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Polyunsaturated Fatty Acids in Fish Tissues More Closely Resemble Algal Than Terrestrial Diet Sources

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Polyunsaturated Fatty Acids in Fish Tissues More Closely Resemble Algal Than Terrestrial Diet Sources Hydrobiologia (2021) 848:371–383 https://doi.org/10.1007/s10750-020-04445-1 (0123456789().,-volV)( 0123456789().,-volV) PRIMARY RESEARCH PAPER Polyunsaturated fatty acids in fish tissues more closely resemble algal than terrestrial diet sources Nadine Ebm . Fen Guo . Michael T. Brett . Stuart E. Bunn . Martin J. Kainz Received: 15 July 2020 / Revised: 13 October 2020 / Accepted: 15 October 2020 / Published online: 16 November 2020 Ó The Author(s) 2020 Abstract The River Continuum Concept implies which is essential for neural development in fish and that consumers in headwater streams have greater other vertebrates. We sampled subalpine streams to dietary access to terrestrial basal resources, but recent investigate how the PUFA composition of neural studies have highlighted the dietary importance of (brain and eyes), muscle, and liver tissues of fresh- high-quality algae. Algae provide consumers with water fish is related to their potential diets (macroin- physiologically important omega-3 (n-3) polyunsatu- vertebrates, epilithon, fresh and conditioned terrestrial rated fatty acids (PUFA), particularly eicosapen- leaves). The PUFA composition of consumers was taenoic acid (EPA). However, terrestrial plants and more similar to epilithon than to terrestrial leaves. most benthic stream algae lack the long-chain (LC) Storage lipids of eyes most closely resembled dietary n-3 PUFA docosahexaenoic acid (DHA, 22:6n-3), PUFA (aquatic invertebrates and algae). However, DHA and arachidonic acid (ARA, 20:4n-6) were not directly available in the diet but abundant in organs. Handling editor: Michael Power This implies that algal PUFA were selectively retained Electronic supplementary material The online version of or were produced internally via enzymatic PUFA this article (https://doi.org/10.1007/s10750-020-04445-1) con- conversion by aquatic consumers. This field study tains supplementary material, which is available to authorized demonstrates the nutritional importance of algal users. N. Ebm Á M. J. Kainz (&) M. T. Brett WasserCluster Lunz – Inter-university Center for Aquatic Department of Civil and Environmental Engineering, Ecosystem Studies, 3293 Lunz Am See, Austria University of Washington, Seattle, WA 98195, USA e-mail: [email protected] e-mail: [email protected] N. Ebm S. E. Bunn e-mail: [email protected] Australian Rivers Institute, Griffith University, Nathan, QLD 4111, Australia N. Ebm e-mail: s.bunn@griffith.edu.au Functional and Evolutionary Ecology, Faculty of Life Sciences, University of Vienna, 1090 Vienna, Austria M. J. Kainz Department for Biomedical Research, Danube University F. Guo Krems, Krems an der Donau, Austria Simon F.S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, China e-mail: [email protected] 123 372 Hydrobiologia (2021) 848:371–383 PUFA for neural organs in aquatic consumers of 1996; Tocher et al., 2001; Murray et al., 2014). These headwater regions. fish are able to transform dietary ALA via stearidonic acid (SDA) and EPA to DHA, but direct incorporation Keywords Stream food webs Á Food quality Á of dietary DHA is preferred by fish as it reduces the Headwaters Á Fish brain Á Fish eyes Á Docosahexaenoic more energy-demanding endogenous production path- acid way. However, in contrast to such experimental studies, little is known about the PUFA pathways to and within fish in natural ecosystems deprived in DHA (Gladyshev et al., 2018), and especially how fish in Introduction streams acquire their PUFA and subsequently allocate these FA to different organs, including neural organs At the base of aquatic food webs, primary producers, (Guo et al., 2017). e.g., microalgae, provide consumers with dietary Neural organs, e.g., brain and eyes, are rich in DHA nutrients, including essential polyunsaturated fatty (Mourente & Tocher, 1998; Farkas et al., 2000; acids (PUFA), that are crucial constituents of cell Stoknes et al., 2004), which is key for proper membranes (e.g., phospholipids). A steady supply of functioning of these organs and eventually optimal dietary PUFA to aquatic consumers, particularly fish physiological performance. Common stream fish omega-3 (n-3) long-chain (LC) PUFA, such as eicos- in alpine headwaters (e.g., salmonids and European apentaenoic acid (EPA; 20:5n-3) and docosahex- bullhead) are visual predators that prey mostly on aenoic acid (DHA; 22:6n-3), is critical as these fatty moving or drifting invertebrates oftentimes at night acids (FA) support somatic growth and reproduction (Elliott, 1973; Mills & Mann, 1983). A reduced visual (Mu¨ller-Navarra et al., 2000; Brett et al., 2009). performance (Bell et al., 1995) or learning