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No one is perfect, and organisms that perform well in some habitat or with respect to some tasks, do so at the cost of performance in others: there are inescapable trade-offs. Organismal trade-offs govern the structure and function of ecosystems and attempts to demonstrate and quantify trade-offs have therefore been an important goal for ecologists. In addition, trade-offs are a key component in trait-based ecosystem models. Here, I synthesise evidence of trade-offs in plankton organisms, from bacteria to zooplankton, and show how a slow-fast gradient in life histories emerges. I focus on trade-offs related to the main components of an organism's Darwinian fitness, that is resource acquisition, survival, and propagation. All consumers need to balance the need to eat without being eaten, and diurnal vertical migration, where zooplankton hide at depth during the day to avoid visual predators but at the cost of missed feeding opportunities in the productive surface layer, is probably the best documented result of this trade-off. However, there are many other more subtle but equally important behaviours that similarly are the result of an optimisation of these trade-offs. Most plankton groups have also developed more explicit defence mechanisms, such as toxin production or evasive behaviours that are harnessed in the presence of their predators; the costs of these have often proved difficult to quantify or even demonstrate, partly because they only materialise under natural conditions. Finally, all multicellular organisms must allocate time and resources among growth, reproduction, and maintenance (e.g. protein turnover and DNA repair), and mate finding may compromise both survival and feeding. The combined effects of all these trade-offs is the emergence of a slow-fast gradient in the pace-of-life, likely the most fundamental principle for the organisation of organismal life histories. This crystallisation of trade-offs may offer a path to further simplification of trait-based models of marine ecosystems., (© 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.)

Some dinoflagellates produce toxic secondary metabolites that correlate with increased resistance to grazers. The allocation costs of toxin production have been repeatedly addressed, but with conflicting results. Few studies have considered the potential costs of this defense to the photosystem, even though defense toxins (e.g., karlotoxins and brevetoxins) are closely linked to the photoprotective process. Here, we used chemical cues from copepods to induce paralytic shellfish toxin (PST) production in resource-limited Alexandrium minutum and quantitatively determined the growth rate and potential trade-offs with the photosystem process. The results show that grazer-induced, more toxic A. minutum had larger cell volume, lower cell division rate, and lower pigment content under nitrogen-limited conditions than control cells. In addition, predator cues led to a lower relative abundance of photoprotective xanthophylls and a reduced de-epoxidation efficiency of the xanthophyll cycle under high light conditions, reducing the ability of the cells to resist photodamage. Decreased photoprotective capacity may reflect an overlooked defense cost of toxin production., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2024 Elsevier B.V. All rights reserved.)

Coevolution between predator and prey plays a central role in shaping the pelagic realm and may have significant implications for marine ecosystems and nutrient cycling dynamics. The siliceous diatom frustule is often assumed to have coevolved with the silica-lined teeth of copepods, but empirical evidence of how this relationship drives natural selection and evolution is still lacking. Here, we show that feeding on diatoms causes significant wear and tear on copepod teeth and that this leads to copepods becoming selective feeders. Teeth from copepods feeding on thick-shelled diatoms were more likely to be broken or cracked than those feeding on a dinoflagellate. When fed a large diatom, all analyzed teeth had visible wear. Our results underscore the importance of the predator-prey arms race as a driving force in planktonic evolution and diversity., Competing Interests: Competing interests statement:The authors declare no competing interest.

The phagotrophic flagellates described as "typical excavates" have been hypothesized to be morphologically similar to the Last Eukaryotic Common Ancestor and understanding the functional ecology of excavates may therefore help shed light on the ecology of these early eukaryotes. Typical excavates are characterized by a posterior flagellum equipped with a vane that beats in a ventral groove. Here, we combined flow visualization and observations of prey capture in representatives of the three clades of excavates with computational fluid dynamic modeling, to understand the functional significance of this cell architecture. We record substantial differences amongst species in the orientation of the vane and the beat plane of the posterior flagellum. Clearance rate magnitudes estimated from flow visualization and modeling are both like that of other similarly sized flagellates. The interaction between a vaned flagellum beating in a confinement is modeled to produce a very efficient feeding current at low energy costs, irrespective of the beat plane and vane orientation and of all other morphological variations. Given this predicted uniformity of function, we suggest that the foraging systems of typical excavates studied here may be good proxies to understand those potentially used by our distant ancestors more than 1 billion years ago., Competing Interests: Competing interests statement:The authors declare no competing interest.

