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Impact of predation by gastropods and crabs recruiting onto culture enclosures on the survival of the scallop Euvola ziczac (L.) in suspended culture
Journal of Experimental Marine Biology and Ecology 244 (2000) 297–303
L
www.elsevier.nl / locate / jembe
Impact of predation by gastropods and crabs recruiting onto culture enclosures on the survival of the scallop Euvola ziczac (L.) in suspended culture ´ Luis Freites a , John H. Himmelman b , *, Cesar J. Lodeiros a a
´ Pesquera, Instituto Oceanografico ´ de Venezuela, Universidad de Oriente, Departamento de Biologıa Cumana´ 6101, Venezuela b ´ Departement de Biologie, Universite´ Laval, Quebec City, Quebec, Canada G1 K 7 P4 Received 15 May 1999; received in revised form 1 July 1999; accepted 6 October 1999
Abstract We evaluated the impact of predation from carnivores settling onto suspended culture enclosures on the production of scallops, Euvola ziczac, in the Golfo de Cariaco, Venezuela. Seven potential predator species were found on 70 pearl nets which were immersed from mid-February to mid-April 1994. The crabs Mythrax forceps and Pilumnus caribbaeus and the gastropod Cymatium poulseni, were found on a high proportion of the nets (56, 44 and 48%, respectively). Studies in which the various potential predator were maintained in pearl nets with 25 scallops indicated that six of the seven predators would cause significant mortality within 30 days. A single P. caribbaeus or C. poulseni destroyed 22–25 of the 25 scallops in 30 days. Observations in aquaria of attacks by three species of Cymatium suggested the scallops are subdued using secreted substances. High losses in production due to recruiting predators poses a major problem to growing E. ziczac, and possibly other tropical bivalves, in intermediate suspended culture. 2000 Elsevier Science B.V. All rights reserved. Keywords: Scallop; Euvola Ziczac; Suspension culture; Predation losses; Cymatium; Golfo de Cariaco
1. Introduction Many types of invertebrates prey on bivalves and a major element in the suspension culture strategy for commercially growing bivalves is the reduction of losses due to benthic predators (Quayle and Newkirk, 1990; Hickman, 1992). However, maintaining *Corresponding author. Tel.: 1 1-418-656-2131; fax: 1 1-418-656-2339. E-mail address: [email protected] (J.H. Himmelman) 0022-0981 / 00 / $ – see front matter 2000 Elsevier Science B.V. All rights reserved. PII: S0022-0981( 99 )00149-5
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bivalves in suspension does not guarantee against losses from predation, as many predators with pelagic larvae can recruit onto suspended enclosures (Ventilla, 1982; Quayle and Newkirk, 1990; Hardy, 1991; Friedman and Bell, 1996). In temperate seas, where the majority of aquaculture studies have been conducted, predation by species settling onto enclosures is usually a minor problem as most predators can not attain a size capable of attacking the cultured species within the grow-out period. However, this may be different in tropical regions where the growth rate of predators may be rapid. This has been suggested by two studies in the Golfo of Cariaco, Venezuela, where predators such as gastropods, of the genus Cymatium, and crabs recruit onto enclosures ´ and been associated with increases in mortality of cultured bivalves (Velez et al., 1995; Freites et al., 1995). The present study evaluates the impact of predation on the culture of juvenile scallops, Euvola ziczac (L.), in the Golfo de Cariaco. We first identify the types of predators which colonize suspended enclosures and which can rapidly attain a size where they can prey on scallops, and secondly quantify predation rates on scallops during intermediate culture.
