Discrimination between freshwater and marine fish using fatty acids: ecological implications and future perspectives
Abstract
Fatty acids (FA) are a major source of nutrients and energy in aquatic food webs, as well as serving as the main components of all cell membranes. Increasing anthropogenic impacts (e.g., climate change) are predicted to selectively alter the production of these critical compounds, with potential cascading effects reaching higher trophic level organisms, including humans. To provide a more comprehensive assessment of these potential effects, we synthesized and systematically explored differences in the abundance and distribution of FA in fish, due to their pivotal role in aquatic ecosystems and value to humans. An extensive data set consisting of 1382 fish FA profiles was analyzed to identify the main differences in FA composition of freshwater vs. marine fish, taking into account the effects of taxonomic, geographic (i.e., latitude zone), and functional (i.e., feeding mode) factors. Freshwater fish had relatively high contents of 18:2n-6 (linoleic acid, LNA) and 20:4n-6 (arachidonic acid, ARA) indicative of freshwater algae and terrestrial dietary sources. In contrast, 20:1n-9 and 22:1n-11, well known as marine zooplankton biomarkers, typified the FA composition of marine fish. Using this result, we constructed a new metric (i.e., a specific C18–C22 unsaturated FA ratio) that we propose can assist in characterizing the feeding habitat (freshwater vs. marine) and, to some extent, the diet of fish. Our analysis also revealed that carnivores from high latitudes had higher contents of 20:5n-3 (eicosapentaenoic acid, EPA) and 22:6n-3 (docosahexaenoic acid, DHA), thus making them an excellent source of essential FA for human consumption. In parallel, unsaturated FA contents were higher overall at temperate and polar latitudes than in the tropics. The latter two trends may be driven by water temperature variation across latitudes, which is known to affect FA composition of cell membranes in ectotherms. Last, a strong retention of DHA was observed in both freshwater and marine fish. We conclude that our discrimination between freshwater and marine fish provides a quantitative tool that is applicable to a broad range of research and conservation initiatives.
Résumé
Les acides gras (AG) constituent une source majeure de nutriments et d’énergie dans les réseaux alimentaires aquatiques et font aussi partie des principaux éléments de toutes les membranes cellulaires. On prévoit que l’augmentation des impacts anthropiques (par exemple, les changements climatiques) modifiera de manière sélective la production de ces composés essentiels, avec des effets en cascade potentiels atteignant les organismes de niveau trophique supérieur, y compris les humains. Afin de fournir une évaluation plus complète de ces effets potentiels, les auteurs ont synthétisé et exploré systématiquement les différences quant à l’abondance et à la distribution des AG chez les poissons, en raison de leur rôle essentiel dans les écosystèmes aquatiques et de leur importance pour l’humain. Un vaste ensemble de données comprenant 1382 profils d’AG chez les poissons a été analysé afin d’identifier les principales différences dans la composition en AG chez les poissons d’eau douce par rapport aux poissons marins, en tenant compte des effets des facteurs taxonomiques, géographiques (c.-à-d. la zone de latitude) et fonctionnels (c.-à-d. le mode d’alimentation). Les poissons d’eau douce présentaient des teneurs relativement élevées en 18:2n-6 (acide linoléique) et en 20:4n-6 (acide arachidonique), des indicateurs de la présence d’algues d’eau douce et autres sources alimentaires terrestres. Par contre, les teneurs en 20:1n-9 et en 22:1n-11, bien connus comme biomarqueurs du zooplancton marin, caractérisaient la composition en AG des poissons marins. En utilisant ce résultat, ils ont construit une nouvelle mesure (c.-à-d. un rapport spécifique en AG insaturé C18–C22) qui, selon eux, peut aider à caractériser l’habitat d’alimentation (eau douce ou eau de mer) et, dans une certaine mesure, le régime alimentaire des poissons. Cette analyse a également révélé que les carnivores des hautes latitudes présentaient des teneurs plus élevées en 20:5n-3 (acide eicosapentaénoïque, EPA) et en 22:6n-3 (acide docosahexaénoïque, DHA), ce qui en fait d’excellentes sources en AG essentiels pour la consommation humaine. Parallèlement, les teneurs en acides gras insaturés étaient en général plus élevées sous les latitudes tempérées et polaires que sous les tropiques. Ces deux dernières tendances peuvent être dues à la variation de la température de l’eau d’une latitude à l’autre, dont on sait qu’elle affecte la composition des membranes cellulaires en AG chez les organismes ectothermes. Enfin, une forte rétention de DHA a été observée chez les poissons d’eau douce et les poissons marins. Les auteurs concluent que leur discrimination entre les poissons d’eau douce et les poissons marins fournit un outil quantitatif applicable à un vaste spectre d’initiatives de recherche et de conservation. [Traduit par la Rédaction]
Introduction
Aquatic ecosystems cover the majority of the Earth’s surface (marine systems, 71%; freshwater systems, <1%), and provide numerous and important services to humans, including food provisioning and carbon sequestration (Barange et al. 2017; Beaumont et al. 2019). Global environmental challenges, including rising surface air temperatures (Allen et al. 2018), water pollution (Nel 2005; Kampa and Castanas 2008), eutrophication of waterbodies (Gray et al. 2002), ocean acidification (Hoegh-Guldberg and Bruno 2010), and overexploitation of natural resources (Crowder et al. 2008), are threatening not only the functioning and stability of aquatic ecosystems, but also the ecosystem services they provide (Bendell 2018). It is, therefore, crucial to improve our knowledge of these systems, to better assess the multi-faceted effects of the numerous global anthropogenic impacts on them, as well as effects on human populations. In this context, the analysis of fatty acid (FA) biomarkers represents an effective tool to study structure and dynamics of aquatic ecosystems (Howell et al. 2003; Kharlamenko et al. 2013). Furthermore, it also allows the assessment of the effects of abiotic factors (Pernet et al. 2006, 2007; Pond et al. 2014) and anthropogenic impacts (Wilcox et al. 2018) on aquatic organisms and habitats, including the consequences of global environmental threats (Kopprio et al. 2015; Hixson and Arts 2016).
FA are major components of cell membranes, as well as tissues and organs (e.g., brains and eyes). In addition, FA are a key source of essential nutrients and energy, including certain polyunsaturated omega-3 and omega-6 FA (hereafter n-3 and n-6 PUFA; the numbers 3 and 6 refer to the position of the first double bond from the methyl end of the molecule) in aquatic ecosystems (Arts et al. 2001; Tocher 2003; Parrish 2013). Their utility as biomarkers is based on the fact that the FA composition of consumers typically reflects that of their diet (Graeve et al. 1997; Brett et al. 2006). In fact, once ingested, FA are not always immediately metabolized, but instead are incorporated into various tissues as is, or with minimal alteration (Iverson et al. 2004). Thereby, FA are transferred from one trophic level to the next within food webs in a mostly conservative manner (Iverson et al. 2004). Although their dietary signal typically decreases as they move up the food chain (Kürten et al. 2013), certain FA are more efficiently retained than others, reflecting their importance within species and ecosystems (Brett et al. 2006; Connelly et al. 2014). For instance, Kainz et al. (2004) explored retention patterns of individual FA in four size-categories of zooplankton and in rainbow trout (Oncorhynchus mykiss). They found that these patterns varied according to both body size and taxonomy, and that eicosapentaenoic acid (EPA, 20:5n-3) and arachidonic acid (ARA, 20:4n-6) were highly retained in zooplankton, whereas rainbow trout preferentially accumulated docosahexaenoic acid (DHA, 22:6n-3) in their tissues.