Phagotrophic flagellates are the main consumers of bacteria and picophytoplankton. Despite their ecological significance in the 'microbial loop', many of their predation mechanisms remain unclear. 'Typical excavates' bear a ventral groove, where prey is captured for ingestion. The consequences of feeding through a 'semi-rigid' furrow on the prey size range have not been explored. An unidentified moving element called 'the wave' that sweeps along the bottom of the groove toward the site of phagocytosis has been observed in a few species; its function is unclear. We investigated the presence, behavior, and function of the wave in four species from the three excavate clades (Discoba, Metamonada, and Malawimonadida) and found it present in all studied cases, suggesting the potential homology of this feature across all three groups. The wave displayed a species-specific behavior and was crucial for phagocytosis. The morphology of the feeding groove had an upper-prey size limit for successful prey captures, but smaller particles were not constrained. Additionally, the ingestion efficiencies were species dependent. By jointly studying these feeding traits, we speculate on adaptations to differences in food availability to better understand their ecological functions., (© 2023 International Society of Protistologists.)

Sessile barnacles feed by sweeping their basket-like cirral fan through the water, intercepting suspended prey. A primary component of the diet of adult barnacles is copepods that are sensitive to fluid disturbances and capable of escaping. How do barnacles manage to capture copepods despite the fluid disturbances they generate? We examined this question by describing the feeding current architecture of 1 cm sized Balanus crenatus using particle image velocimetry, and by studying the trajectories of captured copepods and the escapes of evading copepods. We found that barnacles produce a feeding current that arrives both from behind and the sides of the barnacle. The flow from the sides represents quiescent corridors of low fluid deformation and uninterrupted by the beating cirral fan. Potential prey arriving from behind are likely to encounter the cirral fan and, hence, capture here is highly unlikely. Accordingly, most captured copepods arrived through the quiet corridors, while most copepods arriving from behind managed to escape. Thus, it is the unique feeding flow architecture that allows feeding on evasive prey. We used the Landau-Squire jet as a simple model of the feeding current. For the Reynolds number of our experiments, the model reproduces the main features of the feeding current, including the lateral feeding corridors. Furthermore, the model suggests that smaller barnacle specimens, operating at lower Reynolds numbers, will produce a fore-aft symmetric feeding current without the lateral corridors. This suggests an ontogenetic diet shift from non-evasive prey to inclusion of evasive prey as the barnacle grows., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2024. Published by The Company of Biologists Ltd.)

Heterotrophic nanoflagellates are the main consumers of bacteria and picophytoplankton in the ocean and thus play a key role in ocean biogeochemistry. They are found in all major branches of the eukaryotic tree of life but are united by all being equipped with one or a few flagella that they use to generate a feeding current. These microbial predators are faced with the challenges that viscosity at this small scale impedes predator-prey contact and that their foraging activity disturbs the ambient water and thus attracts their own flow-sensing predators. Here, I describe some of the diverse adaptations of the flagellum to produce sufficient force to overcome viscosity and of the flagellar arrangement to minimize fluid disturbances, and thus of the various solutions to optimize the foraging-predation risk trade-off. I demonstrate how insights into this trade-off can be used to develop robust trait-based models of microbial food webs.

Larvaceans are gelatinous zooplankton abundant throughout the ocean. Larvaceans have been overlooked in research because they are difficult to collect and are perceived as being unimportant in biogeochemical cycles and food-webs. We synthesise evidence that their unique biology enables larvaceans to transfer more carbon to higher trophic levels and deeper into the ocean than is commonly appreciated. Larvaceans could become even more important in the Anthropocene because they eat small phytoplankton that are predicted to become more prevalent under climate change, thus moderating projected future declines in ocean productivity and fisheries. We identify critical knowledge gaps and argue that larvaceans should be incorporated into ecosystem assessments and biogeochemical models to improve predictions of the future ocean., Competing Interests: Declaration of interests No interests are declared., (Copyright © 2023 The Authors. Published by Elsevier Ltd.. All rights reserved.)

We show how to construct and apply a setup to acoustically tether and enable behavioral observations of individual microorganisms using simple laboratory equipment and a standard light microscope. We explore the capability of the setup with the freely swimming dinoflagellate Alexandrium minutum as the study organism. The setup allows us to tether cells in focus in the mid-plane of the sample chamber and make observations of individual organisms at high magnification without affecting their flagellar beat frequencies. We discuss the prospect of the method to explore appendage motion and swimming kinematics of other flagellates and ciliates, and we argue that the method will be applicable to a broad range of cell sizes and shapes., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2022. Published by The Company of Biologists Ltd.)

