Environmental effects on the growth of the Chilean oyster Ostrea chilensis in five mariculture locations in the Chiloé Island, Southern Chile

ELSEVIER

Aquaculture 136 (1995) 153-164

Environmental effects on the growth of the Chilean oyster Ostrea chilensis in five mariculture locations in the Chilo6 Island, Southern Chile Jorge E. Toro *, Mario A. Sanhueza, Jiirgen E. Winter, Carolina M. Senn, Pablo Aguila, Ana M. Vergara Institutede Biologia Marina, Universidad Austral de Chile, Casilla 567, Valdivia, Chile Accepted 30 April 1995

Abstract A cohort of juvenile oysters (Osrrea chilensis), produced in the laboratory using mass spawning, were grown in pearl nets, at three different depths and stocking densities, at five mariculture farms in southern Chile. Live weight, shell height and mortality were monitored monthly over 24 months. Chlorophyll a, seston, seawater temperature, salinity, and dissolved oxygen were recorded monthly during the study period. Oysters grew at different rates among locations (P < 0.001)) that are explained by differences in salinity, chlorophyll a, temperature, and the proportion of particulate organic and inorganic matter in the seston. The position within the water column ( 1, 4 and 8 m) produced a significant effect on oyster growth (P < 0.001)) and the gain in live weight declined at higher stocking density (P 0.05). The overall survival was 71.8% with lower values in the estuarine location, caused probably by the low salinity and high concentrations of particulate inorganic matter in sexually mature oysters. Keywords:

Growth; Environment;

Oysters; Ostrea chilensis; Chile

1. Introduction

Southern Chile has an enormous potential for aquaculture activities; its geographical formation with numerous sheltered bays and estuaries and the number of species of algae, molluscs and finfish now in production or with aquaculture potential, have set the stage for the development of more intensive aquaculture activities (Winter et al., 1984a; Boeuf and Medina, 1990; Gajardo, 1990; Toro and Newkirk, 199 1) . * Corresponding

author.

0044-8486/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDIOO44-8486(95)01050-5

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The first attempt to farm Ostrea chilensis (Philippi, 1845) occurred in 1930 with the creation of a state farm that produced oyster spat in the Quetalmahue Gulf (ChiloC Island), however, it is only since 1973 that commercial aquaculture of 0. chilensis has been undertaken (Lepez, 1983; Toro and Chaparro, 1990). The chilean oyster represent an important resource and its culture has been progressing for the last two decades (Lepez, 1983; Toro and Chaparro, 1990)) in particular after the increasing demand by the north-america market (Gajardo, 1990; Bustos et al., 1991). However, the slow annual growth of this species in southern Chile, caused by the very short growing season (November-February), has became an important restriction for the oyster farmers. Oysters are marketable at a shell height of about 50 mm, which is attained after 4-5 years of growth in natural beds (Solis, 1967; Winter et al., 1984a) and in less than 30 months in suspended culture (Toro and Varela, 1988; Kino and Valencia, 1990). The literature describing the environmental factors affecting the growth of the chilean oyster is small. Husbandry studies in relation to the effect of stocking density on the growth rate of 0. chilensis are very scarce in the literature. A study carried out by DiSalvo and Martinez ( 1985) in a north central chilean coastal bay reports that the Chilean oyster is apparently well adapted for growout under relatively crowded conditions, suggested by the lack of difference in shell growth between oysters maintained at various densities. However, in a previous study DiSalvo et al. ( 1984) showed that density was indeed important in the early stages of their growth. The present study describes the relationships between environmental variables and patterns of growth and mortality of 0. chilensis of a cohort maintained in culture at five different sites, three depths and three stocking densities in the ChiloC Island, Southern Chile.

