Stocking density effect on the growth and mortality of juvenile European flat oyster (Ostrea edulis Linnaeus, 1758)

Abstract

The effect of stocking density on the growth and mortality of the European flat oyster (Ostrea edulis Linnaeus, 1758) reared in lantern nets was evaluated, starting from spat up to the end of juvenile phase. Oysters were deployed in a raft on the Basque coast (SE Bay of Biscay) for 18 months. Oysters were divided into four densities ranging from 25% to 100% of surface coverage. At the end of the experiment, oysters from an initial mean height and wet weight of 22.79 ± 3.70 mm and 1.00 ± 0.30 g reached mean values of 55.86 ± 8.21 mm and 19.08 ± 9.66 g, respectively. Although significant differences were detected in the growth of oysters reared at different stocking densities, these differences were not density dependent. On the other hand, mortality increased with time showing relatively high values (27%–38%), but especially at the end of the study when oysters at the highest density showed values up to 50%. In conclusion, stocking density had no effect on the growth, but had a negative effect on the survival at the highest density. A stocking density of 75% is recommended as the optimum for rearing O. edulis in the Basque coast.

INTRODUCTION

Offshore mollusc production is an emerging activity in waters of the Basque Country, Spain (SE Bay of Biscay). However, there is also interest in diversifying the production by cultivating new species such as the European flat oyster (Ostrea edulis Linnaeus, 1758). Indeed, the flat oyster is an attractive candidate not only because of its high market demand (van der Schatte Oliver et al., 2020), but also because natural populations in Europe have dropped dramatically and much effort is dedicated for the restoration of this native species (Maathuis et al., 2020). Although the production of flat oysters in Basque waters seems feasible (González et al., 2017), culture techniques still need optimisation. For instance, high stocking density may lead to space and food limitation causing reductions of growth and survival in bivalves (Liu et al., 2019; Taylor et al., 1997), especially when individuals attain a larger size (Cubillo et al., 2012; Fréchette et al., 1992). However, although stocking density can have important influence on the success of aquaculture operations (Fréchette, 2005), very few studies address this issue on O. edulis (Carlucci et al., 2010; Jarayabhand, 1988; Sheldom, 1968). Therefore, the aim of the present study was to assess the effect of stocking density on the growth and mortality of flat oysters, from spat to the end of juvenile phase.

MATERIAL AND METHODS

The study was conducted in a raft installed in Mutriku (43°18′40.35′′, 2°22′36.03′′) on the Basque coast. Flat oysters obtained from a hatchery were reared in a suspended system consisting of cylindrical vertical layered polyethylene lantern nets and were deployed at 1 m depth. From May 2018 to January 2019, a lantern net of 4.5 mm mesh size and flat oysters with an initial mean height and weight of 22.79 ± 3.70 mm and 1.00 ± 0.30 g were used, while after the thinning out, from January 2019 to November 2019, a lantern net of 9 mm mesh size and flat oysters of a mean height and weight of 39.54 ± 7.79 mm and 6.03 ± 3.39 g were used. In each lantern net four experimental stocking density treatments were assayed using 4 levels of the lantern net with a diameter of 50 cm and a surface area of 0.196 m² per level (Figure 1). The selected densities corresponded to 25%, 50%, 75% and 100% of surface coverage of each level and were estimated covering all the surface of the lantern level, counting the number of oysters to determine 100% coverage and back calculated from there. Hence, densities of 135, 270, 405 and 540 oysters level⁻¹ were cultivated before the thinning out and densities of 33, 66, 99 and 132 oysters level⁻¹ were used after the thinning out (Table 1). Samplings were carried out approximately every one or two months during the experiment. At each sampling time, all the oysters of each stocking density were counted to calculate mortality. However, for height and wet weight determination, 135 flat oysters were measured per level before the thinning out, while after the thinning out all the individuals of each level were measured. Once the measurements were made, live and dead oysters were returned to their corresponding lantern net level not to affect the stocking density. Cumulative mortality (%) was estimated as: [(Number of oysters placed in lantern net level at T₀ – Number of oysters alive at T_i)/(Number of oysters placed in lantern net level at T₀)] × 100, where T₀ = Time 0 and T_i = Time of a particular sampling. Shell height and total wet weight were measured with a digital calliper (0.01 mm of precision) and a balance (0.01 g of precision). Additionally, environmental parameters were determined monthly using a CTD sensor.

