Polyunsaturated fatty acids in stream food webs – high dissimilarity among producers and consumers

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Polyunsaturated fatty acids in fish tissues more closely resemble algal than terrestrial diet sources

The River Continuum Concept implies that consumers in headwater streams have greater dietary access to terrestrial basal resources, but recent studies have highlighted the dietary importance of high-quality algae. Algae provide consumers with physiologically important omega-3 (n-3) polyunsaturated fatty acids (PUFA), particularly eicosapentaenoic acid (EPA). However, terrestrial plants and most benthic stream algae lack the long-chain (LC) n-3 PUFA docosahexaenoic acid (DHA, 22:6n-3), which is essential for neural development in fish and other vertebrates. We sampled subalpine streams to investigate how the PUFA composition of neural (brain and eyes), muscle, and liver tissues of freshwater fish is related to their potential diets (macroinvertebrates, epilithon, fresh and conditioned terrestrial leaves). The PUFA composition of consumers was more similar to epilithon than to terrestrial leaves. Storage lipids of eyes most closely resembled dietary 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. This implies that algal PUFA were selectively retained or were produced internally via enzymatic PUFA conversion by aquatic consumers. This field study demonstrates the nutritional importance of algal PUFA for neural organs in aquatic consumers of headwater regions.

     

The importance of high‐quality algal food sources in stream food webs – current status and future perspectives

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Efficiency of transfer of essential polyunsaturated fatty acids versus organic carbon from producers to consumers in a eutrophic reservoir

One of the central paradigms of ecology is that only about 10% of organic carbon production of one trophic level is incorporated into new biomass of organisms of the next trophic level. Many of energy-yielding compounds of carbon are designated as ‘essential’, because they cannot be synthesized de novo by consumers and must be obtained with food, while they play important structural and regulatory functions. The question arises: are the essential compounds transferred through trophic chains with the same efficiency as bulk carbon? To answer this question, we measured gross primary production of phytoplankton and secondary production of zooplankton and content of organic carbon and essential polyunsaturated fatty acids of ω-3 family with 18–22 carbon atoms (PUFA) in the biomass of phytoplankton and zooplankton in a small eutrophic reservoir during two summers. Transfer efficiency between the two trophic levels, phytoplankton (producers) and zooplankton (consumers), was calculated as ratio of the primary production versus the secondary (zooplankton) production for both carbon and PUFA. We found that the essential PUFA were transferred from the producers to the primary consumers with about twice higher efficiency than bulk carbon. In contrast, polyunsaturated fatty acids with 16 carbon atoms, which are synthesized exclusively by phytoplankton, but are not essential for animals, had significantly lower transfer efficiency than both bulk carbon, and essential PUFA. Thus, the trophic pyramid concept, which implicitly implies that all the energy-yielding compounds of carbon are transferred from one trophic level to the next with the same efficiency of about on average 10%, should be specified for different carbon compounds.     

The role of highly unsaturated fatty acids in aquatic foodweb processes

1. Polyunsaturated fatty acids (PUFA) are almost exclusively synthesized by plants. Animals can convert from one form of PUFA to another through elongation and desaturation, but very few can synthesize PUFA de novo. PUFA play an important role in regulating cell membrane properties, serve as precursors for important animal hormones and are essential for animals. 2. In aquaculture studies, highly unsaturated fatty acids (HUFA), a subset of PUFA, have been found to be critical for maintaining high growth, survival and reproductive rates and high food conversion efficiencies for a wide variety of marine and freshwater organisms. 3. The plankton literature suggests high food-quality algae species are rich in HUFA and low food-quality algae are poor in HUFA. Adding semi-pure emulsions of HUFA to algae monocultures can markedly increase the growth rates of zooplankton feeding on these mixtures. 4. A study measuring zooplankton biomass accrual when feeding on natural phytoplankton found a strong correlation between phytoplankton HUFA (specifically eicosapentaenoic acid) content and herbivorous zooplankton production. 5. The aquatic ecology literature suggests that planktonic foodwebs with high HUFA content phytoplankton have high zooplankton to phytoplankton biomass ratios, while systems with low HUFA phytoplankton have low zooplankton biomass. Also, the seasonal succession of plankton in many temperate lakes follows patterns tied to phytoplankton HUFA content, with intense zooplankton grazing and ‘clear-water-phases’ characteristic of periods when the phytoplankton is dominated by HUFA-rich species. 6. Herbivorous zooplankton production is constrained by the zooplankton’s ability to ingest and digest phytoplankton. It is becoming increasingly clear, however, that much of the phytoplankton which is assimilated may be nutritionally inadequate. HUFA may be key nutritional constituents of zooplankton diets, and may determine energetic efficiency across the plant–animal interface, secondary production and the strength of trophic coupling in aquatic pelagic foodwebs.     

