Abstract
The present study was conducted to determine the possible usage of dried Schizochytrium limacinum as a replacement of Arthrospira maxima in a ration of the adult freshwater mussel (Unio crassus). The experimental diets were prepared with the different concentrations of protein-rich green freshwater algae A. maxima and docosahexaenoic acid (DHA)-rich diatom S. limacinum. Combinations were done by replacing A. maxima with 0%, 30%, 70%, and 100% of dried S. limacinum then named AM100, AM70, AM30, and AM0, respectively. These diets were used to feed 180 individuals (15 mussels/tank) of U. crassus in 12 independent glass (4 groups and 3 replicates) tanks. Live weight gain, shell dimensions, biochemical compositions, and fatty acid contents of U. crassus from whole tissue were examined before and after 30 days of feeding trial. The live weight gain was significantly higher in the AM100 (1.66 ± 1.32 g, 5.00 ± 3.95%) and AM70 (1.32 ± 0.83 g, 4.05 ± 2.56%) groups than in the (0.06 ± 1.91 g, 0.31 ± 5.73%) and AM0 (− 0.17 ± 0.61 g, − 0.52 ± 1.84%) groups. We were able to detect increasing levels of DHA in the U. crassus tissues, while the given ratios of S. limacinum were increased in the diet. The results showed that S. limacinum was digested by adult U. crassus to some extent and DHA was retained in the mussel tissue. These results showed that the dependence on live algae can be decreased in the conservation effort of U. crassus by using S. limacinum in a ration.
Similar content being viewed by others
Data availability
Research data will be made available if it is requested by an editor of the journal.
References
Abad M, Ruiz C, Martinez D, Mosquera G, Sánchez JL (1995) Seasonal variations of lipid classes and fatty acids in flat oyster, Ostrea edulis, from San Cibran (Galicia, Spain). Comp Biochem Physiol 110C:109–118. https://doi.org/10.1016/0742-8413(95)00006-A
Ackman RG (1983) Fatty acid metabolism of bivalves. In: Bio-chemical and Physiological Approaches to Shellfish Nutrition. Proc. 2nd International Conference Aquaculture Nutrition, World Mariculture Society Specific Publication No. 2. Louisiana State University Louisiana, 358–376. https://doi.org/10.1016/0044-8486(84)90293-X
AOAC (1990) Official methods of analysis (13th Ed.) Association of Official Analytical Chemists, Official method 950.46, Washington, D.C., USA
AOAC (1995) Official methods of analysis, (14th. Ed.) Association of Official Analytical Chemists, Washington, DC., USA
AOAC (2001) Official method 996.06 fat (total, saturated and unsaturated) in foods, hydrolytic extraction gas chromatographic method, First Action 1996 Revised 2001
AOAC (2002) Protein content in meat. 928.08. Official Method of Analysis, 17th edn. Association of Official Analytical Chemists, Gaithersburg
Arney B, Liu W, Falconer I, McKinley RS, Pearce CM (2015) Feasibility of dietary substitution of live microalgae with spray-dried Schizochytrium sp. or Spirulina in the hatchery culture of juveniles of the Pacific geoduck clam (Panopea Generosa). Aquaculture 444:117–133. https://doi.org/10.1016/j.aquaculture.2015.02.014
Barclay WR, Meager KM, Abril JR (1994) Heterotrophic production of long chain omega-3 fatty acids utilizing algae and algae-like microorganisms. J Appl Phycol 6:123–129. https://doi.org/10.1007/BF02186066
Bleakley S, Hayes M (2017) Algal proteins: extraction, application, and challenges concerning production. Foods 6(5):33. https://doi.org/10.3390/foods6050033
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/o59-099
Boeing P (1997) Use of spray-dried Schizochytrium sp. as a partial algal replacement for juvenile bivalves. J Shellfish Res 16:284
Bouchet P, Falkner G, Seddon M (1999) Listing of protected land and freshwater molluscs in the Bern Convention and European Habitats Directive: are they relevant to conservation? Biol Conserv 90:21–31. https://doi.org/10.1016/S0006-3207(99)00009-9
Carvalho F, Lima P, Goncalves F, Russel-Pinto F, Machado J (2007) Development of suitable maintenance diet for Anodonta cygnea. J World Aquac Soc 35:189–198. https://doi.org/10.1111/j.1749-7345.2004.tb01074.x
Dobler AH, Geist J, Stoeckl K, Inoue K (2019) A spatially explicit approach to prioritize protection areas for endangered freshwater mussels. Aquat Conserv Mar Freshw Ecosyst 29:12–23. https://doi.org/10.1002/aqc.2993