2. Methods The study was carried out at Turpialito in the Golfo de Cariaco, northeastern Venezuela (108 279 300 N, 648 019 520 W). We evaluated the predators which might affect scallop culture, by identifying the species which recruited onto 70 pearl nets (6-mm mesh) which were suspended at 5–10 m in depth from 15 February 1994 to 17 April 1994. The carnivores found on the nets were identified using the descriptions of Warmke ´ and Abbott (1974) and Humphrey (1975) for gastropods and by Rodrıquez (1980) for decapod crustaceans. We subsequently quantified the impact of seven species which were potential scallop predators. We did this by measuring mortalities in 24 pearl nets, each stocked with 25 Euvola ziczac, which were suspended at 5 m in depth from a long-line on 20 April 1994. The scallops were from laboratory-produced spat (using the ´ techniques described by Velez and Freites, 1993) which had been grow in suspended culture to a mean shell height of 32.3 mm (S.D. 5 3.5) and a mean dry mass of 0.17 g (S.D. 5 0.01). For each of the seven predator species, one individual measuring near the mean size found for that species on the 70 pearl nets (Fig. 1A) was placed in each of three of the pearl nets. The predators were maintained in large tanks amply supplied with sea water between taking them from the collectors (17 April) and the beginning of the experiment (20 April). Three of the pearl nets were suspended without a predator, as a control for other sources of mortality. All pearl nets were collected 30 days later, on 20 May, to determine the numbers of living and dead scallops in each net. We further made observations in aquaria, continuously supplied with water pumped in from the Golfo de Cariaco, of the method of attack used by three gastropods of the genus Cymatium, as no signs of attack were observed on the shells of scallops eaten by these species. To insure that we did not disturb the organisms, the sides of the aquaria were covered except for a small zone across one wall through which the observations were made.
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Fig. 1. Percentage of pearl nets colonized (A) and mean density per net (B) for gastropod and crab predators settling onto 70 pearl nets which had been immersed for a 2-month period, 17 February to 17 April 1994, at Turpialito in the Golfo de Cariaco. Horizontal lines represent standard errors. Mean shell length of gastropod predators and carapace width of crab predators are indicated in parentheses.
3. Results The predators which colonized the highest proportion of the 70 pearl nets over the 2-month immersion period were two crabs, Mythrax forceps (A. Milne Edwards, 1875) (56% of the nets) and Pilumnus caribbaeus (Desbonne and Schramum, 1867) (44%), ¨ and the gastropod, Cymatium poulseni (Morch, 1877) (48%) (Fig. 1A). Another ¨ gastropod, Cymatium muricinum (Roding, 1798), was present on an intermediate proportion of net and the gastropod, Cymatium pileare L. 1758, and two other crabs, Menippe nodifrons (Stimpson, 1859) and Macrocoeloma diplacantum (Stimpson, 1886), were only found on a low number of nets. The mean density of the above predators on the nets followed a similar pattern (Fig. 1B). A number of other species colonized the
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pearl nets but were not likely predators of scallops. These included sea urchins, nudibranchs, cirripeds, anemones, sponges, bivalves and tunicates. Mortality rate in the experiments where each potential predator was individually maintained in pearl nets with 25 juvenile scallops indicated that mortalities were higher than in the pearl nets without predators (controls) for six of the predators (P , 0.05, Kruskal–Wallis comparisons with a control, Zar, 1984). Cymatium poulseni and Mythrax forceps inflicted 92–96% mortality over 30 days, Cymatium piliare and Pilumnus caribbaeus 48–56% mortality and Cymatium muricinum and Menippe nodifrons 35–36% mortality (Fig. 2). Macrocoeloma diplacantum did not appear to prey on Euvola ziczac as the mortality rate in pearl nets with this species was about the same as for the nets without predators (11.7 compared to 8.0%, P 5 0.55) and the scallops showed no signs of attacks. The estimated daily feeding rates on scallops for the six predators which caused significant mortality, adjusted for other mortality factors (thus subtracting the mean mortality in pearl nets without predators; 0.067 scallops day 21 ), varied markedly for the different predators, from 0.22 to 0.73 scallops day 21 (Table 1). These feeding rates are underestimates in that prey availability was not maintained constant, but decreased during the 30-day trials. The observations of gastropods feeding in aquaria indicated a similar method of attack for the three species of Cymatium. The first step was to climb onto the upper valve of a scallop and secondly the outer lip of the shell was inserted between the valves of the scallop, which prevented valve closure. Then the proboscis was extended to near the valve opening for about 4 min. The proboscis did not appear to touch the scallop. After this the gastropod withdrew the proboscis and outer lip but remained on the upper valve. After 15–25 min the valves of the scallop slowly opened. Then the gastropod slowly reinserted its shell lip between the valves and fed on the soft tissues for 4 to 16 h during which the scallop was partly or completely eaten. That the shells of the scallops opened
Fig. 2. Percentage mortality caused by various carnivores when placed individually in pearl nets stocked with 25 juvenile (32 mm) scallops Euvola ziczac for a 30-day period, 20 April to 20 May 1994, and in control nets which contained no predators. Horizontal lines represent standard errors.
