Captive breeding of European freshwater mussels as a conservation tool : A review

This is a self-archived version of an original article. This version may differ from the original in pagination and typographic details. Author(s): Title: Year: Version: Copyright: Rights: Rights url: Please cite the original version: CC BY 4.0 https://creativecommons.org/licenses/by/4.0/ Captive breeding of European freshwater mussels as a conservation tool : A review © 2023 The Authors. Aquatic Conservation: Marine and Freshwater Ecosystems published by John Wiley & Sons Ltd. Published version Geist, Juergen; Thielen, Frankie; Lavictoire, Louise; Hoess, Rebecca; Altmueller, Reinhard; Baudrimont, Magalie; Blaize, Christine; Campos, Miquel; Carroll, Paul; Daill, Daniel; Degelmann, Wolfgang; Dettmer, Rainer; Denic, Marco; Dury, Pierrick; de Eyto, Elvira; Grunicke, Felix; Gumpinger, Clemens; Jakobsen, Per J.; Kaldma, Katrin; Klaas, Kunnar; Legeay, Alexia; Mageroy, Jon Hamner; Moorkens, Evelyn A.; Motte, Grégory; Nakamura, Keiko; Ondina, Paz; Österling, Martin; Pichler‐Scheder, Christian; Spisar, Ondřej; Reis, Joaquim; Schneider, Lea D.; Schwarzer, Arno; Selheim, Heidi; Soler, Joaquín; Taskinen, Jouni; Taylor, John; Strachan, Ben; Wengström, Niklas; Zając, Tadeusz Geist, J., Thielen, F., Lavictoire, L., Hoess, R., Altmueller, R., Baudrimont, M., Blaize, C., Campos, M., Carroll, P., Daill, D., Degelmann, W., Dettmer, R., Denic, M., Dury, P., de Eyto, E., Grunicke, F., Gumpinger, C., Jakobsen, P. J., Kaldma, K., . . . Zając, T. (2023). Captive breeding of European freshwater mussels as a conservation tool : A review. Aquatic Conservation : Marine and Freshwater Ecosystems, 33(11), 1321-1359. https://doi.org/10.1002/aqc.4018 2023 REVIEW ARTICLE Captive breeding of European freshwater mussels as a conservation tool: A review Juergen Geist 1 | Frankie Thielen 2 | Louise Lavictoire 3 | Rebecca Hoess 1 | Reinhard Altmueller 4 | Magalie Baudrimont 5 | Christine Blaize 6 | Miquel Campos 7,8 | Paul Carroll 9 | Daniel Daill 10 | Wolfgang Degelmann 11 | Rainer Dettmer 12 | Marco Denic 13 | Pierrick Dury 14 | Elvira de Eyto 15 | Felix Grunicke 16 | Clemens Gumpinger 10 | Per J. Jakobsen 17 | Katrin Kaldma 18,19 | Kunnar Klaas 19 | Alexia Legeay 5 | Jon Hamner Mageroy 20 | Evelyn A. Moorkens 21 | Grégory Motte 22 | Keiko Nakamura 23,24 | Paz Ondina 25 | Martin Österling 26 | Christian Pichler-Scheder 10 | Ondˇ rej Spisar 27 | Joaquim Reis 28 | Lea D. Schneider 29 | Arno Schwarzer 30 | Heidi Selheim 31 | Joaquín Soler 32 | Jouni Taskinen 33 | John Taylor 34 | Ben Strachan 35 | Niklas Wengström 36 | Tadeusz Zając 37 Correspondence Juergen Geist, Aquatic Systems Biology Unit, Department of Life Science Systems, Technical University of Munich, Mühlenweg 22, D-85354 Freising, Germany. Email: [email protected] Funding information COST (European Cooperation in Science and Technology), Grant/Award Number: COST Action CA18239 Abstract 1. Freshwater mussels are declining throughout their range. Their important ecological functions along with insufficient levels of natural recruitment have prompted captive breeding for population augmentation and questions about the usefulness and applicability of such measures. 2. This article reviews the current state of captive breeding and rearing programmes for freshwater mussels in Europe. It considers the various species, strategies, and techniques of propagation, as well as the different levels of effort required according to rearing method, highlighting the key factors of success. 3. Within the last 30 years, 46 breeding activities in 16 European countries have been reported, mainly of Margaritifera margaritifera and Unio crassus. Some facilities propagate species that are in a very critical situation, such as Pseudunio auricularius,Unio mancus, and Unio ravoisieri, or multiple species concurrently. In some streams, the number of released captive-bred mussels already exceeds the size of the remaining natural population. Juergen Geist, Frankie Thielen and Louise Lavictoire are the Principal authors. For affiliations refer to page 35 Received: 28 April 2023 Revised: 20 July 2023 Accepted: 31 August 2023 DOI: 10.1002/aqc.4018 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. © 2023 The Authors. Aquatic Conservation: Marine and Freshwater Ecosystems published by John Wiley & Sons Ltd. Aquatic Conserv: Mar Freshw Ecosyst. 2023;1–39. wileyonlinelibrary.com/journal/aqc 1 4. Rearing efforts range from highly intensive laboratory incubation to lower intensity methods using in-river mussel cages or silos. Most breeding efforts are funded by national and EU LIFE(+) grants, are well documented, and consider the genetic integrity of the propagated mussels. Limited long-term funding perspectives, the availability of experienced staff, water quality, and feeding/ survival during early life stages are seen as the most important challenges. 5. Successful captive breeding programmes need to be combined with restoration of the habitats into which the mussels are released. This work will benefit from an evidence-based approach, knowledge exchange among facilities, and an overall breeding strategy comprising multiple countries and conservation units. KEYWORDS aquaculture, captive breeding, conservation translocation, freshwater mussel culturing, Margaritifera margaritifera, propagation, reintroduction, Unio crassus 1|INTRODUCTION The global decline of freshwater biodiversity has prompted many efforts addressing its conservation (Geist, 2011). This holds particularly true for freshwater mussels, which are among the most threatened taxa throughout Europe (Lopes-Lima et al., 2017). From a conservation perspective, endangered freshwater mussels, particularly the freshwater pearl mussel (Margaritifera margaritifera L.), are considered target species for the conservation of aquatic ecosystems, as they simultaneously fulfil the criteria of flagship, indicator, keystone, and umbrella species (Geist, 2010). The continuing declines and lack of natural recruitment of freshwater mussels in Europe has led to an increasing number of rearing approaches for population augmentation. It has also led to controversies about the usefulness of captive breeding in the context of mussel conservation, particularly if such activities are not properly monitored or are conducted without considering habitat restoration (Preston, Keys & Roberts, 2007; Schmidt & Vandré, 2010; Gum, Lange & Geist, 2011; Patterson et al., 2018). Rearing methods developed for North American mussel species and conditions (Gatenby, Neves & Parker, 1996; Beaty & Neves, 2004; Neves, 2004; Jones, Mair & Neves, 2005; Barnhart, 2006; Hua & Neves, 2007; Patterson et al., 2018) have often been transferred to European mussel species, but without systematic evaluation of the success of such actions. Recent studies reveal that some captive breeding practices, such as the use of a low number of parents, can result in erosion of the genetic constitution of offspring compared with the original populations, both in freshwater mussels (Geist et al., 2021) as well as fishes (Stoeckle et al., 2022). Coadaptation or co-evolution of mussels to certain fish hosts (Geist & Kuehn, 2008; Taeubert et al., 2010; Taeubert, Gum & Geist, 2012; Salonen et al., 2017; Taskinen & Salonen, 2022), the effects of host fish age (Marwaha et al., 2019), duration of the parasitic phase (Marwaha et al., 2017), water temperature (Taeubert, El-Nobi & Geist, 2014), and rearing