Contrary to what was thought for many decades, it is now becoming increasingly evident that not only primary producers (Napolitano 1999), but also a wide range of aquatic invertebrates (Kabeya et al. 2018) have the requisite molecular apparatus to synthesize short-chain PUFA (i.e., 18-carbon) de novo. Furthermore, some organisms, including crustaceans (Brett et al. 2006; De Troch et al. 2012) have the ability to convert these short-chain precursors (e.g., α-linolenic acid ALA, 18:3n-3, and linoleic acid LNA, 18:2n-6) to their long-chain counterparts (LC-PUFA, ≥20 carbons; i.e., EPA, DHA, and ARA). Despite this ability, LC-PUFA are mainly acquired through the diet (Castro et al. 2016). Whether of dietary origin or endogenously produced, EPA, DHA, and ARA are vital to consumers, in that they are involved in numerous physiological processes that affect their growth, reproduction, and survival. In particular, studies have shown that they play a crucial role in growth and survival at early life stages of both invertebrates (Goedkoop et al. 2007) and vertebrates (Bae et al. 2010; Xu et al. 2010; Paulsen et al. 2014). Furthermore, dietary EPA, DHA, and ARA have been shown to improve reproductive success and increase the quality of broodstock eggs (Furuita et al. 2003; Mazorra et al. 2003). Because of their importance in the general health of organisms, together with the inefficiency of most consumers to synthesize them from their precursors (i.e., ALA and LNA), EPA, DHA, and ARA are considered essential dietary FA in aquatic ecosystems (Dalsgaard et al. 2003; Tocher 2003; Parrish 2009).
Hixson et al. (2015) and Colombo et al. (2016) showed that organisms in freshwater and marine ecosystems typically have higher contents of LC-PUFA, mainly EPA, DHA, and ARA, than organisms in terrestrial ecosystems. This dichotomy between aquatic and terrestrial systems is ultimately due to the fact that microalgae and seaweeds are able to synthesize EPA and DHA de novo (Parrish 2009, 2013). In contrast, although some mosses and fungi can produce relatively high contents of LC-PUFA (Gill and Valivety 1997), higher (i.e., vascular) terrestrial plants typically do not contain ARA, EPA, and DHA in their tissues (except for transgenic plants; Napier 2006), but can have high contents of ALA and LNA. However, although previous studies have highlighted differences in the distribution and abundance of FA between organisms in freshwater and marine ecosystems (e.g., Tocher 2003; Brett et al. 2009a), these differences have not yet been formally and systematically organized or analyzed on a broad and more comprehensive scale.
Due to increasing anthropogenic impacts, the synthesis, abundance, and distribution of FA in aquatic ecosystems is predicted to vary in the future, with cascading effects throughout food webs up to top predators, including humans (Hixson and Arts 2016; Colombo et al. 2020). In this context, we analyzed an extensive data set comprising 1382 FA profiles of freshwater and marine fish with the main objective being to tease out differences in FA distribution and relative abundances (i.e., FA proportions) between fish in the two biomes. We focused our assessment on fish due to their key role in most aquatic food webs, and also because they represent a valuable dietary source of essential LC-PUFA for humans (Fernandes et al. 2014; Strandberg et al. 2017). Indeed, 2–3 servings of fish (e.g., salmon) per week, which is equivalent to 300–500 mg of EPA+DHA per person per day, is recommended for a healthy diet (Beheshti Foroutani et al. 2018; Tocher et al. 2019). In particular, the consumption of either EPA or DHA has been linked to reduced cardiovascular and inflammatory diseases (Siriwardhana et al. 2012), as well as improved neuronal and cognitive function (Swanson et al. 2012). However, the majority of fish stocks are at the maximum sustainable limits (Osmond and Colombo 2019; FAO 2020), such that it may become increasingly difficult to meet this dietary recommendation in the future. Furthermore, although aquaculture provides more than half of the global seafood production, and this industry is expected to grow to satisfy the increasing demand (Osmond and Colombo 2019), most current fish farming practices are not yet fully sustainable (Ottinger et al. 2016). In this regard, identifying and describing differences in the FA composition of fish across different biological and environmental parameters may help detect those species that could provide an alternative and nutritional dietary option, both as a source of fish meal and fish oil (incorporated in feed used in aquaculture) and for direct human consumption.
For a more comprehensive understanding of the distribution of FA in fish, we also studied variations in FA composition across different latitude zones (i.e., polar, temperate, and tropical) and feeding modes (i.e., herbivore, omnivore, and carnivore). More specifically, we hypothesized, (i) that freshwater fish are characterized by higher contents of ALA and LNA than marine fish due to their closer links to terrestrial ecosystems. Furthermore, independent of biome (freshwater or marine), we predicted, (ii) increasing contents of EPA and DHA in fish tissue from tropical to polar latitudes, following similar results from previous studies (Colombo et al. 2016; Parzanini et al. 2019); and, (iii) a strong retention of DHA with progressing trophic level (i.e., herbivorous, then omnivorous, and then carnivorous fish), considering that DHA is an essential FA in the biology and ecology of fish. Retention of DHA was already observed in rainbow trout by Kainz et al. (2004) when analyzing the planktonic food web of a coastal lake system.
Methodological approach
Data collection
The FA profiles of freshwater (n = 697) and marine fish (n = 685) (Supplementary Table S11) were collected from peer-reviewed scientific literature listed in Google Scholar and Scopus portals using the following key words: arachidonic acid, ARA, biomarker, diet, DHA, docosahexaenoic acid, eicosapentaenoic acid, EPA, fatty acid, fish, freshwater, marine, trophic ecology. In addition to this literature search, more fish data were gathered from other sources, including the FA profiles of the European eel (Anguilla anguilla) by Parzanini, Arts, Rohtla, Koprivnikar, Power, Skiftesvik, Browman, Milotic, and Durif (unpublished data, 2019–2020) and those generated by Arts, Kainz, and Wacker (unpublished data, 2001–2015). Experimental studies were excluded a priori from the search to avoid biases due to feeding and (or) environmental manipulations (which are known to influence FA profiles), unless they also reported data from wild individuals (as controls). Studies reporting data for early life stages (i.e., eggs and larvae) were also discarded from this analysis. Generally, information on developmental stage and (or) sex of the fish was available for only a small proportion of data (<11%), and therefore, age and sex could not be taken into account as a source of variation in the FA profiles of the fish. Only FA data from the total lipid fraction of white muscle, the main storage tissue of most fish species (Tocher 2003), and whole bodies (when the collection and analysis of target tissues, such as muscle, was prevented by the small size of fish, or when fish were analyzed as prey items; 23% of the data set) were included in this investigation, as our aim was to explore trends and differences in dietary FA. Muscle tissue by far is also the largest tissue in the body of fish, and it typically represents the part of a fish often exclusively consumed by humans. Although the majority of the studies considered here reported FA data as proportions of total FA (%) a small portion (<1%) presented them as mass fractions (g FA per g dry or wet weight); for this reason, the mass fraction data were converted to proportional data, prior to analysis. Last, when transferring data from the literature, FA were here considered as “not detected” if their values were omitted by the authors of the source material, as below any threshold established by the authors themselves (although their presence was acknowledged); or reported as ‘–’ or ‘0′.
The fish FA data that we retrieved from the literature encompassed two biomes (freshwater and marine), three latitude zones (tropical, 0–30°; temperate, 30–60°; and polar, 60–90°), three feeding modes (herbivore, omnivore, and carnivore), and 43 Orders of fish (Table S11). Although the information about biome and latitude zone was retrieved from the respective studies, feeding mode and taxonomic classifications were obtained from the Fish Base portal (Froese and Pauly, 2020), when not available in the original source. In addition, when the source paper provided information on development stage (i.e., juvenile/adult), ontogenetic dietary differences were taken into account. Last, for diadromous species (e.g., salmon and eel), we referred to the collection site listed in the publication to categorize the biome to which each fish species was assigned.