Highly unsaturated fatty acids in nature: what we know and what we need to learn

The supply and demand of omega‐3 highly unsaturated fatty acids (ω‐3 HUFA) in natural ecosystems may lead to resource limitation in a diverse array of animal taxa. Here, we review why food quality in terms of ω‐3 HUFAs is important, particularly for neural tissue, across a diversity of animal taxa ranging from invertebrate zooplankton to vertebrates (including humans). Our review is focused on ω‐3 HUFAs rather than other unsaturated fatty acids because these compounds are especially important biochemically, but scarce in nature. We discuss the dichotomy between ω‐3 HUFA availability between aquatic primary producers, which are often rich in these compounds, and terrestrial primary producers, which are contain little to none of them. We describe the use of fatty acids as qualitative and quantitative tracers for reconstructing animal diets in natural ecosystems. Next, we discuss both direct and indirect ecological implications of ω‐3 HUFA limitation at the individual, population, food web, and ecosystem scales, which include: changes in behavior, species composition, secondary production rates, trophic transfer efficiency and cross‐ecosystem subsidies. We finish by highlighting future research priorities including a need for more research on ω‐3 HUFAs in terrestrial systems, more research their importance for higher order consumers, and more research on the food web and ecosystem‐scale effects of ω‐3 HUFA limitation. Synthesis Mismatches between the supply of and demand for omega‐3 highly unsaturated fatty acids (ω‐3 HUFA) in natural ecosystems have the potential to result in resource limitation across a diverse array of ecosystems. We combined perspectives from ecology and nutritional science to develop a unified synthesis of ω‐3 HUFA ecology. We reviewed the importance of ω‐3 HUFAs for animals, the striking differences in ω‐3 HUFA availability at the base of terrestrial versus aquatic food webs, and the implications of ω‐3 HUFA limitation for food webs. We finished by highlighting research priorities in the field including more research on ω‐3 HUFAs in terrestrial systems, on higher order consumers, and at the food web and ecosystem‐scales.     

Comparison of fatty acid contents and composition in major lipid classes of larvae and adults of mosquitoes (Diptera: Culicidae) from a steppe region

Emerging aquatic insects, including mosquitoes, are known to transfer to terrestrial ecosystems specific essential biochemicals, such as polyunsaturated fatty acids (PUFA). We studied fatty acid (FA) composition and contents of dominant mosquito populations (Diptera: Culicidae), that is, Anopheles messeae, Ochlerotatus caspius, Oc. flavescens, Oc. euedes, Oc. subdiversus, Oc. cataphylla, and Aedes cinereus, inhabited a steppe wetland of a temperate climate zone to fill up the gap in their lipid knowledge. The polar lipid and triacylglycerol fractions of larvae and adults were compared. In most studied mosquito species, we first found and identified a number of short‐chain PUFA, for example, prominent 14:2n‐6 and 14:3n‐3, which were not earlier documented in living organisms. These PUFA, although occurred in low levels in adult mosquitoes, can be potentially used as markers of mosquito biomass in terrestrial food webs. We hypothesize that these acids might be synthesized (or retroconverted) by the mosquitoes. Using FA trophic markers accumulated in triacylglycerols, trophic relations of the mosquitoes were accessed. The larval diet comprised green algae, cryptophytes, and dinoflagellates and provided the mosquitoes with essential n‐3 PUFA, linolenic, and eicosapentaenoic acids. As a result, both larvae and adults of the studied mosquitoes had comparatively high content of the essential PUFA. Comparison of FA proportions in polar lipids versus storage lipids shown that during mosquito metamorphosis transfer of essential eicosapentaenoic and arachidonic acids from the reserve in storage lipids of larvae to functional polar lipids in adults occurred.     

How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems?