2. Material and methods 2.1. Experimental

organisms

Oyster (Ostrea chiZensis Philippi, 1845) juveniles with a mean shell height of 11.63 f 2.76 mm and a mean live weight of 0.24 + 0.06 g, from a cohort produced using mass release over time (n = 400) in the Quempillen Hatchery, ChiloC Island, were utilized in this experiment. These juveniles (n = 8 100) were randomly distributed among 90 pearl nets using three stocking densities (60,90 and 120 per net). Pearlnets have a base dimensions of 35 cm X 35 cm. 2.2. Study site and experimental

design

Five sites were selected along the east coast of the Chilot Island, southern Chile, in existing aquaculture farming areas (Fig. 1). The Hueihue sampling site (Hueihue Bay) was located 500 m from a commercial oyster farm; the Linao sampling site (Linao Bay), was situated in a salmon farm; the Quempillen sampling site (Quempillen estuary) was located over a oyster natural bed; the Putemlin sampling site (Putemun Channel) was located around a mussel (Mytilus chilensis) farm, and the Yaldad sampling site (Yaldad Bay) was situated in a mussel farm. Sites were monitored monthly during 24 months (from

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Fig. 1. Map of the Child Island (southern Chile), showing the position of the five locations evaluated present study ( QuempillCn, Hueihue, Linao, Putemlin and Yaldad).

in the

1991 to September 1993). At each site, the pearl nets (5 mm) containing the three stocking densities (60, 90, 120 per net) were suspended in the water column at three different depths ( I,4 and 8 m) with two replicates. The pearl nets were cleaned every field trip if the amount of fouling organisms appeared to impede water circulation; and their mesh size adjusted according to the oyster size by changing the nets from 5 mm to 12 mm within the first 12 months of culture.

October

2.3. Field measurements Each month, shell heights (the maximum distance between dorsal (hinge) and ventral margin (Seed, 1980) and total live weight of 50 randomly selected oysters from each pearl net were measured using vernier callipers ( + 0.5 mm) and a portable A&D AK 120 balance (0.01 g) . Fouling organisms were removed from the oyster shell and their surface dried with towel paper before weighing. The environmental variables were determined at every depth at which the oysters were cultured and during half-tide situations. Water temperature

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( &O.l”C) and salinity ( fO.l p.p.t.) were measured using a WTW LF196 conductivity meter. Dissolved oxygen was measured using the Winkler titration method (Strickland and Parsons, 1982). Water samples for chlorophyll a and seston determination were collected with one replicate using a 1 1 Ruttner bottle and passed through a 200 pm mesh prior to filtration. The chlorophyll a concentration was determined using the spectrophotometric method of Strickland and Parsons ( 1982). The total particulate matter (TPM) , particulate organic matter (POM) and particulate inorganic matter (PIM) , were determined filtering 1 1 of water sample using 47 mm diameter Millipore AP40 filters, previously ashed for 2 h at 450°C and weighted (Jones and Iwama, 1991). Number of dead oysters were recorded in each net and percent mortalities calculated by expressing the numbers of dead at the end of the sampling interval (30 days) as a proportion of the number alive at the beginning of the interval. 2.4. Statistical analyses Analysis of variance (ANOVA) was used to determine any statistically significant differences in the data. Homogeneity of variance was evaluated using the Bartlett’s test (Sokal and Rohlf, 1981). To satisfy the assumption of normality and/or homogeneity of variance the growth data were transformed (logr) and arcsine transformation were carried out on mortality data which were measured as percentages. Monthly instantaneous growth rate was calculated as (C-+30) G3e= (log,(Z,+,/Z,)!(log~)) X30, where Z,,, is the mean shell height (cm) or live weight (g) of the current month; Z, is the mean shell height or live weight of the previous month; D is the number of days between observations (Ricker, 1975). The main variables temperature and chlorophyll a were strongly correlated (r = 0.83, P < 0.001)) making a multivariate regression analysis inappropriate because of the effect of multicollinearity. Single parameter regression analyses were carried out to determine the relative effects of the environmental variables on the growth rate of oysters. The statistical analyses were carried out using the SYSTAT 5.1 statistical package (Wilkinson, 1991).