Plankton imaging systems supported by automated classification and analysis have improved ecologists' ability to observe aquatic ecosystems. Today, we are on the cusp of reliably tracking plankton populations with a suite of lab-based and in situ tools, collecting imaging data at unprecedentedly fine spatial and temporal scales. But these data have potential well beyond examining the abundances of different taxa; the individual images themselves contain a wealth of information on functional traits. Here, we outline traits that could be measured from image data, suggest machine learning and computer vision approaches to extract functional trait information from the images, and discuss promising avenues for novel studies. The approaches we discuss are data agnostic and are broadly applicable to imagery of other aquatic or terrestrial organisms., Competing Interests: None declared., (© 2022 The Authors. Limnology and Oceanography published by Wiley Periodicals LLC on behalf of Association for the Sciences of Limnology and Oceanography.)

Toxic phytoplankton blooms have increased in many waterbodies worldwide with well-known negative impacts on human health, fisheries and ecosystems. However, why and how phytoplankton evolved toxin production is still a puzzling question, given that the producer that pays the costs often shares the benefit with other competing algae and thus provides toxins as a 'public good' (e.g. damaging a common competitor or predator). Furthermore, blooming phytoplankton species often show a high intraspecific variation in toxicity and we lack an understanding of what drives the dynamics of coexisting toxic and non-toxic genotypes. Here, by using an individual-based two-dimensional model, we show that small-scale patchiness of phytoplankton strains caused by demography can explain toxin evolution in phytoplankton with low motility and the maintenance of genetic diversity within their blooms. This patchiness vanishes for phytoplankton with high diffusive motility, suggesting different evolutionary pathways for different phytoplankton groups. In conclusion, our study reveals that small-scale spatial heterogeneity, generated by cell division and counteracted by diffusive cell motility and turbulence, can crucially affect toxin evolution and eco-evolutionary dynamics in toxic phytoplankton species. This contributes to a better understanding of conditions favouring toxin production and the evolution of public goods in asexually reproducing organisms in general.

Phytoplankton employ a variety of defence mechanisms against predation, including production of toxins. Domoic acid (DA) production by the diatom Pseudo-nitzschia spp. is induced by the presence of predators and is considered to provide defence benefits, but the evidence is circumstantial. We exposed eight different strains of P. seriata to chemical cues from copepods and examined the costs and the benefits of toxin production. The magnitude of the induced toxin response was highly variable among strains, while the costs in terms of growth reduction per DA cell quota were similar and the trade-off thus consistent. We found two components of the defence in induced cells: (i) a 'private good' in terms of elevated rejection of captured cells and (ii) a 'public good' facilitated by a reduction in copepod feeding activity. Induced cells were more frequently rejected by copepods and rejections were directly correlated with DA cell quota and independent of access to other food items. By contrast, the public-good effect was diminished by the presence of alternative prey suggesting that it does not play a major role in bloom formation and that its evolution is closely associated with the grazing-deterrent private good.

Inducible defences in phytoplankton are often assumed to come at a cost to the organism, but trade-offs have proven hard to establish experimentally. A reason for this may be that some trade-off costs only become evident under resource-limiting conditions. To explore the effect of nutrient limitation on trade-offs in toxin-producing dinoflagellates, we induced toxin production in Alexandrium minutum by chemical cues from copepods under different levels of nitrogen limitation. The effects were both nitrogen- and grazer-concentration dependent. Induced cells had higher cellular toxin content and a larger fraction of the cells was rejected by a copepod, demonstrating the clear benefits of toxin production. Induced cells also had a higher carbon and nitrogen content, despite up to 25% reduction in cell size. Unexpectedly, induced cells seemed to grow faster than controls, likely owing to a higher specific nutrient affinity due to reduced size. We thus found no clear trade-offs, rather the opposite. However, indirect ecological costs that do not manifest under laboratory conditions may be important. Inducing appropriate defence traits in response to threat-specific warning signals may also prevent larger cumulative costs from expressing several defensive traits simultaneously.

