Reviews in Aquaculture, 1–46 doi: 10.1111/raq.12529 Sustainable large-scale production of European flat oyster (Ostrea edulis) seed for ecological restoration and aquaculture: a review Berenger Colsoul1,2 , Pierre Boudry3 , Marıa Luz Perez-Parall e4 , Ana Bratos Cetinic5 , Tristan Hugh-Jones6, Isabelle Arzul7 , Nicolas Merou 7, Karl Mathias Wegner8 , Corina Peter1 , Verena Merk1 and Bernadette Pogoda1,8 1 Biological Institute Helgoland, Alfred-Wegener-Institut Helmholtz-Zentrum fur€ Polar- und Meeresforschung, Helgoland, Germany 2 Faculty of Mathematics and Natural Sciences, Christian-Albrechts-Universitat€ zu Kiel, Kiel, Germany 3 LEMAR, Ifremer, CNRS, IRD, Univ. Brest, Plouzane, France 4 Instituto de Acuicultura, Universidade de Santiago de Compostela, Santiago de Compostela, Spain 5 Department of Aquaculture, University of Dubrovnik, Dubrovnik, Croatia 6 Atlantic Shellfish Ltd, Cork, Ireland 7 LGPMM, Ifremer, La Tremblade, France 8 Wadden Sea Station, Alfred-Wegener-Institut Helmholtz-Zentrum fur€ Polar- und Meeresforschung, List/Sylt, Germany Correspondence Abstract Berenger Colsoul, Alfred-Wegener-Institut Helmholtz-Zentrum fur€ Polar- und The conservation and active restoration of European flat oyster (Ostrea edulis) Meeresforschung, Am Handelshafen 12, populations are a major focus of ecological restoration efforts to take advantage 27570 Bremerhaven, Germany. of the wide-ranging ecosystem functions and services this species provides. Email: [email protected] Accordingly, additional and new demands for seed oysters have arisen. In com- mercial aquaculture (mariculture), the production of O. edulis is still largely Received 20 March 2020; In Revised form 3 based on natural seed collection. Considering the specific requirements, related to December 2020; accepted 17 December 2020. ecological restoration, such as the absence of pathogens and the preservation of high genetic diversity, the current supply is insufficient. Despite the development of breeding and controlled reproduction techniques for this species since the late 1930s, seed production today is mainly based on empirical concepts. Several of the issues that producers still face are already subjects of research; many others are still unanswered or even unaddressed. This review provides a summary of all available knowledge and technologies of O. edulis seed production. Furthermore, it provides a detailed reflection on implications for restoration, future challenges, open questions and it identifies relevant research topics for sustainable seed sup- ply. The study covers the following aspects on (i) biology of the species, (ii) stres- sors – including pathogens and pollutants, (iii) genetics, (iv) history of production technologies, (v) seed production in polls, (vi) seed production in ponds and (vii) seed production in hatcheries. Future research needs on sex deter- minism, gametogenesis, cryopreservation, nutrition, selective breeding, pathogens and disease, and the development of reliable protocols for production are high- lighted. Key words: breeding, hatchery, reproduction biology, shellfish, spat, technology. its culinary, medicinal and ecological virtues, this oyster Introduction species is today at the core of many scientific projects or In Europe, the conservation of the European flat oyster actions by governmental and non-governmental organiza- Ostrea edulis (Linnaeus 1758) populations is in the focus of tions for its aquaculture, restocking, restoration or reintro- ecological restoration efforts to profit from the ecosystem duction in its former range all over European coasts services of this biogenic reef-engineer species. Praised for (Pogoda et al. 2019). Ostrea edulis and its beds (referred to © 2021 The Authors. Reviews in Aquaculture published by John Wiley & Sons Australia, Ltd. 1 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. B. Colsoul et al. here as ‘reefs’) provide many ecosystem services and func- techniques does not allow for a regular, substantial and sus- tions such as substrate formation and biodiversity enhance- tainable seed production meeting the specific expectations ment (Haelters & Kerckhof 2009; Todorova et al. 2009). It and objectives of the two sectors (i.e. aquaculture and therefore contributes to objectives defined by: the OSPAR restoration; Pogoda et al. 2019). In addition to the previ- Convention for the Protection of the Marine Environment ously mentioned shortage of seeds, there are also different of the North-East Atlantic, the EU Habitats Directive objectives in regard to the need in seed quality. The needs (Directive 92/43/EEC) and the EU Marine Strategy Frame- of O. edulis aquaculture are generally focused on: survival, work Directive (Directive 2008/56/EC) (Pogoda 2019). growth, weight gain, gastronomic aspect (visual and con- Over the 20th century, European stocks of O. edulis have tent), tolerance to exoneration or resistance to diseases, been severely depleted by overfishing, leading to numerous whereas for ecological restoration, the needs are mainly reseeding and restocking projects, mostly based on translo- high genetic variability and survival and/or disease toler- cations (Bromley et al. 2016a; Pogoda 2019). Those ance (Sas et al. 2020). included 19th and 20th century translocations from adult, The higher the genetic diversity within a population, the seed and juveniles of O. edulis within Europe and from less vulnerable it is for any disturbance as for example being non-European areas to Europe (Bromley et al. 2016a). infected and depleted by a pathogen (Hughes et al. 2008). These shellfish movements, as a consequence, are most According to this, it seems obvious that any ecological likely responsible for the introduction and further dispersal restoration project will aim for the highest possible genetic of parasites and pests such as the introduction of bonamio- diversity in order to increase population resillience (e.g. fit- sis into Europe from the USA in 1979, the introduction of ness, response to diseases), avoid inbreeding and ensure its gill disease into Wales from the Netherlands in the 1960s long-term adaptability (e.g. changing environment). and the introduction of Asian rapa whelk into the Black Today, a plethora of ways of producing or collecting Sea from the Far East in 1949 (Zolotarev & Terentyev 2012; O. edulis seed exists, ranging from traditional methods Brenner et al. 2014; Bromley et al. 2016a). Some of these based on sea-based collection of seed to very modern pro- diseases and pests have drastically reduced or depleted the duction in controlled environments, that is land-based stocks and beds of O. edulis throughout European waters hatcheries. Protocols for the production and collection of (Zolotarev & Terentyev 2012; Pogoda 2019). As the aqua- O. edulis seed depend on site conditions, technology and culture of European flat oyster has also been affected exten- the physiological condition of the spawning broodstock. sively by some diseases, a large part of the oyster industry The knowledge about ecophysiological and environmental has turned away from cultivating this species (see Sec- drivers is still limited for this species and this limits the tion Bonamiosis). This has had obvious consequences for development of successful breeding methods. It is essential the development of production technologies when com- to define and compare technical achievements, research pared to other shellfish species of commercial interest, such gaps, advantages and disadvantages of different seed-supply as the Pacific oyster (Crassostrea gigas). technologies to identify optimal seed quality for the specific Today, as Lallias et al. (2010) have listed, oyster popula- goals and settings of ecological restoration. tion restoration can be conducted in three distinct ways: (i) For this reason, this review focuses on the description of The strategy of releasing larvae into the wild; (ii) The strat- production systems (Chapter 7) and biological knowledge egy of producing older seeds (spat) and releasing them into of O. edulis (Chapter 3–4). the wild; (iii) The strategy of translocating adult oysters. In addition, in Chapter 6, the history of seed production Considering the risks of transferring pathogens and inva- is reviewed to understand present production systems and sives by adults translocations and the potential negative future development. Depending on the historical period, impact on remaining wild beds, the third strategy should technological progress and geographical location, the sup- not be applied (Bromley et al. 2016a; Pogoda et al. 2019). ply of seed had different goals. The technological progress Given the fertility rate of O. edulis, the low survival rate of was always directly related to the goals, which were mainly larvae in the wild, the availability or the lack of suitable shaped by the demands of their historical period. From the substrates for settlement (Smyth et al. 2018; Colsoul et al. beginnings of aquaculture to today’s ecological restoration, 2020), as well as the lack of control within a restoration a short synthesis of the historical development of the supply area, the first strategy is certainly not viable unless applying of seed from O. edulis is presented here. it under specific, risk limiting conditions. Consequently, In order to overcome current barriers and limitations of the second strategy, seeding with juveniles (i.e. seed or oyster