Copepoda – Cladocera – Tunicata: The role of three major mesozooplankton groups in pelagic food webs

Copepods, cladocerans and tunicates form major groups of herbivorous mesozooplankton. The former two are found in fresh and marine waters, while the latter are restricted to marine systems. In the present review, we compile existing ecophysiological knowledge about between-group differences in metabolic and reproductive rates, feeding selectivity and elemental composition. From this, we derive predictions about their impact on the lower trophic levels (phytoplankton and microbial food web) and predictions about their prevalence under different ecological conditions (e.g. nutrient richness, Si : N ratio, phytoplankton size structure and top-down control).     

Retention versus export food chains: processes controlling sinking loss from marine pelagic systems

The role of export and retention food chains forpelagic-benthic coupling is considered by evaluatingdifferent food chain scenarios and processes such asaggregation, grazing and zooplankton-mediated fluxes.The consequences of grazing of primary production bydifferent zooplankton for the vertical export ofparticulate organic matter from the euphotic zone arediscussed. Reference is made to existing data andalgorithms regarding primary production and verticalexport of carbon from the euphotic zone, both onannual and daily time scales. Examples regarding therole of nutrient addition, removal of pelagiccarnivores and zooplankton grazing for vertical fluxare presented. It is speculated how variable grazingimpact of micro- and mesozooplankton, as well asherbivorous, omnivorous and carnivorous feedingstrategies of mesozooplankton could compete withaggregation during phytoplankton blooms and influenceexport fluxes. It is concluded that the transport ofparticulate organic matter to depth not only dependson bottom-up regulation as determined by physicalforcing, but also on the structure and function of theprevailing planktonic food web. Scenarios arepresented which indicate that top-down regulationplays a pivotal role for the regulation of verticalflux. This conclusion may have crucial consequencesfor future biogeochemical programmes investigatingpelagic-benthic coupling in the ocean. The endeavoursof many research programmes are dominated by lines ofthought where straightforward biogeochemistry andbottom-up regulation is the focus. Phyto- andzooplankton as well as process-oriented researchactivities have to be the focal point of futureresearch if the current comprehension of export fromand retention in the upper layers is going to makedistinct progress. This revised version was published online in July 2006 with corrections to the Cover Date.     

Copepods act as a switch between alternative trophic cascades in marine pelagic food webs

A recent meta‐analysis indicates that trophic cascades (indirect effects of predators on plants via herbivores) are weak in marine plankton in striking contrast to freshwater plankton ( Shurin et al. 2002 , Ecol. Lett., 5, 785–791). Here we show that in a marine plankton community consisting of jellyfish, calanoid copepods and algae, jellyfish predation consistently reduced copepods but produced two distinct, opposite responses of algal biomass. Calanoid copepods act as a switch between alternative trophic cascades along food chains of different length and with counteracting effects on algal biomass. Copepods reduced large algae but simultaneously promoted small algae by feeding on ciliates. The net effect of jellyfish on total algal biomass was positive when large algae were initially abundant in the phytoplankton, negative when small algae were dominant, but zero when experiments were analysed in combination. In contrast to marine systems, major pathways of energy flow in Daphnia‐dominated freshwater systems are of similar chain length. Thus, differences in the length of alternative, parallel food chains may explain the apparent discrepancy in trophic cascade strength between freshwater and marine planktonic systems.     

Trophic cascades and trophic trickles in pelagic food webs

Prey-dependent models, with the predation rate (per predator) a function of prey numbers alone, predict the existence of a trophic cascade. In a trophic cascade, the addition of a top predator to a two-level food chain to make a three-level food chain will lead to increases in the population size of the primary producers, and the addition of nutrients to three-level chains will lead to increases in the population numbers at only the first and third trophic levels. In contrast, ratio-dependent models, with the predation rate (per predator) dependent on the ratio of predator numbers to prey, predict that additions of top predators will not increase the population sizes of the primary producers, and that the addition of nutrients to a three-level food chain will lead to increases in population numbers at all trophic levels. Surprisingly, recent meta-analyses show that freshwater pelagic food web patterns match neither prey-dependent models (in pelagic webs, ''prey'' are phytoplankton, and ''predators'' are zooplankton), nor ratio-dependent models. In this paper we use a modification of the prey-dependent model, incorporating strong interference within the zooplankton trophic level, that does yield patterns matching those found in nature. This zooplankton interference model corresponds to a more reticulate food web than in the linear, prey-dependent model, which lacks zooplankton interference. We thus reconcile data with a new model, and make the testable prediction that the strength of trophic cascades will depend on the degree of heterogeneity in the zooplankton level of the food chain.     

