Environmental drivers alter PUFA content in littoral macroinvertebrate assemblages via changes in richness and abundance.

Shallow littoral areas in lakes are productive and highly diverse ecotonal zones, providing habitats for both invertebrate and vertebrate species. We developed a Bayesian modeling framework to elucidate the relationships between environmental drivers (lake typology, habitat, water chemistry, and latitude) and taxon richness, abundance, as well as the content of polyunsaturated fatty acids (PUFAs) in littoral macroinvertebrate communities in 95 boreal lakes. PUFAs, particularly arachidonic acid (ARA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA), are critical micronutrients to maintain normal physiological functions in consumers. Lake typology was a significant predictor for PUFA content in the invertebrate assemblages, which was connected to taxon richness and/or abundance. Benthic communities in large humus-poor or nutrient-rich lakes displayed higher abundance, taxon richness, and more PUFA-rich taxa, whereas those in medium- and large-sized humic (color 30-90 mg Pt/L) and humus-rich lakes (color >90 mg Pt/L) were characterized by decreased abundance and subsequently low PUFA content. The abundance, taxon richness, and nutritional quality of the communities were also strongly related to latitude. Lakes with lower pH were characterized by lower benthic invertebrate diversity and low frequency of taxa with high somatic EPA and DHA content. The complexity of littoral habitats dominated by various macrophyte assemblages creates an environment that favors higher benthic abundance and increased presence of taxonomic groups with high PUFA content. Nutritional quality of benthic invertebrates for upper trophic levels can be modulated by a complex interplay between external stressors and abiotic factors that typically shape the structure of littoral benthic communities. Supplementary Information: The online version contains supplementary material available at 10.1007/s00027-023-00996-2.

Eutrophication effect on production and transfer of omega-3 fatty acids in boreal lake food webs.

Eutrophication, i.e. increasing level of nutrients and primary production, is a central environmental change of lakes globally with wide effects on food webs. However, how eutrophication affects the synthesis of physiologically essential biomolecules (omega-3 fatty acids) and their transfer to higher trophic levels at the whole food web level is not well understood. We assessed food web (phytoplankton, zooplankton, and fish) biomass, community structure and fatty acid content (eicosapentaenoic acid [EPA], and docosahexaenoic acid [DHA]), together with fatty acid specific primary production in 12 Finnish boreal lakes covering the total nutrient gradient from oligotrophic to highly eutrophic lakes (4-140 µg TP l-1; 413-1814 µg TN l-1). Production was measured as the incorporation of 13C-NaHCO3 into phytoplankton fatty acids and differentiated into volumetric production (production per litre of water) and productivity (production per phytoplankton biomass). Increases in nutrients led to higher biomass of phytoplankton, zooplankton and fish communities while also affecting community composition. Eutrophication negatively influenced the contribution of phytoplankton biomass preferentially grazed by zooplankton (<35 µm). Total volumetric production saturated at high phytoplankton biomass while EPA volumetric production presented a logarithmic relationship with nutrient increase. Meanwhile, total and EPA productivity had unimodal responses to this change in nutrients. DHA volumetric production and productivity presented large variation with increases in total phosphorus, but a unimodal model best described DHA changes with eutrophication. Results showed that eutrophication impaired the transfer of EPA and DHA into zooplankton and fish, showing a clear negative impact in some species (e.g. perch) while having no effect in other species (e.g. roach, ruffe). Results show non-linear trends in fatty acid production and productivity peaking at nutrient concentrations 22-35 µg l-1 TP followed by a gradual decrease.

Allochthony, fatty acid and mercury trends in muscle of Eurasian perch (Perca fluviatilis) along boreal environmental gradients.

Environmental change, including joint effects of increasing dissolved organic carbon (DOC) and total phosphorus (TP) in boreal northern lakes may affect food web energy sources and the biochemical composition of organisms. These environmental stressors are enhanced by anthropogenic land-use and can decrease the quality of polyunsaturated fatty acids (PUFAs) in seston and zooplankton, and therefore, possibly cascading up to fish. In contrast, the content of mercury in fish increases with lake browning potentially amplified by intensive forestry practises. However, there is little evidence on how these environmental stressors simultaneously impact beneficial omega-3 fatty acid (n3-FA) and total mercury (THg) content of fish muscle for human consumption. A space-for-time substitution study was conducted to assess whether environmental stressors affect Eurasian perch (Perca fluviatilis) allochthony and muscle nutritional quality [PUFA, THg, and their derivative, the hazard quotient (HQ)]. Perch samples were collected from 31 Finnish lakes along pronounced lake size (0.03-107.5 km2), DOC (5.0-24.3 mg L-1), TP (5-118 µg L-1) and land-use gradients (forest: 50.7-96.4%, agriculture: 0-32.6%). These environmental gradients were combined using principal component analysis (PCA). Allochthony for individual perch was modelled using source and consumer δ2H values. Perch allochthony increased with decreasing lake pH and increasing forest coverage (PC1), but no correlation between lake DOC and perch allochthony was found. Perch muscle THg and omega-6 fatty acid (n6-FA) content increased with PC1 parallel with allochthony. Perch muscle DHA (22:6n3) content decreased, and ALA (18:3n3) increased towards shallower murkier lakes (PC2). Perch allochthony was positively correlated with muscle THg and n6-FA content, but did not correlate with n3-FA content. Hence, the quality of perch muscle for human consumption decreases (increase in HQ) with increasing forest coverage and decreasing pH, potentially mediated by increasing fish allochthony.