conditions (Eybe et al., 2013; Eybe et al., 2015; Lavictoire et al., 2016; Lavictoire et al., 2020) all have an impact on the performance of captive-bred mussels, with potential consequences if such interactions are not taken into account. Crossexposure experiments indicate that stock origin and environmental conditions affect both the survival and the growth of juvenile freshwater mussels after their release (Denic et al., 2015). Based on an earlier review of European and North American captive breeding programmes, Gum, Lange & Geist (2011) suggested that captive breeding should only be a rescue tool to retain the evolutionary potential of priority populations that would not persist long enough to benefit from habitat restoration practices. This is in line with Rytwinski et al. (2021), who identified a need for evidence to evaluate the effectiveness of conservation-oriented captive breeding and release programmes for imperilled freshwater mussels. This is particularly important given the worldwide increase in captive breeding programmes for highly threatened freshwater mussels (Strayer et al., 2004; Barnhart, 2006; Thomas, Taylor & Garcia de Leaniz, 2010; Gum, Lange & Geist, 2011; Patterson et al., 2018). The aim of this article is to review the current state of freshwater mussel captive breeding programmes in Europe. The critical challenges associated with these activities were identified from personal interviews with key groups involved in the captive breeding of freshwater mussels throughout Europe, including information on the context of these programmes, the coverage of species, the intensity and type of rearing practices, and their timelines. This information was then used to make recommendations for effective conservation of freshwater mussels through captive breeding, and to identify priorities for its future use. 2|METHODS All the institutions and organizations listed in Table 1were contacted by one of the three main authors and interviewed using the same questions, to gather standardized information. The interviews took 2GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 Captive breeding methods of freshwater mussels utilized by different projects in Europe. See table legend for explanation of abbreviations. Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References Austria Upper Austria/ blattfisch e.U. Consultancy Company M.m. 2011–present LI: medium–high HF: Salmo trutta (hatchery) MB: kept permanently at the breeding facility IC: incubator boxes OC: sediment boxes, Buddensiek cages, and mussel silos in the stream In total: 2,100 reared ind. still in caging systems. 30 mussels (11 years old) released (compared with 19 remaining adult mussels in this population) Survival of mussels >1 mm in the first winter is about 50% National & EU PM and JM High mortality among juveniles shortly after harvesting High mortality among parent mussels, with low fitness presumed Long-term funding unsure Gumpinger C., Daill D. (pers. comm., 2022) Pichler-Scheder C. (pers. comm., 2011) Geist et al. (2021) Belgium Ardennes Region/ Service Public de Wallonie (SPW) Since 2017 cooperation with Luxembourg (see Luxembourg in this Table) M.m. 2005–present LI: medium HF: Salmo trutta (hatchery) MB: glochidia collected in the field; mussels stay in the river IC: none OC: side channel in catchment of rivers Arlune and Rulles Between 2007 and 2014, 95% of freshly metamorphosed mussels released in two outdoor rearing channels. No survival or no mussels found during follow-up monitoring in the years 2007, 2014, and 2018 5% of juveniles released directly in River Anlier (2% of this population come from cultured ind.)Rulles River: 99% of this population come from cultured ind. National & EU LIFE-project PM Limited budget and staff Cleaning of channels difficult because of changing staff Emerging beaver populations make it difficult to find good release sites Geist et al. (2021); Motte G. (pers. comm., 2022) Czech Republic South Bohemia/ Nature Conservation Agency of the M.m. 1990–present LI: high HF: Salmo trutta (wild and hatchery) Approx. 1,000 released into Zlatý potok and approx. 50,000 released National & EU PM Collection of natural food (detritus) in winter difficult Spisar O., Zelenková E., ˇ Svaˇ ríˇ cková J. & Dort B. (pers. comm., 2022) (Continues) GEIST ET AL.3 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References Czech Republic, ˇ Sumava National Park Administration; practical work Gammarus cz, s.r. o., Bohumil Dort West Bohemia BIVALVIA s.r.o.: Ondˇ rej Spisar MB: glochidia collected in the field IC: incubator boxes OC: sediment boxes in side channels into Blanice in 1995–; in 2019, 72 ind. 6+; in 2022, 322 ind. 6+ Blanice: released juveniles make up 10% of the total population Vltava River: May/June 2021, release of 1,000 8– 10 year olds; May/June 2022, release of >1,000 6–7 year olds, 1,000 5-year-old ind. are planned to be released 2023/2027 Malse River: approx. 300 small juveniles have already been released; approx. 1,000 ind. are planned to be released in 2022/24 Luˇzní Potok: 810 juveniles aged 3+ to 5+years released in 2016– 2019 Difficulties in monitoring released juveniles Vltava River: carplike fish (cyprinids) spread upstream from Lipno dam, with impacts on trout, which are being displaced from mussel localities Long-term funding is unsure Ensure the quality and quantity of breeding station staff Hruska (1999); Hruska (2000); ˇ Svanyga et al. (2013); Simon et al. (2015); Simon et al. (2017); Bílý et al. (2018); ˇ Cerná et al. (2018); Bílý et al. (2021); Miloˇ s Holub (pers. Comm., 2022) Estonia North of Estonia/ State Forest Management Centre M.m. 2020–present LI: medium–high HF: Salmo trutta (wild) MB: mussels stay in the river and are not disturbed. Host fish are In total 10,000 0+ mussels in incubator boxes and approx. 440 1+and 150 2+ mussels in the National & EULIFE projects No –plan to do in near future Mussel growth in incubator boxes is low (less than 1 mm on average) by the end of the first autumn; as a result, mortality in Klaas K. & Kaldma K. (pers. comm., 2023) 4GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References caught by electrofishing and detached juveniles are collected with nets. Approx. 100 infested trout are caught from between three and seven river sections and transported to a quarantine centre. If possible, host fish are released after the collection of M.m. juveniles IC: incubator boxes OC: Buddensiek cages native river in Buddensiek cages Incubator boxes: during the first summer juvenile survival was 70%. During the first year, mussel survival was approx. 60% Buddensiek cages in river: in the first summer juvenile survival was 25%. In the first winter 0+mussel survival was 17%. In the second summer 1-year-old mussel survival was 65%. In the second winter 1+mussel survival was 82% the cages was high in the first winter Silt and fine sediments in the river Active beaver population, despite constant hunting Finland University of Jyväskylä/ Konnevesi Research Station M.m. 2016–present LI: high HF: Salmo trutta (hatchery), Salmo salar (hatchery). Local fish used, if available in hatcheries. If local fish not available, at least the preferred host (salmon or trout) used, if the most suitable host fish species is known. If it is not known whether the M.m. River Mustionjoki/ Svartå: 200 1-yearold juveniles introduced in gravel boxes in 2019; 93% alive after 3 years. 