3. Results 3.1. Environmental

variables

The water temperature ranged from a minimum of 9.2”C to a maximum of 18.8”C at the Quempilltn estuary (0.5 m), in July 1992 and January 1992, respectively. Among the other locations, temperatures ranged between 11.7”C to 16.3”C. Temperature differences in depth were detected (0.6-1.8”C) during November-February (warmest period) associated with stratification of the water column, with the exception of Quempilltn estuary. The annual cycles of temperatures were correlated between locations (P < 0.05, d.f. = 24) ; however, the mean temperatures between locations were different (P < 0.05). The warmer locations were Quempilltn and Putemun while the colder locations were Yaldad, Linao and Hueihue (Table 1).

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Table 1 Mean ( f se.) temperature study period (n = 72)

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and salinity for the water column at the five different locations

Location

Temperature

Quempillbn Putemtin Yaldad Linao Hueihue

14.7 13.6 11.2 11.7 12.3

(“C)

157

monitored

over the

f s.e.

Salinity(p.p.t.)

f s.e.

0.31 0.23 0.19 0.22 0.13

22.4 30.6 31.3 32.2 31.8

0.53 0.08 0.12 0.06 0.09

Salinity was generally within the range 28-33 p.p.t. presenting reduced seasonal variation at most locations. Within sampling site the salinity stratification was more pronounced during winter months (May-August), resulting from freshwater influx during rain storm events. Markedly reduced salinities, recorded at Quempillen estuary during the winter months was caused principally by the increased freshwater input from the Quempilltn river. The annual cycles of salinity were highly correlated between four locations (P cO.05, d.f. = 24)) presenting also, no significant differences between means over the period (Yaldad, Putemun, Linao, Hueihue; Table 1). Quempillen estuary showed a more seasonal variation and the mean salinity over the sampling period between the estuary and any of the other locations was different (P < 0.05). Chlorophyll a concentration varied seasonally presenting bi-annually blooms at the five sites, once in late summer or early fall (March-May) and again in spring (SeptemberNovember), Very low chlorophyll a values were observed during winter months (minimum 0.11 pg l- ’ in Hueihue Bay at 8 m, July 1992), while the maximum values were determined during the spring bloom (maximum 12.7 pg 1-r in Yaldad Bay at 4 m, November 1992). No statistically significant differences in chlorophyll a concentration (P > 0.05) were found between the different depths of culture at each location. Chlorophyll a concentrations did vary significantly between sites (P < 0.0 1) during the sampling period. The concentrations of chlorophyll a were significantly higher (P 0.05) with those of Linao Bay. The mean (and range) chlorophyll a concentration (pg 1-l) over the sampling period (n=72, obtained using the mean of two replicates, considering three depths and 24 months) were 4.84,0.4-8.3 for Quempillen, 2.71,0.3-6.9 for Putemun, 3.64, 0.1-12.7 for Yaldad, 4.92, 0.3-9.1 for Linao and 3.64, 0.1-8.3 for Hueihue. Particulate organic matter (POM) values closely corresponded to seasonal variation in chlorophyll a concentration, except for Linao Bay, where the concentration of POM showed low variability during the study period. Concentrations of POM were significantly (P < 0.01) higher at Linao Bay, location associated with the salmon farm than any other sampled location. No significant differences in the of POM were found in the water column within the locations (P>O.O5). The mean (and range) for POM concentration over the sampling period (II = 72) were 2.32 ( 1.2-8.2) mg l- ’ for Quempillen, 1.97 (0.94.7) mg 1-l for Putemtin, 2.67 (1.6.1-5.1) mg 1-l for Yaldad, 5.36 (2.1-8.4) mg 1-l for Linao, and 2.04

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Table 2 Mean squares (MS) and degree of freedom (DF) and probability (P) for the ANOVA for live weight of Ostrea chilensis after 24 months of age of experimental culture. The three sources of variation are site (five locations), depth ( 1.4 and 8 m) and stocking density (60.90 and 120 per net) Source

