A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods

1. Analyses of zooplankton fatty acid (FA) composition in laboratory experiments and samples collected from lakes in New Zealand spanning a wide gradient of productivity were used to assess the extent to which FAs might infer their diet. We used the cladocerans, Daphnia and Ceriodaphnia, and the calanoid copepod, Boeckella, as test organisms, and monocultures of cryptophytes, chlorophytes and cyanobacteria as food. Based on reproductive success, cryptophytes were the highest food quality, chlorophytes were intermediate and cyanobacteria the poorest. 2. Several FA groups were highly correlated between zooplankton and their diets. They were monounsaturated fatty acids (MUFAs), and ω3 and ω6 polyunsaturated fatty acids (PUFAs) for cladocerans, and saturated fatty acids (SAFAs) and ω3 PUFAs for copepods. Several FAs varied significantly less in the zooplankton than in their monoculture diets, e.g. MUFAs in Daphnia, and ω3 and ω6 PUFAs in Ceriodaphnia, despite clear dietary dependency for these FAs. 3. Zooplankton collected from lakes in New Zealand had more eicosapentaenoic acid (EPA) (Daphnia), more highly unsaturated ω3 and ω6 FAs (C₂₀, C₂₂; Daphnia, Ceriodaphnia, Boeckella) and less ω3 C₁₈ PUFAs (Daphnia, Ceriodaphnia, Boeckella) and ω6 C₁₈ PUFAs (Daphnia, Ceriodaphnia) than measured in the same species reared on phytoplankton in the laboratory. 4. Analyses of FA composition of seston and freshwater zooplankton globally showed that, in general, zooplankton had a significantly higher proportion of arachidonic acid and EPA than seston, and copepods also had a higher percentage of docosahexaenoic acid than seston. 5. These results suggest that zooplankton selectively incorporate the most physiologically important FAs. This could be a consequence of preferential assimilation, selective feeding on more nutritious cells or locating and feeding within higher food quality food patches.     

Particulate fatty acids in two small Siberian reservoirs dominated by different groups of phytoplankton

SUMMARY 1. We studied the composition of fatty acids (FAs) in the seston from two small freshwater reservoirs (Bugach and Lesnoi) with distinct periodicity of domination by cyanobacteria and eukaryotic algae during the growth season.
2. The diatoms in the both reservoirs were characterised by a high content of 14:0 and C16 unsaturated acids, whereas that of the essential FA 20:5ω3 [eicosapentanoic acid (EPA)] was low. The correlation between this polyunsaturated FA (PUFA) and diatom biomass was not significant in either reservoir. The percentage of 20:5ω3 in seston significantly correlated with the biomass of euglenophyta in Bugach and dinophyta in Lesnoi. Hence the diatoms, usually referred as a valuable food for zooplankton, were not an important source of the essential PUFA in these systems.
3. The dominant cyanobacteria in Bugach, and the green algae in Lesnoi, both contained the same marker acids: 18:3ω3 and 18:2ω6. Hence, a discrimination between these two phytoplanktonic groups on the basis of FA biomarkers may be difficult in some cases.
4. We found no significant correlation between the content of 20:5ω3 in seston and the biomass of the dominant daphniids in either reservoir. This is contrary to expectations, based on the literature, that EPA is generally important. Rather, the biomass of the two dominant Daphnia species in Bugach correlated strongly with the content of 18:3ω3 in the seston. The cyanobacteria were a probable source of this ω3 FA for Daphnia . We conclude that EPA is not always important for Daphnia populations although, in such cases, some other PUFA (e.g. 18:3ω3) might be related to their growth.     