14,000 0+ juveniles introduced in gravel boxes in 2022. Current population size in river is 1,200. Adult mussels have lost their National, EU & EU LIFE projects PM Problem with copper in pipes when new facility established Only two suitable detritus sources. Collection of detritus difficult in winter Problems with clogging of culture installations Detachment of high numbers of juveniles within a short period of time—high Hyvärinen et al. (2021) Taskinen J. (pers. comm., 2022). (Continues) GEIST ET AL.5 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References population is adapted to salmon or trout, then both species are used at the beginning MB: glochidia collected in the field and glochidia collected from adult mussels kept in the facility. In two cases, mussels in poor condition were rehabilitated in the facility for 2 years and they started releasing glochidia. Adult mussels fed with shellfish diet, Nanno, and detritus IC: incubator boxes and trough/flume. Pulsed flowthrough system tested but not in regular use now. Fed with shellfish diet, Nanno, and detritus OC: in-river cages, sediment boxes, and Buddensiek cages reproductive capacity, but recovered with 2-year rehabilitation in captivity River Ähtävänjoki/ Esseå: 1,200 2-year-old juveniles introduced in gravel boxes in 2021; 94% survival over 1 year. Current size of the natural population is 800. Adult mussels have lost their reproductive capacity, but recovered with 2-year rehabilitation in captivity River Lutto: 2,000 0+juveniles introduced in gravel boxes in 2021; 60% survival over 1 year. 4,000 0+-year-old juveniles introduced in gravel boxes in 2022. Current size of the natural population is 30,000, but the required salmon host cannot ascend to the river seasonal variation in laboratory Continuation and sustainability of funding 6GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References River Isojoki: 125,000 0+ juveniles introduced in gravel boxes and Buddensiek cages in 2022. Current size of the natural population is 150 France Brittany & Normandy/ Fédération de Pêche du Finistère Bretagne Vivante, CPIE des Collines Normandes M.m. 2011–present LI: high HF: Salmo trutta (hatchery) MB: glochidia collected in the field IC: trough/flume fed with commercial algae OC: side channel, sediment boxes, mussel silos, inriver cages Production: since 2012, several million 0+M.m. harvested and cultured in the trough/flume (in six rivers) Release: several millions, but 96% were 0+, with little indication of survival. Older mussels released at 3–4 cm in size (kept inside facility for 3 years and further kept in outdoor systems until they reach 3– 4 cm) Release of approx. 200,000 ind. ranging in age between 1+and 4+years Natural population consists of approx. 14,000 adults National & EU LIFE-project PM & JM Cessation of growth in indoor systems after about 3–4 years Funding difficulties after 10 years of operation Geist et al. (2021); Blaize C. (pers. comm. 2022) France Département Dordogne – Région Nouvelle Aquitaine/ M.m. 2016–2020 LI: high HF: Salmo trutta (hatchery) During the LIFE programme a total of approx. 30,000 juveniles >8 EU LIFE-project PM No continuation of rearing activities at the end of the LIFE project Legeay A. & Baudrimont M. (pers. comm., 2022) (Continues) GEIST ET AL.7 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References Université de Bordeaux - Parc Naturel Régional Périgord Limousin MB: glochidia collected in the field IC: trough/flume fed with commercial and freshly cultured algae OC: in-river cages (cylinder cages) months (3,300 aged 3 years and between 5–9mm +4,300 2 years + 14,800 1 year + 8,000 8 months) and 115,000 postparasitic ind. have been reintroduced directly in the river 50% of this population come from culture No monitoring of released mussels as the LIFE project ended Culture of fresh algae as food difficult From time to time water quality issues (pollution) from river used for culture Predation of juvenile mussels in sand trough systems Belamy et al. (2020) France Region Centre-Val de Loire/ Département Indre-et-Loire/ Université de Tours P.a. 2014–2018 LI: high HF: Acipenser baerii (hatchery) MB: new mussels collected in the wild every year and kept at breeding facility until release of glochidia IC: incubator boxes and trough/flume fed with commercial algae diet, self-prepared detritus with leaves. Use of egg white as protein source OC: none Juveniles collected/ year: >10,000 Not able to produce animals older than 4 months No survival in artificial channel No release of older juveniles Freshly metamorphosed juveniles released (2,000) No monitoring of released juveniles EU LIFE-project PM & JM Water quality used in culture. Silt? Pollution? Survival low during first few months Project duration was short. Not enough staff for rearing activity Soler J. (pers. comm., 2022). Soler et al. (2018a); Soler et al. (2018b); Soler et al. (2019); Wantzen et al. (2019) Germany Lower Saxony/ University of Hannover, Lower Saxony State M.m. 1986–2002; 2009– present (Gerdau) LI: Low –medium HF: Salmo trutta (wild) Survival rate 5%– 20% after 1–2 years and <5% after 52 months National and private None N/A Buddensiek (1995) Altmüller & Dettmer (2006); Altmüller (2023) 8GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References bottom (straight and circular tanks used). Different tank for each year class. Half were buried in best habitat patches and other half released into open water. Survival confirmed 1 year later; more comprehensive checks to take place in 2024 Total was approx. 15,000 juveniles across all cohorts (up to 28 months old and approx. 2.5 mm shell length) juveniles and many of adult broodstock Danger of another high-silt event possible Ireland County Mayo/ Marine Institute M.m. 2020–present LI: medium HF: Salmo salar (hatchery), Salmo trutta in future MB: adult mussels kept at facility to collect glochidia IC: no OC: juveniles drop off hosts into gravel on the tank bottom (straight and circular tanks used). Different tank for each year class Checked juveniles in gravel at bottom of tank for survival and growth in October and December 2021. Some found and they had grown Wild population consists of approx. 50,000. Plan to put some back into Newport River and perhaps use these juveniles for putting into other rivers, too. Plan to be confirmed National None Still in licensing and learning process Limited experience Very steep learning curve De Eyto E. (pers. comm., 2022) Ireland County Waterford/ Kilmeaden Water Treatment Plant M.m. 2019–present LI: high HF: Salmo trutta (wild and hatchery in season 4) Good encystment on fish but juvenile capture level was low (none in years National None Capture of juveniles post excystment Carroll P. (pers. comm., 2022) (Continues) GEIST ET AL.15 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References MB: adult mussels kept at facility to collect glochidia IC: limited success in capturing juveniles to date OC: none 1 and 2; 50 juveniles in year 3) Poor survival rates of host fish from the wild Luxembourg Ardennes Eifel Region/Fondation Hëllef fir d'Natur by natur & ëmwelt M.m. 2008–present LI: high HF: Salmo trutta (hatchery) MB: glochidia collected in the field. IC: incubator boxes, sand aquaria, and trough/flumes OC: sediment boxes, silos, and floating cages on a pond Juveniles >3 mm produced/year: 3,000–4,000 Released at length of 10 mm/year: 1,000–1,500 River Our strain released in cages: 1,300 3–4 years old River Our strain released in cages alive in 2021: 570 7–9 years old. 100% of this population from cultured ind. Belgium strains released: 8,000 3– 4 years old 94% of this population come from cultured ind. German strains released: 800 3–4 years old 100% of this population from cultured ind. Survival at facility until release approx. 