Fatty acid composition of consumers in boreal lakes – variation across species,space and time

1. Fatty acids (FAs) have been widely applied as trophic biomarkers in aquatic food web studies. However, current knowledge of inter‐ and intraspecific variation in consumer FA compositions across spatial and temporal scales is constrained to a few pelagic taxa. 2. We analysed the FAs of 22 taxa of benthic macroinvertebrates, zooplankton and fish collected from the littoral, pelagic and profundal habitats of nine boreal oligotrophic lakes over spring, summer and autumn. We quantified and compared the FA variance partitions contributed by species identity (i.e. an integrative effect of phylogenetic origin, life history and functional feeding guild of individual taxa), site and season using partial redundancy analysis both on all consumers and on benthic arthropods alone. 3. Species identity alone contributed 84.4 and 72.8% of explained FA variation of all consumers and benthic arthropods, respectively. Influences of site, season and all joint effects accounted for 0–11.3% only. Fatty acid profiles of primary consumers differentiated below class level, but those of predators were distinguishable only when they became more taxonomically distinct (i.e. among classes or higher). 4. Pelagic and profundal consumers showed stronger reliance on autochthonous resources than did their littoral counterparts as reflected by their higher ω3 to ω6 FA ratios. Polyunsaturated FAs (PUFAs) were increasingly retained with trophic levels, and saturated FAs (e.g. FA 16 : 0) gradually reduced. Ecologically, this trade‐off enhances the trophic transfer efficiency and confirms the importance of PUFA‐rich autotrophs in aquatic food webs. 5. Our findings indicate strong interspecific differences in FA requirements and assimilation among aquatic consumers from a wide range of taxonomic levels, habitats and lakes. Consumers were able to maintain homoeostasis in FA compositions across spatial and temporal changes in resource FAs, but consumer homoeostasis did not limit the effectiveness of FAs as trophic biomarkers.     

Lake responses to long‐term disturbances and management practices

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Variable Production by Different Pelagic Energy Mobilizers in Boreal Lakes

We studied production by three key pelagic energy mobilizer communities, phytoplankton (PP), heterotrophic bacteria (HB), and methanotrophic bacteria (MOB), in five boreal lakes of varying size and concentration of dissolved organic carbon (DOC). Production by PP was responsible for most (>55%) of the total pelagic energy mobilization in all five lakes. Production by HB and PP estimated for the whole water column during the ice-free period were positively correlated, but with the exception of the clearest and most eutrophic lake PP apparently could not support the total carbon demand of bacteria. However, the DOC concentration did not explain the variability of heterotrophic bacterial production (HBP) within or between the lakes. Thus, our results provide circumstantial evidence for the “priming effect” whereby labile organic matter from autochthonous production enhances decomposition of allochthonous DOC. However, HBP was only 10–23% of the total pelagic energy mobilization in the lakes, suggesting that only a minor fraction of allochthonous DOC became available for higher trophic levels. High MOB activity was detected in the water columns of the stratified lakes when the molar ratio of CH₄:O₂ varied between 0.5 and 12. In the small stratified lakes (area < 0.01 km²), MOB production contributed 13–52% of the total pelagic energy mobilization, being greatest during the autumn mixing period. Our results indicate that in small stratified lakes (area < 0.01 km²) bacteria, especially MOB, are potentially quantitatively important supplementary food resources for zooplankton. However, in larger lakes primary producers are the most important (>70%) potential food source for zooplankton.     