Mixotrophy and the toxicity of Ochromonas in pelagic food webs

1. Toxic compounds produced by many phytoplankton taxa are known to have negative effects on competitors (allelopathy), anti‐predatory effects on grazers (mortality or impaired reproduction) or both. Although mixotrophs of the genus Ochromonas are known to be toxic to zooplankton, it has often been assumed in studies of plankton community processes that all flagellates in the size range of this taxon are edible to typical zooplankton grazers (i.e. cells ≤30 μm for Daphnia, ≤6 μm for rotifers). 2. We explored the toxicity of a species of Ochromonas to other planktonic taxa, including its competitors (two species of phytoplankton and protists) and consumers (two species of zooplankton). To test if mode of nutrition by this mixotroph influences its toxicity to other taxa, we exposed each test species to Ochromonas cultured in chemostats under four different nutritional regimes: osmotrophy (labile dissolved organic carbon) and phagotrophy (bacterial prey) in both light and dark conditions (i.e. with or without photosynthesis). 3. Filtrate from osmotrophically fed Ochromonas had a significant negative effect on the population growth rate of two obligate phototrophic phytoplankton, Cryptomonasozolini and Chlamydomonas reinhardtii. The protists Tetrahymena tetrahymena and Paramecium aurelia were also negatively affected by Ochromonas filtrate. Ochromonas cells were toxic to both the rotifer Brachionus calicyflorus and the cladoceran Daphnia pulicaria, with the toxic effects significantly more severe when fed at high cell densities (75 000 cells mL⁻¹) than at low densities (7500 cells mL⁻¹). Ochromonas cultured osmotrophically in the light was more toxic to the Daphnia than cells cultured under other conditions. In contrast, Ochromonas from all nutritional conditions was equally highly toxic to Brachionus. 4. Our findings support the view that Ochromonas can be toxic to other components of the food web with which it interacts. It is especially toxic to zooplankton that directly consume it, although the effect depends upon Ochromonas cell density and whether or not a good food source is simultaneously present. Our results call into question the common practice of pooling flagellates into a single ‘functional group’ included in an ‘edible phytoplankton’ category of cells <30 μm in diameter.     

Energetics of microbial food webs

The energetic demand of microorganisms in natural waters and the flux of energy between microorganisms and metazoans has been evaluated by empirical measurements in nature, in microcosms and mesocosms, and by simulation models. Microorganisms in temperate and tropical waters often use half or more of the energy fixed by photosynthesis. Most simulations and some experimental results suggest significant energy transfer to metazoans, but empirical evidence is mixed. Considerations of the range of growth yields of microorganisms and the number of trophic transfers among them indicate major energy losses within microbial food webs. Our ability to verify and quantify these processes is limited by the variability of assimilation efficiency and uncertainty about the structure of microbial food webs. However, even a two-step microbial chain is a major energy sink. As an energetic link to metazoans, the detritus food web is inefficient, and its significance may have been overstated. There is not enough bacterial biomass associated with detritus to support metazoan detritivores. Much detritus is digestible by metazoans directly. Thus, metazoans and bacteria may to a considerable degree compete for a common resource. Microorganisms, together with metazoans, are important to the stability of planktonic communities through their roles as rapid mineralizers of organic matter, releasing inorganic nutrients. The competition for organic matter and the resultant rapid mineralization help maintain stable populations of phytoplankton in the absence of advective nutrient supply. At temperatures near O °C, bacterial metabolism is suppressed more than is the rate of photosynthesis. As a result, the products of the spring phytoplankton bloom in high-temperate latitudes are not utilized rapidly by bacteria. At temperatures below 0°C microbial food webs are neither energy sinks or links: they are suppressed. Because the underlying mechanism of low-temperature inhibition is not known, we cannot yet generalize about this as a control of food web processes. Microorganisms may operate on several trophic levels simultaneously. Therefore, the realism of the trophic level concept and the reality of the use of ecological efficiency calculations in ecosystem models is questionable.     