3% EU LIFE project and national funding from LU, BE & DE PM & JM Keep survival high during the first year Adequate feeding of 0+,1+, and 2+ animals at facility Water quality issues in the streams in the area Eybe et al. (2013); Eybe et al. (2015) 16 GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References Luxembourg Ardennes Eifel Region/Fondation Hëllef fir d'Natur by natur & ëmwelt U.c. 2012–present LI: high HF: Phoxinus phoxinus (minnow) caught in the wild MB: new mussels collected in the wild every year and kept at breeding facility until release of glochidia. Mussels returned to river IC: incubator boxes, sand aquaria, and trough/flumes OC: sediment boxes, silos, and floating cages on a pond Juveniles >5 mm produced/year: 2,500–3,000 Released at length of 10 mm/year: 1,000–1,500 River Our strain 2,200 > 2 years old released 13% of this population come from cultured ind. River Sauer strain 3,400 > 2 years old released 22% of this population come from cultured ind. Survival at facility until release approx. 5% EU LIFE project & national funding from LU & BE PM Keep survival high during the first year Adequate feeding of 0+and 1+animals at facility Water quality issues in the streams in the area Eybe et al. (2013); Eybe et al. (2015) Luxembourg Ardennes Eifel Region/Fondation Hëllef fir d'Natur by natur & ëmwelt U.p. 2020 single try LI: medium HF: Squalius cephalus caught in the wild MB: mussels collected in the wild and kept at breeding facility until release of glochidia. Mussels returned to lake IC: not used OC: not used No success in 2020 Almost complete loss of infested host fish Not able to collect juvenile mussels during single try in 2020 National None Find adequate host fish strain for this species Thielen F. (pers. comm., 2022) (Continues) GEIST ET AL.17 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References Norway Austevoll in Vestland County/University of Bergen M.m. 2012–present LI: high HF: Salmo salar and Salmo trutta (2+) bred from wild strains MB: adult mussels collected in the field and kept at the facility to collect glochidia. Mussels returned to the wild after 1 year in quarantine IC: incubator boxes and trough/flume with live algae and detritus OC: sediment boxes In 2022, 5,400 2+ mussels released directly into three rivers. In 2021, 14,000 mussels released directly into one river. In addition, 50,000 recently dropped mussels were released directly into another river (excess production). Previous releases total 6,400 1to 7-year-old juveniles into 22 rivers. Releases into boxes for the first years; now (since 2021) only releases into river gravel Releasing ind. at 4 mm length in boxes is acceptable, but free release at larger sizes is better Rivers that have no recruitment are priorities. Many populations have very few mussels left. In most populations, propagated juveniles account for at least 10–100 National PM & JM Initially getting systems in place for high survival was a challenge, but systems now refined and no longer a problem Releasing juveniles into rivers with poor water quality limits survival in the wild Evaluating success Jakobsen P. & Mageroy J.H. (pers. comm., 2022) 18 GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References times the number of wild adults Norway Storelva River, Tingvoll Municipality, Møre og Romsdal County/ Naturfaglige Konsulenttjenester and Fisk og miljøundersøkelse M.m. 2017–2020 LI: high HF: Salmo salar (2+) bred from wild strains MB: adult mussels collected in the field and kept at the facility to collect glochidia. Mussels returned to the wild after 1 year in quarantine IC: incubator boxes and trough/flume with live algae and detritus OC: sediment boxes This was done as a precautionary measure, together with other measures, associated with road construction. The number of mussels released (28) was low compared with the population estimate of at least 3,000 mussels Regional None Difficulties with water quality at the cultivation facility led to very few mussels being produced Mageroy J.H. (pers. comm., 2022) Poland South–Central Poland/The Institute of Nature Conservation of the Polish Academy of Sciences in Krakow U.c. 2020–present LI: high HF: Cottus gobio and trials with Phoxinus phoxinus and Gobio gobio (wild) MB: new mussels collected in the wild every year and kept at breeding facility until release of glochidia. Mussels returned to river IC: incubator boxes, sand aquaria, and trough/flumes OC: none In the first year, 30 fish infested with larvae from 30 adult mussels Juveniles collected approx. 100 ind. Approx. 35 10 months old ind. in early 2022 left No release of mussels yet 50–60 adult mussels left in River Nida EU LIFE+Project PM Lack of mussel culture experience at the beginning of project Breeding facility long distance from project river Not possible to use river water for rearing systems Cages used to keep infested fish in the River Nida were removed and destroyed Zajac T. (pers. comm., 2022) Portugal District Vila Real/ Boticas Parque – Boticas municipality – M.m. 2019–present LI: high HF: Salmo trutta (hatchery) About 35,000 juveniles from the target populations (rivers Beça and Rabaçal) produced National/private PM Time consuming to train technicians as no previous experience with freshwater mussels Reis J. (pers. comm., 2022) (Continues) GEIST ET AL.19 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References MARE (University of Lisbon) MB: glochidia collected in the field IC: incubator boxes and trough/flume OC: in-river cages and encysted trout in rivers so far. To date, no juveniles released to river. Very good survival and growth in raceways. 2020, first drop off, 1,500; 2021, second drop off, 5,000. Trying to grow to taggable size Portugal Northern Portugal/ Castrelos aquatic rearing facility M.m. 2019–2021 LI: high HF: Salmo trutta (hatchery) MB: glochidia collected in the field IC: incubator boxes and trough/flume OC: release of encysted trout in rivers About 6,500 juveniles from the target populations (rivers Paiva, Neiva, and Rabaçal) produced intensively. Estimated 60,000 dropped off from trout in raceways. Encysted trout also released in rivers EU & National PM Time consuming to train technicians as no previous experience with freshwater mussels High fine sediment content of water leading to high fish mortality Reis J. (pers. comm., 2022) Portugal District Viseu/ Campelo aquatic rearing facility managed by Quercus M.m. 2013–2016 LI: high HF: Salmo trutta (hatchery) MB: glochidia collected in the field IC: incubator boxes and trough/flume OC: in-river cages and sediment boxes Over 225,000 juveniles from the target population (River Paiva) produced in 3 years (2013– 2015). High mortality caused by lack of detritus in closed systems. Good survival and growth in flowthrough systems Some mussels released after 1 year in captivity (2–4 mm in length) EU LIFE None No source for detritus collection to feed the mussels in closed systems Administrative constraints in organization meant follow-up project not possible Reis J. (pers. comm., 2022) 20 GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References Portugal District Viseu/ Campelo aquatic rearing facility managed by