Reconstructing marine plankton food web interactions using DNA metabarcoding

Knowledge of zooplankton in situ diet is critical for accurate assessment of marine ecosystem function and structure, but due to methodological constraints, there is still a limited understanding of ecological networks in marine ecosystems. Here, we used DNA‐metabarcoding to study trophic interactions, with the aim to unveil the natural diet of zooplankton species under temporal variation of food resources. Several target consumers, including copepods and cladocerans, were investigated by sequencing 16S rRNA and 18S rRNA genes to identify prokaryote and eukaryote potential prey present in their guts. During the spring phytoplankton bloom, we found a dominance of diatom and dinoflagellate trophic links to copepods. During the summer period, zooplankton including cladocerans showed a more diverse diet dominated by cyanobacteria and heterotrophic prey. Our study suggests that copepods present trophic plasticity, changing their natural diet over seasons, and adapting their feeding strategies to the available prey spectrum, with some species being more selective. We did not find a large overlap of prey consumed by copepods and cladocerans, based on prey diversity found in their guts, suggesting that they occupy different roles in the trophic web. This study represents the first molecular approach to investigate several zooplankton–prey associations under seasonal variation, and highlights how, unlike other techniques, the diversity coverage is high when using DNA, allowing the possibility to detect a wide range of trophic interactions in plankton communities.     

Consistent trophic amplification of marine biomass declines under climate change

The impact of climate change on the marine food web is highly uncertain. Nonetheless, there is growing consensus that global marine primary production will decline in response to future climate change, largely due to increased stratification reducing the supply of nutrients to the upper ocean. Evidence to date suggests a potential amplification of this response throughout the trophic food web, with more dramatic responses at higher trophic levels. Here we show that trophic amplification of marine biomass declines is a consistent feature of the Coupled Model Intercomparison Project Phase 5 (CMIP5) Earth System Models, across different scenarios of future climate change. Under the business‐as‐usual Representative Concentration Pathway 8.5 (RCP8.5) global mean phytoplankton biomass is projected to decline by 6.1% ± 2.5% over the twenty‐first century, while zooplankton biomass declines by 13.6% ± 3.0%. All models project greater relative declines in zooplankton than phytoplankton, with annual zooplankton biomass anomalies 2.24 ± 1.03 times those of phytoplankton. The low latitude oceans drive the projected trophic amplification of biomass declines, with models exhibiting variable trophic interactions in the mid‐to‐high latitudes and similar relative changes in phytoplankton and zooplankton biomass. Under the assumption that zooplankton biomass is prey limited, an analytical explanation of the trophic amplification that occurs in the low latitudes can be derived from generic plankton differential equations. Using an ocean biogeochemical model, we show that the inclusion of variable C:N:P phytoplankton stoichiometry can substantially increase the trophic amplification of biomass declines in low latitude regions. This additional trophic amplification is driven by enhanced nutrient limitation decreasing phytoplankton N and P content relative to C, hence reducing zooplankton growth efficiency. Given that most current Earth System Models assume that phytoplankton C:N:P stoichiometry is constant, such models are likely to underestimate the extent of negative trophic amplification under projected climate change.     

Size‐based interactions across trophic levels in food webs of shallow Mediterranean lakes

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Size‐based interactions and trophic transfer efficiency are modified by fish predation and cyanobacteria blooms in Lake Mývatn,Iceland

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A review of planktivorous fishes: Their evolution,feeding behaviours,selectivities, and impacts