Microscopic sessile suspension feeders live attached to surfaces and, by consuming bacteria-sized prey and by being consumed, they form an important part of aquatic ecosystems. Their environmental impact is mediated by their feeding rate, which depends on a self-generated feeding current. The feeding rate has been hypothesized to be limited by recirculating eddies that cause the organisms to feed from water that is depleted of food particles. However, those results considered organisms in still water, while ambient flow is often present in their natural habitats. We show, using a point-force model, that even very slow ambient flow, with speed several orders of magnitude less than that of the self-generated feeding current, is sufficient to disrupt the eddies around perpendicular suspension feeders, providing a constant supply of food-rich water. However, the feeding rate decreases in external flow at a range of non-perpendicular orientations due to the formation of recirculation structures not seen in still water. We quantify the feeding flow and observe such recirculation experimentally for the suspension feeder Vorticella convallaria in external flows typical of streams and rivers.

Unicellular flagellated protists are a key element in aquatic microbial food webs. They all use flagella to swim and to generate feeding currents to encounter prey and enhance nutrient uptake. At the same time, the beating flagella create flow disturbances that attract flow-sensing predators. Protists have highly diverse flagellar arrangements in terms of number of flagella and their position, beat pattern, and kinematics, but it is unclear how the various arrangements optimize the fundamental trade-off between resource acquisition and predation risk. Here we describe the near-cell flow fields produced by 15 species and demonstrate consistent relationships between flagellar arrangement and swimming speed and between flagellar arrangement and flow architecture, and a trade-off between resource acquisition and predation risk. The flow fields fall in categories that are qualitatively described by simple point force models that include the drag force of the moving cell body and the propulsive forces of the flagella. The trade-off between resource acquisition and predation risk varies characteristically between flow architectures: Flagellates with multiple flagella have higher predation risk relative to their clearance rate compared to species with only one active flagellum, with the exception of the highly successful dinoflagellates that have simultaneously achieved high clearance rates and stealth behavior due to a unique flagellar arrangement. Microbial communities are shaped by trade-offs and environmental constraints, and a mechanistic explanation of foraging trade-offs is a vital part of understanding the eukaryotic communities that form the basis of pelagic food webs., Competing Interests: The authors declare no competing interest.

Many planktonic suspension feeders are attached to particles or tethered by gravity when feeding. It is commonly accepted that the feeding flows of tethered suspension feeders are stronger than those of their freely swimming counterparts. However, recent flow simulations indicate the opposite, and the cause of the opposing conclusions is not clear. To explore the effect of tethering on suspension feeding, we use a low-Reynolds-number flow model. We find that it is favorable to be freely swimming instead of tethered since the resulting feeding flow past the cell body is stronger, leading to a higher clearance rate. Our result underscores the significance of the near-field flow in shaping planktonic feeding modes, and it suggests that organisms tether for reasons that are not directly fluid dynamical (e.g., to stay near surfaces where the concentration of bacterial prey is high)., Competing Interests: The authors declare no competing interest., (Copyright © 2020 the Author(s). Published by PNAS.)

Sponges are suspension feeders that filter vast amounts of water. Pumping is carried out by flagellated chambers that are connected to an inhalant and exhalant canal system. In 'leucon' sponges with relatively high-pressure resistance due to a complex and narrow canal system, pumping and filtering are only possible owing to the presence of a gasket-like structure (forming a canopy above the collar filters). Here, we combine numerical and experimental work and demonstrate how sponges that lack such sealing elements are able to efficiently pump and force the flagella-driven flow through their collar filter, thanks to the formation of a 'hydrodynamic gasket' above the collar. Our findings link the architecture of flagellated chambers to that of the canal system, and lend support to the current view that the sponge aquiferous system evolved from an open-type filtration system, and that the first metazoans were filter feeders., Competing Interests: SA, TK, PL, SL, GY, JW No competing interests declared, (© 2020, Asadzadeh et al.)

Gleaners and exploiters (opportunists) are organisms adapted to feeding in nutritionally poor and rich environments, respectively. A trade-off between these two strategies-a negative relationship between the rate at which organisms can acquire food and ingest it-is a critical assumption in many ecological models. Here, we evaluate evidence for this trade-off across a wide range of heterotrophic eukaryotes from unicellular nanoflagellates to large mammals belonging to both aquatic and terrestrial realms. Using data on the resource acquisition and ingestion rates in >500 species, we find no evidence of a trade-off across species. Instead, there is a positive relationship between maximum clearance rate and maximum ingestion rate. The positive relationship is not a result of lumping together diverse taxa; it holds within all subgroups of organisms we examined as well. Correcting for differences in body mass weakens but does not reverse the positive relationship, so this is not an artifact of size scaling either. Instead, this positive relationship represents a slow-fast gradient in the "pace of life" that overrides the expected gleaner-exploiter trade-off. Other trade-offs must therefore shape ecological processes, and investigating them may provide deeper insights into coexistence, competitive dynamics, and biodiversity patterns in nature. A plausible target for study is the well-documented trade-off between growth rate and predation avoidance, which can also drive the slow-fast gradient we observe here., Competing Interests: The authors declare no competing interest.