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

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Seasonal correlations of elemental and ω3 PUFA composition of seston and dominant phytoplankton species in a eutrophic Siberian Reservoir

The elemental and fatty acid composition of seston was studied for 3 years, from May to October, in a small Reservoir. Under comparatively low C:P ratio, multivariate canonical analysis revealed no straightforward simple correlations between phosphorus and single ω3 PUFA species, but complex significant interaction between elemental composition (stoichiometry) of seston and total sestonic ω3 PUFA as a whole. Since sestonic C, P and N were found to originate mostly from phytoplankton, the contents of particulate elements and PUFA were attributed to single species in periods of their pronounced dominance. Phytoplankton species of genera of Stephanodiscus, Peridinium, Gomphosphaeria, Planktothrix and Anabaena in periods of their pronounced dominance had relatively constant species-specific elemental and PUFA composition. Phytoplankton species significantly differed in their elemental and PUFA composition, as well as in ratios of C:N, N:P, PUFA:P and partly C:P that indicate food quality for zooplankton. Hence, there were no phytoplankton species of clearly high or low nutritional value. All of phytoplankters, or at least detritus, that originated from them, may meet specific elemental and biochemical requirements of specific groups of zooplankton. Dividing phytoplankton on basis of their elemental and biochemical composition, i.e., nutrition quality, into large taxa (cyanobacteria, diatoms, etc.) appeared to be too coarse for assessing nutritional value for zooplankton.     

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

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The transfer of fatty acids in a freshwater planktonic foodweb of the Kuibyshevskoe reservoir (middle reaches of the Volga)

The fatty acid composition of seston (small-size fraction, < 50 m) and of Daphnia galeata, Bythotrephes longimanusand adult individuals of Leptodora kindtii was analysed in the summer of 1997. When comparing the eicosapentaenoic acid (EPA) content of seston with Daphnia, Daphnia with Bythotrephes; Daphniawith Leptodora, we found similarities in the dynamics of EPA accumulation, in most cases. The content of EPA in seston was found to be significantly correlated with numerical abundance of small diatoms (r =0.662).Maximally the % EPA increased from seston (traces – 4% of total fatty acids) to Daphnia (traces – 12.2%). Both the lower and upper relative EPA contents were higher in Bythotrephes (10.8–16%), whereas the maximum value was lower in Leptodora (0.4–6.3%) compared to Daphnia. Correlation coefficients between the EPA content of the organisms at different trophic levels were not significant. The existence of species-specific differences in accumulation and /or transformation of polyunsaturated fatty acids in freshwater crustaceans is proposed.     

Effects of iron deficiency on the growth and photosynthesis of three bloom‐forming cyanobacterial species isolated from Lake Taihu

Cyanobacterial blooms are found in many freshwater ecosystems around the world, but the effect of environmental factors on their growth and the proportion of species still require more investigation. In this study, the physiological responses of bloom‐forming cyanobacteria M icrocystis aeruginosa FACHB912, M icrocystis flos‐aquae FACHB1028 and P seudanabaena sp. FACHB1282 to iron deficiency were investigated. Their specific growth rates were found to decrease as the available iron concentration decreased. At low available iron concentrations of 1 × 10^?7 M (pFe 21.3) and 5 × 10^?8 M (pFe 21.6), M . aeruginosa had the lowest specific growth rate among three studied species. The cell sizes of M . flos‐aquae and Pseudanabaena sp. were significantly smaller under the lowest iron concentration. The chlorophyll a content of the three species decreased at the lowest iron concentration. The maximal relative electron transport rate, photosynthetic efficiency, and light‐saturation parameter of M . aeruginosa were lower than the other two cyanobacteria at pFe 21.3. Therefore, M . aeruginosa was the least able to adapt to iron deficiency. Under iron deficiency, the functional absorption cross‐section of PSII and electron transport rate on the acceptor side of PSII decreased in M . aeruginosa, while the connectivity factor between individual photosynthetic units increased in M . flos‐aquae, and the electron transport rate on the acceptor side of PSII and between PSII and PSI decreased in P seudanabaena sp. The ability to store iron was highest in M . flos‐aquae, followed by P seudanabaena sp. and M . aeruginosa. Thus, these results provide necessary information for detecting the role of iron in the succession of cyanobacterial species in Lake Taihu, the third largest freshwater lake in China, because all three species were isolated from this lake.     