The classical approach of limnologists has been to consider the interactions between lake ecosystem components as an unidirectional flow of influence from nutrients to the phytoplankton, to the zooplankton, and finally to the fish, through successive controls by physical, chemical, and biological processes (Strakraba, 1967). The effect of planktivorous fishes on zooplankton and phytoplankton communities was not recognized until the studies of Hrbáek et al. (1961), Hrbáek (1962), Brooks & Dodson (1965) and Strakraba (1965). They showed that (1) in ponds and lakes in the presence of planktivorous fishes the zooplankton communities were composed of smaller bodied species than in those lacking planktivores, and (2) the resulting small-bodied zooplankton communities affected the phytoplankton communities. Although the variability of the phytoplankton response to fish predation showed the importance of other factors (such as nutrient limitation and interspecific competition of algae), these studies emphasized that zooplankton and phytoplankton communities can be affected by the feeding selectivity of planktivorous fishes. During the last two decades, many limnological studies have focused on this dramatic impact of fish on plankton communities. The direct response of zooplankton communities to visual fish predation (i.e. particulate feeding) has been of major interest, whereas the multilevel effects of filter-feeding fish (predation on zooplankton plus grazing on phytoplankton) have been neglected. The objectives of this review are to document fish-plankton interrelationships in order to (1) provide insights into the impact of fish on plankton communities, and (2) outline mechanistic models of planktivory according to the feeding repertory and the selectivity of the fish, the adaptive responses of the plankton, and the environmental conditions.The approach adopted here is based on field and laboratory experimental results derived from the literature on tropical and temperate freshwater (occasionally marine) systems. Four types of planktivorous fish are distinguished: the gape-limited larvae and small fish species, the particulate feeders, the pump filter feeders, and the tow-net filter feeders. For each type of planktivore, the mechanisms of prey selection are analyzed from the point of view of both the predator and the prey. To investigate the main determinants of the predator feeding selectivity, and to discuss its potential effects on prey communities, the predation-act is divided into a sequence of successive events (Holling, 1966): detection, pursuit, capture, retention, and digestion for particulate feeders; and capture, retention, and digestion for filter feeders. The strengths and weaknesses of various measures of selectivity (i.e. electivity indices), as well as their appropriate usages are considered. Available prey selection models and optimal foraging theories are analyzed for the different planktivore feeding modes. Mechanistic models based on Holling's (loc. cit.) approach are proposed for each feeding mode to determine differential prey vulnerabilities and optimal diet breadth.This review has application to several fields, including general ecology, limnology, fisheries management (for example, utilization of planktonic resources, stocking, introduction, or maintenance of natural fish populations), and biological control of the eutrophication processes (biomanipulation approaches). It emphasizes the real need for more knowledge of the feeding selectivity and food utilization of planktivores. It concludes that predator and prey are mutually adapted. Thus, in most cases, study of plankton dynamics and water quality should include the assessment of fish predation and grazing pressures.     

Poor nutritional quality of primary producers and zooplankton driven by eutrophication is mitigated at upper trophic levels

Eutrophication and rising water temperature in freshwaters may increase the total production of a lake while simultaneously reducing the nutritional quality of food web components. We evaluated how cyanobacteria blooms, driven by agricultural eutrophication (in eutrophic Lake Köyliöjärvi) or global warming (in mesotrophic Lake Pyhäjärvi), influence the biomass and structure of phytoplankton, zooplankton, and fish communities. In terms of the nutritional value of food web components, we evaluated changes in the ω‐3 and ω‐6 polyunsaturated fatty acids (PUFA) of phytoplankton and consumers at different trophic levels. Meanwhile, the lakes did not differ in their biomasses of phytoplankton, zooplankton, and fish communities, lake trophic status greatly influenced the community structures. The eutrophic lake, with agricultural eutrophication, had cyanobacteria bloom throughout the summer months whereas cyanobacteria were abundant only occasionally in the mesotrophic lake, mainly in early summer. Phytoplankton community differences at genus level resulted in higher arachidonic acid, eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) content of seston in the mesotrophic than in the eutrophic lake. This was also reflected in the EPA and DHA content of herbivorous zooplankton (Daphnia and Bosmina) despite more efficient trophic retention of these biomolecules in a eutrophic lake than in the mesotrophic lake zooplankton. Planktivorous juvenile fish (perch and roach) in a eutrophic lake overcame the lower availability of DHA in their prey by more efficient trophic retention and biosynthesis from the precursors. However, the most efficient trophic retention of DHA was found with benthivorous perch which prey contained only a low amount of DHA. Long‐term cyanobacterial blooming decreased the nutritional quality of piscivorous perch; however, the difference was much less than previously anticipated. Our result shows that long‐term cyanobacteria blooming impacts the structure of plankton and fish communities and lowers the nutritional quality of seston and zooplankton, which, however, is mitigated at upper trophic levels.     

