 0.63 SD min length was 382.7 ± 36.6 SD J/ capsule, including both capsule wall and the contained embryos. Total embryos accounted for 141.3 J ± 23.2 SD and the wall for 241.4 ± 22.5 SD J, corresponded to 36.9% and 63.1% of the total energy, respectively. This calculation does not take into account the metabolic cost of producing and mobilising the capsules during spawning. Gallardo (1981) reported 197 capsules produced by one snail of C. giganteus and Jaramillo (1986) describes four reproductive events for this species during the year. Based on these results and on the energetic value of the 788 capsules laid during a year, the reproductive output represented an energetic cost of c. 302 J/year (Table 2). These results represent an approximation of the energy spent in capsule production and it can he different depending on the experimental conditions.

DISCUSSION Chorus giganteus shows significantly higher feeding rates with T. dombeii than with M. chilensis. These findings may be related to the fact that the soft tissues of Tagelus are not totally enclosed by the shell, allowing the snail to consume this bivalve without expending energy in penetrating the shell. Conversely, M. chilensis is a prey that shuts its valves tightly, avoiding easy attack by C. giganteus. This feeding behaviour agrees with the prediction of Hughes (1980) optimal foraging theory, in which the predator elects the prey option that yields the best return per unit of effort (usually in terms of energy). These results are in agreement with Pearce (1967) working on the red whelk Neptunea antiqua, who found that after 8 days in the presence of living

M. edulis, this gastropod did not show any attempt to open the mussels and feed, however when an opened Mytilus was offered, it started to feed immediately. The greater feeding rates obtained with Tagelus can also be related to the fact that this bivalve represents the natural prey of C. giganteus, suggesting a learned behaviour to feed on it. Conversely, there was no observed acquired (learned) behaviour in foraging activity during the 5 months in which C. giganteus was fed with M. chilensis. Edwards (1975) recorded that the snail Polinices duplicatus "trained" on a pure diet of M. edulis initially fed on Mya arenaria at lower rates than snails already trained on pure diets of this clam and that in both groups of snails, the feeding rate on Mya increased with experience with that prey. More recently Rovero et al. (1999) found that Nucella lapillus with different fieldbased experience of mussels showed different handling behaviour, and concluded that experience of specific prey in the field, by reducing handling time, could promote fitness by reducing exposure to environmental hazards. The variation of absorption efficiency in C. giganteus, between 47 and 83%, falls within the wide range of values reported for gastropods. Peck et al. (1987) reported absorption efficiencies between 78 and 81% in Haliotis tuberculata. Our results are slightly lower than those found for other species of carnivorous gastropods, 82-98% for Clione limacina, 81-97% for Thais haemastoma (Bayne & Newell 1983), and 81-95% for Concholepas concholepas (Navarro & Torrijos 1995). Absorption efficiency was similar for both diets, suggesting similar nutritive value for both bivalves despite the different preference the snails showed for each prey species. The highest absorption efficiency of C. giganteus when fed with Mytilus at 18ºC may be related to the low ingestion rate and with the increase of the residence time of the food in the gut.

Navarro et al.-Energetics of growth and reproduction in Chorus giganteus Temperature appears not to affect absorption efficiency in C. giganteus, which is in agreement with results found for other molluscs that indicate that absorption efficiency is not strongly influenced by temperature across normal ranges at which airmails experience in the field (Ansell 1981; Bayne & Newell 1983). Oxygen uptake was significantly (P < 0.05) affected across the temperature range of 13-18ºC, showing that C. giganteus does not have the same capacity for temperature acclimation describes for other species of muricids, such as for Concholepas concholepas, where no significant differences in oxygen uptake were observed between 10 and 20ºC (Méndez & Cancino 1992). The decrease of oxygen uptake showed by C. giganteus from 13 to 15ºC when fed with Tagelus seems to be related to a compensatory mechanism to save energy at the highest temperatures where the ingestion rate decreases. These findings can also he related to the lower oxygen consumed and the highly reduced ingestion rates when this species was fed with Mytilus. The significant increase (P < 0.05) of oxygen uptake observed in individuals of C. giganteus fed with T. dombeii at 15ºC during the reproductive conditioning period (from August to November), is in agreement with the increase of the gonad condition index of this species during the same period of study (Carrasco 2001), suggesting the presence of a positive relationship between oxygen consumption and gametogenesis. Similar significant positive relationships between oxygen uptake and gonad development has been reported for many species of bivalves, i.e., Cerastoderma edule (Newell & Bayne 1980), M. edulis (Bayne & Widdows 1978), and Modiolus modiolus (Navarro & Thompson 1996). Energy losses associated with ammonia excretion represented a small percentage of the energy absorbed when C. giganteus was fed with Tagelus (3.7-7.5%). Values between 9 and 16% were reported for the gastropod Nucella lapillus (Hughes 1986) and between 4.9 and 7.2% for Concholepas concholepas (Navarro & Torrijos 1995). The ammonia excreted by C. giganteus fed with Mytilus represents a high percentage of the absorbed energy, suggesting the presence of endogenous nitrogen resulting from protein catabolism. Only diet has a significant effect on this physiological variable during some months, probably related to the higher feeding rates measured with T. dombeii as prey. Mucus has important roles in locomotion and feeding activity in marine organisms (Davies &