Omnivory does not prevent trophic cascades in pelagic food webs

1. Strong trophic cascades have been well documented in pelagic food webs of temperate lakes. In contrast, the limited available evidence suggests that strong cascades are less typical in tropical lakes.
2. To measure the effects of omnivorous tilapia on planktonic communities and water transparency of a small man-made tropical lake, we performed a 5-week in situ enclosure experiment with five densities of fish randomly allocated to 20 enclosures. Zooplankton and Phytoplankton biomasses as well as water transparency were measured weekly.
3. Results show that omnivorous tilapia significantly decreased the abundance of large Cladocerans, increased the abundance of small algae (greatest axial linear dimension <50  μ m) and decreased water transparency as predicted by trophic cascade theory.
4. Therefore, omnivory was not a sufficient factor to prevent a trophic cascade in this pelagic community, although the cascade effect was weaker than reported from many north temperate, nutrient-rich lakes.     

Benthic suspension feeders: their paramount role in littoral marine food webs

In recent years, particular attention has been paid to coupling and energy transfer between benthos and plankton. Because of their abundance, certain benthic suspension feeders have been shown to have a major impact in marine ecosystems. They capture large quantities of particles and might directly regulate primary production and indirectly regulate secondary production in littoral food chains. Suspension feeders develop dense, three-dimensional communities whose structural complexity depends on flow speed. It has been postulated that these communities can self-organize to enhance food capture and thus establish boundary systems capable of successfully exploiting a less structured system, namely, the plankton.     

Macroalgal palatability and the flux of ciguatera toxins through marine food webs

The benthic dinoflagellate Gambierdiscus toxicus produces polyether toxins that cause ciguatera fish poisoning in humans. The toxins initially enter food webs when fish forage on macroalgae, or other substrates, hosting this epiphytic dinoflagellate. Population studies of G. toxicus and risk assessments in ciguatera-prone regions often rely on quantifying dinoflagellates on macroalgae. Underlying these studies is the assumption that the algae sampled represent a readily consumable resource equally available for benthic grazers. However, many algal hosts of G. toxicus possess a variety of defenses against grazing, and host–dinoflagellate associations may act as toxin sources or sinks depending on their palatability. Marine macroalgae may tolerate or avoid herbivory by exhibiting fast growth, by having poor nutritional quality, by utilizing spatial or temporal escapes or by using chemical or structural defenses. Thus, rapidly consumed algae that cope with herbivores by growing fast, such as many filamentous turfs, could be responsible for a high toxin flux even at low dinoflagellate densities. In contrast, ubiquitous unpalatable algae with much higher dinoflagellate densities might contribute little to toxin flux, and effectively act as refuges for G. toxicus. To date, G. toxicus has been reported from 56 algal genera, two cyanobacteria, one diatom, and one seagrass; 63% of these contain species that are defended from fish grazing and other grazers via chemical, morphological or structural defenses, by low nutritional quality, or by a combination of defensive strategies. High dinoflagellate densities on unpalatable macroalgae could indicate passive accumulation of cells on undisturbed hosts, rather than population explosions or active toxin sources for food webs. Understanding the flow of ciguatoxins in nature requires consideration of the ecology of both G. toxicus and its algal hosts. The complexity of marine algal–herbivore interactions also has consequences for other benthic dinoflagellates that produce toxins, which accumulate in consumers.     