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Table 1 Calculation of mortality losses from predators and other causes during suspended culture of juvenile Euvola ziczac in the Golfo de Cariaco a Predator
Feeding rate
Density
Mortality day 21
Cymatium poulseni Mythrix forceps Pilumnus caribbeaus Cymatium muricinum Cymatium pileare Menippe nodifrons
0.733 0.700 0.333 0.222 0.400 0.222
1.143 1.171 0.857 0.314 0.114 0.071
0.838 0.820 0.286 0.070 0.046 0.016
a
Total loss of scallops per day due to predation (sum of above) 5 2.075; loss of scallops per day from other causes (controls) 5 0.067; loss of scallops per day from all causes 5 2.141.
without a sustained physical attack by the gastropods suggested that the scallops were subdued using chemical substances.
4. Discussion We show that numerous carnivores colonize suspended enclosures in the Golfo de Cariaco. All likely originated from pelagic larvae, as the suspended pearl nets were isolated from the bottom. Losses due to predation from organisms recruiting from pelagic larvae would likely be a major obstacle in using suspension culture to produce Euvola ziczac in the Golfo of Cariaco. Earlier studies considering the potential for culturing E. ziczac focused on the effects of temperature, abundance and quality of the seston and of fouling on growth and ´ survival (Lodeiros and Himmelman, 1994, 1996; Velez et al., 1995; Lodeiros, 1996). Predators recruiting onto the suspended enclosures were removed at 4–6-week intervals during the grow-out phase to facilitate evaluating the factors under study. We show that many of carnivores recruiting onto suspended enclosures rapidly attain a size where they can prey on juvenile scallops. Our 30-day predation trails indicated that six of the carnivores studied (all of which had recruited from larval stages within 2 months prior to the experiment) would cause significant mortality of scallops in pearl nets. In the case of the gastropod Cymatium poulseni and the crab Mythrax forceps, 22–25 out of 25 scallops were destroyed in 30 days, with only one predator per pearl net. In our study, 80% of the pearl nets retrieved in April contained at least one of these two predators. Other carnivores destroyed scallops at a lower rate, but would cause considerable losses if the grow-out period were more prolonged. For Euvola ziczac, a grow-out period of 4–6 months is required for 30 ´ mm individuals to attain a commercial size of 60–70 mm (Velez et al., 1995; Lodeiros, 1996). Calculations taking into account the average abundance of the six predators on the 70 pearl nets in mid-April, after 2 months of immersion, and their daily predation rates as estimated in our 30-day experiment, indicate that these predators would cause a 50% mortality in pearl nets stocked with 25 juvenile (32 mm) scallops in 6 days (the calculated loss from the six predators together was 2.075 scallops day 21 per net, Table
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1). With an initial density of 40 juveniles, the maximum suggested by Ventilla (1982), a 50% mortality would occur in 10 days. This is an overestimate in that recruiting predators would take 2 months to feed at rates we used in the calculations. Nevertheless, it is clear that severe losses would occur in less than 2.5 months. Although we only quantified predators recruiting onto pearl nets during February to April, in the course of previous studies we have also observed that the most important of the predators, Mythrax forceps, Cymatium poulseni and Cymatium caribbaeus, recruit onto pearl nets deployed during other periods of the year. During these studies we further observed other carnivores which are potential predators of scallops, the gastropod Thais haemastoma floridana (Conrad, 1837) and portunid crabs. February to April corresponds to a period of wind-driven upwelling, which results in high primary productivity and favours growth of scallops (Lodeiros and Himmelman, 1994; Lodeiros, 1996). However, these conditions may also favour recruitment of carnivores and other organisms onto pearl nets as Urosa (1980) reports of high abundance of invertebrate larvae during January to April in the Golfo de Cariaco. Rates of recruitment and growth of predators likely varies seasonally and may be less during periods of eased upwelling (with lower primary productivity and high temperatures). The period of our study (February to May) represents the first months of intermediate culture for E. ziczac produced from the preceding reproductive season (August). The predation method which we observed for the three