Browning reduces the availability—but not the transfer—of essential fatty acids in temperate lakes

Abstract

Atmospheric changes are leading to the browning of northern lakes (i.e. increases in catchment‐derived dissolved organic matter [DOM]), consequently altering phytoplankton biomass and community composition. We hypothesised that lake browning and the concurrent increase in nutrients drive a shift towards greater cyanobacteria biomass. We further hypothesised that, as a consequence of this shift in phytoplankton, the content of ω‐3 (n‐3) essential fatty acids (EFA) in seston would decline, affecting the subsequent transfer of EFA to consumers across the plant–animal interface in pelagic regions of lakes. We tested these hypotheses in the epilimnion of 30 temperate lakes in Ontario (Canada), representing a gradient of lake browning, with dissolved organic carbon (DOC) ranging from 2 to 10 mg/L and total phosphorus ranging from 6.0 to 48.5 μg/L. In each of these lakes, the concentration and composition of DOM, the biomass of phytoplankton and cyanobacteria, and the EFA content of seston, cladocerans, and copepods were measured. An increase in aromatic DOM was associated with increased phytoplankton and cyanobacteria biomass. Due to the lower content of the EFA eicosapentaenoic acid (EPA; 20:5n‐3) and docosahexaenoic acid (DHA; 22:6n‐3) in cyanobacteria, this increase in phytoplankton biomass was associated with a decline in EPA and DHA content in lake seston. However, there was no significant change in EFA content of cladocerans and copepods. This homeostatic (diet‐independent) EFA composition in zooplankton suggested that, as the phytoplankton community shifted towards more cyanobacteria with lower EFA content, the cladocerans and copepods may have met their nutritional requirements by relying on alternative food sources (e.g. heterotrophic ciliates and flagellates) capable of either trophically upgrading phytoplankton‐produced EPA and DHA, or synthesising EPA and DHA de novo. Results from this study indicate that increasing DOC from low (2 mg DOC/L) to moderate levels (15 mg DOC/L) may increase the importance of the microbial pathway in the trophic transfer of EPA and DHA from basal resources to zooplankton. However, this supplementary transfer of EFA through the microbial food web may not sustain high EPA and DHA levels in zooplankton when lake browning starts to limit primary production (>15 mg DOC/L).

Increasing concentration of polyunsaturated fatty acids in browning boreal lakes is driven by nuisance alga Gonyostomum

“…This is supported by the results from Lake € At€ ask€ o in the current study, which was the only lake with any relevant anthropogenic input of carbon and nutrients (Palviainen et al 2016). Lake € At€ ask€ o was distinct from the other high DOC lakes due to its absence of Gonyostomum and correspondingly lower phytoplankton biomass and PUFA concentration (although not as low as in the oligotrophic lakes), which is in accordance with previous studies (Bergstr€ om and Karlsson 2019, Senar et al 2019. This suggests that trajectories of lake browning and the basal production of PUFA may differ depending on large-scale climatic factors and vegetation zones, as well as local factors, such as anthropogenic nutrient and carbon loading.…”

“…Cyanobacteria do not contain any EPA or DHA but may contain C18 PUFA (Los and Mironov 2015), thus maintaining some level of PUFA production (Strandberg et al 2015b). The dominance of cyanobacteria in browning temperate lakes may be related to longer and warmer growing season and higher nutrient levels or less acidic conditions compared to the naturally brown boreal lakes in the current study (Palviainen et al 2016, Senar et al 2019. This is supported by the results from Lake € At€ ask€ o in the current study, which was the only lake with any relevant anthropogenic input of carbon and nutrients (Palviainen et al 2016).…”

“…Lake browning and its effects on seston PUFA concentration may differ between boreal and temperate lakes and are most likely strongly affected by landscape and the level of anthropogenic activity in the watershed. Moderate browning of temperate lakes together with elevated nutrient loading may promote cyanobacteria growth and decrease seston PUFA content (Senar et al 2019). In boreal lakes, browning is often due to increased loading of DOC from nutrient-poor and more acidic peatlands, which may lead to the dominance of another nuisance alga, Gonyostomum, and increased seston PUFA concentration.…”

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

“…There are many differences in life-history strategies between different zooplankton taxa, where the calanoid Eudiaptomus graciloides, the dominant copepod in cold oligotrophic lakes, tends to accumulate lipids (including FAs) to survive winter, whereas short-lived cladocerans form resting stages and do not need high body fat reserves (Grosbois et al, 2017;Hiltunen et al, 2016). In a recent study, Senar et al (2019) investigated a similar nutrient (total phosphorus 6-48 µg/L) and colour (dissolved organic carbon 2-10 mg/L) gradient in Canadian lakes, but did not record clear decrease in zooplankton taxa FA content. However, their study region was warmer and did not contain strong temperature gradients, which have clear influence on lipid rich copepod abundance in zooplankton communities and thus PUFA content (Gladyshev et al, 2011;Hiltunen et al, 2016;Senar et al, 2019).…”

Global changes may be promoting a rise in select cyanobacteria in nutrient‐poor northern lakes

“…Greater relative biovolumes of cyanobacteria in northern lakes have potential food web implications. Cyanobacteria, compared to their eukaryotic competitors, generally do not contain long‐chain poly‐unsaturated fatty acids (Buse, Ruess, & Filser, 2013; Senar, Creed, Strandberg, & Arts, 2019), do not produce sterols (Volkman, 2003) and are an insufficient source of vitamin B 12 (Helliwell et al, 2016). In freshwater ecosystems, cyanobacteria blooms are known to reduce resource quality of the food base (cf.…”