Decoupling of pelagic and littoral food webs in oligotrophic Canadian Shield lakes

The importance of top-down effects of piscivorous fish on phytoplankton in natural oligotrophic lakes is still debated. In this study, we analyzed patterns in phytoplankton and zooplankton abundance in 37 oligotrophic Canadian Shield lakes in relation to variations in both piscivorous fish predation and resources (total phosphorus; TP). Zooplankton community structure (but not total biomass) was partially affected by the variation in fish predation while the phytoplankton community structure and total biomass showed no response. Carbon isotope analyses revealed that the lack of top-down effects is due to the uncoupling of the littoral and the pelagic food webs. We found that the fish community depends mostly on benthic resources, suggesting that only low planktivory occurred in our study lakes. Due to the absence of specialized zooplanktivorous fish, zooplankton is poorly exploited in these lakes and thus able to control phytoplankton by grazing. A comparison of our data with published studies on the TP–chlorophyll a relationships in both natural and manipulated systems shows that the phytoplankton biomass per unit of TP is relatively low in Canadian Shield lakes.     

On the different nature of top-down and bottom-up effects in pelagic food webs

SUMMARY 1. Each individual planktonic plant or animal is exposed to the hazards of starvation and risk of predation, and each planktonic population is under the control of resource limitation from the bottom up (growth and reproduction) and by predation from the top down (mortality). While the bottom-up and top-down impacts are traditionally conceived as compatible with each other, field population-density data on two coexisting Daphnia species suggest that the nature of the two impacts is different. Rates of change, such as the rate of individual body growth, rate of reproduction, and each species' population growth rate, are controlled from the bottom up. State variables, such as biomass, individual body size and population density, are controlled from the top down and are fixed at a specific level regardless of the rate at which they are produced.
2. According to the theory of functional responses, carnivorous and herbivorous predators react to prey density rather than to the rate at which prey are produced or reproduced. The predator's feeding rate (and thus the magnitude of its effect on prey density) should hence be regarded as a functional response to increasing resource concentration.
3. The disparity between the bottom-up and top-down effects is also apparent in individual decision making, where a choice must be made between accepting the hazards of hunger and the risks of predation (lost calories versus loss of life).
4. As long as top-down forces are effective, the disparity with bottom-up effects seems evident. In the absence of predation, however, all efforts of an individual become subordinate to the competition for resources. Biomass becomes limited from the bottom up as soon as the density of a superior competitor has increased to the carrying capacity of a given habitat. Such a shift in the importance of bottom-up control can be seen in zooplankton in habitats from which fish have been excluded.     

Bacterivory and herbivory: Key roles of phagotrophic protists in pelagic food webs

Research on microbial loop organisms, heterotrophic bacteria and phagotrophic protists, has been stimulated in large measure by Pomeroy's seminal paper published in BioScience in 1974. We now know that a significant fate of bacterioplankton production is grazing by < 20-µm-sized flagellates. By selectively grazing larger, more rapidly growing and dividing cells in the bacterioplankton assemblage, bacterivores may be directly cropping bacterial production rather than simply the standing stock of bacterial cells. Protistan herbivory, however, is likely to be a more significant pathway of carbon flow in pelagic food webs than is bacterivory. Herbivores include both < 20-µm flagellates as well as > 20-µm ciliates and heterotrophic dinoflagellates in the microzooplankton. Protists can grow as fast as, or faster than their phytoplankton prey. Phototrophic cells grazed by protists range from bacterial-sized prochlorophytes to large diatom chains (which are preyed upon by extracellularly-feeding dinoflagellates). Recent estimates of microzooplankton herbivory in various parts of the sea suggest that protists routinely consume from 25 to 100% of daily phytoplankton production, even in diatom-dominated upwelling blooms. Phagotrophic protists should be viewed as a dominant biotic control of both bacteria and of phytoplankton in the sea.     