species of Cymatium was similar to that previously described by Houbrick and Fretter (1969) for the same genus and also for the genus Bursa. Houbrick and Fretter suggest that these gastropods secrete an anesthetizing substance. Perron et al. (1985) report that Cymatium muricinum is an important predator of several tridacnid bivalves in Micronesia. Although no previous study has examined the predatory activity of Cymatium poulseni, Freites et al. (1995) reported an increase in mortality of Euvola ziczac in suspended culture coincident with an increase of this species on the pearl nets. Also, mortalities associated with C. poulseni have also been noted when Pinna carnea and Pinctada imbricata were grown in suspended culture in the Golfo de Cariaco (Lodeiros, unpublished data). The high rate of loss due to predation by carnivores recruiting onto enclosures poses a major limitation to culturing Euvola ziczac in suspended culture in the Golfo de Cariaco. As the minimal commercial size of 60–70 mm in shell height, which would take a 4–6-month grow-out period when starting with 30-mm individuals, the impact of predators alone, would exclude the possibility of growing scallops to commercial size without cleaning or changing enclosures at least once. High mortalities from predators have also been noted during suspended culture studies on scallops (E. ziczac, and Lyropecten nodosus) in the Colombian Caribbean (J.-P. de La Roche, INVEMAR, Santa Marta, Colombia, personnel communication). A second factor reducing the feasibility of a prolonged grow-out period for E. ziczac in suspended culture is colonization of scallops and enclosures by fouling organisms, such as other bivalves, cirripeds and ´ anemones (Velez et al., 1995; Lodeiros, 1996; Lodeiros and Himmelman, 1996). The high vulnerability to both predators and fouling likely means that suspension culture is only feasible as an intermediate culture step for E. ziczac. Mortality due to predators settling onto culture enclosures is likely to be substantial when Euvola ziczac and other bivalves are grown in suspended culture in the Golfo de Cariaco and possibly other tropical areas. Steps, such as periodically transferring the
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bivalves to new enclosures, removing predators from enclosures, or developing biological controls of predators, will be required to limit the effects of predators, and will add to production costs.
Acknowledgements The study was supported by a grant from project No. S1-2456 of CONICIT (Consejo ´ Nacional de Investigaciones Cientificos y Tecnologicas). [SS]
References ´ Freites, L., Vera, B., Velez, A., Lodeiros, C., 1995. Efecto de la densidad sobre el crecimiento y la produccion secundaria de juveniles de Euvola (Pecten) ziczac (L.) bajo condiciones de cultivo suspendido. Ciencias Marinas 21, 361–372. Friedman, K.J., Bell, J.D., 1996. Effects of different substrata and protective mesh bags on collection of spat of the pearl oyster, Pinctada margaritifera (Linnaeus, 1758) and Pinctada maculata (Gould, 1850). J. Shellfish Res. 15, 535–541. Hardy, D. (Ed.), 1991. Scallop Farming, Fishing News Books, Oxford, p. 237. Hickman, R.W., 1992. Mussel cultivation. In: Gosling, E. (Ed.), The Mussel Mytilus: Ecology, Physiology, Genetics and Culture, Elsevier, New York, pp. 455–504. Houbrick, J.R., Fretter, V., 1969. Some aspects of the functional anatomy and biology of Cymatium and Bursa. Proc. Malacol. Soc. Lond. 38, 415–429. Humphrey, M. (Ed.), 1975. Sea Shells of the West Indies. A Guide to the Marine Molluscs of the Caribbean, Collins, London, p. 351. ´ Lodeiros, C. 1996. Influence des facteurs environnementaux sur la croissance du petoncle tropical Euvola ´ ´ (Pecten) zicac (L. 1758) cultive´ en suspension au Golfo de Cariaco, Venezuela. PhD thesis, Universite´ Laval, Quebec City, Canada. Lodeiros, C.J., Himmelman, J.H., 1994. Relation among environmental conditions and growth in the tropical scallop Euvola (Pecten) ziczac. Aquaculture 119, 345–358. Lodeiros, C.J., Himmelman, J.H., 1996. Influence of fouling on the growth and survival of the tropical scallop Euvola (Pecten) ziczac in suspended culture. Aquat. Res. 27, 749–756. Perron, F.E., Heslinga, G.A., Fagolimul, J.O., 1985. The gastropod Cymatium muricinum, a predator on juvenile tridacnid clams. Aquaculture 48, 211–221. Quayle, B.D., Newkirk, G.F., 1990. Farming bivalve molluscs: methods for study and development. In: Sandifer, P.A. (Ed.), Advances in World Aquaculture, World Aquaculture Society, Louisiana State University, Baton Rouge, p. 293. ´ ´ ´ Rodrıquez, G. (Ed.), 