Depth gradients in food‐web processes linking habitats in large lakes: Lake Superior as an exemplar ecosystem

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Benthic carbon is inefficiently transferred in the food webs of two eutrophic shallow lakes

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Biogenic methane in freshwater food webs

1. It has long been known that substantial amounts of methane are produced in anoxic lake sediments, and the components of the methane cycle in lakes have been well described. At oxic–anoxic interfaces, methane‐oxidising bacteria (MOB) convert methane to microbial biomass and can be highly productive. However, only recently has methane been recognised as a potentially important carbon and energy source for lake food webs, and some instances have also been reported of methane contribution to river food webs. Stable isotope analysis (SIA) has provided compelling evidence in this respect and has been supplemented by other lines of evidence. 2. In the benthic food webs of lakes, profundal chironomid larvae appear to be the main conduits for trophic transfer of biogenic methane via grazing on MOB. The mode of feeding of these larvae and the microhabitats they generate both promote larval ability to exploit MOB production. Support to chironomid larvae from methane is rather widespread, but its degree is highly variable; estimates suggest that in some lakes methane‐carbon might contribute more than 60% of chironomid carbon biomass. 3. Evidence of crustacean zooplankton in lakes deriving part of their carbon from methane is currently more limited. Reports from some lakes have indicated Daphnia with a substantial (>50%) contribution of methane‐carbon in their biomass. However, for this to happen, an oxic–anoxic interface where sufficient MOB production can occur needs to be within the range of vertical migrations by zooplankton, which may only rarely be the case. Hence, a significant methane subsidy of pelagic food webs in lakes is probably much less widespread than for benthic food webs. 4. There is also recent and currently very limited evidence that some stream benthos derives biomass carbon (reported values up to 30%) from methane. This can occur in stagnant backwater pools where conditions can be analogous to those in lake sediments. However, groundwater aquifers can also supply water supersaturated with methane to some rivers, providing a basis for a microbially‐mediated transfer of methane‐carbon to river benthos. 5. Evidence for significant transfer of methane‐derived carbon to higher trophic levels is still very limited. Within some lakes, those fish species that feed extensively on chironomid larvae can derive a substantial part (perhaps up to 20%) of their carbon biomass from methane. It is also likely that methane‐carbon produced in lakes or rivers is exported to riparian ecosystems when emerging chironomids or other insects are eaten by invertebrate or avian predators. 6. We argue that conceptual models of freshwater food webs, and especially those for lakes, need to be modified to enable incorporation of biogenic methane as a carbon and energy source. For some types of lakes, carbon and energy budgets certainly need to take account of the production and utilisation of biogenic methane, and the accumulating evidence indicates that this is a more widespread phenomenon that has generally been acknowledged hitherto.     

Discrete foraging niches promote ecological, phenotypic, and genetic divergence in sympatric whitefish (Coregonus lavaretus)

Natural populations often vary in their degree of ecological, morphological and genetic divergence. This variation can be arranged along an ecological speciation continuum of increasingly discrete variation, with high inter-individual variation at one end and well defined species in the other. In postglacial fishes, evolutionary divergence has commonly resulted in the co-occurrence of a pelagic and a benthic specialist. We studied three replicate lakes supporting sympatric pelagic and benthic European whitefish (Coregonus lavaretus (L.)) morphs in search for early signs of possible further divergence into more specialized niches. Using stomach content data (recent diet) and stable isotope analyses (time-integrated measure of trophic niche use), we observed a split in the trophic niche within the benthic whitefish morph, with individuals specializing on either littoral or profundal resources. This divergence in resource use was accompanied by small but significant differences in an adaptive morphological trait (gill raker number) and significant genetic differences between fish exploiting littoral and profundal habitats and foraging resources. The same pattern of parallel divergence was found in all three lakes, suggesting similar natural selection pressures driving and/or maintaining the divergence. The two levels of divergence (a clear and robust benthic – pelagic and a more subtle littoral – profundal divergence) observed in this study apparently represent different stages in the process of ecological speciation.     

Does the introduced signal crayfish occupy an equivalent trophic niche to the lost native noble crayfish in boreal lakes?