Statistical analysis
Both univariate and multivariate statistics were performed to study variations in FA composition of fish collected within the biomes, and across different latitude zones and feeding modes. Most analyses included only those FA occurring with mean proportions ≥0.5% (i.e., 18 different FA), as these FA were assumed to contribute most to the overall variability (Table 1). Nonetheless, as a parallel evaluation, rare FA (i.e., 17 individual FA whose proportions ranged between 0.1 and 0.5%) were also analyzed to assess whether a given FA was specific for either biome. However, caution must be taken when interpreting the result of the latter assessment, as the data set for less abundant FA may have been incomplete (e.g., the authors from the original references often reported only a portion of the total possible FA, i.e., the most abundant of the FA obtained through their analyses and (or) the identified portion).
Table 1.
Note: All unsaturated FA reported are in the cis configuration, whereas the complete list of individual FA used to calculate ΣSFA, ΣMUFA, and ΣPUFA is provided in Table S21. A letter code in parentheses highlights significant differences in the composition of the most important FA (Fig. 1), and FA sums and ratios between freshwater and marine fish species. DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; F, freshwater; FA, fatty acid; M, marine; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid; SFA, saturated fatty acid; UI, unsaturation index.
Statistical analyses were separately performed on individual FA, on FA sums (i.e., saturated FA, ΣSFA; monounsaturated FA, ΣMUFA; polyunsaturated ΣPUFA; Σn-3 PUFA, Σn-3; Σn-6 PUFA, Σn-6; and ΣEPA+DHA), and on FA ratios (18:1n-9/18:1n-7; n-3/n-6) to avoid multi-collinearity. Individual FA data were square-root transformed to ensure data normality and to stabilize the variance (Greenacre and Primicerio 2014). Further details about the included FA are provided in Table S21. The 18:1n-9/18:1n-7 ratio was used as an indicator of carnivorous vs. omnivorous feeding behavior (Graeve et al. 1997; Falk-Petersen et al. 2000); whereas ΣEPA+DHA and the n-3/n-6 ratio are widely recognized as indicators of seafood quality in nutritional studies (Huynh and Kitts 2009; Fernandes et al. 2014). In addition, the unsaturation index (UI; as the Σnumber of double bonds of each FA in a sample multiplied by its percentage; Poerschmann et al. 2004) was calculated for each previously reported fish FA profile.
Distance-based linear model (DistLM) analysis was used to assess whether the variables considered (i.e., biome, latitude zone, feeding mode, and taxonomy) had a significant effect on fish FA composition, and, if so, which FA were contributing the most to the observed variability. In addition, principal coordinates analysis (PCoA) provided a representation of which FA best differentiated between the two biomes. Also, permutational multivariate analysis of variance (PERMANOVA), which does not assume multivariate normality, was performed to study strength and significance level of these variations (“Biome” was considered a “Fixed Factor”). PCoA and PERMANOVA were performed on both the main and the rare FA data sets. Last, similarity percentage (SIMPER) analysis indicated the proportion of similarity of fish from the same biome. PERMANOVA was also used to analyze variations across latitude zones and feeding modes. The DistLM, PCoA, and PERMANOVA analyses were performed on resemblance matrices, which were based on Euclidean distance as recommended for proportional FA data (Happel et al. 2017). Finally, univariate statistics were run to test the presence of any significant variations of target individual FA, sum, ratio and (or) index between biomes (Mann–Whitney rank sum test) and across latitude zones and feeding modes (Kruskal–Wallis one-way analysis of variance (ANOVA) on ranks, abbreviated below to Kruskal–Wallis ANOVA on ranks).
As a further assessment, we took a closer look at FA profiles from selected orders of fish (i.e., those that had a statistically valid data representation among the various categories considered, i.e., those with a sample size >10 for each category). In particular, differences between biomes (i.e., freshwater and marine) were tested (PERMANOVA) for fish from the orders Clupeiformes, Osmeriformes, Perciformes, Salmoniformes, and Scorpaeniformes (Table S11). In addition, Kruskal–Wallis ANOVA on ranks, which does not assume normally distributed data, was run to study latitudinal differences in the FA composition of marine perciforms, as only they were represented across all three different latitude zones (Table S11). Last, trends across feeding modes were analyzed (Kruskal–Wallis ANOVA on ranks) in freshwater Cypriniformes, which had only freshwater representatives, and in Perciformes, which had both freshwater and marine representatives.
Based on our results (Fig. 1), the following new FA metric was established to aid in the identification of marine (M) vs. freshwater (F) fish,
(1)
Fig. 1.
For this metric, higher values (≥11) represent “true” marine fish species, as these were characterized by greater proportions of 20:1n-9, 22:1n-11, EPA, and DHA overall (∼30%; Table 1). In contrast, lower values of this ratio (<2) are indicative of “true” freshwater species as, in this study, freshwater fish overall contained high proportions of ALA, LNA, ARA (∼13.0%; Table 1) in their tissues. Mann–Whitney rank sum tests and two-way equal variance ANOVA, in conjunction with Holm–Sidak pairwise comparisons, were run to test for the differences in M/F ratios between freshwater and marine fish, and across latitude zones and feeding modes. Once threshold values for the identification of “true” freshwater and marine fish were recognized (see Results and Discussion), PCoA and PERMANOVA were then performed on a clean data set of fish FA profiles (nF = 685, nM = 281) to assess the power of this metric. This metric was developed to help identify diet and feeding habitat of fish, with potential management implications for many species (see the Potential management implications section below).
Multivariate statistics (i.e., DistLM, PCoA, PERMANOVA, and SIMPER) were performed using Primer 7 with the PERMANOVA+ add on package, whereas ANOVA tests were run using SigmaPlot (ver. 12.5). All results were reported as mean proportions (± standard deviation). In addition, only statistically significant results were presented. For this reason, when any given result was “higher/greater” vs. “lower” or “increased” vs. “decreased”, the implication here is that the specific comparison or relationship was statistically significant, even though not formally stated.
Data synthesis findings
FA composition in freshwater and marine fish
Overall, the most abundant FA present within fish tissues were 16:0 (19.1 ± 6.2%), 18:1n-9 (14.8 ± 9.3%), DHA (14.1 ± 9.9%), EPA (6.4 ± 4.1%), 18:0 (5.7 ± 3.3%), 16:1n-7 (4.9 ± 4.0%), ARA (3.8 ± 3.6%), and LNA (3.3 ± 3.7%). At 35.4 ± 14.8%, PUFA made the greatest contribution to total FA, followed by MUFA (31.1 ± 14.5%) and then SFA (26.9 ± 8.6%). In addition, mean contents of Σn-3 and Σn-6 FA were 25.6 ± 13.7% and 9.1 ± 6.3%, respectively.
The variables “taxonomy”, “biome”, “latitude”, and “feeding mode” all contributed significantly (p = 0.0001; DistLM analysis) to the variability of the fish FA data. Specifically, the factor “taxonomy” contributed the most to the variation (19.6%), followed by “biome” (10.6%), “latitude zone” (5.8%), and “feeding mode” (4.6%). In addition, PERMANOVA detected a significant difference between freshwater and marine fish FA profiles (Pseudo-F = 163.9, p = 0.0001; Table 1), with average similarity within groups of 74.0%, for freshwater fish, and 73.7%, for marine fish. Overall, freshwater fish were characterized by higher contents of ALA, LNA, and ARA; whereas 16:1n-7, 20:1n-9, 22:1n-11, EPA, and DHA were greater in marine fish (Fig. 1). Moreover, Mann–Whitney rank sum tests revealed that freshwater fish also had greater contents of ΣSFA (U = 201277.5, p ≤ 0.001), ΣPUFA (U = 212754.0, p ≤ 0.001), and Σn-6 (U = 77282.5, p ≤ 0.001) than their marine counterparts that, instead, had higher contents of ΣMUFA (U = 224187.0, p = 0.05), Σn-3 (U = 199705.0, p ≤ 0.001), and ΣEPA+DHA (U = 162526.5, p ≤ 0.001; Fig. 2). The separation between freshwater and marine fish FA composition was also observed when analyzing the less abundant FA (Pseudo-F = 72.8, p = 0.0001). Freshwater fish were characterized by generally higher contents of 15:0, 18:3n-6, 20:0, 20:3n-3, 20:2n-6, and 20:3n-6, whereas marine fish had greater contents of 20:1n-7, 20:4n-3, 22:1n-9, and 24:1 (Fig. S31).