1980. Crustaceos decapodos de Venezuela, Instituto Venezolano de Investigaciones ´ Cientıficas, Caracas, p. 494. ´ diurna de la temperatura en la ensenada de Turpialito Urosa, L., 1980. Nauplii balanomorfos y variacion ´ del Instituto Oceanografico ´ Venezuela. Boletın de la Universidad de Oriente 19, 73–91. Ventilla, R.F., 1982. The scallop industry in Japan. Adv. Mar. Biol. 20, 310–382. ´ Velez, A., Freites, L., 1993. Cultivo de semillas de Pecten ziczac (L., 1758) bajo condiciones ambientales controladas (hatchery). In: Memorias IV Congreso Latinoamericano de Ciencias del Mar, pp. 311–317, Serie ocasional no. 2. ´ ` ´ N., 1995. Growth of the tropical scallop, Euvola Velez, A., Freites, L., Himmelman, J.H., Senior, W., Marın, (Pecten) ziczac (L.), in bottom and suspended culture in the Golfo de Cariaco Venezuela. Aquacuture 136, 257–276. Warmke, G.L., Abbott, R.T. (Eds.), 1974. Caribbean Sea Shells, Dover, New York, p. 348. Zar, J.H., 1984. Biostatistical Analysis, 2nd ed, Prentice-Hall, Englewood Cliffs, NJ.
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www.elsevier.nl / locate / jembe
Impact of predation by gastropods and crabs recruiting onto culture enclosures on the survival of the scallop Euvola ziczac (L.) in suspended culture ´ Luis Freites a , John H. Himmelman b , *, Cesar J. Lodeiros a a
´ Pesquera, Instituto Oceanografico ´ de Venezuela, Universidad de Oriente, Departamento de Biologıa Cumana´ 6101, Venezuela b ´ Departement de Biologie, Universite´ Laval, Quebec City, Quebec, Canada G1 K 7 P4 Received 15 May 1999; received in revised form 1 July 1999; accepted 6 October 1999
Abstract We evaluated the impact of predation from carnivores settling onto suspended culture enclosures on the production of scallops, Euvola ziczac, in the Golfo de Cariaco, Venezuela. Seven potential predator species were found on 70 pearl nets which were immersed from mid-February to mid-April 1994. The crabs Mythrax forceps and Pilumnus caribbaeus and the gastropod Cymatium poulseni, were found on a high proportion of the nets (56, 44 and 48%, respectively). Studies in which the various potential predator were maintained in pearl nets with 25 scallops indicated that six of the seven predators would cause significant mortality within 30 days. A single P. caribbaeus or C. poulseni destroyed 22–25 of the 25 scallops in 30 days. Observations in aquaria of attacks by three species of Cymatium suggested the scallops are subdued using secreted substances. High losses in production due to recruiting predators poses a major problem to growing E. ziczac, and possibly other tropical bivalves, in intermediate suspended culture. 2000 Elsevier Science B.V. All rights reserved. Keywords: Scallop; Euvola Ziczac; Suspension culture; Predation losses; Cymatium; Golfo de Cariaco
1. Introduction Many types of invertebrates prey on bivalves and a major element in the suspension culture strategy for commercially growing bivalves is the reduction of losses due to benthic predators (Quayle and Newkirk, 1990; Hickman, 1992). However, maintaining *Corresponding author. Tel.: 1 1-418-656-2131; fax: 1 1-418-656-2339. E-mail address: [email protected] (J.H. Himmelman) 0022-0981 / 00 / $ – see front matter 2000 Elsevier Science B.V. All rights reserved. PII: S0022-0981( 99 )00149-5
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bivalves in suspension does not guarantee against losses from predation, as many predators with pelagic larvae can recruit onto suspended enclosures (Ventilla, 1982; Quayle and Newkirk, 1990; Hardy, 1991; Friedman and Bell, 1996). In temperate seas, where the majority of aquaculture studies have been conducted, predation by species settling onto enclosures is usually a minor problem as most predators can not attain a size capable of attacking the cultured species within the grow-out period. However, this may be different in tropical regions where the growth rate of predators may be rapid. This has been suggested by two studies in the Golfo of Cariaco, Venezuela, where predators such as gastropods, of the genus Cymatium, and crabs recruit onto enclosures ´ and been associated with increases in mortality of cultured bivalves (Velez et al., 1995; Freites et al., 1995). The present study evaluates the impact of predation on the culture of juvenile scallops, Euvola ziczac (L.), in the Golfo de Cariaco. We first identify the types of predators which colonize suspended enclosures and which can rapidly attain a size where they can prey on scallops, and secondly quantify predation rates on scallops during intermediate culture.