The mechanism of competition between two bloom‐forming Microcystis species

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Linking biotic interactions and climate change to the success of exotic Daphnia lumholtzi

1. Warmer temperatures may increase cyanobacterial blooms in freshwater ecosystems, yet few ecological studies examine how increases in temperature and cyanobacterial blooms will alter the performance of non‐native species. We evaluated how competitive interactions and interactions between these two drivers of ecological change influence the performance of non‐native species using the native zooplankton Daphnia pulex and the non‐native zooplankton Daphnia lumholtzi as a model system. Based on the literature, we hypothesised that D. lumholtzi would perform best in warmer temperatures and in the presence of cyanobacteria. 2. Laboratory competition experiments showed that in the absence of competitors, growth rates of D. pulex (but not D. lumholtzi) were reduced at higher temperatures and with the cyanobacterial foods Anabaena flos‐aquae and Microcystis aeruginosa. In the presence of competitors, however, D. pulex emerged as the superior resource competitor at both temperatures with cyanobacterial food. We therefore predicted that, if competitive interactions are important to its establishment, D. lumholtzi would perform best in the absence of cyanobacteria in heated environments. 3. As predicted, when both species were introduced at low densities in field mesocosms, D. lumholtzi performed best at high temperatures without added cyanobacteria and worst at ambient temperatures with added cyanobacteria, indicating that competitive interactions are likely to be important for its establishment. 4. Taken together, these studies indicate that, while D. lumholtzi may benefit from increases in temperature, associated increased cyanobacterial blooms may hinder its performance. Thus, our findings underscore the importance of considering biotic interactions such as competition when predicting the future establishment of non‐native species in response to climate warming.     

Polyunsaturated fatty acids in zooplankton: variation due to taxonomy and trophic position

1. Food quality has major effects on the transfer of energy and matter in food webs, and essential long‐chained polyunsaturated fatty acids (PUFAs) can affect the quality of phytoplankton as food. In a study of oligotrophic lakes in north‐western Sweden, we investigated the fatty acid composition of four planktonic cladocerans and two calanoid copepods, representing herbivorous and carnivorous species. We also collected seston samples. 2. The proportions of long‐chain PUFAs in the organisms increased with their increasing trophic position. Thus, both their quality as food for other organisms, as well as their requirement for fatty acids (FAs), differed among taxa and depended on their trophic position. 3. We found taxon‐specific differences in the FA composition of zooplankton that were not related to sestonic FA composition. This implies that the variation in zooplankton FA composition is constrained by phylogenetic origin, life history characteristics, or both. 4. The cladoceran taxa contained 12–23% eicosapentaenoic acid (EPA) but only 0.9–2.1% docosahexaenoic acid (DHA) of the total FA content. In contrast, the calanoid copepods contained 7–11% EPA and 14–21% DHA. Thus, our results show that differences in the PUFA content among zooplankton species could have repercussions for both food web structure and function.     

Fatty acid profiles of algae mark the development and composition of harpacticoid copepods

1. The value of algal fatty acids (FA) as diet biomarkers for benthic harpacticoid copepods was investigated. A high proportion of 18:1ω9 and 18:2ω6 FA was observed in the lipid reserve fraction of copepods fed with cyanobacteria. In contrast, a high proportion of 16:1ω7 and ω3 FA (including eicosapentaenoic) was present in the lipid reserve fraction of copepods grown on diatoms. 2. Copepods that were grown on cyanobacteria showed reduced survival and took 26% more time to develop from the first copepodid stage to adult than copepods that were grown on diatoms. Copepods feeding on the cyanobacteria showed reduced FA content when compared with animals fed with diatoms. This reduction in FA content was more pronounced in the apolar lipid fraction (mainly reserve lipids) than in the polar (mainly structural) lipid fraction. 3. The FA profiles of algae were used to calculate a function discriminating between diatoms and cyanobacteria. This function was applied to the FA profiles in the reserve lipid fraction of copepods and correctly classified copepod diet. 16:1ω7, 18:2ω6 and 20:5ω3 were the most important FA in the discriminant function. The suitability of this chemometric method to infer copepod diet was further tested by using algal class FA data from literature to derive the discriminant functions. The correct classification of the diet when the functions were applied to FA composition of the copepod reserve lipids suggests that this method may be employed in trophic web studies. 18:3ω3, 18:1ω9 and 16:1ω7 were the most important FA in the functions discriminating diatoms, cyanobacteria and green algae. The identification and quantification of the whole suit of 16:1ω7, 18:1ω9, 18:2ω6, 18:3ω3 and 20:5ω3 in trophic web studies is therefore of paramount importance to infer diet origin of aquatic herbivores. 4. The FA profile of copepod polar lipids did not reflect that of the diet. The presence of long chain polyunsaturated FAs in the polar lipid fraction of copepods feeding on the cyanobacterium suggests that C18 FAs from the diet may be elongated and desaturated by the copepod. The ability to elongate and desaturated FAs may reduce the importance of some FAs as diet biomarkers while it may turn the copepods into valuable trophic intermediaries in transferring organic matter from microorganisms to higher trophic levels.     