Quercus U.t. 2013–2016 LI: high HF: Squalius alburnoides and Squalius aradensis (hatchery) MB: collection of glochidia in the wild IC: trough/flume OC: in-river cages About 25,000 juveniles from the target population (River Torgal) produced in 2013 and 5,000 in 2015. High mortality owing to inadequate water quality (calcium deficiency) and need to optimize diet. Juveniles could survive up to 10 weeks and grow up to 1 mm EU LIFE project None No source for detritus collection to feed the mussels in closed systems. Administrative constraints in organization meant follow-up project not possible Reis J (pers. comm., 2022) Spain Galicia –Lugo/ University of Santiago de Compostela M.m. 2012–present LI: high HF: Salmo trutta (hatchery and wild) and Salmo salar (hatchery) MB: adult mussels kept at facility to collect glochidia. Mussels returned to rivers IC: incubator boxes and suspended sieves on opencircuit aquaria supplied by river water and fed with algae OC: in-river cages (Buddensiek) and sediment boxes Box culture: achieved a survival rate close to 90% during the first 100 days. Survival after 6 months dropped to approx. 50%. Aquaria: currently, survival to 6 months is around 90% Buddensiek cages: survival results highly variable, survival rate of 50% in the first 6 months Production: incubator boxes, 20,000 (0+years); aquaria, 30,000 (from 0–2 years); Buddensiek cages, EU LIFE & National PM Perform genotyping of successive cohorts prior to release Conservation status of the species in the Ulla basin not clear. Impact of LIFE project actions not clear Find suitable release sites. Improve breeding protocol for M.m. that improves survival and growth while being more efficient Get long-lasting funding from relevant administration Ondina P. & Varela C. (pers. comm., 2022) Araujo et al. (2018); Castrillo et al. (2020); Castrillo et al. (2021); Castrillo et al. (2022) (Continues) GEIST ET AL.21 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References 25,000 (0–8 years); in-river cages (sediment boxes), 300 (7, 8 and 9 years old). Total of 75,000 juveniles from different cohorts, 0–9 years old In 2017, 25,400 juveniles at size of 1 mm released in two stretches of the Ulla River Populations in the wild: Eo River, 45,500, hope to release 200 within next 5 years; Arnego River, 20,500, hope to release 1,000 within next 5 years; Ulla basin, 11,500, hope to release 20,000 within next 5 years Spain Arag on/Government of Arag on P.a. 2001–present LI: high HF: Acipenser baerii (hatchery) and Salaria fluviatilis (wild) MB: new mussels collected in the wild every year and kept at breeding facilities until release of glochidia. Juveniles (0+) collected/year: 2,000,000– 3,000,000 (99% goes to the Ebro River and canals; 1% is used for breeding in captivity and to perform ecotoxicological tests) EU (Feader/ Leader) & National PM one river basin More planned Question on how and where to release the cultured >50 mm animals needs to be solved Issues with adult fertility in the wild Mortality is still high during the first year. Space issues for larger animals at the OC facility Nakamura K. (pers. comm., 2022) Nakamura et al. (2019) 22 GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References Broodstock returned to rivers IC: incubator boxes and sand aquaria OC: outdoor trough/ flume supplied with river water; sediment boxes at the bottom of the Ebro River Juveniles >1 mm produced/year: 500–2,000. Juveniles 20–50 mm > 1,200 in 2022 Release: trials in sediment boxes in Ebro River with few ind. (>40 mm) in summer 2021. Good results (100% survival). Subsequently more than 300 juveniles >40 mm were incorporated in sediment boxes in summer 2022. Once all animals are released, 20%– 30% in this population from cultured ind. Spain Girona/Laboratory for breeding naiads at l'Estany de Banyoles, managed by the Consorci de l'Estany U.m. 2010–present LI: high HF: Barbus meridionalis (main use), Luciobarbus graellsii,Squalius laietanus, and Salaria fluviatilis (wild) MB: new mussels collected in the wild every year and kept at breeding facility until release of glochidia. Mussels returned to rivers Ter and Fluvià river basins (in the river and tributaries) Released infested fish: 4,475 ind. Stocking of released newly excysted juveniles: 87,724 ind. Stocking of juveniles >2 years: 3,596 ind. Banyoles Lake, water intake streams and their drainage channels: estimated EU LIFE projects & National None Adequate feeding and automation of dosage during the first year of life Technical improvements in the feeding and maintenance of juveniles during the fattening phase (from the second year of life) Implementation of the in vitro culture technique Genetic study of parents and Araujo et al. (2015) Compos M. (pers. comm., 2022) (Continues) GEIST ET AL.23 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References IC: trough/flume with cages and sand OC: pools and trough/flume with natural sand at the bottom. Continuous water recirculation and renewal with natural water from Lake Banyoles. Cages placed at the bottom of the lake and floating cages population of 1,000–2,000 ind. Released infested fish: 3,100 ind. Stocking of released newly excysted juveniles: 71,651 ind. Stocking of juveniles >2 years: 1,267 ind. An overall survival at facility of 5% is estimated captive bred juveniles Spain Girona/Laboratory for breeding naiads at l'Estany de Banyoles, managed by the Consorci de l'Estany U.r. 2010–present LI: high HF: Barbus meridionalis (main use), Luciobarbus graellsii,Squalius laietanus, and Salaria fluviatilis (wild) MB: new mussels collected in the wild every year and kept at breeding facility until release of glochidia. Mussels returned to rivers IC: trough/flume with cages and sand OC: pools and trough/flume with natural sand at the bottom, and continuous water recirculation and Banyoles Lake, water intake streams and drainage channels: Between 2010– 2013, a population of between 100– 200 ind. Was estimated. Released infested fish: 1,910 ind. Stocking of juveniles >2 years: 741 ind. An overall survival of 5% is estimated for this facility EU LIFE projects & National None See Spain U.m. See Spain U.m. 24 GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License TABLE 1 (Continued) Country Region/institution Species Years/since (ending date) Level of intensity and method Rearing success, release, and ratio to wild population age or size Funding source GM Main challenges References Environment Agency Salmo salar (hatchery unsuccessful) MB: mussels kept at hatchery to infest fish IC: incubator boxes OC: juveniles moved to flow-through trough/flume supplied with river water. Release of artificially infested fish glochidia released: 825,000. Current living juveniles from 2017/2018 spring/summer collection approx. 20 > 1.5 cm, 2019 spring/summer collection approx. 200 > 5 mm, 2021 spring/summer collection approx. 80 > 1 mm, 2022 winter collection approx. 