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Hawkins 1998). The highest amount of mucus produced by C. giganteus fed on Tagelus seems to be related to the larger amount of food consumed. Branch (1981) reported that mucus production in Patella longicosta represented 8-9% of the energy budget and Navarro & Torrijos (1995) reported 5.7-20.3% of the energy absorbed for C. concholepas. Both studies describes higher percentages than those found in the present study when C. giganteus was fed with Tagelus. However, when Mytilus was used as a diet, mucus production represented very high percentages of the energy absorbed, even when the absolute values were lower than with the Tagelus diet. Effects of diet plus temperature on C. giganteus are reflected in the SFG index. The positive SFG obtained with all combinations of temperature and Tagelus diet at each month correspond with the high ingestion rates measured. Conversely, the negative SFG observed at all the combinations of temperature and Mytilus diet at each sampling month occurred because of the severe reduction in ingestion rate of this snail. Méndez & Cancino (1992) reported significant differences in the growth of C. concholepas as a function of diet. Although these authors attributed the differences in growth to diet composition, for C. giganteus the main difference between diets was the energy required to attack and access prey tissues. Thus, T. dombeii, a bivalve that is not totally enclosed by its shell, is far more vulnerable to attack than M. chilensis. Hughes & Dunkin (1984), Garton (1986), and Palmer (1990) report that some species of gastropod optimise foraging behaviour when restricted to a monospecific diet. The negative SFG with Mytilus as prey during the four experimental months confirm that adult C. giganteus did not develop a successful foraging behaviour for this prey. In this study, diet was the main factor affecting SFG, and temperature, although significant, accounted for a lower percentage of the variation in SFG. Similarly, a significant but lesser effect appeared with the diet*temperature interaction on SFG. Therefore, the lowest SFG observed at 18ºC with the Tagelus diet corresponds to low ingestion rate. This temperature exceeds the range observed in the natural environment inhabited by C. giganteus (between 11 and 16ºC; Jaramillo et al. 1998). This suggests that the "fitness" of C. giganteus is significantly reduced at 18ºC, even when they are fed with a suitable diet (T. dombeii). The highest amount of energy available for growth and reproduction observed with the combination Tagelus/15ºC was more related to the high ingestion rate facilitated by the greater

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efficiency in attacking this prey than with differential metabolic costs and/or other physiological processes. Such a pattern of relationships would account for the highest growth rate experienced by the snails when maintained at 15ºC and fed with Tagelus, where incremental growth marks were clearly observed on the shells after a period of 4 months. No incremental marks were observed on individuals maintained at 18ºC, explaining the reduction in the SFG as well as the significant mortality observed at this temperature. In a parallel study, Carrasco (2001) found similar results, where he reported an increase in gonadic tissue and total tissue weight when C. giganteus was fed with Tagelus at different experimental temperatures. He also reported a significant decrease of tissue weight with the Mytilus diet. Gastropods laying capsules need to invest a significant amount of energy in these structures, the main function of which is protection of the embryos (Perron 1981). SFG of C. giganteus fed with T. dombeii was always higher than the energy required by this species to produce the capsules per year. The larger availability of energy for growth and/or reproduction occurred at 15ºC, when the snails had the highest feeding rates and SFG. Conversely, when C. giganteus was fed with the prey M. chilensis, SFG was negative, without energy to be allocated to reproduction or growth. The reproductive effort index of Tinkle & Hadley (1975) represents the proportion of the total energy budget of an organism that is allocated to reproduction, and it could only he applied in species showing positive SFG. Reproductive effort in C. giganteus was calculated considering the four reproductive events per year reported by Jaramillo (1986). Thus, the highest values measured in C. giganteus fed with Tagelus (52%) occurred at the highest temperature (18ºC), and the lowest RE (25%) at 15ºC. In agreement with Calow & Woolhead (1977), the ingestion rate appeared to be the physiological process playing the most significant role in determining reproductive effort in C. giganteus. Our data suggest that an optimum reproductive conditioning of the gastropod C. giganteus will in a large part be determined by an appropriate diet, consistent in vulnerable preys, easily attacked by this snail, and second, by using suitable temperatures, no higher than those found in the natural environment inhabited by this species. Under these conditions C. giganteus will be able to show a positive SFG with enough energy to he allocated to growth and to

the reproductive processes. Because of logistical reasons we had little control over the experimental design and no true replications were included, which resulted in the fact that we were not able to test the tank effects reducing the accuracy of the measurements. The design for similar studies must be improved by using the necessary replicates, even when the requirements to set up these types of experiments requires large laboratory space.

ACKNOWLEDGMENTS Thanks to Maritza Araneda, Geysi Urrutia, and Claudio Carrasco for the help during the field and laboratory experiments. Thanks also to Gloria Martínez and Cristian Aguilera for their help with the calorimetric analysis of the capsules. The study was carried out with financial support from the Programa Acuicultura y Biotecnología Marina, 1 (97), Fondap, Chile (Subprograma Invertebrados). We also thank the Canadian lntemational Development Agency (CIDA) for support during the preparation of the manuscript.

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