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Climate warming is predicted to reduce omega‐3, long‐chain,polyunsaturated fatty acid production in phytoplankton

Phytoplankton are the main source of energy and omega‐3 (n‐3) long‐chain essential fatty acids (EFA) in aquatic ecosystems. Their growth and biochemical composition are affected by surrounding environmental conditions, including temperature, which continues to increase as a result of climate warming. Increasing water temperatures may negatively impact the production of EFA by phytoplankton through the process of homeoviscous adaptation. To investigate this, we conducted an exploratory data synthesis with 952 fatty acid (FA) profiles from six major groups of marine and freshwater phytoplankton. Temperature was strongly correlated with a decrease in the proportion of n‐3 long‐chain polyunsaturated FA (LC‐PUFA) and an increase in omega‐6 FA and saturated FA. Based on linear regression models, we predict that global n‐3 LC‐PUFA production will be reduced by 8.2% for eicosapentaenoic acid (EPA) and 27.8% for docosahexaenoic acid (DHA) with an increase in water temperature of 2.5 °C. Using a previously published estimate of the global production of EPA by diatoms, which contribute to most of the world's supply of EPA, we predict a loss of 14.2 Mt of EPA annually as a result of ocean warming. The n‐3 LC‐PUFA are vitally important for an array of key physiological functions in aquatic and terrestrial organisms, and these FA are mainly produced by phytoplankton. Therefore, reduced production of these EFA, as a consequence of climate warming, is predicted to negatively affect species that depend on these compounds for optimum physiological function. Such profound changes in the biochemical composition of phytoplankton cell membranes can lead to cascading effects throughout the world's ecosystems.     

Comparison of fatty acids and elemental nutrients in periphyton, invertebrates, and cutthroat trout (Oncorhynchus clarki) in conifer and alder streams of western Washington state

Organism growth and reproduction are often limited by nutrient availability in freshwater ecosystems where, in some cases, food webs are primarily supported by allochthonous organic matter. Therefore, we hypothesized that the composition of riparian vegetation would influence the variability of N, P, and fatty acid content of in-stream consumers. Specifically, we predicted that organisms living in alder streams would have higher levels of N, P, and polyunsaturated fatty acids than organisms in coniferous streams. To determine this, we sampled fresh and aged leaf litter, periphyton, invertebrates, and cutthroat trout (Oncorhynchus clarki) from 6 streams in western Washington state: 3 streams had high densities of nitrogen-fixing red alder (Alnus rubra) in the riparian zone, whereas 3 had high densities of conifers. We found fresh alder litter had twice the total polyunsaturated fatty acid concentrations of hemlock vegetation while there were few statistical differences among aged alder and aged hemlock vegetation. Multidimensional plots showed fatty acid profiles were unique to vegetation and fish while periphyton and invertebrates shared the same multidimensional space. We used a mixed model to determine the relative importance of vegetation type (fixed factor: conifer or alder), trophic levels (fixed factor: periphyton, primary consumer, or fish), and streams (random factor) on individual fatty acid concentrations. Total polyunsaturated fatty acids, 16:0, 20:1, 20:3n6 and total n3 were the only fatty acids influenced by stream vegetation (vegetation + stream model or full model). 67% of the fatty acids were best supported by the trophic + stream model. Nitrogen, P, Ca, Fe, C:N, N:P, and C:N:P were all best supported by the trophic level + stream model, and Zn was the only nutrient supported best by the full model. Correlations of n3 and n6 fatty acid concentrations between periphyton and primary consumers, and primary consumers with trout indicated several fatty acid metrics, such as n3:n6, showed food resources may affect relative fatty acid abundances of consumers. Although vegetation type did not influence relative fatty acids of stream organisms, the importance of trophic level likely indicates organisms have different physical requirements for fatty acids. The significance of a random factor, ‘stream,’ suggests that the relative abundances of fatty acids in periphyton, invertebrates, and trout are stream-specific and are responding to local environmental or communal variables.     

Preliminary estimation of the export of omega-3 polyunsaturated fatty acids from aquatic to terrestrial ecosystems in biomes via emergent insects

Some terrestrial consumers may be limited by food quality, namely by contents of essential polyunsaturated fatty acids (PUFA), eicosapentaenoic acid (20:5n−3, EPA) and docosahexaenoic acid (22:6n−3, DHA) in their food. Since EPA and DHA are mainly produced in aquatic ecosystems, for future estimating of the potential limitation by food quality in global scale, the water-land fluxes of these PUFA with the biomass of emergent aquatic insects in several biomes were calculated. The water /land area ratios for each biome were calculated by dividing the water area of each biome by its terrestrial area. Data on insect emergence from water bodies (g of dry mass m⁻² year⁻¹), were summarized and averaged for each biome. From available data, EPA and DHA contents (mg g⁻¹dry mass), in the biomass of emergent aquatic insects were calculated first so that annual fluxes of PUFA to land area via aquatic insect emergence could be estimated for each biome. PUFA fluxes occurred between the biomes, ranging from 0.04 to 4.39 mg m⁻² year⁻¹. In this study, the aquatic PUFA supply to land area appeared to be significantly lower than estimated earlier. This suggests that terrestrial consumers may experience food quality limitations mediated by shortage of PUFA compounds.     