200 < 1 mm. High mortality in each year group, especially in first few months, common obvious cause of mortality Saprolegnia infection Plan to release mussels when >15 mm encystment density) High mortality in each year group especially in first few months, common obvious cause of mortality: Saprolegnia infection (mortality rates >60%) Note: Method level of intensity (LI) is provided together with details about host fish used (HF), mussel broodstock situation (MB), indoor culture (IC), and outdoor culture (OC) systems used. GM, genetic monitoring (PM, parent mussels; JM, juvenile mussels). Abbreviations: A.a., Anodonta anatina; ind., individuals; M.d., Margaritifera durrovensis;M.m., Margaritifera margaritifera;P.a., Pseudunio auricularius;P.l., Potomida littoralis;U.c., Unio crassus;U.m., Unio mancus;U.p., Unio pictorum;U.r., Unio ravoisieri;U.t., Unio tumidiformis. GEIST ET AL.31 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License place primarily via video-conferencing, by phone, or, to a lesser degree, by email. The answers given were formatted in a standardized way, to enable comparison, and are presented in Table 1. 3|RESULTS AND DISCUSSION 3.1 |Existing rearing and culturing programmes for freshwater mussels in Europe In this review, 46 captive rearing and culturing initiatives dating back to 1989 were identified (Table 1). These initiatives cover 16 countries and 10 species of freshwater mussels. This includes the endangered freshwater pearl mussel M. margaritifera and the Irish Margaritifera durrovensis, as well as the giant freshwater pearl mussel Pseudunio auricularius, occurring only in Spain and France. Five Unio species (the thick-shelled river mussel Unio crassus, the painter’s mussel Unio pictorum, as well as Unio mancus,Unio ravoisieri, and Unio tumidiformis) and Potomida littoralis have also been propagated. Among the pond mussels (Anodontinae), only Anodonta anatina has been propagated. The efforts for captive breeding are very unevenly distributed among these 10 species, with the vast majority of activities being exclusively focused on M. margaritifera, and, to a lesser but increasing extent, on U. crassus. Some activities focus on propagating species in a very critical situation, such as P. auricularius,U. mancus, and U. ravoisieri, or multiple species concurrently. In proportion with the efforts put into captive breeding, most is known about glochidial release times as well as culturing and rearing practices for the freshwater pearl mussel, followed by the thick-shelled river mussel and the giant freshwater pearl mussel, whereas far less is known about these aspects for all other species. In most cases, existing breeding programmes cover the core areas of species distribution, with some exceptions. For instance, it is alarming that currently only the Spanish captive breeding programme is in place for the highly endangered P. auricularius, as previous programmes covering the remaining core distribution area of this species in France have come to an end. Several countries operate multiple breeding stations for the same species to address geographical coverage and risk mitigation, whereas some programmes serve populations in several countries. Most breeding programmes have received funding through either national or EU LIFE(+) projects of limited duration (typically a maximum of 5–8 years; Table 1). In M. margaritifera, the species upon which the majority of captive breeding efforts have been focused, there is already evidence that some of the released captive-bred mussels have started to reproduce, e.g. in the River Lutter (Germany). In some streams, the number of released captive-bred mussels already exceeds the size of the remaining natural population. 3.2 |Different intensities of rearing techniques Most rearing techniques try to bridge the critical juvenile stages in the life cycle of mussels (i.e. the parasitic and early post-parasitic phases) by providing optimal conditions during this time. Breeding approaches vary greatly in the intensity, size, species, numbers of juveniles produced, and the age/size at which they are released into the wild (Figure 1; Table 1,). They also differ in monitoring intensity with regards to the genetic monitoring of the offspring, which is in place in about half of the programmes. At the highest intensity level, parent mussels are collected in the wild and transferred into a hatchery where they remain either permanently (ark-type system) or for extended periods of time. Examples are the Windermere station in the UK, where freshwater pearl mussels from five rivers are kept, typically for between 2 and 36 months, before being returned to the wild, although one broodstock population has been present at the Ark for 13 years. Upon glochidial release, host fish, also maintained at the facility, are infested, and after drop-off juvenile mussels are maintained in a variety of recirculating and flow-through systems until they reach a size of about 15–20 mm. Sizes can vary depending on species and location. Such highly intensive systems are usually free from many of the adverse conditions in mussel rivers, but also bear a greater risk of a total loss of multiple populations owing to the aggregation of mussels in one place (e.g. when systems fail and suitable emergency systems are absent). These high-intensity programmes tend to be looked upon less favourably by conservationists, unless habitat and catchment restoration is being carried out concurrently with the captive breeding activities. The feeding of juveniles is considered a major challenge as maintaining mussels in the hatchery often requires the labourintensive collection of detritus from natural sources. In addition, commercially available algal food is often used (Gatenby, Neves & Parker, 1996), which together with water and detritus from the same habitat as the parent mussels, have yielded successful results for juvenile survival and growth. At the other extreme, some programmes, such as the freshwater pearl mussel conservation programme in the River Lutter, are largely field based and independent of technical facilities. Each year a small number of ripe mussels are collected from the river and used to infest wild electrofished or hatchery-reared host fish with those glochidia, before releasing the infested fish into the river. This system has a low risk of affecting the genetic constitution of the offspring, especially if different parent mussels are used each year, but it bears the risk of being largely unsuccessful if stages other than the parasitic phase of the life cycle are the main bottleneck. This is often the case with the freshwater pearl mussel, where colmated and oxygen-deficient stream beds are considered the main bottleneck for recruitment in Europe (Geist & Auerswald, 2007; Denic & Geist, 2015; Simon et al., 2015), as low oxygen levels evidently compromise the survival of juveniles (Hyvärinen et al., 2022). The methods used in any particular facility depend upon factors such as the infrastructure available, the water source, and the amount of staff time and funding available. Where specialist facilities are available and there are staff to monitor broodstock, fish, and juveniles, high and medium intensity methods, as described in Figure 1,canbe used. Pulsed flow-through systems (Patterson et al., 2018; Hyvärinen et al., 2021), incubator/detritus boxes (Eybe et al., 2013; Scheder et al., 2014; Nakamura et al., 2018; Grunicke et al., 2023), flumes, aquaria systems (Lavictoire et al., 2016; Lavictoire et al., 2020), and the 32 GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License Floating Upweller System (FLUPSYS) (Patterson et al., 2018) all require medium to high levels of attention. The most resource-intensive systems per juvenile reared are the incubator/box and the pulsed flow-through systems (Kunz et al., 2020; Hyvärinen et al., 2021). In the incubator system, juveniles are kept in static water in boxes (with usually 200–500 individuals per box) and are cleaned and