An approach for the assessment of risk from chronic radiation to populations of phytoplankton and zooplankton

A conceptual model of the effects of chronic radiation on a population of phytoplankton and zooplankton in an oceanic nutrient layer is presented. The model shows that there are distinct threshold dose rates at which the different plankton populations become unsustainable. These are 10,400 μGy h⁻¹ for phytoplankton and 125 μGy h⁻¹ for zooplankton. Both these values are considerably greater than the current screening values for protection of 10 μGy h⁻¹. The model highlights the effects of predator–prey dynamics in predicting that when the zooplankton is affected by the radiation dose, the phytoplankton population can increase. In addition, the model was altered to replicate the dose rates to the plankton of a previous ERICA Irish Sea assessment (24 μGy h⁻¹ for zooplankton and 430 μGy h⁻¹ to phytoplankton). The results showed only a 10% decrease in the zooplankton population and a 15% increase in the phytoplankton population. Therefore, at this level of dose, the model predicts that although the dose rate exceeds the guideline value, populations are not significantly affected. This result highlights the limitations of a single screening value for different groups of organisms.     

Can export of organic matter from estuaries support zooplankton in nearshore,marine plumes?

Marine and terrestrial ecosystems are connected via transfers of nutrients and organic matter in river discharges. In coastal seas, such freshwater outflows create prominent turbidity plumes. These plumes are areas of high biological activity in the pelagos, of which zooplankton is a key element. Conceptually, the increased biomass of zooplankton consumers in plumes can be supported by two alternative trophic pathways—consumption of fresh marine phytoplankton production stimulated by riverine nutrients, or direct trophic subsidies through the uptake of terrestrial and estuarine organic matter flushed to sea. The relative importance of these two pathways has not been established previously. Isotopic tracing (carbon and nitrogen) was used to measure the extent of incorporation of marine versus terrestrial matter into mesozooplankton consumers in the plumes off a small estuary in eastern Australia. Replicate zooplankton samples were taken during baseflow conditions with minimal freshwater influence to the sea, and during pulsed discharge events that generated turbidity plumes in coastal waters. Food sources utilized by zooplankton differed among locations and with the strength of freshwater flow. Terrestrial and estuarine carbon only made a sizeable contribution (47%) to the carbon demands of zooplankton in the lower estuary during pulsed freshwater flows. By contrast, in plumes that developed in nearshore marine waters, phytoplankton supplied up to 90% of the dietary carbon of zooplankton feeding in the plumes. Overall, it was “fresh” carbon, fixed by marine phytoplankton, the growth of which became stimulated by fluvial nutrient exports, that dominated energy flows in plume regions. The trophic role of terrestrial and estuarine organic exports was comparatively minor. The trophic dynamics of plankton in small coastal plumes is closely linked to variations in freshwater flow, but this coupling operates mainly through the enhancement of in-situ phytoplankton production rather than cross-boundary transfers of organic matter to marine food webs in the pelagos.     

Body size variation in aquatic consumers causes pervasive community effects,independent of mean body size

Intraspecific phenotypic variation is a significant component of biodiversity. Body size, for example, is variable and critical for structuring communities. We need to understand how homogenous and variably sized populations differ in their ecological responses or effects if we are to have a robust understanding of communities. We manipulated body size variation in consumer (tadpole) populations in mesocosms (both with and without predators), keeping mean size and density of these consumers constant. Size‐variable consumer populations exhibited stronger antipredator responses (reduced activity), which had a cascading effect of increasing the biomass of the consumer's resources. Predators foraged less when consumers were variable in size, and this may have mediated the differential effects of predators on the community composition of alternative prey (zooplankton). All trophic levels responded to differences in consumer size variation, demonstrating that intrapopulation phenotypic variability can significantly alter interspecific ecological interactions. Furthermore, we identify a key mechanism (size thresholds for predation risk) that may mediate impacts of size variation in natural communities. Together, our results suggest that phenotypic variability plays a significant role in structuring ecological communities.     