The introduced North-American signal crayfish (Pacifastacus leniusculus) has become widespread throughout Europe where it has often replaced the native noble crayfish (Astacus astacus). The impact of this replacement on ecosystem processes in boreal lakes is still largely unknown. We compared the trophic niches of these two crayfish species in 16 small to medium sized boreal lakes in southern Finland; eight lakes with noble crayfish and eight lakes where the native crayfish populations had been lost and replaced by signal crayfish. We analysed carbon and nitrogen stable isotopes from samples of the crayfish and their putative food sources, and used stable isotope models to compare trophic niche widths of the two species of crayfish and to quantify the food sources used by them. At species level the signal crayfish exhibited a substantially larger trophic niche than that of the noble crayfish, but within-lake populations of the species did not differ in their niche widths. The isotopic niches of the two species strongly overlapped, and while the estimated proportions of food resources (profundal and littoral macroinvertebrates, terrestrial leaf detritus and macrophytes) used by crayfish varied considerably among individual populations, they did not differ consistently between the species. Our results suggest that, contrary to often expressed concerns, replacement of lost noble crayfish populations by the signal crayfish may not greatly alter the littoral food web structure in boreal lakes.     

Effects of Multi-chain Omnivory on the Strength of Trophic Control in Lakes

Omnivory has been implicated in both diffusing and intensifying the effects of consumer control in food chains. Some have postulated that the strong, community level, top-down control apparent in lakes is not expressed in terrestrial systems because terrestrial food webs are reticulate, with high degrees of omnivory and diverse plant communities. In contrast, lake food webs are depicted as simple linear chains based on phytoplankton-derived energy. Here, we explore the dynamic implications of recent evidence showing that attached algal (periphyton) carbon contributes substantially to lake primary and secondary productivity, including fish production. Periphyton production represents a cryptic energy source in oligotrophic and mesotrophic lakes that is overlooked by previous theoretical treatment of trophic control in lakes. Literature data demonstrate that many fish are multi-chain omnivores, exploiting food chains based on both littoral and pelagic primary producers. Using consumer-resource models, we examine how multiple food chains affect fourth-level trophic control across nutrient gradients in lakes. The models predict that the stabilizing effects of linked food chains are strongest in lakes where both phytoplankton and periphyton contribute substantially to production of higher trophic levels. This stabilization enables a strong and persistent top down control on the pelagic food chain in mesotrophic lakes. The extension of classical trophic cascade theory to incorporate more complex food web structures driven by multi-chain predators provides a conceptual framework for analysis of reticulate food webs in ecosystems.     

Influences of fish on food web structure and function in mountain lakes

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Primary production under hypertrophic conditions and its relationship with bacterial production

In shallow hypertrophic lakes where light availability restricts the growth of macrophytes and benthic phytoplankton, pelagic phytoplankton modulates importantly ecosystem production and the energy transfer to heterotrophic bacteria. Diel and seasonal variations in primary production (PP) were studied in the hypertrophic Albufera de Valencia (Spain). Additionally, the relationship between PP and heterotrophic bacterial production (BP) was assessed. PP was extremely high, exceeding most values reported for hypertrophic lakes to date. PP displayed marked diurnal variations defined by the solar radiation curve. Likewise, PP changed importantly across seasons. Minimum PP coincided with maximum water transparency and short water residence times in winter, whereas maximum PP was observed in late spring associated with high chlorophyll a. The spring PP maximum contrasted with the summer maximum often observed in hypertrophic lakes. When compared to spring PP values, summer PP values were lower as a result of strong nitrogen limitation. In contrast to PP, BP remained fairly constant across seasons. Nonetheless, there was a joint diminution during increased water transparency followed by an increase in early spring. Phytoplankton was always the most relevant input to particulate carbon production, but the BP/PP ratio showed clear seasonal variations. The BP/PP ratio was minimum in spring, low in summer and highest in winter. The extracellular dissolved organic carbon released by phytoplankton was sufficient to meet bacterial carbon demand in all experimental dates, suggesting that allochthonous carbon sources play a minor role in sustaining BP, though they cannot be excluded. However, we hypothesize that high availability of dissolved organic carbon might explain the lack of coupling observed between BP and PP.     