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TABLE 1 Number of individuals used for each stocking density along the experiment

Period	May 2018 to January 2019	January 2019 to November 2019
Lantern net mesh size (mm)	4.5	9
Oyster mean shell height (mm)	22.79 ± 3.70	39.54 ± 7.79
Oyster mean wet weight (g)	1.00 ± 0.30	6.03 ± 3.36
Stocking density	Individuals level−1	Individuals m−2	Individuals level−1	Individuals m−2
25%	135	688	33	168
50%	270	1377	66	336
75%	405	2066	99	505
100%	540	2755	132	673

Kruskal–Wallis one-way test followed by the Mann–Whitney U post hoc test were employed for comparing the median values of height and weight among stocking density treatments at the thinning out period and at the end of the study (α = 0.05). Chi-square test followed by Fisher post hoc test (Shan & Gerstenberger, 2017) was used to determine differences in mortality rates (α = 0.05).

RESULTS AND DISCUSSION

Environmental variables were in the range of those previously reported in Mutriku (Bilbao et al., 2020) showing seasonal temperature fluctuations (12.4–23.5°C), low chlorophyll a concentrations (0.05–1.3 μg L⁻¹) and relatively constant water salinity (34.1–35.2) and oxygen saturation (93.3%–112.1%) (Figure 2). The mortality of flat oysters reared at different densities increased throughout the exposure period (Table 2) and in most samplings, oysters at the lowest stocking density showed higher mortality than oysters at the highest density probably because a minimum density is needed for a good performance in gregarious animals (Okamura, 1986). At the thinning out period, mortality values tended to equalise ranging from 33% to 40%, without significant differences among different stocking densities. At the end of the study, oysters at the highest stocking density presented significantly higher mortality values (52%) than oysters reared at the remaining densities (27%–38%, Table 2). Mortality values at the end of the study were in the range of previously reported values in flat oysters grown in the Mediterranean Sea (26%–75%) (Cano & Rocamora, 1996), but were higher than those found in the North Sea (1%–3.2%) (Pogoda et al., 2011). High stocking density had no effect on mortality at most of the samplings, as occurred in other studies (Carlucci et al., 2010; Chávez-Villalba et al., 2010). In contrast, at the end of the study, significantly higher mortality was detected at the highest stocking density comparing with the remaining densities, but we ignore what would have happened if one extra sampling had taken place. However, a density dependent mortality was also reported in other bivalves (Liu et al., 2019; Taylor et al., 1997). The highest water temperatures recorded in summer in Mutriku could have contributed partly to increase mortality at all stocking densities, since temperatures over 19°C appear to induce summer die-offs in France (Samain et al., 2007). Nevertheless, other causes not measured herein, such as Marteilia refringens (Alderman, 1979) or Bonamia ostreae (Pichot et al., 1980), could not be discarded since all the densities presented substantial mortalities (> 27%). On the other hand, the physiological stress coupled with gonad maturation could be considered negligible in juvenile or immature oysters since spawning-associated weight loss was not detected. Accordingly, the abundance of epifauna or predators was not very remarkable.

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TABLE 2 Cumulative mortality (%) of flat oysters at each sampling time and for each of the stocking density treatments

Sampling time	Immersion days	Stocking density
25%	50%	75%	100%
May-18	0	0	0	0	0
June-18	17	17.8	3.3	0.7	0
July-18	64	31.1	6.7	7.4	5.6
August-18	–	–	–	–	–
September-18	–	–	–	–	–
October-18	147	40	29.3	30.1	33.3
November-18	–	–	–	–	–
December-18	204	40	32.6	38.3	35.7
January-19	261	40a	32.6a	39a	40.4a
February-19	–	–	–	–	–
March-19	295	0	0	0	0
April-19	–	–	–	–	–
May-19	352	6.1	0	0	3.2
June-19	–	–	–	–	–
July-19	413	18.2	0	4	10.3
August-19	–	–	–	–	–
September-19	492	27.3	10.4	21.2	25.4
October-19	–	–	–	–	–
November-19	546	27.3a	35.8a	38.4a	51.6b