Zooplankton community structure, micro-zooplankton grazing impact, and seston energy content in the St. Johns river system, Florida as influenced by the toxic cyanobacterium Cylindrospermopsis raciborskii

Zooplankton can influence the phytoplankton community through preferential grazing. In turn, nuisance cyanobacteria may affect zooplankton community structure by allowing certain species to out-compete others. We examined zooplankton-phytoplankton interactions, micro-zooplankton (< 200 m) grazing, and biochemical components of the seston in the St. Johns River System (SJR), Florida in the presence and absence of the toxin-producing cyanobacterium Cylindrospermopsis raciborskii. We tested whether this cyanobacterium would cause a decrease in the size structure of the zooplankton community and postulated a resultant decline in the metabolic energy and carbon available to higher consumers (i.e. fish). When numbers of C. raciborskii were low or undetectable, zooplankton were more diverse and were comprised of larger species. Rotifers were the dominant zooplankton, and their numbers relative to other zooplankton increased as C. raciborskii concentrations increased. Micro-zooplankton grazing was higher in times of C. raciborskii abundance, suggesting competitive and predatory exclusion by larger zooplankton in times of higher phytoplankton diversity. Total caloric content of the seston was higher in times of C. raciborskii abundance. However, essential fatty acids and phosphorus may be lacking in the seston, or nutrients may potentially be sequestered by the cyanobacteria and remain as organic matter in the water column. In such cases, higher trophic levels would not be able to obtain optimal energy requirements. Overall, there was a greater impact of micro-grazers on phytoplankton in the presence of C. raciborskii and apparent negative effects on the larger zooplankton species, suggesting a potential for changes in zooplankton and higher trophic level community structure.     

Seasonal variations in the diel vertical distribution of phytoplankton and zooplankton in a shallow pond

The seasonal succession of phytoplankton diversity, and the variations in the diel vertical distribution of phyto‐ and zooplankton were investigated in a small shallow pond (1.7 m water depth) in 2003. It was inferred that the water tended to stratify weakly in the daytime from February to June. In February and April, the green alga Golenkinia radiata Chodat dominated the phytoplankton assemblage. The cell density of G. radiata greatly decreased in April, when rotifers increased near the bottom. The vertical mixing was attenuated in June, large populations of the euglenoids (Lepocinclis salina Fritsch, Phacus acuminatus Stokes, Trachelomonas hispida (Perty) Stein et Deflandre) developed, and the cyanobacterium Aphanizomenon flos‐aquae var. klebahnii Elenk. appeared at low density. Euglenoids and A. flos‐aquae were mostly distributed in the bottom layer. In late September, when the water was mixed throughout the day, euglenoids and A. flos‐aquae were distributed evenly throughout the water column. The zooplankton (cyclopoid copepods and rotifers) densities in September were the lowest throughout the year. The vertical mixing increased in November, and the phytoplankton community was composed of A. flos‐aquae, P. acuminatus, T. hispida and the green alga Ankistrodesmus falcatus (Corda) Ralfs. In November, at the final stage of water bloom of A. flos‐aquae, its population density decreased with depth. The two euglenoids exhibited similar cell distributions at 0.8 m and 1.6 m during 1–3 November. A. falcatus was distributed evenly throughout the water column; however, when the vertical mixing lessened, the cells at the surface started to sink. Copepod nauplii and rotifers appeared at high densities in November. Seasonal variation in the phytoplankton community structure in the pond seemed to be related to the vertical mixing of the water. In addition, zooplankton, especially rotifers, might play an important role in initiating a spring clear‐water phase and in the bloom collapse of A. flos‐aquae.     