Waterbugs (Heteroptera: Nepomorpha and Gerromorpha) as sources of essential n‐3 polyunsaturated fatty acids in Central Siberian ecoregions

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The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella

In food-web studies, parasites are often ignored owing to their insignificant biomass. We provide evidence that parasites may affect trophic transfer in aquatic food webs. Many phytoplankton species are susceptible to parasitic fungi (chytrids). Chytrid infections of diatoms in lakes may reach epidemic proportions during diatom spring blooms, so that numerous free-swimming fungal zoospores (2-3 microm in diameter) are produced. Analysis shows that these zoospores are rich in polyunsaturated fatty acids and sterols (particularly cholesterol), which indicates that they provide excellent food for zooplankters such as Daphnia. In life-table experiments using the large diatom Asterionella formosa as food, Daphnia growth increased significantly in treatments where a parasite was present. By grazing on the zoospores, Daphnia acquired important supplementary nutrients and were able to grow. When large inedible algae are infected by parasites, nutrients within the algal cells are consumed by these chytrids, some of which, in turn, are grazed by Daphnia. Thus, chytrids transfer energy and nutrients from their hosts to zooplankton. This study suggests that parasitic fungi alter trophic relationships in freshwater ecosystems and may be the important components in shaping the community and the food-web dynamics of lakes.     

Direct and indirect effects of UV radiation on benthic communities: epilithic food quality and invertebrate growth in four montane lakes

The direct harmful effects of ultraviolet radiation (UVR) on benthic and planktonic organisms have been well studied in aquatic systems. Less clear, however, is how UVR might affect aquatic communities through its effects on trophic interactions. The focus of this study was twofold: first, to examine the direct effect of UVR on benthic invertebrates and epilithon, the rock-dwelling matrix of algae, bacteria, viruses, fungi and detritus, and second, to examine the indirect effect of UVR-mediated shifts in epilithic food quality on epilithic consumers. Food quality was assessed by measuring carbon to nutrient ratios and the concentration of polyunsaturated fatty acids (PUFA) in the epilithic matrix; the effect of its change on epilithic consumers was measured using a feeding experiment. The study was conducted in four montane lakes, where downwelling UVR can be intense. Of these lakes, the benthic community of only one was strongly affected by UVR. In this lake, exposure to UVR decreased epilithic accrual and invertebrate colonization, and, contrary to our expectations, increased food quality in the shallows through decreased carbon to phosphorus ratios and increased PUFA concentrations. In another of the four study lakes, the feeding experiment showed no significant difference in growth rates between invertebrates fed UVR-exposed and UVR-shielded epilithon, or invertebrates directly exposed to or shielded from UVR. This study demonstrates that although UVR can play an important role in structuring the trophic dynamics of benthic communities, its effects will not be constant across systems, or important in all environments.     

Spatial variation in periphyton fatty acid composition in subtropical streams

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Climate effects on fish body size–trophic position relationship depend on ecosystem type

The energetic demand of consumers increases with body size and temperature. This implies that energetic constraints may limit the trophic position of larger consumers, which is expected to be lower in tropical than in temperate regions to compensate for energy limitation. Using a global dataset of 3635 marine and freshwater ray‐finned fish species, we addressed if and how climate affects the fish body size–trophic position relationship in both freshwater and marine ecosystems, while controlling for the effects of taxonomic affiliation. We observed significant fish body size–trophic position relationships for different ecosystems. However, only in freshwater systems larger tropical fish presented a significantly lower trophic position than their temperate counterparts. Climate did not affect the fish body size–trophic position relationship in marine systems. Our results suggest that larger tropical freshwater fish may compensate for higher energetic constraints feeding at lower trophic positions, compared to their temperate counterparts of similar body size. The lower latitudinal temperature range in marine ecosystems and/or their larger ecosystem size may attenuate and/or compensate for the energy limitation of larger marine fish. Based on our results, temperature may determine macroecological patterns of aquatic food webs, but its effect is contingent on ecosystem type. We suggest that freshwater ecosystems may be more sensitive to warming‐induced alterations in food web topology and food chain length than marine ecosystems.     