Coupled predator–prey oscillations in a chaotic food web

Coupling of several predator–prey oscillations can generate intriguing patterns of synchronization and chaos. Theory predicts that prey species will fluctuate in phase if predator–prey cycles are coupled through generalist predators, whereas they will fluctuate in anti-phase if predator–prey cycles are coupled through competition between prey species. Here, we investigate predator–prey oscillations in a long-term experiment with a marine plankton community. Wavelet analysis of the species fluctuations reveals two predator–prey cycles that fluctuate largely in anti-phase. The phase angles point at strong competition between the phytoplankton species, but relatively little prey overlap among the zooplankton species. This food web architecture is consistent with the size structure of the plankton community, and generates highly dynamic food webs. Continued alternations in species dominance enable coexistence of the prey species through a non-equilibrium 'killing-the-winner' mechanism, as the system shifts back and forth between the two predator–prey cycles in a chaotic fashion.     

Rising temperature and marine plankton community dynamics: Is warming bad?

Global warming is a major threat to the natural environment worldwide with potential adverse impact on plankton community. This will ultimately lead to a change in the dynamics of aquatic food webs. In this study we used seasonally forced multi-species version of the classic Rosenzweig–MacArthur predator–prey model to understand the role and stochastic influence of increasing temperature on marine plankton. First, stable coexistence of four phytoplankton and three zooplankton species was created in a system and then the level of temperature changed to achieve our research goal. We found that the stable coexistence of phytoplankton and zooplankton was related to periodic shifts in species biomass, variation in inter-specific competition and niche configuration. Warming significantly reduced total plankton biomass and changed turnover time of a species, with gradual warming breaking the stable coexistence of phytoplankton and zooplankton. In addition, we found that warming make specialist species more vulnerable than generalist species. After adding noise, a significant variation was observed in plankton biomass and amplification of noise was higher for phytoplankton compared to zooplankton. These results suggest that stochastic or unpredictable nature of temperature fluctuations may create a window of opportunity for the emergence of new species. Overall, warming would induce a shift in plankton dynamics and thereby exert pressure on plankton dependent communities such as fish in the long run.     

The biogeography of marine plankton traits

Changes in marine plankton communities driven by environmental variability impact the marine food web and global biogeochemical cycles of carbon and other elements. To predict and assess these community shifts and their consequences, ecologists are increasingly investigating how the functional traits of plankton determine their relative fitness along environmental and biological gradients. Laboratory, field and modelling studies are adopting this trait‐based approach to map the biogeography of plankton traits that underlies variations in plankton communities. Here, we review progress towards understanding the regulatory roles of several key plankton functional traits, including cell size, N₂‐fixation and mixotrophy among phytoplankton, and body size, ontogeny and feeding behaviour for zooplankton. The trait biogeographical approach sheds light on what structures plankton communities in the current ocean, as well as under climate change scenarios, and also allows for finer resolution of community function because community trait composition determines the rates of significant processes, including carbon export. Although understanding of trait biogeography is growing, uncertainties remain that stem, in part, from the paucity of observations describing plankton functional traits. Thus, in addition to recommending widespread adoption of the trait‐based approach, we advocate for enhanced collection, standardisation and dissemination of plankton functional trait data.     

Predicted warming and browning affect timing and magnitude of plankton phenological events in lakes: a mesocosm study

1. Aquatic ecosystems in Northern Europe are expected to face increases in temperature and water colour (TB) in future. While effects of these factors have been studied separately, it is unknown whether and how a combination of them might affect phenological events and trophic interactions. 2. In a mesocosm study, we combined both factors to create conditions expected to arise during the coming century. We focused on quantifying effects on timing and magnitude of plankton spring phenological events and identifying possible mismatches between resources (phytoplankton) and consumers (zooplankton). 3. We found that the increases in TB had important effects on timing and abundance of different plankton groups. While increased temperature led to an earlier peak in phytoplankton and zooplankton and a change in the relative timing of different zooplankton groups, increased water colour reduced chlorophyll‐a concentrations. 4. Increased TB together benefitted cladocerans and calanoid copepods and led to stronger top‐down control of algae by zooplankton. There was no sign of a mismatch between primary producers and grazers as reported from other studies. 5. Our results point towards an earlier onset of plankton spring growth in shallow lakes in future with a stronger top‐down control of phytoplankton by zooplankton grazers.     