supplied with fresh water, food, and detritus one or two times per week. The pulsed flow-through system provides water (and food) changes at regular intervals (as much as once per hour), but there are usually no more than 50–100 juveniles per beaker. The lower resource-intensive systems are the downwelling aquarium system (with 1000 juveniles per sieve, and containing 12–15 sieves, cleaned every 2 weeks), the sand aquaria (with 150–500 juveniles per system, and a weekly water exchange), FLUPSYS (with several hundred to 1000 juveniles per bucket, and cleaned when necessary), and flumes (with several thousand individuals per flume, and cleaned when necessary). The lower intensity and more field-based systems (boxes 6-10, Figure 1) can be used when space in specialist facilities is limited or absent. The smallest juveniles (freshly excysted from fish) can be placed into in-river cage systems. These systems, placed in mussel rivers, still need regular cleaning and maintenance, but are relatively low effort in relation to facility-based systems. Juveniles of >4 mm can be placed into mussel silos, again with regular cleaning (monthly), whereas slightly larger juveniles (>10 mm) can be placed in sediment boxes (Bílý et al., 2018) or into side channels (often referred to as Hruˇ ska channels; Hruska, 1999; Hruska, 2001; Gum, Lange & Geist, 2011), as a soft-release method before being stocked into final release sites. Sediment boxes need some cleaning and maintenance, but the side-channel method requires almost no maintenance. 3.3 |Challenges associated with mussel captive breeding programmes The primary challenges identified in the majority of captive breeding programmes are related to limitations in budget or staffing, and to rearing conditions such as water quality, feeding, and the survival of juveniles during early life stages (Table 1). Concerning budget limitations, the short duration of funding schemes over only a few years, especially for long-lived species such as M. margaritifera,isa more serious constraint than the funding level when starting new programmes. As M. margaritifera only become mature at an age of 10–15 years (Young & Williams, 1984), the typical funding schemes, with a maximum duration of 3–6 years in this species, only cover the rearing of a few cohorts of sexually immature juveniles. Furthermore, uncertainty in the continuation of funding decreases the retention of experienced staff and is out of step with the biological pace of some freshwater mussel species. Frequently, setting up and maintaining FIGURE 1 Captive breeding methods used for freshwater mussels throughout Europe. Coloured dots on the map refer to the different techniques described in the note boxes. Boxes 1 and 2 describe high-intensity methods, requiring maintenance at least once per week; boxes 3–5 describe medium-intensity methods, requiring maintenance at least once per fortnight; and boxes 6–10 describe low-intensity methods, requiring maintenance approximately monthly, or as needed GEIST ET AL.33 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License breeding programmes can also be complicated by water quality issues, the provision of natural or purchased feed for early life stages, and high mortality rates, sometimes culminating in the loss of an entire year cohort. Rearing systems dependent on an external water supply especially face a greater risk of unforeseen water quality issues, such as cyanobacteria blooms (Norwegian breeding station Austevoll), excess turbidity, and fine sediment loading (Austrian breeding station), as well as water quantity issues (as observed in dry summers in the German breeding station near Hof). At later stages of the mussel life cycle, the identification and limited availability of habitat of sufficient quality into which the juveniles can be released are reported as additional challenges (Table 1). In addition to the challenges directly associated with the captive breeding of mussels, monitoring them after their release is another key issue. Such monitoring is essential for assessing the suitability of recipient water bodies for captive-bred juveniles, identifying the ideal release sites, and determining the ideal captive breeding procedures that result in the greatest survival in the wild. 3.4 |Recommendations for the future Despite progress in the captive breeding of freshwater mussels, their sustainable conservation will always depend on the conservation or restoration of habitats and catchments. While conservation and restoration projects continue, captive breeding programmes can help to save small populations from extinction and boost the number of individuals for eventual release back into the wild once the habitats are capable of supporting early-stage juvenile mussels. Based on information from current freshwater mussel breeding stations in Europe, the following measures are suggested for improvement. 3.4.1 | Provision of speciesand basin-wide European conservation strategies for freshwater mussel species with long-term funding commitments The provision of long-term funding options to secure acquired specific knowledge and continuous action for long-lived mussel species is crucial and key to success. The fauna discussed here are long-lived, slow-growing species, and mussel catchments are so significantly degraded that in most cases habitat restoration may take more than a decade. Also, from a genetic point of view, continued captive breeding over multiple generations can help to prevent the erosion of genetic diversity (Geist et al., 2021). Owing to the dominance of funding for captive breeding provided by the European Union LIFE/LIFE+programmes and national funds with limited running times of 5 years or less, easy options for project extensions following an objective and independent review at intermediate stages would be most welcome and useful. Speciesand basin-wide European conservation strategies for freshwater mussels will ensure that programmes have the best chance of success. 3.4.2 | Scienceand evidence-based support in the development and evaluation of breeding programmes A significant volume of work has been carried out by breeding programmes to improve efficiencies and increase the number of juveniles surviving in captivity. However, much of this valuable work does not get published in the primary literature, limiting its impact. Although there is a strong and collaborative European network of mussel breeding programmes, more scienceand evidence-based support (with the subsequent publication and dissemination of results) is needed to drive faster paced positive outcomes. The development of breeding programmes requires the integration of genetic information, as demonstrated for the freshwater pearl mussel (Geist et al., 2021), as well as a critical evaluation of the impacts of captive breeding procedures on the progeny, and ultimately on the long-term success of different rearing methods in aiding the reestablishment of functional populations in the wild. 3.4.3 | Increased knowledge exchange and training opportunities Although the diversity of different approaches to mussel breeding is generally useful, by increasing the overall system resilience and minimizing the high losses of juvenile mussels, e.g. related to feeding, these issues could be reduced by an increased level of information exchange and training. There are often very limited or no funds for exchange and training opportunities. Therefore, there is a need to provide trans-European funding, which allows scientific and practical exchange among existing and newly planned breeding programmes. In the past, most of the exchange among breeding stations has happened through local conferences held, for example, within existing LIFE(+) projects, thus being sporadic in time and place. Within the European COST project CONFREMUS (2023), an intensified exchange among mussel experts and mussel breeders has been initiated for the first time, albeit time-limited to when this project ends in 2024. Continuation and expansion (where appropriate) of such successful initiatives is important for ensuring a well-connected network of experts who communicate new findings in a timely manner and who are available for training those new to mussel conservation. 