2. Methods The study was carried out at Turpialito in the Golfo de Cariaco, northeastern Venezuela (108 279 300 N, 648 019 520 W). We evaluated the predators which might affect scallop culture, by identifying the species which recruited onto 70 pearl nets (6-mm mesh) which were suspended at 5–10 m in depth from 15 February 1994 to 17 April 1994. The carnivores found on the nets were identified using the descriptions of Warmke ´ and Abbott (1974) and Humphrey (1975) for gastropods and by Rodrıquez (1980) for decapod crustaceans. We subsequently quantified the impact of seven species which were potential scallop predators. We did this by measuring mortalities in 24 pearl nets, each stocked with 25 Euvola ziczac, which were suspended at 5 m in depth from a long-line on 20 April 1994. The scallops were from laboratory-produced spat (using the ´ techniques described by Velez and Freites, 1993) which had been grow in suspended culture to a mean shell height of 32.3 mm (S.D. 5 3.5) and a mean dry mass of 0.17 g (S.D. 5 0.01). For each of the seven predator species, one individual measuring near the mean size found for that species on the 70 pearl nets (Fig. 1A) was placed in each of three of the pearl nets. The predators were maintained in large tanks amply supplied with sea water between taking them from the collectors (17 April) and the beginning of the experiment (20 April). Three of the pearl nets were suspended without a predator, as a control for other sources of mortality. All pearl nets were collected 30 days later, on 20 May, to determine the numbers of living and dead scallops in each net. We further made observations in aquaria, continuously supplied with water pumped in from the Golfo de Cariaco, of the method of attack used by three gastropods of the genus Cymatium, as no signs of attack were observed on the shells of scallops eaten by these species. To insure that we did not disturb the organisms, the sides of the aquaria were covered except for a small zone across one wall through which the observations were made.
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Fig. 1. Percentage of pearl nets colonized (A) and mean density per net (B) for gastropod and crab predators settling onto 70 pearl nets which had been immersed for a 2-month period, 17 February to 17 April 1994, at Turpialito in the Golfo de Cariaco. Horizontal lines represent standard errors. Mean shell length of gastropod predators and carapace width of crab predators are indicated in parentheses.