Transfer efficiency of carbon,nutrients, and polyunsaturated fatty acids in planktonic food webs under different environmental conditions

The trophic transfer efficiency (TTE) is an important indicator of ecosystem functioning. However, TTE data from freshwater food webs are ambiguous due to differences in time scales and methods. We investigated the transfer of essential substances (carbon, nutrients, and polyunsaturated fatty acids) through plankton communities in 30 Polish lakes with different trophic status in the middle of summer. The results of our study revealed that different essential substances were transferred from phytoplankton to zooplankton with varying efficiencies. The average TTE of C, N, P, and the sum of ω‐3 PUFA were 6.55%, 9.82%, 15.82%, and 20.90%, respectively. Our results also show a large mismatch between the elemental and biochemical compositions of zooplankton and their food during the peak of the summer stagnation, which may further promote the accumulation of essential substances. There were also large differences in TTEs between trophic conditions, with the highest efficiencies in oligotrophic lakes and the lowest in dystrophic and eutrophic lakes. Therefore, our study indicates that disturbances like eutrophication and dystrophication similarly decrease the TTE of essential substances between phytoplankton and zooplankton in freshwater food webs.     

Timing of blooms,algal food quality and Calanus glacialis reproduction and growth in a changing Arctic

The Arctic bloom consists of two distinct categories of primary producers, ice algae growing within and on the underside of the sea ice, and phytoplankton growing in open waters. Long chain omega‐3 fatty acids, a subgroup of polyunsaturated fatty acids (PUFAs) produced exclusively by these algae, are essential to all marine organisms for successful reproduction, growth, and development. During an extensive field study in the Arctic shelf seas, we followed the seasonal biomass development of ice algae and phytoplankton and their food quality in terms of their relative PUFA content. The first PUFA‐peak occurred in late April during solid ice cover at the onset of the ice algal bloom, and the second PUFA‐peak occurred in early July just after the ice break‐up at the onset of the phytoplankton bloom. The reproduction and growth of the key Arctic grazer Calanus glacialis perfectly coincided with these two bloom events. Females of C. glacialis utilized the high‐quality ice algal bloom to fuel early maturation and reproduction, whereas the resulting offspring had access to ample high‐quality food during the phytoplankton bloom 2 months later. Reduction in sea ice thickness and coverage area will alter the current primary production regime due to earlier ice break‐up and onset of the phytoplankton bloom. A potential mismatch between the two primary production peaks of high‐quality food and the reproductive cycle of key Arctic grazers may have negative consequences for the entire lipid‐driven Arctic marine ecosystem.     

两种水华藻——球形棕囊藻和铜绿微囊藻的脂肪酸组成特征与水华形成机制

浮游植物所含的不饱和脂肪酸是测定其作为食物质量的指标,并在浮游植物向浮游动物及其它动物能量转化过程中起着关键的作用,必需不饱和脂肪酸的缺乏有利于水华的形成。球形棕囊藻(Phaeocystis globosa)和铜绿微囊藻(Microcystis aeruginosa)分别是常见的海洋和淡水水华藻类,该文分析了它们在不同生长期的脂肪酸组成,探讨了这两种藻类的脂肪酸组成特征。球形棕囊藻和铜绿微囊藻的脂肪酸碳链长为14~20个碳原子,脂肪酸种类组成都比较简单,以饱和脂肪酸为主,未检测到二十碳五烯酸(Eicosapentaenoic acid,EPA)和二十二碳六烯酸 (Docosahexaenoic acid,DHA)等动物的必需脂肪酸。球形棕囊藻的总脂肪酸含量在247.294~735.44 μg·g^-1干重之间,在对数期和延滞期含量最高的脂肪酸分别是C14:0和C16:0;而两株铜绿微囊藻的总脂肪酸在1 405.095~6 087.617μg·g^-1干重之间,以C16:0含量最高。两株铜绿微囊藻的脂肪酸含量在对数期和延滞期差异明显(p<0.05),但球形棕囊藻的脂肪酸含量在不同生长期差别不大。由于缺乏必需脂肪酸EPA和DHA,球形棕囊藻和铜绿微囊藻不能为高营养级的生物提供必需的不饱和脂肪酸,不是浮游动物等生物的良好食物。因此球形棕囊藻和铜绿微囊藻作为浮游动物的食物质量较低,浮游动物对它们的捕食压力也较小,可能是这两种藻容易暴发水华的重要原因。