DF

MS

F

P

Site Dept Stocking density Error

4 2 2 3224

11.725 18.963 8.483 0.145

80.800 130.682 58.458

0.001 0.001 0.001

( 1B-6.3) mg l- ’ for Hueihue. Seston particulate inorganic matter PIM, were more variable throughout the study period, showing increasing concentrations during the winter months associated with heavy rain and wind storms. Concentration of PIM at all sites, were significantly higher (P < 0.001) at the lowest sampling in the water column. The Mean PIM concentration over the study period was higher at Quempilltn estuary differing significantly (P < 0.05)) from any of other locations. The mean (and range) for PIM concentration over the sampling period at the maximum depth (n= 24) were 12.63 (6.8-14.8) mg I-’ for Quempillen, 5.97 (4.1-8.78) mg I-’ for Putemun, 7.43 (5.6-9.2) mg 1-i for Yaldad, 4.95 (3.2-6.6) mg I-’ for Linao, and 5.34 (3.7-7.6) mg 1-l for Hueihue. The sea water dissolved oxygen among the different locations and depths ranged between a minimum of 6.8 mg 1-i to a maximum of 13.5 mg I- ’ over the study period; well over the minimum requirements by the oysters (Quayle, 1969). 3.2. Growth and husbandry conditions Amount of oyster growth after 24 month of age showed no significant differences between replicates within a site (P > 0.05). The oyster live weight growth after 24 months of age were significantly different between locations (P < 0.001) , positions in the water column (P < 0.001) and stocking densities (P < 0.001, see Table 2). The growth in shell height after 24 months of age was significantly different between locations (P
DF

MS

F

P

Site Depth Stocking density Error

4 2 2 3224

4.189 4.193 0.044 0.025

170.691 170.870 1.790

0.001 0.001 0.167

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159

Table 4 Mean ( f s.d.) for shell height and live weight of oysters grown at different locations after 24 months of age Location

Shell height (mm)

f s.d.

Live weight (g)

Quempilldn Putemtin Yaldad Linao Hueihue

36.6 39.2 41.1 48.2 43.8

6.1 6.5 5.9 6.2 6.9

14.5 16.0 17.1 23.0 18.5

f s.d. 5.7 6.6 6.1 6.8 6.4

in the Linao site followed by Hueihue, Yaldad, Putemlin and QuempillCn (Table 4) ; which presented significant differences between them (Tukey’s HSD multiple comparisons test, Wilkinson, 1991). In each of the five locations the average individual grew more slowly (P < 0.001) with increasing the depth of culture in the water column. Within each location, the oysters average live weight gain between the different stocking density decrease significantly with increasing the stocking density. However, for shell height gain the stocking density was not a significant effect. 3.3. Growth and environmental

variables

Most of the environmental variables varied between sites and in depth within a site. The shell height growth (C&) was affected by temperature (? range = 0.55-0.67, P < 0.05) and chlorophyll a (? range = 0.64-0.88, P < 0.05) in all sites at depths of 1 and 4 m, except Quempillkn estuary with ? = 0.12 and 0.21 (P > 0.05) for temperature and chlorophyll a respectively. In Quempillhn salinity was the variable that explained variation in amount of shell height growth (2 = 0.78, P < 0.05). The live weight instantaneous growth rate was related to POM (2 range = 0.62-0.76, P < 0.05) at Linao, Putemtin, Yaldad and Hueihue. The live weight and shell height growth (G& at a depth of 8 m, showed a negative relationship with the amount of PIM (P < 0.05) at all sites except Linao and Hueihue (Fig. 2). Variation in dissolved oxygen between sites and depths did not affect growth rate at any site. Seventy two percent of the experimental oysters survived over the 24 months of culture; survival was not affected by stocking density nor by the depth of culture in the water column. Many oyster died within the first month after transferring the juveniles to the natural environment. Significant differences in survival (P < 0.05) were found after 17 months of age among the different sites. QuempillCn estuary showed the lowest survival (62.4%), followed by Yaldad (66.7%).