Fig. 2.
Freshwater and marine fish of the selected orders analyzed (i.e., Clupeiformes, Osmeriformes, Perciformes, Salmoniformes, and Scorpaeniformes) had significantly different FA profiles (PERMANOVA, p < 0.01). Table S41 reports sample sizes, pseudo-F, and p-values of the PERMANOVA analyses for each fish order. Overall, ALA, LNA, and ARA were higher in freshwater fish from these orders, except for Scorpaeniformes, where freshwater fish had lower contents of ALA and ARA than their marine counterparts (Table S51). Although DHA was typically higher in marine fish, freshwater Osmeriformes had higher, within order, contents of this FA than their marine counterparts (Table S51).
The mean M/F ratios were significantly greater in marine than freshwater fish species (11.9 ± 12.6, marine fish; 1.9 ± 3.5, freshwater fish; U = 42763.5, p ≤ 0.001; Mann–Whitney rank sum test). In freshwater species, the ratio ranged from 0.3 (Beloniformes) to 17.8 ± 23.8 (Acipenseriformes) (Table S61); whereas in marine species, mean values ranged between 0.3 ± 0.1 (Orectolobiformes) and 31.6 ± 26.9 (Argentiniformes) (Table S61). PERMANOVA on the clean data set (i.e., after the metric application) of “true” freshwater (i.e., M/F < 2) and marine (M/F ≥ 11) fish FA profiles detected a greater differences between groups (Pseudo-F = 219.2, p = 0.0001; Fig. 3).
Fig. 3.
Latitudinal gradients
PERMANOVA revealed significant differences in fish FA composition across latitude zones (Pseudo-F = 42.8, p = 0.0001). In addition, when freshwater and marine fish were analyzed separately, latitudinal trends for certain FA were also revealed. Specifically, mean contents of EPA (Kruskal–Wallis ANOVA on ranks, H = 239.3, p ≤ 0.001) and DHA (ANOVA, F = 74.5, p ≤ 0.001) in freshwater fish increased towards the poles (Fig. 4); whereas LNA had the opposite trend (H = 48.1, p ≤ 0.001) (Table 2). Moreover, ΣPUFA (H = 69.5, p ≤ 0.001), Σn-3 (H = 169.5, p ≤ 0.001), together with UI (H = 131.6, p ≤ 0.001) and M/F ratio (H = 194.0, p ≤ 0.001), were higher in polar regions in freshwater fish, whereas contents of ΣSFA (H = 151.0, p ≤ 0.001), ΣMUFA (H = 15.0, p ≤ 0.001), Σn-6 (H = 57.5, p ≤ 0.001) were higher in tropical latitudes (Table 2). Similarly, for marine fish, EPA (H = 102.1, p ≤ 0.001) and DHA (H = 8.1, p = 0.017) increased towards the poles (Fig. 4), together with 16:1n-7 (H = 55.2, p ≤ 0.001) and 22:1n-11 (H = 55.6, p ≤ 0.001); whereas mean contents of 16:0 (H = 52.6, p ≤ 0.001), 18:0 (H = 172.9, p ≤ 0.001), LNA (H = 47.1, p ≤ 0.001), and ARA (H = 126.7, p ≤ 0.001) were higher in tropical latitudes compared to polar and temperate latitudes (Table 2). Overall, contents of ΣMUFA (H = 154.0, p ≤ 0.001), ΣPUFA (H = 7.3, p = 0.026), Σn-3 (H = 28.0, p ≤ 0.001) were higher towards the polar regions, in marine fish, whereas contents of ΣSFA (H = 136.3, p ≤ 0.001) and Σn-6 (H = 203.6, p ≤ 0.001) were greater in tropical regions (Table 2). Last, UI contents were higher in polar latitudes (H = 22.4, p ≤ 0.001), but the difference was not significant between temperate and tropical marine fish; and pairwise comparisons also revealed a latitudinal gradient in the M/F ratio, with increasing values towards the polar regions (H = 234.4, p ≤ 0.001).
Fig. 4.
Table 2.
Note: All the unsaturated FA reported are in the cis configuration, whereas the complete list of individual FA used to calculate ΣSFA, ΣMUFA, and ΣPUFA is provided in Table S21. A letter code in parentheses highlights significant differences in the composition of the most important FA (Fig. 1), and FA sums and ratios of freshwater and marine fish species across latitude zones. DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; F, freshwater; FA, fatty acid; M, marine; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid; SFA, saturated fatty acid; UI, unsaturation index.
Similar results were obtained when ANOVA tests were performed on marine perciforms. In particular, 16:0 (H = 19.5, p < 0.001) and 18:0 (H = 53.6, p < 0.001) increased from polar to tropical latitudes, together with LNA (H = 23.6, p ≤ 0.001) and ARA (H = 62.9, p ≤ 0.001). By contrast, 16:1n-7 (H = 8.3, p = 0.016), 20:1n-9 (H = 38.3, p ≤ 0.001), EPA (H = 51.1, p ≤ 0.001) and DHA (H = 11.3, p = 0.004), were greater in higher latitudes than in tropical zones.
Differences among feeding modes
Several orders of fish had representatives of multiple feeding modes, including Anguilliformes, Beloniformes, Characiformes, Clupeiformes, Cypriniformes, Gadiformes, Perciformes, Scorpaeniformes, Siluriformis, Synbranchiformes, and Tetraodontiformes. Further information about the species representative of each of these orders, along with characteristic feeding modes, is provided in Table S11.
PERMANOVA revealed significant differences in fish FA content among feeding groups (Pseudo-F = 33.3, p = 0.0001). In particular, Kruskal–Wallis ANOVA on ranks showed that DHA and UI increased with increasing trophic level (i.e., from herbivorous to omnivorous and then to carnivorous fish) in both freshwater (DHA, H = 57.3, p ≤ 0.001; UI, H = 49.7, p ≤ 0.001) and marine fish (DHA, H = 26.0, p ≤ 0.001). ARA was only higher in carnivorous freshwater fish (H = 11.8, p = 0.003), whereas the opposite trend was observed in marine fish (H = 29.3, p ≤ 0.001; Fig. 5). In addition, in marine fish, 20:1n-9 (H = 28.4, p ≤ 0.001) and 22:1n-11 (H = 20.2, p ≤ 0.001) were higher in carnivorous compared to omnivorous and herbivorous fish. The 18:1n-9/18:1n-7 ratio was higher in omnivorous and carnivorous fish, although the trend was significant only for freshwater fish (H = 17.3, p ≤ 0.001; Table 3). Furthermore, carnivorous fish had higher contents of ΣEPA+DHA than herbivorous fish from both freshwater (H = 53.6, p ≤ 0.001) and marine (H = 17.4, p ≤ 0.001) systems; whereas n-3/n-6 ratios were greater in herbivorous freshwater fish (H = 54.6, p ≤ 0.001) and carnivorous marine fish species (H = 33.3, p ≤ 0.001; Table 3). Last, pairwise comparisons showed a trophic gradient in the M/F ratio of marine fish, with increasing values in higher trophic level consumers (H = 50.5, p ≤ 0.001).
Fig. 5.
Table 3.