DNA metabarcoding reveals that 200‐μm‐size‐fractionated filtering is unable to discriminate between planktonic microbial and large eukaryotes

Microeukaryotic plankton (0.2–200 μm) are critical components of aquatic ecosystems and key players in global ecological processes. High‐throughput sequencing is currently revolutionizing their study on an unprecedented scale. However, it is currently unclear whether we can accurately, effectively and quantitatively depict the microeukaryotic plankton communities using traditional size‐fractionated filtering combined with molecular methods. To address this, we analysed the eukaryotic plankton communities both with, and without, prefiltering with a 200 μm pore‐size sieve –by using SSU rDNA‐based high‐throughput sequencing on 16 samples with three replicates in each sample from two subtropical reservoirs sampled from January to October in 2013. We found that ~25% reads were classified as metazoan in both size groups. The species richness, alpha and beta diversity of plankton community and relative abundance of reads in 99.2% eukaryotic OTUs showed no significant changes after prefiltering with a 200 μm pore‐size sieve. We further found that both >0.2 μm and 0.2–200 μm eukaryotic plankton communities, especially the abundant plankton subcommunities, exhibited very similar, and synchronous, spatiotemporal patterns and processes associated with almost identical environmental drivers. The lack of an effect on community structure from prefiltering suggests that environmental DNA from larger metazoa is introduced into the smaller size class. Therefore, size‐fractionated filtering with 200 μm is insufficient to discriminate between the eukaryotic plankton size groups in metabarcoding approaches. Our results also highlight the importance of sequencing depth, and strict quality filtering of reads, when designing studies to characterize microeukaryotic plankton communities.     

Long‐term zooplankton responses to nutrient and consumer subsidies arising from migratory sockeye salmon (Oncorhynchus nerka)

Migratory animals, such as Pacific salmon, can significantly shape communities in recipient habitats both by altering the flux of resources, and changing community composition and subsequent trophic interactions. Here we mainly used paleoecological records from natural sockeye salmon nursery lakes to quantify the response of plankton communities to the influx of salmon‐derived nutrients and consumers (juvenile salmon). Our long‐term data show that increases in the density of spawning salmon often elevated influx of nutrients, and, in turn, zooplankton production over the past few centuries. In contrast, significant correlations were not detected in two lakes with extremely low or high average spawner densities (i.e. 1.5 and 34.7 × 10³ spawners km^?2 year^?1 respectively). With increasing spawner densities across lakes, analysis of the size structure of subfossils in sediments revealed a strong decrease in body size of a main juvenile salmon prey item (Eubosmina longispina; r²= 0.36, p < 0.001, n = 67), consistent with an overriding effect of predation in lakes with high salmon densities. These long‐term data not only highlight the key role of salmon‐derived nutrients in stimulating plankton communities, but also suggest that the relative effect of nutrient and consumer subsidies varies along gradients of lake production, despite a single ultimate causal mechanism (migrating fish).     

Prey size diversity hinders biomass trophic transfer and predator size diversity promotes it in planktonic communities

Body size exerts multiple effects on plankton food-web interactions. However, the influence of size structure on trophic transfer remains poorly quantified in the field. Here, we examine how the size diversity of prey (nano-microplankton) and predators (mesozooplankton) influence trophic transfer efficiency (using biomass ratio as a proxy) in natural marine ecosystems. Our results support previous studies on single trophic levels: transfer efficiency decreases with increasing prey size diversity and is enhanced with greater predator size diversity. We further show that communities with low nano-microplankton size diversity and high mesozooplankton size diversity tend to occur in warmer environments with low nutrient concentrations, thus promoting trophic transfer to higher trophic levels in those conditions. Moreover, we reveal an interactive effect of predator and prey size diversities: the positive effect of predator size diversity becomes influential when prey size diversity is high. Mechanistically, the negative effect of prey size diversity on trophic transfer may be explained by unicellular size-based metabolic constraints as well as trade-offs between growth and predation avoidance with size, whereas increasing predator size diversity may enhance diet niche partitioning and thus promote trophic transfer. These findings provide insights into size-based theories of ecosystem functioning, with implications for ecosystem predictive models.     