3. Results The predators which colonized the highest proportion of the 70 pearl nets over the 2-month immersion period were two crabs, Mythrax forceps (A. Milne Edwards, 1875) (56% of the nets) and Pilumnus caribbaeus (Desbonne and Schramum, 1867) (44%), ¨ and the gastropod, Cymatium poulseni (Morch, 1877) (48%) (Fig. 1A). Another ¨ gastropod, Cymatium muricinum (Roding, 1798), was present on an intermediate proportion of net and the gastropod, Cymatium pileare L. 1758, and two other crabs, Menippe nodifrons (Stimpson, 1859) and Macrocoeloma diplacantum (Stimpson, 1886), were only found on a low number of nets. The mean density of the above predators on the nets followed a similar pattern (Fig. 1B). A number of other species colonized the
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pearl nets but were not likely predators of scallops. These included sea urchins, nudibranchs, cirripeds, anemones, sponges, bivalves and tunicates. Mortality rate in the experiments where each potential predator was individually maintained in pearl nets with 25 juvenile scallops indicated that mortalities were higher than in the pearl nets without predators (controls) for six of the predators (P , 0.05, Kruskal–Wallis comparisons with a control, Zar, 1984). Cymatium poulseni and Mythrax forceps inflicted 92–96% mortality over 30 days, Cymatium piliare and Pilumnus caribbaeus 48–56% mortality and Cymatium muricinum and Menippe nodifrons 35–36% mortality (Fig. 2). Macrocoeloma diplacantum did not appear to prey on Euvola ziczac as the mortality rate in pearl nets with this species was about the same as for the nets without predators (11.7 compared to 8.0%, P 5 0.55) and the scallops showed no signs of attacks. The estimated daily feeding rates on scallops for the six predators which caused significant mortality, adjusted for other mortality factors (thus subtracting the mean mortality in pearl nets without predators; 0.067 scallops day 21 ), varied markedly for the different predators, from 0.22 to 0.73 scallops day 21 (Table 1). These feeding rates are underestimates in that prey availability was not maintained constant, but decreased during the 30-day trials. The observations of gastropods feeding in aquaria indicated a similar method of attack for the three species of Cymatium. The first step was to climb onto the upper valve of a scallop and secondly the outer lip of the shell was inserted between the valves of the scallop, which prevented valve closure. Then the proboscis was extended to near the valve opening for about 4 min. The proboscis did not appear to touch the scallop. After this the gastropod withdrew the proboscis and outer lip but remained on the upper valve. After 15–25 min the valves of the scallop slowly opened. Then the gastropod slowly reinserted its shell lip between the valves and fed on the soft tissues for 4 to 16 h during which the scallop was partly or completely eaten. That the shells of the scallops opened
Fig. 2. Percentage mortality caused by various carnivores when placed individually in pearl nets stocked with 25 juvenile (32 mm) scallops Euvola ziczac for a 30-day period, 20 April to 20 May 1994, and in control nets which contained no predators. Horizontal lines represent standard errors.
L. Freites et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 297 – 303
301
Table 1 Calculation of mortality losses from predators and other causes during suspended culture of juvenile Euvola ziczac in the Golfo de Cariaco a Predator
Feeding rate
Density
Mortality day 21
Cymatium poulseni Mythrix forceps Pilumnus caribbeaus Cymatium muricinum Cymatium pileare Menippe nodifrons
0.733 0.700 0.333 0.222 0.400 0.222
1.143 1.171 0.857 0.314 0.114 0.071
0.838 0.820 0.286 0.070 0.046 0.016
a
Total loss of scallops per day due to predation (sum of above) 5 2.075; loss of scallops per day from other causes (controls) 5 0.067; loss of scallops per day from all causes 5 2.141.
without a sustained physical attack by the gastropods suggested that the scallops were subdued using chemical substances.
4. Discussion We show that numerous carnivores colonize suspended enclosures in the Golfo de Cariaco. All likely originated from pelagic larvae, as the suspended pearl nets were isolated from the bottom. Losses due to predation from organisms recruiting from pelagic larvae would likely be a major obstacle in using suspension culture to produce Euvola ziczac in the Golfo of Cariaco. Earlier studies considering the potential for culturing E. ziczac focused on the effects of temperature, abundance and quality of the seston and of fouling on growth and ´ survival (Lodeiros and Himmelman, 1994, 1996; Velez et al., 1995; Lodeiros, 1996). Predators recruiting onto the suspended enclosures were removed at 4–6-week intervals during the grow-out phase to facilitate evaluating the factors under study. We show that many of carnivores recruiting onto suspended enclosures rapidly attain a size where they can prey on juvenile scallops. Our 30-day predation trails indicated that six of the carnivores studied (all of which had recruited from larval stages within 2 months prior to the experiment) would cause significant mortality of scallops in pearl nets. In the case of the gastropod Cymatium poulseni and the crab