4. Discussion The growth rates recorded in this study correspond to previous findings for 0. chilensis in suspended culture (Toro and Varela, 1988; Toro and Newkirk, 1991). Differences in growth rates (live weight and shell height) between the five geographically isolated sites were mainly related to food availability, with the exception of Quempillkn estuary, where

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0.300

QUEYPIILSN

. = Q.107

0.250

b = -0.009 r= a.807 p = 0.001

0.200

0.000

.

.

L,......_

D.0 2.D 4.0 0.0 8.0 10.012.014.0

PUTWUW

0.250 --

a= 0243 b = -0.024 c - a.739 p = 0.001

. 0.200 --

.

l

*

s: CJ 0.150.-

l

. ._j\_\ . .

0.100 --

.*.

.

. .

l

.*

0.050 --

0.000

.

e

0.0

2.0

4.0

6.0

0.300 0.250

0.200 0

s

I

YALDAD

10.0

*=

b = -0.021 r = a.648

. .

\

0.0

0.242

.

0.150 1

.*

‘.

l

l

.

p=

0.001

.

;;;I: :;“-, 0.0

2.0

Particulate

4.0

6.0

inorganic

Fig. 2. Ostrea chitensis. Influence on monthly instantaneous

8.0

matter

10.0 (mg/l)

growth rate C&from oysters mantained at the lowest depth in the water column, with a stocking density of 60 individuals per pearl net for 24 months (Quempill& Putemhn and YaIdad) , vs mean of particulate inorganic matter ( PIM)

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161

the low salinity ( < 20 p.p.t.) during several months every year was affecting the growth of the oysters. Similar results, regarding the effect of low salinity upon the growth rate of bivalves have been reported in the literature (Bernard, 1983; Bayne and Newell, 1983; Brown and Hartwick, 1988; Brown, 1988). The positive relation between POM and oyster growth found is in agreement with previous findings (Malouf and Breese, 1977; Widdows et al., 1979; Brown, 1988; Jones and Iwama, 1991). High growth rates of oysters in Linao bay were associated with high concentrations of chlorophyll a, high values of POM, high temperatures and salinities over 29 p.p.t. during the growing season, which results in a high scope for growth (Bayne and Newell, 1983; Winter et al., 1984b). These good growing conditions for oysters in Linao Bay are probably caused by a nutrient input made by the salmon farm (Jones and Iwama, 1991). Organic waste from fecal and some unutilized feed pellets, containing high amounts of Nitrogen may cause the elevated concentrations of chlorophyll and POM in the sea water of this area (Penczac et al., 1982; Kaspar et al., 1988). The significantly slower growth rates found at greater depth in the water column can not be clearly explained through the environmental variables in most cases within a site. Temperature, salinity and chlorophyll a showed no great difference in the depths where the experimental oysters were maintained. The amount of POM showed also no difference (P > 0.05) among the different depths. However, according to Widdows et al. ( 1979) and Vahl ( 1980) the increase in the PIM fraction can dilute the useful POM fraction of seston, thereby decreasing the rate of energy acquisition in bivalves. Studies by Wallace and Reinsnes ( 1985) confirmed the negative impact of PIM on Chlumys islundicu. In the present study, this negative relationship between the G3e and the amount of PIM was found in three locations at the deepest culture (8 m), affected by high amounts of PIM carried into the site by freshwater affluents (Quempillen, Putemun, and Yaldad Bay). This greater amount of PIM at greater depth may partially explain why lower growth rates were found at those depths. The relationship between POM and PIM is an important factor to consider in bivalve feeding and growth studies. However, it does not provide the necessary information on biochemical composition, nutritional value of the organic fraction (MacDonald and Boume, 1989; Navarro et al., 1993). MacDonald and Bourne (1989) working in Departure Bay, British Columbia, reported that at greater water depth the energy content of available particulate was lower. If these results apply to our study area, this may explain the lower growth rates at 8 m. The results of the present study indicate that the stocking density used in suspended culture of 0. chilensis in their first 24 months has a major effect on the live weight growth rate. In all five locations and three s of suspended culture monitored, the rate of live weight gain decreased with increasing stocking density, probably because of competition for food and the greater amount of silt accumulation between the oysters within the sampling period. Quayle and Newkirk (1989) concluded that high concentrations of silt, can affect the feeding efficiency of oysters. However, the differential growth rate obtained under different stocking densities in 0. chilensis, for live weight, did not affect the shell height growth rate. This lack of effect of stocking density on shell height is in accordance with the results obtained by DiSalvo and Martinez ( 1985) in the same species, using 180 and 400 juveniles per pearl net in the Herradura Bay, north of Chile. They found a lack of difference in growth between these oysters after 18 months of suspended culture. Holliday et al. ( 1991), Holliday