ability However, most aquatic consumers have limited abil- (Lund et al., 2014) of fish due to LC-PUFA-poor diets ities to synthesize EPA and DHA and thus have to take can reduce feeding success, predator avoidance (e.g., up these biomolecules directly from their diets (Brett escape latency, swimming speed) and other behavioral &Mu¨ller-Navarra, 1997; Arts et al., 2009; Torres- traits, e.g., schooling behavior (Ishizaki et al., 2001). Ruiz et al., 2010). Vascular plants synthesize the short- Despite the fact that neural organs have the highest chain PUFA: alpha-linolenic acid (ALA; 18:3n-3) and lipid contents and are the most energy-demanding the n-6 PUFA linoleic acid (LA, 18:2n-6), but tissues in animals, our current knowledge about generally lack EPA and DHA (Brett et al., 2009; but energy flows in aquatic food webs is primarily derived see Napier, 2006). Although epilithic algae (especially from studies on fish muscle and liver tissues (Volk & diatoms) in freshwater ecosystems are comparatively Kiffney, 2012; Kainz et al., 2017; Sushchik et al., rich in EPA, they are low in DHA (Brett et al., 2009; 2018). Previous research indicated that FA in neutral Hixson et al., 2015; Guo et al., 2018). However, DHA lipids (NL) of fish muscles, such as triacylglycerols is essential for all vertebrates including freshwater (TAG), reflect those from the diet, while FA in the fishes (Ahlgren et al., 1994; Guo et al., 2017) where it polar lipids (PL) of fish muscles are driven by is associated with high membrane fluidity (e.g., signal taxonomy (Iverson 2009; Sushchik et al., 2020). Total transduction, neurotransmission or hormone regula- lipids and TAG contents vary among fish organs tion, Farkas et al., 2000), anti-inflammatory and— (Tocher & Harvie, 1988; Budge et al., 2006; Hong oxidative effects (e.g., neuroprotection, Bazan, 2005), et al., 2014) and thus different organs may vary in proper neural development (cognitive performance, correspondence to dietary FA. Lund et al., 2014), and sensory functioning (visual Most vertebrate and fish brains consist mainly of PL acuity, Bell et al., 1995). (Soengas & Aldegunde, 2002), which are rich in DHA In contrast to marine fish (Agaba et al., 2005; (Tocher & Harvie, 1988; Iverson, 2009), making them Tocher et al., 2006; Mohd-Yusof et al., 2010), indispensable for cell functionality and relatively previous studies have reported that enzymatic conver- stable to dietary lipid intake. In contrast, fish eyes sions to LC-PUFA are functional in some freshwater are rich in TAG (Mourente et al., 1991; Geurden et al., fish (e.g., Oncorhynchus mykiss (Walbaum, 1792), 1998; Stoknes et al., 2004) and thus eye lipids may Salvelinus alpinus (Linnaeus, 1758), Buzzi et al., reflect dietary PUFA sources better than brain lipids 123 Hydrobiologia (2021) 848:371–383 373 (Brodtkorb et al., 1997). Bell et al. (1995) demon- parameter (N-NO3, N-NH4, P-PO4), soluble reactive strated that DHA-poor diets resulted in DHA-deficit phosphorus (SRP), and dissolved organic matter retina membranes with impaired vision under natural (DOM) concentrations in these study streams were light intensities. It is thus important to understand how reported in a previous study (Guo et al., 2018). lipid classes in neural organs are affected by dietary FA. However, this has not been tested yet for stream Sample collection fish which receive very little DHA directly from organisms at the base of the food chain. Potential dietary resources for fishes, including Motivated by the ambiguities outlined above, we epilithon, conditioned terrestrial leaves, and aquatic designed a field study to investigate the PUFA invertebrates were collected in October 2016. Condi- distribution in freshwater fish and their potential diet tioned leaves (submerged, senescent, and brownish sources in subalpine streams. We compared the PUFA leaves of various vascular plant species) were col- composition of various fish organs, i.e., muscle, liver, lected from streams). Epilithon from each of the brain, and eyes, with PUFA of potential diet sources sampling sites was transferred into sample containers (terrestrial plants, benthic algae and macroinverte- from small cobbles using soft brushes and inverte- brates), and also explored the FA distribution of brates were picked from rocks. The taxonomic com- salmonid brain and eyes in an effort to discern how position of epilithon and periphyton (biofilm on different lipid classes (NL versus PL) of these neural submerged leaves) was not examined because we organs are affected by dietary PUFA sources. We were primarily interested in their dietary and bio- tested the hypotheses that, (1) the PUFA composition chemical composition (Guo et al., 2018). Fresh leaves of stream consumers (macroinvertebrates and fish) is were picked directly from riparian vegetation in generally more similar to epilithon than to the leaves summer (July
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