3.4.4 | Coordinated action related to species and geographical representation as well as genetic aspects Despite the success stories of many captive breeding efforts at the European scale, there is still no coordinated approach among them in terms of species, geographical, and genetic representation. The development of a coordinated European strategy for captive mussel breeding, ideally integrated into habitat and catchment restoration plans –all of which should be evidence-based and supported by scientific research –would be needed to increase the effectiveness of 34 GEIST ET AL. 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License such programmes. This should ideally be integrated into the development of minimal standards for captive mussel breeding, concerning animal welfare aspects of host fish use, disease prevention, maintaining genetic integrity of captive-bred mussels, and minimizing extinction risk, as well as requirements of tracking and assessing the success of mussel releases. It may also be necessary to prioritize conservation actions (Geist, 2015) to ensure the best remaining occupied sites within each catchment are secured, rather than spreading conservation action too thinly to attempt to conserve marginal populations and risk failure owing to a lack of resources. 3.4.5 | Guidelines for assessment of success of the breeding action and risk mitigation Together with the production of country-wide/European conservation strategies, the production of guidelines to assess breeding programme success and how to mitigate risks would be valuable for new programmes. Guidelines would also help to standardize the way in which current breeding programmes communicate their outputs, driving an increased awareness of factors affecting success and how risks can be minimized. In future, information on which species, numbers, and sizes/ages of mussels are being stocked at which locations needs to be collected more systematically and beyond the level of individual stations. The successful development and implementation of a standard approach for monitoring freshwater pearl mussel (M. margaritifera) populations in European rivers (Boon et al., 2019) and the continuing development of a new European Committee for Standardization (CEN) standard on mussel monitoring for a wider range of species illustrate that such action is possible, even with limited levels of funding. This parallels strategic conservation approaches in North America, where a national strategy for the conservation of native freshwater molluscs has been developed (FMCS, 2016). CONFLICT OF INTEREST The authors have no conflicts of interest associated with this work. AUTHOR CONTRIBUTIONS JG, LL, and FT jointly led the study, conducted and analysed the interviews, and are the principal authors. Conceptualization: JG, LL, and FT. Methodology: JG, LL, and FT. Data curation: all authors. Visualization: LL, FT, and RH. Investigation: JG, LL, and FT. Writing— original draft: JG. Writing—review and editing: all authors. All authors have read and agreed to the published version of the article. AFFILIATIONS 1 Aquatic Systems Biology Unit, TUM School of Life Sciences, Technical University of Munich, Freising, Germany 2 Fondation Hëllef fir d'Natur/natur & ëmwelt, Marnach, Luxembourg 3 Freshwater Biological Association, YMCA North Campus, Newby Bridge, UK 4 Lachendorf, Germany 5 Univ. Bordeaux, CNRS, Bordeaux INP, Pessac, France 6 Bretagne Vivante –Société pour l’ Etude et la Protection de la Nature en Bretagne (SEPNB), Brest, France 7 Freshwater Mussel Breeding Laboratory of Lake Banyoles, Banyoles, Spain 8 Wildlife Conservation Medicine Research Group (WildCoM), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona, Catalonia, Spain 9 Friend of the River Clodiagh Group, Kilmeaden Water Plant, Kilmeaden, Ireland 10 Consultants in Aquatic Ecology and Engineering –blattfisch e.U., Wels, Austria 11 Bund Naturschutz Hof, Hof, Germany 12 Hannover, Germany 13 Landschaftspflegeverband Passau e.V., Passau, Germany 14 Fédération de Pêche du Finistère, Pisciculture du Favot, Brasparts, France 15 Marine Institute, Furnace, Newport, Co. Mayo, Ireland 16 Institute of Hydrobiology, Technical University of Dresden, Dresden, Germany 17 Department of Bioscience, University of Bergen, Bergen, Norway 18 Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Tartu, Estonia 19 State Forest Management Centre, Haljala Municipality, Lääne-Viru County, Estonia 20 Norwegian Institute for Nature Research, Oslo, Norway 21 Trinity Centre for the Environment, School of Natural Sciences, Department of Zoology, Trinity College Dublin, The University of Dublin, Dublin, Ireland 22 Public Service of Wallonia, Agriculture, Natural Resources and the Environment, DEMNA, Directorate of Nature and Water, Gembloux, Belgium 23 Environmental Service Department, Sociedad Aragonesa de Gesti on Agroambiental (SARGA), Zaragoza, Spain 24 Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain 25 Department of Zoology, Genetics and Physical Anthropology, University of Santiago de Compostela, Campus Terra, Lugo, Spain 26 Biology, Institution of Environmental and Life Sciences, Karlstad University, Karlstad, Sweden 27 BIVALVIA s.r.o., Zábˇ reh, Czech Republic 28 Marine and Environmental Sciences Centre (MARE)/Aquatic Research Network (ARNET), Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal 29 The Rural Economy and Agricultural Society, Eldsberga, Sweden 30 Lüsslingen, Switzerland 31 Biologische Station Städte Region Aachen e.V., Stolberg, Germany 32 Université de Tours, Centre National de la Recherche Scientifique (CNRS) l’UMR 7324 CItés, TERritoires, Environnement et Sociétés (CITERES), Tours, France 33 Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland 34 Cynrig Fish Culture Unit, Llanfryanch, UK GEIST ET AL.35 10990755, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/aqc.4018 by University Of Jyväskylä Library, Wiley Online Library on [02/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 35 Kielder Salmon Centre, Environment Agency, Northumberland, UK 36 Swedish Anglers Association, Göteborg, Sweden 37 Institute of Nature Conservation, Polish Academy of Sciences, Krak ow, Poland ACKNOWLEDGEMENTS This publication is based upon work from COST Action CA18239, supported by COST (European Cooperation in Science and Technology). We also thank F. Jecke, M. Koester, M. Pagel, and E. Zelenková for supporting this study. Open Access funding enabled and organized by Projekt DEAL. DATA AVAILABILITY STATEMENT The data that support the findings of this study are available from the corresponding author, upon reasonable request. 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