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et al. (1993) using different stocking densities in the Sydney rock oyster (Succostrea commercialis) found significant differences in shell length and whole weight. As stated by several authors (Askew, 1978; Spencer et al., 1985; Holliday et al., 1991, Holliday et al., 1993), the final stocking density for an oyster commercial culture should be based on economic considerations, because better growth of individual oysters cultured under low stocking densities can be unprofitable by the less effective use of the culture units and lease space. Mortality was high within the first month of culture in the natural environment; no apparent pattern was detected. Conditions of temperature or the change in culture system between the hatchery and the natural environment may probably account for this early mortality. The survival after 24 months was lower at Quempillen estuary, but in accordance with previous studies in the same estuary (Toro and Varela, 1988) and could be produced by the low salinity (Bernard, 1983), or high amount of PIM (Quayle and Newkirk, 1989)) combined with high seawater temperature. However, at present the hypotheses that a disease might have affected the oysters at this location can not be discarded. Further studies are needed to evaluate the relation between energy of suspended particulate material and growth rate of oysters in southern Chile. Also, we need to evaluate the contribution of the increasing number of salmon farms to the Nitrogen enrichment of surrounding waters, its relationship with phytoplankton growth and the suitability to establish a polyculture with bivalve mollusts in the Chit06 Island.

Acknowledgements This study was supported by the Fondo National de Investigation Cientffica y Tecnol6gica of Chile (FONDECYT) Grant 9 l-0897; Direction de Investigaci6n y Desarrollo de la Universidad Austral de Chile (Grant S-94-18) and the I.F.S. (Grant A/O621 ).

References Askew, C.G., 1978. A generalized growth and mortality model for assessing the economics of bivalve culture. Aquaculture, 14: 91-104. Bayne, B.L. and Newell, R.C., 1983. Physiologicalenergetics of marine molluscs. In: A.S.M. Saleuddin and K.M. Wilbur (Editors), The Mollusca: Physiology (Vol. 4, part 1). Academic Press, New York, pp. 407-515. Bernard, R.F., 1983. Physiology and the mariculture of some northeasten Pacific bivalve molluscs. Can. Spec. Publ. Fish. Aquat. Sci., 63: 24 pp. Boeuf, G. and Medina, A., 1990. Chile, the promise and the problems. World Aquaculture, 21: 14-24. Brown, J.R., 1988. Multivariate analyses of the role of environmental factors in seasonal and site-related growth variation in the Pacific oyster Crarsosrrea gigas. Mar. Ecol. P.S., 45: 225-236. Brown, J.R. and Hartwick, E.B., 1988. Intluences of temperature, salinity and available food upon suspended culture of the Pacific oyster, Crassostrea gigas. I. Absolute and allometric growth. Aquaculture, 70: 231-251. Bustos, E., Guihez, R., Olavanfa, A., Paredes, A. and Valencia, J., 1991. Desarrollo de tecnicas de producci6n de semillas y repoblaci6n de recursos bent6nicos. II Investigaciones en la ostra chilena Tiostrea chifensis (Philippi, 1845). Inst. Fom. Pesq. Chile. lnforme Tecnico (unpubl.), 23 pp. DiSalvo, L.H., Alar&i, E. and Martinez, E., 1984. Progress in hatchery production of seeds of Ostrea chifensis (Philippi, 1845). In: H. Fuentes, J. Castillo and L. DiSalvo (Editors), Proceedings International Symposium.

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