Douda K, Haag WR, Escobar-Calderón F, Vodáková B, Reichard M, Chen X, McGregor M, Yang J, Lopes-Lima M (2021) Effects of in vitro metamorphosis on survival, growth, and reproductive success of freshwater mussels. Biol Conserv 254:108964. https://doi.org/10.1016/j.biocon.2021.108964
Ercan E, Tarkan AS (2014) Effect of salinity on the growth and survival of the freshwater mussel, Unio Crassus, in an environmentally disturbed river. Pak J Zool 46:1399–1406
Eybe T, Thielen F, Bohn T, Sures B (2013) The first millimetre-rearing juvenile freshwater pearl mussels (Margaritifera margaritifera L.) in plastic boxes. Aquat Conserv Mar Freshw Ecosyst 23(6):964–75. https://doi.org/10.1002/aqc.2384
Fearman JA, Bolch CJS, Moltschaniwskyj NA (2009) Energy storage and reproduction in mussels, Mytilus galloprovincialis: the influence of diet quality. J Shellfish Res 28(2):305–312. https://doi.org/10.2983/035.028.0212
Galley TH, Batista FM, Braithwaite R, King J, Beaumont AR (2009) Optimization of larval culture of the mussel Mytilus edulis (L.). Aquac Int 18:315–325. https://doi.org/10.1007/s10499-009-9245-7
Gąsienica-Staszeczek M, Zając K, Zając T, Olejniczak P (2017) In vitro culture of glochidia of the threatened freshwater mussel Unio crassus Philipsson 1788 the dilution problem. Invertebr Reprod Dev 62:1–9. https://doi.org/10.1080/07924259.2017.1362482
Gatenby CM, Parker BC, Neves RJ (1997) Growth and survival of juvenile rainbow mussels, Villosa iris (Lea, 1829) (Bivalvia: Unionidae), reared on algal diets and sediment. Am Malacol Bull 14:57–66
Gatenby CM, Orcutt DM, Kreeger DA, Parker BC, Jones VA, Neves RJ (2003) Biochemical composition of three algal species proposed as food for captive freshwater mussels. J Appl Phycol 15:1–11. https://doi.org/10.1023/A:1022929423011
Gillis PL, Mackie GL (1994) Impact of the zebra mussel, Dreissena polymorpha, on populations of Unionidae (Bivalvia) in Lake St. Clair Can J Zool 72:1260–1271. https://doi.org/10.1139/z94-168
Gillis PL, McInnis R, Salerno J, de Solla SR, Servos MR, Leonard EM (2017) Freshwater mussels in an urban watershed: impacts of anthropogenic inputs and habitat alterations on populations. Sci Total Environ 574:671–679. https://doi.org/10.1016/j.scitotenv.2016.09.110
Ichihara K, Shibahara A, Yamamoto K, Nakayama T (1996) An improved method for rapid analysis of the fatty acids of glycerolipids. Lipids 31:535–539. https://doi.org/10.1007/BF02522986
Inoue K, Stoeckl K, Geist J (2017) Joint species models reveal the effects of environment on community assemblage of freshwater mussels and fishes in European rivers. Divers Distrib 23:284–296. https://doi.org/10.1111/ddi.12520
Karayücel S, Kaya Y, Karayücel İ (2003) Sinop bölgesinde akdeniz midyesinin (Mytilus gallaprovincialis Lamarck, 1819) kondisyon faktörü ve biyokimyasal kompozisyonu üzerine çevresel faktörlerin etkisi. Turkish J Vet Anim Sci 27:1391–1396
Killeen ID, Aldridge C, Oliver G (2004) Freshwater bivalves of Britain and Ireland. FSC Publications, Shrewsbury (ISBN: 9781851538928)
Langdon CJ, Önal E (1999) Replacement of living microalgae with spray-dried diets for the marine mussel Mytilus galloprovincialis. Aquaculture 180:283–294. https://doi.org/10.1016/S0044-8486(99)00197-0
Lazzara R, Fernandes D, Faria M, López JF, Tauler R, Porte C (2012) Changes in lipid content and fatty acid composition along the reproductive cycle of the freshwater mussel Dreissena polymorpha: its modulation by clofibrate exposure. Sci Total Environ 432:195–201. https://doi.org/10.1016/j.scitotenv.2012.05.094
Lopes-Lima M, Sousa R, Geist J, Aldridge DC, Araujo R, Bergengren J, Bespalaya Y, Bodis E, Burlakova L et al (2017) Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol Rev 92:572–607. https://doi.org/10.1111/brv.12244
Lopes-Lima M, Kebapçı U, Van Damme D (2014) Unio crassus. The IUCN Red List of Threatened Species e.T22736A42465628. https://doi.org/10.2305/IUCN.UK.2014-1.RLTS.T22736A42465628.en
Ma XY, Wen HB, Zou J, Jin W, Hua D, Gu RB, Xu P (2018) An improved method for in vitro culture of glochidia in freshwater mussel Cristaria plicata (Mollusca, Bivalvia). Hydrobiologia 810:133–144. https://doi.org/10.1007/s10750-016-3012-3