Austral Summer Bloom of Loricate Choanoflagellates in the Central Ross Sea Polynya

A bloom of loricate choanoflagellates was recorded for the first time in the Ross Sea polynya during the austral summer 2017. Both individual cells and uncommon large‐size colonies (200 μm length) represent the 42–55% of the total plankton community (i.e. specimens from 5 to 150 μm length). Choanoflagellates serve as a link between low and mid trophic levels since they prey on bacteria and in turn are ingested by zooplankton. This twofold role and the unusual abundance recorded in the Antarctic ecosystem may have relevant but still unknown effects on food web structure and dynamics in that area.     

Environmental constraint of intraguild predation: Inorganic turbidity modulates omnivory in fairy shrimps

1. Omnivory is widespread in food webs, with an important stabilising effect. The strength of omnivorous trophic interactions may change considerably with changes in the local environment.
2. Shallow temporary waters are often characterised by high levels of inorganic turbidity that may directly limit the food uptake of filter-feeding organisms, but there is little evidence on how it might affect omnivorous species. Anostracans are key species of temporary waters and recent evidence suggests that these organisms are omnivorous consumers of both phyto- and zooplankton.
3. Using Branchinecta orientalis as a model species, our aim was to test how turbidity affects the feeding of an omnivorous anostracan. To do this, we used short-term feeding experiments and stable isotope analyses, with animals collected from soda pans in eastern Austria. In the feeding experiments, algae and zooplankton were offered as food either separately or in combination. The prey type treatments were crossed with turbidity levels in a factorial design.
4. There was a pronounced decrease in the ingested algal biomass with increasing turbidity. Conversely, ingestion rates on zooplankton were less affected by turbidity. Stable isotope analyses from field material supported our experimental results by showing a positive relationship of the trophic position of anostracans and the trophic niche of the communities with turbidity.
5. Our results show that turbidity modulates the intraguild trophic relationship between anostracans and their prey by shifting the diet of anostracans from more herbivorous in transparent to more carnivorous in turbid waters. Thus, inorganic turbidity might also have a community-shaping role in plankton communities of temporary waters through altering trophic relationships.

     

Effects of sea surface warming on marine plankton

Ocean warming has been implicated in the observed decline of oceanic phytoplankton biomass. Some studies suggest a physical pathway of warming via stratification and nutrient flux, and others a biological effect on plankton metabolic rates; yet the relative strength and possible interaction of these mechanisms remains unknown. Here, we implement projections from a global circulation model in a mesocosm experiment to examine both mechanisms in a multi‐trophic plankton community. Warming treatments had positive direct effects on phytoplankton biomass, but these were overcompensated by the negative effects of decreased nutrient flux. Zooplankton switched from phytoplankton to grazing on ciliates. These results contrast with previous experiments under nutrient‐replete conditions, where warming indirectly reduced phytoplankton biomass via increased zooplankton grazing. We conclude that the effect of ocean warming on marine plankton depends on the nutrient regime, and provide a mechanistic basis for understanding global change in marine ecosystems.     

Top-down and bottom-up community regulation in marine rocky intertidal habitats

Strong top-down control by consumers has been demonstrated in rocky intertidal communities around the world. In contrast, the role of bottom-up effects (nutrients and productivity), known to have important influences in terrestrial and particularly freshwater ecosystems, is poorly known in marine hard-bottom communities. Recent studies in South Africa, New England, Oregon and New Zealand suggest that bottom-up processes can have important effects on rocky intertidal community structure. A significant aspect of all of these studies was the incorporation of processes varying on larger spatial scales than previously considered (10’s to 1000’s of km). In all four regions, variation in oceanographic factors (currents, upwelling, nutrients, rates of particle flux) was associated with different magnitudes of algal and/or phytoplankton abundance, availability of particulate food, and rates of recruitment. These processes led to differences in prey abundance and growth, secondary production, consumer growth, and consumer impact on prey resources. Oceanographic conditions therefore may vary on scales that generate ecologically significant variability in populations at the bottom of the food chain, and through upward-flowing food chain effects, lead to variation in top-down trophic effects. I conclude that top-down and bottom-up processes can be important joint determinants of community structure in rocky intertidal habitats, and predict that such effects will occur generally wherever oceanographic ‘discontinuities’ lie adjacent to rocky coastlines. I further argue that increased attention by researchers and of funding agencies to such benthic–pelagic coupling would dramatically enhance our understanding of the dynamics of marine ecosystems.