Ecological speciation in postglacial European whitefish: rapid adaptive radiations into the littoral,pelagic, and profundal lake habitats

Understanding how a monophyletic lineage of a species diverges into several adaptive forms has received increased attention in recent years, but the underlying mechanisms in this process are still under debate. Postglacial fishes are excellent model organisms for exploring this process, especially the initial stages of ecological speciation, as postglacial lakes represent replicated discrete environments with variation in available niches. Here, we combine data of niche utilization, trophic morphology, and 17 microsatellite loci to investigate the diversification process of three sympatric European whitefish morphs from three northern Fennoscandian lakes. The morphological divergence in the gill raker number among the whitefish morphs was related to the utilization of different trophic niches and was associated with reproductive isolation within and across lakes. The intralacustrine comparison of whitefish morphs showed that these systems represent two levels of adaptive divergence: (1) a consistent littoral–pelagic resource axis; and (2) a more variable littoral–profundal resource axis. The results also indicate that the profundal whitefish morph has diverged repeatedly from the ancestral littoral whitefish morph in sympatry in two different watercourses. In contrast, all the analyses performed revealed clustering of the pelagic whitefish morphs across lakes suggesting parallel postglacial immigration with the littoral whitefish morph into each lake. Finally, the analyses strongly suggested that the trophic adaptive trait, number of gill rakers, was under diversifying selection in the different whitefish morphs. Together, the results support a complex evolutionary scenario where ecological speciation acts, but where both allopatric (colonization history) and sympatric (within watercourse divergence) processes are involved.     

Eulittoral macroinvertebrate communities of lowland lakes: discrimination among trophic states

1. Nutrient inputs from urban and agricultural land use often result in shifts in species composition of pelagic and profundal invertebrate communities. Here, we test if nutrient enrichment affects the composition of eulittoral macroinvertebrate communities, and, if so, if macroinvertebrate communities of five different habitat types reflect differences in trophic state. 2. Macroinvertebrate community composition of 36 lakes was significantly correlated with total phosphorus (TP) concentration, the proportion of coarse woody debris (CWD) and root habitats and the proportion of grassland. 3. However, macroinvertebrate communities of five major habitat types from eight lakes were more dissimilar among habitats than among trophic states. Community composition of reed and stone habitats was significantly correlated with wind exposure but not TP concentration, while macroinvertebrate composition of sand habitats was related to TP concentration and coarse sediments. In CWD and root habitats, both TP concentration and a predominance of invasive species covaried, which made it difficult to relate the observed compositional differences to either trophic state or to the effects of competition between native and invasive species. 4. Trophic state influenced the composition of eulittoral macroinvertebrate communities but to a lesser extent than has been previously reported for profundal habitats. Moreover, the effects of trophic state were nested within habitat type and were partially superseded by biotic interactions and small‐scaled habitat complexity. Although eulittoral macroinvertebrate communities were not strong indicators of the trophic state of lowland lakes, they may be used to assess other anthropogenic impacts on lakeshores.     

Lake size and fish diversity determine resource use and trophic position of a top predator in high‐latitude lakes

Prey preference of top predators and energy flow across habitat boundaries are of fundamental importance for structure and function of aquatic and terrestrial ecosystems, as they may have strong effects on production, species diversity, and food‐web stability. In lakes, littoral and pelagic food‐web compartments are typically coupled and controlled by generalist fish top predators. However, the extent and determinants of such coupling remains a topical area of ecological research and is largely unknown in oligotrophic high‐latitude lakes. We analyzed food‐web structure and resource use by a generalist top predator, the Arctic charr Salvelinus alpinus (L.), in 17 oligotrophic subarctic lakes covering a marked gradient in size (0.5–1084 km²) and fish species richness (2–13 species). We expected top predators to shift from littoral to pelagic energy sources with increasing lake size, as the availability of pelagic prey resources and the competition for littoral prey are both likely to be higher in large lakes with multispecies fish communities. We also expected top predators to occupy a higher trophic position in lakes with greater fish species richness due to potential substitution of intermediate consumers (prey fish) and increased piscivory by top predators. Based on stable carbon and nitrogen isotope analyses, the mean reliance of Arctic charr on littoral energy sources showed a significant negative relationship with lake surface area, whereas the mean trophic position of Arctic charr, reflecting the lake food‐chain length, increased with fish species richness. These results were supported by stomach contents data demonstrating a shift of Arctic charr from an invertebrate‐dominated diet to piscivory on pelagic fish. Our study highlights that, because they determine the main energy source (littoral vs. pelagic) and the trophic position of generalist top predators, ecosystem size and fish diversity are particularly important factors influencing function and structure of food webs in high‐latitude lakes.     