Marshall R, McKinley S, Pearce CM (2010) Effects of nutrition on larval growth and survival in bivalves. Rev Aquac 2:33–55. https://doi.org/10.1111/j.1753-5131.2010.01022.x
Merrill AL, Watt BK (1974) Energy value of foods-basis and derivations. USDA Agriculture Handbook 74:2-3 Washington DC. https://www.ars.usda.gov/ARSUserFiles/80400525/Data/Classics/ah74.pdf. Accessed 09 Sept 2021
Neves RJ, Widlak J (1987) Habitat ecology of juvenile freshwater mussels (Bivalvia: Unionidae) in a headwater stream in Virginia. Am Malacol Bull 5:1–7
Nobles T, Zhang Y (2011) Biodiversity loss in freshwater mussels: importance, threats, and solutions. In: Biodiversity loss in a Changing Planet., InTechOpen; Rijeka, Croatia. pp. 137–162. https://doi.org/10.5772/25102
O’Beirn FX, Neves RJ, Steg MB (1998) Survival and growth of juvenile freshwater mussels (Unionidae) in a recirculating aquaculture system. Am Malacol Bull 14:165–171
Önal E, Langdon C, Önal U (2005) The evaluation of spray-dried microalgae in diets for juvenile manila clam. Tapes Philippinarum. J Shellfish Res 24:1061–1065. https://doi.org/10.2983/0730-8000(2005)24[1061:TEOSMI]2.0.CO;2
Patel A, Liefeldt S, Rova R, Christakopoulos P, Matsakas L (2020) Co-production of DHA and squalene by thraustochytrid from forest biomass. Sci Rep 10:1992. https://doi.org/10.1038/s41598-020-58728-7
Pazos AJ, Román G, Acosta CP, Sánchez JL, Abad M (1997) Lipid classes and fatty acid composition in the female gonad of Pecten maximus in relation to reproductive cycle and environmental variables. Comp Biochem Physiol 117B:393–402. https://doi.org/10.1016/S0305-0491(97)00135-1
Pettersen AK, Turchini GM, Jahangard S, Ingram BA, Sherman CDH (2010) Effects of different dietary microalgae on survival, growth, settlement and fatty acid composition of blue mussel (Mytilus Galloprovincialis) larvae. Aquaculture 309:115–124. https://doi.org/10.1016/j.aquaculture.2010.09.024
Serdar S, Bulut H, Eden M, Özdemir Y (2019) Determining bioecological and biometric properties of freshwater mussels (Unio crassus Philipsson, 1788). Pol J Environ Stud 28:1917–1924. https://doi.org/10.15244/pjoes/90621
Sousa R, Halabowski D, Labecka AM, Douda K, Aksenova O, Bespalaya Y, Bolotov I, Geist J, Jones HA et al (2021) The role of anthropogenic habitats in freshwater mussel conservation. Glob Chang Biol 27:2298–2314. https://doi.org/10.1111/gcb.15549
Taeubert JE, Gum B, Geist J (2012) Host-Specificity of the endangered thick-shelled river mussel (Unio Crassus, Philipsson 1788) and implications for conservation. Aquat Conserv: Mar Freshw Ecosyst 22:36–46. https://doi.org/10.1002/aqc.1245
Yalçın M (2006) Tatlısu midyesi (Unio pictorum LİNNAEUS, 1758)’nin büyüme, kondisyon ve biyokimyasal parametreleri üzerine çevresel faktörlerin etkisi. Msc Thesis, Ondokuz Mayıs Üniversitesi
Zettler ML, Jueg U (2007) The situation of the freshwater mussel Unio Crassus (Philipsson, 1788) in North-East Germany and its monitoring in terms of the EC Habitats Directive. Mollusca 25:165–174
Acknowledgements
The authors would like to express grateful thanks and appreciations to the HANA Spirulina and MarinBio for providing dried microalgae products. Cansu Metin, Yunus Alparslan, and Mustafa Hacisa helped with the laboratory analysis at the Fisheries Engineering Faculty of Muğla Sıtkı Koçman University. We are grateful to Dr. John Mark Dean and Dr. Robin Dean for their grammatical review. This study was created from the MSc. Thesis of Ergi Bahrioğlu. In additon, corresponding author thanks his parents.
Funding
This research was funded by Scientific Research Support Program (BAP) of Muğla Sıtkı Koçman University (Project: BAP 15/222).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
Animals used in the study are invertebrates, which are exempted from the animal ethics directives.
Conflict of interest
The authors declare no competing interest.
Additional information
Handling Editor: Gavin Burnell
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bahrioğlu, E., Ercan, E. Replacement of dried freshwater alga Arthrospira maxima with marine diatom Schizochytrium limacinum in a diet of freshwater mussel Unio crassus (Philipsson, 1788). Aquacult Int 30, 999–1010 (2022). https://doi.org/10.1007/s10499-022-00852-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-022-00852-4