Increasing temperature and productivity change biomass, trophic pyramids and community-level omega-3 fatty acid content in subarctic lake food webs.

Climate change in the Arctic is outpacing the global average and land-use is intensifying due to exploitation of previously inaccessible or unprofitable natural resources. A comprehensive understanding of how the joint effects of changing climate and productivity modify lake food web structure, biomass, trophic pyramid shape and abundance of physiologically essential biomolecules (omega-3 fatty acids) in the biotic community is lacking. We conducted a space-for-time study in 20 subarctic lakes spanning a climatic (+3.2°C and precipitation: +30%) and chemical (dissolved organic carbon: +10 mg/L, total phosphorus: +45 µg/L and total nitrogen: +1,000 µg/L) gradient to test how temperature and productivity jointly affect the structure, biomass and community fatty acid content (eicosapentaenoic acid [EPA] and docosahexaenoic acid [DHA]) of whole food webs. Increasing temperature and productivity shifted lake communities towards dominance of warmer, murky-water-adapted taxa, with a general increase in the biomass of primary producers, and secondary and tertiary consumers, while primary invertebrate consumers did not show equally clear trends. This process altered various trophic pyramid structures towards an hour glass shape in the warmest and most productive lakes. Increasing temperature and productivity had negative fatty acid content trends (mg EPA + DHA/g dry weight) in primary producers and primary consumers, but not in secondary nor tertiary fish consumers. The massive biomass increment of fish led to increasing areal fatty acid content (kg EPA + DHA/ha) towards increasingly warmer, more productive lakes, but there were no significant trends in other trophic levels. Increasing temperature and productivity are shifting subarctic lake communities towards systems characterized by increasing dominance of cyanobacteria and cyprinid fish, although decreasing quality in terms of EPA + DHA content was observed only in phytoplankton, zooplankton and profundal benthos.

Fatty acid metabolism and modifications in Chironomus riparius.

A priori knowledge of fatty acid modifications in consumers is essential for studies using fatty acids as biomarkers. We investigated fatty acid metabolism and possible modification pathways in benthic invertebrate Chironomus riparius larvae (Diptera). We conducted diet manipulation experiments using natural food sources (two chlorophyte algae, a diatom and a non-toxic cyanobacterium). We also did a diet-switch experiment on two different resources, fish food flakes TetraMin® and cyanobacterium Spirulina, to study fatty acid turnover in Chironomus. Results of the diet manipulation experiments indicate that Chironomus larvae have a strong tendency to biosynthesize 20:5n-3 and 20:4n-6 from precursor fatty acids, and that the dietary availability of polyunsaturated fatty acids (PUFA) does not control larval growth. Fatty acid modifications explain why low dietary availability of PUFA did not significantly limit growth. This has ecologically relevant implications on the role of benthic chironomids in conveying energy to upper trophic level consumers. A diet-switch experiment showed that the turnover rate of fatty acids in Chironomus is relatively fast--a few days. The compositional differences of algal diets were large enough to separate Chironomus larvae into distinct groups even if significant modification of PUFA was observed. In summary, fatty acids are excellent dietary biomarkers for Chironomus, if modifications of PUFA are considered, and will provide high-resolution data on resource use. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.

Influence of littoral periphyton on whole-lake metabolism relates to littoral vegetation in humic lakes.

The role of littoral habitats in lake metabolism has been underrated, especially in humic lakes, based on an assumption of low benthic primary production (PP) due to low light penetration into water. This assumption has been challenged by recent recognition of littoral epiphyton dominance of whole-lake PP in a small highly humic lake and of epiphyton as an important basal food source for humic lake biota. However, as these studies have mostly concerned single lakes, there is a need to test their wider generality. We studied the whole-lake PP and community respiration (CR) in eight small humic lakes in southern Finland during July 2015 using 14 C incorporation to measure pelagic PP and the changes in dissolved inorganic carbon in light and dark in situ incubations to measure CR and littoral PP by epiphyton. Changes in O2 concentration in both pelagic and littoral surface water were measured periodically from each lake and, additionally, continuously with a data logger from one lake during the study period. The results revealed that the littoral dominated whole-lake net primary production (NPP) in five of the eight lakes, which was supported by observed O2 supersaturation in the littoral surface water in most of the lakes. Calculated pelagic:littoral ratios by area correlated negatively with both littoral NPP and littoral contribution to whole-lake NPP. Moreover, there was a significant positive relationship between littoral proportion of whole-lake NPP and the fraction of lake surface area covered by littoral aquatic vegetation. This demonstrates that increased aquatic littoral vegetation cover increases the overall importance of the littoral to whole-lake PP in highly humic lakes. Littoral NPP also correlated strongly with littoral O2 saturation, and the continuously measured O2 revealed substantial temporal variation in O2 saturation, particularly in the littoral zone. Whole-lake gross primary production:community respiration (GPP:CR) ratios revealed that accounting for littoral metabolism produced a marked shift towards lake metabolic balance, although all the eight lakes remained net heterotrophic. This study emphasizes that littoral metabolism needs to be accounted for when estimating whole-lake C fluxes in all lakes, even in highly colored humic waters.