Effects of temperature, salinity and fish in structuring the macroinvertebrate community in shallow lakes: implications for effects of climate change

Climate warming may lead to changes in the trophic structure and diversity of shallow lakes as a combined effect of increased temperature and salinity and likely increased strength of trophic interactions. We investigated the potential effects of temperature, salinity and fish on the plant-associated macroinvertebrate community by introducing artificial plants in eight comparable shallow brackish lakes located in two climatic regions of contrasting temperature: cold-temperate and Mediterranean. In both regions, lakes covered a salinity gradient from freshwater to oligohaline waters. We undertook day and night-time sampling of macroinvertebrates associated with the artificial plants and fish and free-swimming macroinvertebrate predators within artificial plants and in pelagic areas. Our results showed marked differences in the trophic structure between cold and warm shallow lakes. Plant-associated macroinvertebrates and free-swimming macroinvertebrate predators were more abundant and the communities richer in species in the cold compared to the warm climate, most probably as a result of differences in fish predation pressure. Submerged plants in warm brackish lakes did not seem to counteract the effect of fish predation on macroinvertebrates to the same extent as in temperate freshwater lakes, since small fish were abundant and tended to aggregate within the macrophytes. The richness and abundance of most plant-associated macroinvertebrate taxa decreased with salinity. Despite the lower densities of plant-associated macroinvertebrates in the Mediterranean lakes, periphyton biomass was lower than in cold temperate systems, a fact that was mainly attributed to grazing and disturbance by fish. Our results suggest that, if the current process of warming entails higher chances of shallow lakes becoming warmer and more saline, climatic change may result in a decrease in macroinvertebrate species richness and abundance in shallow lakes.     

The role of meiobenthos in lake ecosystems

It is shown that meiobenthos plays an important role in the secondary production by zoobenthos in lakes, as well as in the degradation of organic matter. In large lakes (Lake Ladoga, Lake Onega, Lake Päijänne, Lake Constance), the ratio of meiobenthic production to the production of macrobenthos is on average 50–61%. In the small Latgalian lakes (Latvia), this proportion is different: in the profundal of these lakes it varies from 92.5% in a naturally clean mesotrophic lake to 0.0004% in the most eutrophic lake, and in the littoral of lakes – from 578–1476% in mesotrophic lakes to 148–306% in eutrophic ones. The level of production of littoral meiobenthos does not depend on the trophic status of the lake, and can be equally high both in undisturbed mesotrophic lakes and in strongly eutrophicated lakes. The intensity of production of the littoral meiobenthos in oligotrophic and mesotrophic lakes, on the one hand, and in eutrophic lakes on the other, are not reliably distinguished. There is a clear tendency for a decrease of the role of profundal meiobenthos with regard to the transformation of energy flows in lake ecosystems, both with an increase in eutrophication and with an increase in the amount of organic matter in the benthal available from phytoplankton.     

Microbial and classical food webs: A visit to a hypertrophic lake

Abstract: Plankton community structure and fluxes of carbon for bacteria (production and bacterivory) were investigated in the urban, hypertrophic Lake Rodó (Uruguay) using a short time interval for sampling (5–15 d) during one year. The lake sustains a high phytoplankton biomass (up to 335 μg l⁻¹ chlorophyll a ) always dominated by the filamentous cyanobacteria Planktothrix agardhii . The zooplankton community was numerically dominated by rotifers and ciliates; cladocerans were rare during most of the year. The rotifer abundance was very high (up to 10⁵ individual l⁻¹), the bacterivorous Anuraeopsis fissa being the most abundant species. Predation rates of heterotrophic nanoflagellates (HNF) on bacteria (range: 31–130 bacteria HNF⁻¹ h⁻¹) were higher than those reported in the literature for field studies. A carbon budget showed that HNF can consume on average 91 and 76% of the bacterial carbon production in summer and winter, respectively. Bacterial turnover times are the lowest reported until now from field conditions (5 to 42 h). Consequently, bacterial carbon production was extremely high (72 to 1071 μg C l⁻¹ d⁻¹). Bacterial production was positively correlated to bacterial abundance but the relationship was significantly improved by the inclusion of temperature (82% variability explained). My results support the general trend for increased bacterial production with increasing trophic status, and suggest a lower energy transfer efficiency to higher trophic levels in hypertrophic lakes due to the many trophic interactions involved.     