Note: All unsaturated fatty acids reported are in the cis configuration, whereas the complete list of individual fatty acids used to calculate ΣSFA, ΣMUFA, and ΣPUFA is provided in Table S21. A letter code in parentheses highlights significant differences in the composition of the most important fatty acids (Fig. 1), and fatty acid sums and ratios of freshwater and marine fish species across feeding modes. DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; F, freshwater; FA, fatty acid; M, marine; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid; SFA, saturated fatty acid; UI, unsaturation index.
Likewise, ARA decreased with increasing trophic level in marine carnivorous perciforms (F = 17.2, p ≤ 0.001), whereas freshwater Perciformes (H = 6.8, p = 0.033) and Cypriniformes fish (H = 11.5, p = 0.003) had the opposite trend. ALA was also higher in freshwater herbivorous Cypriniformes (H = 12.5, p = 0.002). DHA was higher in carnivorous fish of both orders, although results were significant only for the Perciformes (freshwater, H = 9.6, p = 0.008; marine, F = 14.2, p < 0.001).
Synthesis and perspectives
Major differences between freshwater and marine fish FA composition
Freshwater fish were characterized by a generally higher overall PUFA content mainly represented by n-6 PUFA, such as LNA and ARA; whereas marine fish had higher MUFA contents, specifically 20:1n-9 and 22:1n-11, and n-3 PUFA contents (e.g., EPA and DHA). This result was obtained when analyses were performed on both the whole data set and on selected orders of fish, suggesting that freshwater and marine fish have access to dietary resources with somewhat different FA profiles.
Although the FA composition of aquatic primary consumers varies considerably according to phylogeny, and certain FA typify specific algal groups (Ahlgren et al. 1992; Dalsgaard et al. 2003; Galloway and Winder 2015), it is difficult to unequivocally attribute the high contents of LNA found in freshwater fish to a unique source of LNA, as many plants contain this PUFA. Nevertheless, we hypothesize that the large contribution of LNA in freshwater fish may be due to the high proportions of LNA contained in cyanobacteria and green algae (phylum Chlorophyta); and, to a lesser extent, to the influence of vascular plants (as fresh and (or) decaying material) and terrestrial organic matter inputs in freshwater food webs (Brett et al. 2009b, 2017; Kühmayer et al. 2020). Indeed, not only do freshwater phytoplankton, the autotrophic fraction of seston, and benthic algae typically represent the main food source for freshwater consumers, they also provide high-quality nutrients (e.g., essential FA, sterols, and amino acids) that support growth and reproduction of freshwater invertebrates and fish (Brett et al. 2009b, 2017; Taipale et al. 2013; Kühmayer et al. 2020). Vascular terrestrial plants may also have relatively high contents of LNA (Kelly and Scheibling 2012; Hixson et al. 2015). However, it is more difficult for aquatic consumers to assimilate terrestrial organic material, such as leaves in streams, partly due to its high lignin and cellulose content. Although the FA content of dietary resources at the base of freshwater and marine food webs were not included in this research, studies report lower n-3/n-6 ratios in freshwater (especially in green algae) than marine algae (e.g., Mansour et al. 1999; Taipale et al. 2013), and the n-3/n-6 ratios in the freshwater fish analyzed in this study were, on average, ∼2x lower than in marine fish (Table 1).
ARA is an essential FA in aquatic ecosystems (Parrish 2009). For instance, ARA supports somatic growth and survival of fish, as in juveniles of the Japanese eel (Anguilla japonica) (Bae et al. 2010), and aquatic insect larvae (Goedkoop et al. 2007). Furthermore, it is the precursor of a wide variety of eicosanoids (i.e., bioactive compounds with hormone-like properties) and other important compounds that play a major role in the pro-inflammatory response (Tocher 2003; King and Smith 2018), as well as in the reproduction of aquatic organisms (Bell and Sargent 2003; Wacker and Von Elert 2004; Asil et al. 2017). Although most marine fish must acquire ARA through diet to meet their dietary/physiological needs (e.g., through diets rich in aquatic insect larvae that, in turn, contain large amounts of LC-PUFA, including ARA: Guo et al. 2016; Martin-Creuzburg et al. 2017), several freshwater fish species, such as European (Kissil et al. 1987) and Japanese (Takeuchi et al. 1980) eels, can synthesize ARA from LNA. In addition, freshwater zooplankton in the genus Daphnia (a common food of planktivorous fish in freshwater ecosystems) can retro-convert dietary docosapentaenoic acid (22:5n-6) to ARA (Strandberg et al. 2014). This may explain the greater contents of ARA in freshwater fish compared to their marine counterparts, as well as the trophic retention of ARA in freshwater fish species (Table 3) as in the Clupeiformes and Perciformes (Table S51).
Algae (i.e., phytoplankton and seaweeds) are the main providers of energy, and essential EPA and DHA to consumers (Dalsgaard et al. 2003; Parrish 2013). However, most higher trophic level marine consumers, including fish, cannot synthesize these two essential FA in sufficient quantities to meet their needs and, therefore, must acquire them through their diet for optimal health (Parrish 2013). The apparent difference in the ability to synthesize, EPA, DHA and ARA between freshwater and marine fish (although based on only a handful of studies), despite their common evolutionary past, has been assumed to be related to the availability of these FA in the two environments (Tocher 2003). For instance, EPA and DHA are mainly synthesized by diatoms and dinoflagellates. Although diatoms may be seasonally abundant in temperate freshwater lakes, diatoms and dinoflagellates are both numerically dominant throughout the seasons in marine systems, especially in temperate and polar regions. Therefore, marine fish (and marine consumers in general) can more consistently obtain these key FA through their diet (Parrish 2013). This may perhaps explain the overall high contents of n-3 LC-PUFA (especially EPA and DHA) in marine fish observed in our study, with the exception of freshwater Osmeriformes representatives that had higher mean levels of DHA than their marine counterparts (Table S51). In contrast, and as discussed above, freshwater systems are characterized by higher overall contents of ALA and LNA; hence, some anadromous fish species, such as rainbow trout (Gregory and James 2014), have evolved the ability to convert ALA into EPA and, from there, to DHA, and LNA into ARA, to supplement dietary intake and support their physiological requirements (Tocher 2003). For example, using hepatocyte bioassays, Murray et al. (2014) reported that up to 25% of DHA in Arctic charr (Salvelinus alpinus) was converted from dietary ALA, a bioconversion ability that is clearly much higher than in truly (i.e., not diadromous) marine fish. Yet, we caution that this argument remains somewhat speculative, as only a small number of fish species (∼20 out of a total of ∼32 000 fish species) have been so far assayed with respect to their biosynthetic capabilities (Gregory and James 2014), and a few of these species are diadromous (e.g., Atlantic salmon, rainbow trout, and European eel). Furthermore, the natural diet of species and their position in the food web may provide greater insights into the physiological differences and essential FA requirements in fish than habitat (i.e., freshwater vs. marine) (Trushenski and Rombenso 2019).