Rescaling the trophic structure of marine food webs

Measures of trophic position (TP) are critical for understanding food web interactions and human‐mediated ecosystem disturbance. Nitrogen stable isotopes (δ¹⁵N) provide a powerful tool to estimate TP but are limited by a pragmatic assumption that isotope discrimination is constant (change in δ¹⁵N between predator and prey, Δ¹⁵N = 3.4‰), resulting in an additive framework that omits known Δ¹⁵N variation. Through meta‐analysis, we determine narrowing discrimination from an empirical linear relationship between experimental Δ¹⁵N and δ¹⁵N values of prey consumed. The resulting scaled Δ¹⁵N framework estimated reliable TPs of zooplanktivores to tertiary piscivores congruent with known feeding relationships that radically alters the conventional structure of marine food webs. Apex predator TP estimates were markedly higher than currently assumed by whole‐ecosystem models, indicating perceived food webs have been truncated and species‐interactions over simplified. The scaled Δ¹⁵N framework will greatly improve the accuracy of trophic estimates widely used in ecosystem‐based management.     

Food quantity and quality regulation of trophic transfer between primary producers and a keystone grazer (Daphnia) in pelagic freshwater food webs

The transfer of energy and nutrients from plants to animals is a key process in all ecosystems. In lakes, inefficient transfer of primary producer derived energy can result in low animal growth rates, accumulation of nuisance phytoplankton blooms and dissipation of energy from the ecosystem. Most research on carbon transfer efficiency in pelagic food webs has focused on either food quantity or food quality, with the latter considered separately as either elemental stoichiometry or biochemical composition. The natural occurrence and magnitude of these types of growth limitations and their combined effects on Daphnia , a keystone grazer in pelagic freshwater ecosystems, are largely unknown. Our empirical models predict that the strength and nature of food quantity and quality limitation varies greatly with lake trophic state (total phosphorus, TP) and that Daphnia growth rates and thus energy and nutrient transfer efficiency are highest in lakes with intermediate trophic status (TP 10–25 μg l⁻¹). We predict that food availability place the greatest constraint on Daphnia growth in nutrient poor lakes (TP≤4 μg l⁻¹). Phosphorus limitation of Daphnia growth increased with decreasing TP, but the overall effect was never predicted to be the dominant constraining factor. Eicosapentaenoic acid (EPA, 20:5ω3) limitation was predicted to occur in both nutrient poor and nutrient rich lakes and placed the primary constraint on food quality in the most productive lakes. Two contrasting EPA-models gave different results on the magnitude of EPA-limitation, implying that additional food quality factors decrease Daphnia growth at high TP. In conclusion, the model predicts that Daphnia growth should peak in mesotrophic lakes, food quantity will place the greatest constraint on growth in oligotrophic lakes and EPA will primarily limit growth in eutrophic lakes.     

Nitrogen subsidies to pelagic food webs through profundal methane-oxidising bacteria in oligotrophic fresh water

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Climate change undermines the global functioning of marine food webs

Sea water temperature affects all biological and ecological processes that ultimately impact ecosystem functioning. In this study, we examine the influence of temperature on global biomass transfers from marine secondary production to fish stocks. By combining fisheries catches in all coastal ocean areas and life‐history traits of exploited marine species, we provide global estimates of two trophic transfer parameters which determine biomass flows in coastal marine food web: the trophic transfer efficiency (TTE) and the biomass residence time (BRT) in the food web. We find that biomass transfers in tropical ecosystems are less efficient and faster than in areas with cooler waters. In contrast, biomass transfers through the food web became faster and more efficient between 1950 and 2010. Using simulated changes in sea water temperature from three Earth system models, we project that the mean TTE in coastal waters would decrease from 7.7% to 7.2% between 2010 and 2100 under the ‘no effective mitigation’ representative concentration pathway (RCP8.5), while BRT between trophic levels 2 and 4 is projected to decrease from 2.7 to 2.3 years on average. Beyond the global trends, we show that the TTEs and BRTs may vary substantially among ecosystem types and that the polar ecosystems may be the most impacted ecosystems. The detected and projected changes in mean TTE and BRT will undermine food web functioning. Our study provides quantitative understanding of temperature effects on trophodynamic of marine ecosystems under climate change.     