Elevated light and nutrients alter the nutritional quality of stream periphyton

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Food sources and lipid retention of zooplankton in subarctic ponds

1. Subarctic ponds are seasonal aquatic habitats subject to short summers but often have surprisingly numerous planktonic consumers relative to phytoplankton productivity. Because subarctic ponds have low pelagic productivity but a high biomass of benthic algae, we hypothesised that benthic mats provide a complementary and important food source for the zooplankton. To test this, we used a combination of fatty acid and stable isotope analyses to evaluate the nutritional content of benthic and pelagic food and their contributions to the diets of crustacean zooplankton in 10 Finnish subarctic ponds. 2. Benthic mats and seston differed significantly in total lipids, with seston (62.5 μg mg^?1) having approximately eight times higher total lipid concentrations than benthic mats (7.0 μg mg^?1). Moreover, the two potential food sources differed in their lipid quality, with benthic organic matter completely lacking some nutritionally important polyunsaturated fatty acids (PUFA), most notably docosahexaenoic acid and arachidonic acid. 3. Zooplankton had higher PUFA concentrations (27–67 μg mg^?1) than either of the food sources (mean benthic mats: 1.2 μg mg^?1; mean seston: 9.9 μg mg^?1), indicating that zooplankton metabolically regulate their accumulation of PUFA. In addition, when each pond was evaluated independently, the zooplankton was consistently more ¹³C‐depleted (δ¹³C ?20 to ?33‰) than seston (?23 to ?29‰) or benthic (?15 to ?27‰) food sources. In three ponds, a subset of the zooplankton (Eudiaptomus graciloides, Bosmina sp., Daphnia sp. and Branchinecta paludosa) showed evidence of feeding on both benthic and planktonic resources, whereas in most (seven out of 10) ponds the zooplankton appeared to feed primarily on plankton. 4. Our results indicate that pelagic primary production was consistently the principal food resource of most metazoans. While benthic mats were highly productive, they did not appear to be a major food source for zooplankton. The pond zooplankton, faced by strong seasonal food limitation, acquires particular dietary elements selectively.     

Diet‐switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia

Zooplankton transfer ecologically important fatty acids (FA) from their diets to upper trophic levels. We used diet‐switching experiments with ¹³C‐labeled food sources to determine the time scale at which dietary uptake is manifested in the FA profiles of Daphnia magna. Daphnia dramatically shifted their FA composition in response to diet change within only four days, however Daphnia switched from a high quality (i.e. Cryptomonas) to a moderate quality (Scenedesmus) diet retained the most physiologically important FA from their original diet source even after 14 days. In particular, Daphnia exhibited long‐term retention of eicosapentaenoic (EPA; 20:5ω3) and arachidonic acid (ARA; 20:4ω6) when switched from Cryptomonas to Scenedesmus. Similarly, when switched from Scenedesmus to Cryptomonas, Daphnia took up a high proportion of EPA and ARA after only two days. The phospholipid fatty acid (PLFA) fraction in Daphnia was preferentially enriched with stearic (18:0), oleic (18:1ω9), and linoleic acid (LIN; 18:2ω6). In contrast with studies of marine copepods, dietary FA also strongly affected the PLFA composition (structural lipids) of Daphnia. Results of δ¹³C signatures of individual FA provided evidence of elongation and desaturation of α‐linolenic (ALA; 18:3ω3) or stearidonic acid (SDA; 18:4ω3) to EPA 10 days after a diet switch to EPA‐deficient Scenedesmus. Differences in the ARA content of Daphnia fed Cryptomonas and Scenedesmus suggest Daphnia consuming Cryptomonas synthesized ARA via retroconversion of ω6‐docosapentaenoic acid (ω6‐DPA; 22:5ω6). Daphnia preferentially accumulate and retain, as well as bioconvert, those FA that are also most physiologically important for fish production. Our results also indicate Daphnia FA composition responds to their diet on a short temporal scale and analyses of lipid biomarkers in zooplankton provide strong insights into the food sources that support their production.     