In addition to n-3 LC-PUFA, high contents of MUFA characterized the FA profiles of marine fish, as in the Osmeriformes (Table S51). These MUFA were mainly represented by 20:1n-9 and 22:1n-11, but the less abundant 20:1n-11, 20:1n-7, 22:1n-9 were also present. The MUFA, specifically of the 20:1 and 22:1 series, are typical of marine herbivorous zooplankton such as Arctic calanoid copepods (Falk-Petersen et al. 2000; Lee et al. 2006; Brett et al. 2009a) and, as was confirmed here (Table 2), are particularly abundant in marine fish from high latitudes which feed on these zooplankton (Ackman 1989). For this reason, these MUFA have been recommended as zooplankton biomarkers in marine fish (Sargent and Henderson 1986; Parrish 2013). Specifically, 20:1 and 22:1 FA and corresponding fatty alcohols are typical of herbivorous Calanus copepods that store them in their wax esters (Lee et al. 2006; Brett et al. 2009a). In addition, it appears that only marine copepods that go through diapause (i.e., dormancy), which is a common strategy in higher latitudes, but not in the tropics, contain 20:1n-9 and 22:1n-11 fatty alcohols. Indeed, these copepods typically accumulate large contents of wax esters rich in 20:1n-9 and 22:1n-11, as a long-term energy reserve (Lee et al. 2006). Consequently, fish and other organisms that feed on these copepods (e.g., omnivorous/carnivorous zooplankton, cnidarians) can retain these specific FA, and store them in their triacylglycerols or wax esters as a major source of energy (Phleger et al. 1997). By contrast, freshwater copepods do not typically store wax esters (except for “glacial relict species”, such as Limnocalanus macrurus and Senecella calanoides, which have a marine origin; Cavaletto et al. 1989) and, generally, accumulate relatively larger contents of EPA and (or) DHA than MUFA (Brett et al. 2009a).
Marine to freshwater ratio
Considering the FA driving the separation of freshwater and marine fish FA profiles obtained through multivariate statistical techniques (Fig. 1), we established a new metric, the M/F ratio, to help differentiate between “true” marine and freshwater fish and, indirectly, their feeding habitat. Specifically, the higher the value of this index (e.g., ≥ 11 in our study) the more marine-based is the diet and habitat of a given fish; whereas lower values (e.g., < 2) are more indicative of freshwater residency. Values in-between are expected to represent fish that, for example, live, at some point in their lives, in each biomes, as may be the case for Anguilliformes and Salmoniformes (Table S61); and likely also includes individuals that live in coastal areas, as in the Petromyzontiformes Lampetra japonica analyzed in this study. This species was the only representative of the order Petromyzontiformes in this data set, and was also the freshwater species with the highest M/F ratio (Table S61). The non-parasitic form of L. japonica is, in fact, a freshwater species, but lives in coastal areas, thus receiving marine dietary inputs from the surrounding marine habitats; whereas the parasitic form is anadromous. However, marine species from tropical areas and (or) with herbivorous feeding habits may present relatively low values of M/F (e.g., Tables 2, 3), thus highlighting the importance of considering the various biological and environmental factors characteristic of a given fish taxon when applying this metric. We note that the threshold values reported here are a guide and are based on the fish species included in this database. Moreover, the precise threshold values may change somewhat according to the fish taxa under examination. A non-exhaustive list of potential uses of this metric are reported in the Potential management implications section below.
Latitudinal gradients in fish FA composition
Overall, fish FA profiles varied across latitude zones, with increasing contents of EPA and DHA towards the poles (Fig. 4), whereas ARA had the opposite trend. Similar latitudinal gradients have already been described for marine organisms of different taxa and from different trophic levels (Colombo et al. 2016) and deep-sea fish (Parzanini et al. 2019). In this study, we showed that not only marine fish, and especially those from the order Perciformes, but also freshwater fish species manifested latitudinal gradients in their FA composition. In addition, our analyses revealed that contents of unsaturated FA (i.e., MUFA and PUFA) and UI were higher in polar latitudes, whereas contents of saturated FA (e.g., 16:0) increased towards the tropical regions. These trends may be associated with a general decrease of the surface-water temperature in polar regions that, in turn, may affect the lipid composition of cell membranes in ectothermic organisms as suggested by the homeoviscous adaptation hypothesis (Sinensky 1974; Hazel 1995). In fact, according to this hypothesis, to counteract the effects due to temperature variations and maintain cell membrane function and stability, ectotherms may respond by re-adjusting the lipid composition of their membranes (Sinensky 1974; Hazel and Landrey 1988; Pernet et al. 2006). Lower temperatures diminish membrane fluidity and viscosity, by promoting “packing” of the membrane phospholipids, and ectotherms also respond by increasing the unsaturation content of their phospholipid FA, as in rainbow trout (Hazel and Landrey 1988) and eastern oyster (Crassostrea virginica) (Pernet et al. 2007). In contrast, a greater incorporation of longer and more saturated FA into membrane phospholipids may occur when temperature increases (Sinensky 1974).
In parallel with these considerations, the differential rate of increase of DHA between freshwater and marine fish may be related to the different depth conditions characterizing the two biomes: the deepest freshwater habitat (i.e., Lake Baikal, Russia) is 1600 m deep, whereas the Mariana Trench in the Pacific Ocean is about 11 000 m deep. Moreover, the marine component of our data set included deep-sea fish that were collected between 200 and 4400 m depth (e.g., Lewis 1967; Parzanini et al. 2017). Increasing depth, along with decreasing temperature and increasing pressure, may diminish membrane fluidity and viscosity, and hence, affect the lipid composition of aquatic organisms (Parzanini et al. 2019), following the homeoviscous adaptation hypothesis mentioned above. The relatively moderate increase in DHA, a key membrane component, along the latitudinal gradient in marine fish may, therefore, be due to a depth effect, which partly overshadows our results. Unfortunately, we were not able to include the variable “Depth” in our analysis to assess this hypothesis, as this information was absent in the majority (i.e., >50%) of the studies considered here.
Another possible explanation for these latitudinal trends could be related to the different planktonic communities (i.e., phytoplankton and herbivorous zooplankton taxa) found in these latitude zones. Changes in the biochemical composition of primary producers and first level consumers may permeate through food webs up to higher trophic level consumers, including fish, which rely on them for food. For instance, diatoms and dinoflagellates, which are major producers of EPA and DHA, respectively, are numerically dominant in temperate and polar areas. Similarly, calanoid copepods are abundant in high latitude regions, and these planktonic crustaceans possess large lipid stores, which mainly consist of FA in the 20:1 and 22:1 series (Lee et al. 2006), but also of 16:1n-7 and 18:1n-9 (Brett et al. 2009a). Indeed, our analyses identified a latitudinal gradient of 16:1n-7, 18:1n-9, 20:1n-9, and 22:1n-11, whose contents increased in temperate and polar latitudes (Table 2). In addition, the phytoplankton community may influence the FA composition of their consumers also in response to increasing water temperatures (Boyd et al. 2013). In this regard, it has been predicted that global warming will diminish the production of n-3 LC-PUFA in phytoplankton (Hixson and Arts 2016) with potential cascading effects throughout food webs, culminating in reduced DHA contents in the food (fish) of humans (Colombo et al. 2020).
Marine tropical fish had much higher contents of ARA than their temperate and polar counterparts, as found previously for muscle (Gibson 1983; Couturier et al. 2013) and gonadal (Suloma and Ogata 2011) tissues of tropical fish. Temperate and polar waters are generally rich in food and nutrients. In contrast, marine habitats from tropical latitudes are oligotrophic (Huston and Wolverton 2009), except for warm-water coral reefs that represent some of the most productive and biodiverse ecosystems on Earth (Brandl et al. 2019; Robinson et al. 2019). These systems host a broad variety of species with a high biomass, including annelids, corals, and echinoderms, which typically have large contents of ARA in their tissues (Howell et al. 2003; Parzanini et al. 2017, 2018). Therefore, the high contents of ARA characterizing tropical fish may be due to their diet being richer in these invertebrates in comparison to fish from temperate and polar regions that have much better access to MUFA-rich zooplankton.