Extracellular dissolved organic carbon released from phytoplankton as a source of carbon for heterotrophic bacteria in lakes of different humic content

The quantitative importance of photosynthetically produced dissolved organic carbon (PDOC) released from phytoplankton as a source of carbon for pelagic, heterotrophic bacteria was investigated in four temperate Swedish lakes, of which two had low (≈20 mg Pt 1⁻¹), and two moderately high (60–80 mg Pt 1⁻¹) humic content. The bacterial assimilation of PDOC was estimated with the ¹⁴C method, and the total production of the heterotrophic bacteria was estimated with the [3H]thymidine incorporation method. The release of PDOC from natural communities of phytoplankton was not restricted to periods of photosynthesis, but often continued during periods of darkness. Heterotrophic bacteria often assimilated the labile components of the PDOC at high rates (up to 73% of the released PDOC was assimilated during the incubation in our experiments). The contribution of PDOC to bacterial production exhibited large within-lake seasonal variations, but PDOC was at certain times, both in humic and non-humic lakes, a quantitatively very important carbon source for the heterotrophic bacteria. Under periods of comparatively low primary production, heterotrophic bacteria in humic lakes appear to utilize allochthonous, humic substances as a substrate.     

Benthos as the basis for arctic lake food webs

Plankton have traditionally been viewed as the basis for limnetic food webs, with zooplankton acting as a gateway for energy passing between phytoplanktonic primary producers and fish. Often, benthic production has been considered to be important primarily in shallow systems or as a subsidy to planktonic food web pathways. Stable isotope food web analyses of two arctic lakes (NE14 and I minus) in the Toolik Lake region of Alaska indicate that benthos are the primary source of carbon for adults of all species of benthic and pelagic fish present. We found no effect of turbidity, which may suppress benthic algae by shading, on food web structure. Even though Secchi transparency varied from 10.2 m in NE14 to 0.55–2.6 m in I minus, food webs in both lakes were based upon benthos, had four trophic levels, and culminated with omnivorous lake trout. We suggest that the importance of benthos in the food webs of these lakes is due to their extreme oligotrophy, resulting in planktonic resources that are insufficient for the support of planktivorous consumers.     

Relating planktonic microbial food web structure in lentic freshwater ecosystems to water quality and land use

Relationships among picoplankton, protozoa, phytoplankton, plantnutrients, lake type, drainage basin morphology and land coverwere studied in 45 water bodies in South Island, New Zealandthat ranged from large, deep, ultra-oligotrophic lakes to shallow,macrophyte-dominated ponds and swamps. The biomasses of mostheterotrophic components of the pelagic microbial food webswere positively related to phytoplankton and features of thedrainage basin that enhanced nutrient input, and imply strongresource-driven structuring of pelagic microbial food webs.Prokaryotic picophytoplankton biomass was negatively relatedto indices of eutrophication, and the picoautotroph contributionto total microbial food web biomass declined with increasingtotal phosphorus concentration from 16.5% in deep lakes to <0.02%in swamps and ponds. Biomass ratios of (picoplankton plus protozoa):phytoplanktonranged from 40:60 in swamps and ponds to >70:30 in deep lakes,and indicate the potential importance of microbial food websin carbon transfer to higher trophic levels in deep, less productivelakes. Strong relationships exist between land use in the catchmentand pelagic microbial food web structure and biomass acrossa wide range in size and trophic state of water bodies in heterogeneouslandscapes.