Essential fatty acids and phosphorus in seston from lakes with contrasting terrestrial dissolved organic carbon content

1. It is often assumed that lakes highly influenced by terrestrial organic matter (TOM) have low zooplankton food quality because of elemental and/or biochemical deficiencies of the major particulate organic carbon pools. We used the biochemical [polyunsaturated fatty acids, especially eicosapentaenoic acid (EPA) – 20:5ω3] and elemental (C : P ratio) composition of particulate matter (PM) as qualitative measures of potential zooplankton food in two categories of lakes of similar primary productivity, but with contrasting TOM influence (clear water versus humic lakes). 2. C : P ratios (atomic ratio) in PM were similar between lake categories and were above 400. The concentration (μg L⁻¹) and relative content (μg mg C⁻¹) of EPA, as well as the particulate organic carbon concentration, were higher in the humic lakes than in the clear‐water lakes. 3. Our results show high fatty acid quality of PM in the humic lakes. The differences in the biochemical quality of the potential zooplankton food between lake categories can be attributed to the differences in their phytoplankton communities. 4. High biochemical quality of the food can result in high efficiency of energy transfer in the food chain and stimulate production at higher trophic levels, assuming that zooplankton are able to ingest and digest the resource available.     

Can tropical freshwater zooplankton graze efficiently on cyanobacteria?

Zooplankton may at times graze cyanobacteria. However, their top-down effects are considered to be low, particularly in tropical regions dominated by small-size grazers that may be unable to consume efficiently filamentous or colonial species. Recently, cyanobacteria blooms were reported in the Senegal River hydrosystem. We conducted feeding experiments to assess the ability of copepods (Pseudodiaptomus hessei and Mesocyclops ogunnus), cladocerans (Moina micrura and Ceriodaphnia cornuta), and rotifers (Brachionus angularis, B. falcatus, and Keratella sp.) to control different cyanobacteria (Cylindrospermopsis raciborskii, Anabaena solitaria, A. flos-aquae, and Microcystis aeruginosa). None of the zooplankton species ingested M. aeruginosa. Mesocyclops ogunnus did not consume any of the cyanobacteria. Both cladocerans consumed the smallest filaments of cyanobacteria, whereas all the rotifers and P. hessei consumed a broader food-size spectrum. The functional feeding responses suggest that the concentration and size of the filaments are not the sole criteria for food consumption. The high zooplankton community grazing rates, estimated by applying the clearance rates measured in the laboratory to the in situ zooplankton abundance, indicate that grazing by zooplankton potentially constitutes an important controlling factor for the filamentous cyanobacteria in the tropics.     

Oligotrophication of a large,deep lake alters food quantity and quality constraints at the primary producer–consumer interface

To assess nutritional consequences associated with lake oligotrophication for aquatic consumers, we analyzed the elemental and biochemical composition of natural seston and concomitantly conducted laboratory growth experiments in which the freshwater key herbivore Daphnia was raised on natural seston of the nowadays (2008) oligotrophic Lake Constance throughout an annual cycle. Food quality mediated constraints on Daphnia performance were assessed by comparing somatic growth rates with seston characteristics (multiple regression analysis) and by manipulating the elemental and biochemical composition of natural seston experimentally (nutrient supplementation). Results were compared to similar experiments carried out previously (1997) during a mesotrophic phase of the lake. In the oligotrophic phase, particulate carbon and phosphorus concentrations were lower, fatty acid concentrations were higher, and the taxonomic composition of phytoplankton was less diverse, with a more diatom‐ and cryptophytes‐dominated community, compared to the previous mesotrophic phase. Multiple regression analysis indicated a shift from a simultaneous limitation by food quantity (in terms of carbon) and quality (i.e. α‐linolenic acid) during the mesotrophic phase to a complex multiple nutrient limitation mediated by food quantity, phosphorus, and omega‐3 fatty acids in the following oligotrophic phase. The concomitant supplementation experiments also revealed seasonal changes in multiple resource limitations, i.e. the prevalent limitation by food quantity was accompanied by a simultaneous limitation by either phosphorus or omega‐3 fatty acids, and thus confirmed and complemented the multiple regression approach. Our results indicate that seasonal and annual changes in nutrient availabilities can create complex co‐limitation scenarios consumers have to cope with, which consequently may also affect the efficiency of energy transfer in food webs.