Differences in fish FA composition across feeding modes
Fish FA profiles also varied across feeding modes. Our analysis highlighted a strong retention of DHA from herbivorous to omnivorous and then to carnivorous fish of both freshwater and marine systems, although the strength of this relationship varied when analyses were performed on selected fish orders (i.e., Cypriniformes and Perciformes). This result reinforces that of Kainz et al. (2004), who observed a preferential retention of DHA in rainbow trout, and Colombo et al. (2016), for marine fish; and hence, further emphasizes the importance of this FA in fish biology and ecology. Indeed, DHA promotes somatic growth in fish (Ballantyne et al. 2003), in particular, during the larval and juvenile phases (Watanabe 1993; Furuita et al. 1996; Paulsen et al. 2014). Furthermore, DHA is a major component of neural and retinal tissues in fish (Mourente 2003), such that deficiencies in this essential FA have been shown to reduce visual acuity, especially at low-light levels (Bell et al. 1995). As Colombo et al. (2016) discussed, a growing number of studies indicate that the supply of DHA is more critical than that of EPA in fish (Furuita et al. 1996; Emery et al. 2016), and that the latter is either selectively catabolized to produce energy or converted to DHA (Murray et al. 2014). Indeed, EPA did not show any specific trend across feeding modes in our study.
Although ARA contents significantly decreased with increasing trophic levels in marine fish, this essential FA was retained across trophic levels in freshwater fish. This result might be related to the differential ability of freshwater and marine fish to convert LNA to ARA; hence, its availability in the environment, as discussed above, and (or) to specific physiological requirements that determine their preferential retention or oxidation. However, it must be stressed that the results obtained in this study, from data collected from the literature, represent general trends, and single species variations may occur. In fact, Kainz et al. (2017) did not observe DHA or ARA to be trophically retained in a few predatory fish species from Lake Lunz (Austria). Our analysis also reveals that ARA is not as prevalently stored in the muscle tissue of omnivorous and carnivorous marine fish as in herbivorous marine fish, but this is not the case for white sharks (Pethybridge et al. 2014).
Last, as expected, the contents of 20:1n-9 and 22:1n-11 increased at higher trophic levels in marine fish; as well as the ratio 18:1n-9/18:1n-7 in both freshwater and marine fish. The high contents of 20:1n-9 and 22:1n-11 in omnivorous and carnivorous marine fish most likely derive from their feeding (either directly or indirectly) on zooplankton that are rich in these MUFA (Ackman 1989; Brett et al. 2009a). Indeed, enhanced trophic retention of 20:1 and 22:1 FA was observed in benthic boundary layer zooplankton from the Beaufort Sea shelf in the Arctic Ocean (Connelly et al. 2014). In addition, 18:1n-9/18:1n-7 is a frequently used indicator of herbivorous/omnivorous vs. carnivorous feeding behaviors (Graeve et al. 1997; Parrish 2013). The basis for this is that oleic acid (18:1n-9) indicates animal dietary inputs (Falk-Petersen et al. 2000), and it is, therefore, typically high in high-level consumers, such as carnivores (Graeve et al. 1997). Oleic acid is an important cell membrane component that helps regulate cell membrane viscosity (Tocher 2003). This FA becomes particularly indicative of omnivorous/carnivorous feeding modes when reported in relation to phytoplankton dietary markers, such as 16:1n-7 and its elongation product, 18:1n-7 (Graeve et al. 1997; Parrish 2013).
Nutritional implications for human consumption
Fish is a significant source of essential FA for humans (e.g., EPA and DHA) (Fernandes et al. 2014; Strandberg et al. 2017) and, indeed, a daily dose of 300–500 mg of EPA and DHA is recommended for a healthy diet (Tocher et al. 2019). As such, the consumption of EPA and DHA, through either a supplement or natural sources (e.g., fish) is beneficial to mitigate chronic cardiovascular, auto-immune, and inflammatory diseases (Parrish 2009), as well as for neurological development and function (Swanson et al. 2012). Given that most existing fish stocks are at maximum sustainable limits (FAO 2020), finding alternative biological sources that can supply the increasing demand for seafood is, therefore, critical (Steinrücken et al. 2017). In this regard, our study revealed that carnivorous fish from polar and temperate latitudes (and marine especially) are particularly nutritious for human consumption, in terms of provisioning these essential FA. In fact, these fish species had the highest contents of ∑EPA+DHA and ∑n-3/n-6; both common indicators of food quality in nutritional studies (Huynh and Kitts 2009; Fernandes et al. 2014). Although Colombo et al. (2016) came to a similar conclusion when they compared the composition of essential FA in marine and terrestrial species, this is the first time that a broad comparison has specifically been made between freshwater and marine fish species. In addition, Osmeriformes and Salmoniformes representatives had high contents of EPA and DHA overall (Table S51), thus highlighting their value as dietary items. Although certain species from these orders are already exploited for their nutritional qualities (e.g., rainbow smelt, (Osmerus mordax) and Atlantic salmon (Salmo salar); Table S11), alternative and likely as valuable dietary sources may be explored and discovered within the same taxonomic groups, as for bioprospecting (Steinrücken et al. 2017). This is possible due to the generally conservative nature of critical biochemical pathways (Peregrin-Alvarez et al. 2003). Thus, fish species that are phylogenetically close should express similar biochemical pathways and, in this case, nutritional characteristics (for their consumers).
A diet rich in MUFA can have beneficial effects on brain activity and the cardiovascular system (Sartorius et al. 2012; Yang et al. 2016; Romano et al. 2017). Marine omnivorous and carnivorous fish from high latitudes also had the greatest contents of ∑MUFA and, in particular, of 16:1n-7, 18:1n-9, 18:1n-7, 20:1n-9, and 22:1n-11 as in Osmeriformes (Tables 2, 3, and S51), further emphasizing their importance as dietary sources of these FA. Specifically, a high dietary intake of oleic acid 18:1n-9, which is often associated with the Mediterranean diet, can help control blood cholesterol, reduce inflammation, and prevent the risk of heart and cognitive diseases (Priore et al. 2017; Romano et al. 2017). In addition, it has been shown that the consumption of 16:1n-7 may have beneficial effects on insulin resistance and diabetes (Frigolet and Gutiérrez-Aguilar 2017). Last, a growing number of animal and human studies suggests that a diet rich in LC-MUFA (>18 C atoms; e.g., 20:1 and 22:1 MUFA) promotes cardiovascular health (Matsumoto et al. 2013; Yang et al. 2016) and may reduce the probability of becoming afflicted by certain chronic diseases, including type-2 diabetes and atherosclerosis (Yang et al. 2016).
Potential management implications
It is clear that FA play many critical roles in the function and survival of all organisms, including humans. As such, our study of the distribution and abundance of FA in freshwater and marine fish represents a valuable tool for further research and may inform conservation efforts. This is even more relevant considering that ∼75% of the FA profiles analyzed in this study were from species that are commercially important (Table S11). For instance, fish from temperate and polar latitude regions, which are characterized by high levels of n-3 LC-PUFA, may be more sensitive to global warming, as their ability to adjust the lipid composition of their cell membranes in response to increasing water temperatures may be altered. In addition, these fish may also have to deal with a diet containing reduced quantities of these critical compounds (Hixson and Arts 2016) as the lipid compositions of cell membranes of the lower trophic level, ectothermic, prey organisms of these fish is also likely to be affected by global warming. As these fish (e.g., Osmeriformes and Salmoniformes) also provide a greater source of essential FA for human consumption, special consideration should be given towards their conservation. Certain fish from these two orders could also represent good sentinels of global warming; in particular, those with a restricted thermal tolerance, including, for example, lake trout (Salvelinus namaycush) and brown trout (Salmo trutta).