A role for brain size and cognition in food webs

Predators tend to be large and mobile, enabling them to forage in spatially distinct food web compartments (e.g. littoral and pelagic aquatic macrohabitats). This feature can stabilise ecosystems when predators are capable of rapid behavioural response to changing resource conditions in distinct habitat compartments. However, what provides this ability to respond behaviourally has not been quantified. We hypothesised that predators require increased cognitive abilities to occupy their position in a food web, which puts pressure to increase brain size. Consistent with food web theory, we found that fish relative brain size increased with increased ability to forage across macrohabitats and increased relative trophic positions in a lacustrine food web, indicating that larger brains may afford the cognitive capacity to exploit various habitats flexibly, thus contributing to the stability of whole food webs.     

Carrion cycling in food webs: comparisons among terrestrial and marine ecosystems

In light of current global changes to ecosystem function (e.g. climate change, trophic downgrading, and invasive species), there has been a recent surge of interest in exploring differences in nutrient cycling among ecosystem types. In particular, a growing awareness has emerged concerning the importance of scavenging in food web dynamics, although no studies have focused specifically on exploring differences in carrion consumption between aquatic and terrestrial ecosystems. In this forum we synthesize the scavenging literature to elucidate differences in scavenging dynamics between terrestrial and marine ecosystems, and identify areas where future research is needed to more clearly understand the role of carrion consumption in maintaining ecosystem function within each of these environments. Although scavenging plays a similar functional role in terrestrial and aquatic food webs, here we suggest that several fundamental differences exist in scavenging dynamics among these ecosystem types due to the unique selection pressures imposed by the physical properties of water and air. In particular, the movement of carcasses in marine ecosystems (e.g. wave action, upwelling, and sinking) diffuses biological activity associated with scavenging and decomposition across large, three‐dimensional spatial scales, creating a unique spatial disconnect between the processes of production, scavenging, and decomposition, which in contrast are tightly linked in terrestrial ecosystems. Moreover, the limited role of bacteria and temporal stability of environmental conditions on the sea floor appears to have facilitated the evolution of a much more diverse community of macrofauna that relies on carrion for a higher portion of its nutrient consumption than is present in terrestrial ecosystems. Our observations are further discussed as they pertain to the potential impacts of climate change and trophic downgrading (i.e. removal of apex consumers from ecosystems) on scavenging dynamics within marine and terrestrial ecosystems.     

Weighting and indirect effects identify keystone species in food webs

Species extinctions are accelerating globally, yet the mechanisms that maintain local biodiversity remain poorly understood. The extinction of species that feed on or are fed on by many others (i.e. ‘hubs’) has traditionally been thought to cause the greatest threat of further biodiversity loss. Very little attention has been paid to the strength of those feeding links (i.e. link weight) and the prevalence of indirect interactions. Here, we used a dynamical model based on empirical energy budget data to assess changes in ecosystem stability after simulating the loss of species according to various extinction scenarios. Link weight and/or indirect effects had stronger effects on food‐web stability than the simple removal of ‘hubs’, demonstrating that both quantitative fluxes and species dissipating their effects across many links should be of great concern in biodiversity conservation, and the potential for ‘hubs’ to act as keystone species may have been exaggerated to date.     

Simple models combining competition,defence and resource availability have broad implications in pelagic microbial food webs

In food webs, interactions between competition and defence control the partitioning of limiting resources. As a result, simple models of these interactions contain links between biogeochemistry, diversity, food web structure and ecosystem function. Working at hierarchical levels, these mechanisms also produce self‐similarity and therefore suggest how complexity can be generated from repeated application of simple underlying principles. Reviewing theoretical and experimental literature relevant to the marine photic zone, we argue that there is a wide spectrum of phenomena, including single cell activity of prokaryotes, microbial biodiversity at different levels of resolution, ecosystem functioning, regional biogeochemical features and evolution at different timescales; that all can be understood as variations over a common principle, summarised in what has been termed the ‘Killing‐the‐Winner’ (KtW) motif. Considering food webs as assemblages of such motifs may thus allow for a more integrated approach to aquatic microbial ecology.