Flat oysters reared at different densities increased in shell height and total wet weight throughout the study. The growth was more pronounced in spring-summer than in autumn-winter as occurred previously (Cano & Rocamora, 1996; Carlucci et al., 2010; Pogoda et al., 2011) (Figure 3). At the end of the experiment, flat oysters reached mean values of 55.86 ± 8.21 mm in height and 19.08 ± 9.66 g in weight. Significant differences were found in median height and weight values of flat oysters reared at different densities, both at the thinning out period and at the end of the study, but these differences did not follow any stocking density gradient (Figure 4). In contrast, flat oysters cultivated at low stocking density (45 ind/reply) in the Taranto Sea (Italy) showed higher growth than those reared at high stocking density (90 ind/reply) (Carlucci et al., 2010). These authors indicated that oysters cultivated at low stocking density have a higher availability of suspended organic particles and feed more, growing faster and attaining greater sizes. Although the tested stocking densities might not be fully comparable with this study, the inconsistency of the results could be partly due to the differences in the mean temperature and chlorophyll a concentrations which were higher in Taranto Sea (18.5°C and 1.2 μg L⁻¹, respectively; Carlucci et al., 2010) than in Mutriku (17.5°C and 0.4 μg L⁻¹) or to the difference in the mean size of the oysters (58.39 ± 8.41 mm vs. 39.54 ± 7.79 mm). Accordingly, other studies also support that there is an inverse relationship between the culture density and growth in different bivalves such as in Pecten maximus (Maguire & Burnell, 2001), Nodipecten nodosus (López-Navarro et al., 2010), Crassostrea gigas (Chávez-Villalba et al., 2010) and Pteria sterna (Treviño et al., 2019).

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CONCLUSION

In conclusion, stocking density had not a relevant effect on the growth but produced a negative effect on the mortality at the highest stocking density at the end of the study. Thus, although from an economical point of view the highest stocking density would be more cost-effective, the intermediate stocking density of 75% of surface coverage (where no mortality effect was detected) is recommended for rearing O. edulis from spat to the end of juvenile phase. However, future studies should be carried out to evaluate the effect of stocking density on flat oysters to market size. Finally, this work provided basic data for the optimisation of flat oyster grow-out phase contributing to the diversification of bivalve mollusc production in the Basque coast.

ACKNOWLEDGEMENTS

This work was supported by the Basque Government through DESOS and AVACON projects. We wish to thank AZTI staff and the Aquaculture School of Mutriku for their valuable assistance. AJ was beneficiary of the Basque Government's technologists training scholarship. This is contribution 1079 from AZTI, Basque Research and Technology Alliance (BRTA). I also declare that the funding statement included in the manuscript is appropriate (Department of Economic Development, Sustainability and Environment and Fisheries and Aquaculture Directorate through European Maritime and Fisheries Funds). Izaskun Zorita, correspondence author, on behalf of all the authors.

CONFLICT OF INTEREST

All authors have no conflict of interest.

AUTHOR CONTRIBUTIONS

Izaskun Zorita: Conceptualisation, funding acquisition, investigation, writing original draft.

Ainhoa Juez: Data curation, investigation, resources.

Oihana Solaun: Conceptualisation, investigation, visualisation, writing-review & editing.

Iñigo Muxika: Formal analysis, visualisation, writing-review & editing.

José Germán Rodríguez: Conceptualisation, investigation, writing-review & editing.

ETHICS

I declare that all individuals listed as authors qualify as authors and have approved the submitted version; that the work is original and is not under consideration by any other journal.

DATA AVAILABILITY STATEMENT

Data available on request from the authors.

PEER REVIEW

The peer review history for this article is available at .

References

Alderman, D.J. (1979) Epizootiology of Marteilia refringens in Europe. Marine Fisheries Review, 41(1/2), 67–69.

Bilbao, J., Muñiz, O., Rodríguez, J.G., Revilla, M., Laza‐Martínez, A. & Seoane, S. (2020) Assessment of a sheltered euhaline area of the southeastern Bay of Biscay to sustain bivalve production in terms of phytoplankton community composition. Oceanologia, 63, 12–26. [DOI: https://dx.doi.org/10.1016/j.oceano.2020.08.007].