Mythrax forceps, 22–25 out of 25 scallops were destroyed in 30 days, with only one predator per pearl net. In our study, 80% of the pearl nets retrieved in April contained at least one of these two predators. Other carnivores destroyed scallops at a lower rate, but would cause considerable losses if the grow-out period were more prolonged. For Euvola ziczac, a grow-out period of 4–6 months is required for 30 ´ mm individuals to attain a commercial size of 60–70 mm (Velez et al., 1995; Lodeiros, 1996). Calculations taking into account the average abundance of the six predators on the 70 pearl nets in mid-April, after 2 months of immersion, and their daily predation rates as estimated in our 30-day experiment, indicate that these predators would cause a 50% mortality in pearl nets stocked with 25 juvenile (32 mm) scallops in 6 days (the calculated loss from the six predators together was 2.075 scallops day 21 per net, Table
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1). With an initial density of 40 juveniles, the maximum suggested by Ventilla (1982), a 50% mortality would occur in 10 days. This is an overestimate in that recruiting predators would take 2 months to feed at rates we used in the calculations. Nevertheless, it is clear that severe losses would occur in less than 2.5 months. Although we only quantified predators recruiting onto pearl nets during February to April, in the course of previous studies we have also observed that the most important of the predators, Mythrax forceps, Cymatium poulseni and Cymatium caribbaeus, recruit onto pearl nets deployed during other periods of the year. During these studies we further observed other carnivores which are potential predators of scallops, the gastropod Thais haemastoma floridana (Conrad, 1837) and portunid crabs. February to April corresponds to a period of wind-driven upwelling, which results in high primary productivity and favours growth of scallops (Lodeiros and Himmelman, 1994; Lodeiros, 1996). However, these conditions may also favour recruitment of carnivores and other organisms onto pearl nets as Urosa (1980) reports of high abundance of invertebrate larvae during January to April in the Golfo de Cariaco. Rates of recruitment and growth of predators likely varies seasonally and may be less during periods of eased upwelling (with lower primary productivity and high temperatures). The period of our study (February to May) represents the first months of intermediate culture for E. ziczac produced from the preceding reproductive season (August). The predation method which we observed for the three species of Cymatium was similar to that previously described by Houbrick and Fretter (1969) for the same genus and also for the genus Bursa. Houbrick and Fretter suggest that these gastropods secrete an anesthetizing substance. Perron et al. (1985) report that Cymatium muricinum is an important predator of several tridacnid bivalves in Micronesia. Although no previous study has examined the predatory activity of Cymatium poulseni, Freites et al. (1995) reported an increase in mortality of Euvola ziczac in suspended culture coincident with an increase of this species on the pearl nets. Also, mortalities associated with C. poulseni have also been noted when Pinna carnea and Pinctada imbricata were grown in suspended culture in the Golfo de Cariaco (Lodeiros, unpublished data). The high rate of loss due to predation by carnivores recruiting onto enclosures poses a major limitation to culturing Euvola ziczac in suspended culture in the Golfo de Cariaco. As the minimal commercial size of 60–70 mm in shell height, which would take a 4–6-month grow-out period when starting with 30-mm individuals, the impact of predators alone, would exclude the possibility of growing scallops to commercial size without cleaning or changing enclosures at least once. High mortalities from predators have also been noted during suspended culture studies on scallops (E. ziczac, and Lyropecten nodosus) in the Colombian Caribbean (J.-P. de La Roche, INVEMAR, Santa Marta, Colombia, personnel communication). A second factor reducing the feasibility of a prolonged grow-out period for E. ziczac in suspended culture is colonization of scallops and enclosures by fouling organisms, such as other bivalves, cirripeds and ´ anemones (Velez et al., 1995; Lodeiros, 1996; Lodeiros and Himmelman, 1996). The high vulnerability to both predators and fouling likely means that suspension culture is only feasible as an intermediate culture step for E. ziczac. Mortality due to predators settling onto culture enclosures is likely to be substantial when Euvola ziczac and other bivalves are grown in suspended culture in the Golfo de Cariaco and possibly other tropical areas. Steps, such as periodically transferring the
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bivalves to new enclosures, removing predators from enclosures, or developing biological controls of predators, will be required to limit the effects of predators, and will add to production costs.
Acknowledgements The study was supported by a grant from project No. S1-2456 of CONICIT (Consejo ´ Nacional de Investigaciones Cientificos y Tecnologicas). [SS]
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