By providing a clearer depiction of freshwater vs. marine fish FA profiles, our study helps better understand the trophic ecology, condition, and habitat preference of those species that have the ability to live across different aquatic ecosystems during their life cycles (e.g., diadromous and (or) euryhaline species), and whose populations need to be managed. In this regard, the M/F ratio would represent a useful proxy of feeding habitat. This would be the case of the semi-catadromous and “critically endangered” European eel (Jacoby and Gollock 2014), for which relevant studies are currently being conducted (Parzanini, Arts, Rohtla, Koprivnikar, Power, Skiftesvik, Browman, Milotic, and Durif, unpublished data, 2019–2020); and of the Baltic Sea populations of the northern pike (Esox lucius), where information on habitat use and movement patterns is key to their conservation (e.g., Rohtla et al. 2012; Jacobsen et al. 2017). Indeed, northern pike populations have dramatically dropped in Baltic Sea coastal and freshwater areas over the past decades (Rohtla et al. 2012; Larsson et al. 2015). Although this predator can tolerate a wide range of salinity, spanning from fresh- to brackish water (Jacobsen et al. 2017), it migrates across different habitats and salinities throughout its life. In this regard, FA analysis would allow researchers and fisheries managers to better understand diet and habitat use of northern pike in the Baltic Sea, thus providing further support to existing studies and management plans (Rohtla et al. 2012; Larsson et al. 2015; Jacobsen et al. 2017).
Likewise, this investigation may support wildlife forensic science, as well as food control management. By looking at the FA profiles of illegally-caught fish or escapees and comparing it with the information provided here (e.g., the M/F ratio; Fig. 3), wildlife managers may be able to assess their primary feeding habitat (especially in the case of diadromous and (or) euryhaline fish), and thereby detect illegal fishing activities and (or) locate escape routes. Similarly, Winkler Villarreal et al. (1994) were able to distinguish wild from farmed individuals of red drum Sciaenops ocellatus, a euryhaline species under the conservation attention of the Texas Parks and Wildlife Department, by identifying four different diagnostic FA in their muscle tissues, including LNA, ARA, adrenic acid (22:4n-6), and docosapentaenoic acid (22:5n-6). Likewise, Vasconi et al. (2019), through the combined use of FA and stable isotope analyses, were able to recognize wild vs. captive-bred European eels. Furthermore, it is not uncommon, in the seafood market, freshwater or marine fish are intentionally traded with incorrect labelling, like sea bass sold as farmed tilapia (Reilly 2018; Warner et al. 2019). The information provided in this study may indeed help food inspectors identify mislabelling issues and other seafood frauds, as a cheaper and faster tool supplementary to the more established DNA barcoding technique (Reilly 2018).
Conclusions
Our analysis of 1382 fish FA profiles provides a first comprehensive effort to characterize FA relative abundance and distribution in freshwater vs. marine fish. In particular, our analysis detected fundamental differences between freshwater and marine fish. The former was characterized by high contents of n-6 PUFA, mainly LNA and ARA, which highlighted primary differences at the base of freshwater vs. marine food webs and the differential ability of fish to synthesize certain essential FA de novo. In contrast, the FA composition of marine fish species was mostly driven by the calanoid copepod/zooplankton biomarkers 20:1n-9 and 22:1n-11, and n-3 PUFA (e.g., EPA and DHA). Furthermore, latitudinal gradients in the FA composition of fish were observed. Overall, the UI content of FA in both freshwater and marine fish increased from tropical to temperate and then to polar regions, suggesting that variations across latitudes of water temperature may influence the lipid composition of fish cell membranes, in agreement with the homeoviscous adaptation hypothesis. In addition, the latitudinal trends of certain FA, such as 20:1n-9, 22:1n-11, EPA, DHA, and ARA indicated that variations in the food type from tropical to polar food webs may also explain these gradients. Our study also showed that DHA was highly retained in both freshwater and marine fish, further emphasizing the importance of this essential FA in fish. Last, marine carnivorous fish species from temperate and polar regions, and specifically those of the orders Osmeriformes and Salmoniformes represent a great source of healthy fats (e.g., 20:1 and 22:1 LC-MUFA) and essential nutrients (e.g., EPA and DHA) for human consumption.
Acknowledgements
This work was funded by Ryerson University and by a Natural Sciences and Engineering Research Council Discovery Grant (#04537-2014) to M.T. Arts. The authors would like to thank Keira McKee and Kyung Kim, a former MSc student and Research Assistant, respectively, at Ryerson University, for their help with data collection. Last, we would like to acknowledge an anonymous reviewer and Maja Ilić for their insightful comments, which have helped improve this manuscript.
Footnote
1
Supplementary data are available with the article through the journal Web site at Supplementary Material.
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Volume 28 • Number 4 • December 2020
Pages: 546 - 559
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Camilla Parzanini, Stefanie M. Colombo, Martin J. Kainz, Alexander Wacker, Christopher C. Parrish, and Michael T. Arts. 2020. Discrimination between freshwater and marine fish using fatty acids: ecological implications and future perspectives. Environmental Reviews.
28(4): 546-559. https://doi.org/10.1139/er-2020-0031
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17. Omega‐3 long‐chain polyunsaturated fatty acids in Atlantic salmon: Functions, requirements, sources, de novo biosynthesis and selective breeding strategies
18. Selective breeding in the noble scallop (Chlamys nobilis) for low-temperature resistance to reduce overwintering losses
19. Escaping malnutrition by shifting habitats: A driver of three‐spined stickleback invasion in Lake Constance
20. Effects of Trace Elements on the Fatty Acid Composition in Danubian Fish Species
21. Fatty acid profiles reveal dietary variability of a large calanoid copepod Limnocalanus macrurus in the northern Baltic Sea
22. The Lipidomic Fingerprints of Common Octopus (Octopus Vulgaris) Arm Muscle Enable the Discrimination between Landing Sites Along the Iberian Atlantic Coast
23. Variability in fatty acids composition in eggs of an omnivorous waterbird, the black-headed gull
Chroicocephalus ridibundus
, foraging in different habitats
24. The evolving story of catadromy in the European eel (
Anguilla anguilla
)
25. Trophodynamics of the Antarctic toothfish (Dissostichus mawsoni) in the Antarctic Peninsula: Ontogenetic changes in diet composition and prey fatty acid profiles
26. What are the most effective biotic and abiotic factors affecting fatty acid composition of Garra rufa (Heckel, 1843)?
27. CRISPR/Cas9-mediated knock-in of masu salmon (Oncorhyncus masou) elongase gene in the melanocortin-4 (mc4r) coding region of channel catfish (Ictalurus punctatus) genome
28. Intra-specific correlations between fatty acids and morphological traits are consistent across fish species
29. Factors affecting nutritional quality in terms of the fatty acid composition of Cyprinion macrostomus
30. Taxonomy and diet determine the polar and neutral lipid fatty acid composition in deep-sea macrobenthic invertebrates
31. Evaluation of Chemical Elements, Lipid Profiles, Nutritional Indices and Health Risk Assessment of European Eel (Anguilla anguilla L.)
32. Benefit-risk assessment of consuming fish and shrimp from a large eutrophic freshwater lake, China
33. Blood-based gene expression as non-lethal tool for inferring salinity-habitat history of European eel (Anguilla anguilla)
34. Living in the Extreme: Fatty Acid Profiles and Their Specificity in Certain Tissues of Dominant Antarctic Silverfish, Pleuragramma antarcticum, from the Antarctic Sound (Southern Ocean) Collected during the Austral Summer
35. Trophic transfer of lipids and fatty acids across habitats in tropical river food webs
36. Essential Fatty Acids—‘Fueling Versus Controlling’
37. Biosynthesis of Polyunsaturated Fatty Acids—‘Many Can, Some Can’t’
38. Trophic Transfer of PUFAs—‘Vital Ones Reach Top Predators’
39. Trophic ecology of the European eel (Anguilla anguilla) across different salinity habitats inferred from fatty acid and stable isotope analysis
40. Freshwater, Landlocked Grand Lake Strain of Atlantic Salmon (Salmo salar L.) as a Potential Genetic Source of Long Chain Polyunsaturated Fatty Acids Synthesis
41. Parasites and their freshwater snail hosts maintain their nutritional value for essential fatty acids despite altered algal diets
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