Activity and autonomous motion are fundamental in living and engineering systems. This has stimulated the new field of 'active matter' in recent years, which focuses on the physical aspects of propulsion mechanisms, and on motility-induced emergent collective behavior of a larger number of identical agents. The scale of agents ranges from nanomotors and microswimmers, to cells, fish, birds, and people. Inspired by biological microswimmers, various designs of autonomous synthetic nano- and micromachines have been proposed. Such machines provide the basis for multifunctional, highly responsive, intelligent (artificial) active materials, which exhibit emergent behavior and the ability to perform tasks in response to external stimuli. A major challenge for understanding and designing active matter is their inherent nonequilibrium nature due to persistent energy consumption, which invalidates equilibrium concepts such as free energy, detailed balance, and time-reversal symmetry. Unraveling, predicting, and controlling the behavior of active matter is a truly interdisciplinary endeavor at the interface of biology, chemistry, ecology, engineering, mathematics, and physics. The vast complexity of phenomena and mechanisms involved in the self-organization and dynamics of motile active matter comprises a major challenge. Hence, to advance, and eventually reach a comprehensive understanding, this important research area requires a concerted, synergetic approach of the various disciplines. The 2020 motile active matter roadmap of Journal of Physics: Condensed Matter addresses the current state of the art of the field and provides guidance for both students as well as established scientists in their efforts to advance this fascinating area.

Diel vertical migration (DVM), the daily movement of organisms through oceanic water columns, is mainly driven by spatio-temporal variations in the light affecting the intensity of predator-prey interactions. Migration patterns of an organism are intrinsically linked to the distribution of its conspecifics, its prey and its predators, each with their own fitness-seeking imperatives. We present a mechanistic, trait-based model of DVM for the different components of a pelagic community. Specifically, we consider size, sensory mode and feeding mode as key traits, representing a community of copepods that prey on each other and are, in turn, preyed upon by fish. Using game-theoretic principles, we explore the optimal distribution of the main groups of a planktonic pelagic food web simultaneously. Within one single framework, our model reproduces a whole suite of observed patterns, such as size-dependent DVM patterns of copepods and reverse migrations. These patterns can only be reproduced when different trophic levels are considered at the same time. This study facilitates a quantitative understanding of the drivers of DVM, and is an important step towards mechanistically underpinned predictions of DVM patterns and biologically mediated carbon export.

We present autofluorescence of six zooplankton species, including salmon lice (Lepeophtheirus salmonis), for the purpose of classification in marine environments. Using a 410 nm excitation wavelength, we find that all measured zooplankton species exhibit broad cyan fluorescence centered around 510-520 nm. Furthermore, salmon lice show an absence of red fluorescence from undigested chlorophyll, which is measured from the gut of the herbivorous zooplankton species. We show the capability to distinguish noneating species, including salmon lice, from algae-eating species using a dual-band analysis of the fluorescence spectra. This shows the potential of autofluorescence as an important signature in real-time monitoring and classification of salmon lice.

Most marine plankton have a high energy (carbon) density, but some are gelatinous with approximately 100 times more watery bodies. How do those distinctly different body plans emerge, and what are the trade-offs? We address this question by modeling the energy budget of planktonic filter feeders across life-forms, from micron-sized unicellular microbes such as choanoflagellates to centimeter-sized gelatinous tunicates such as salps. We find two equally successful strategies, one being small with high energy density (dense dwarf) and the other being large with low energy density (gelatinous giant). The constraint that forces large-but not small-filter feeders to be gelatinous is identified as a lower limit to the size-specific filter area, below which the energy costs lead to starvation. A further limit is found from the maximum size-specific motor force that restricts the access to optimum strategies. The quantified constraints are discussed in the context of other resource-acquisition strategies. We argue that interception feeding strategies can be accessed by large organisms only if they are gelatinous. On the other hand, organisms that use remote prey sensing do not need to be gelatinous, even if they are large.

Diatoms contribute nearly half of the marine primary production. These microalgae differ from other phytoplankton groups in having a silicified cell wall, which is the strongest known biological material relative to its density. While it has been suggested that a siliceous wall may have evolved as a mechanical protection against grazing, empirical evidence of its defensive role is limited. Here, we experimentally demonstrate that grazing by adult copepods and nauplii on diatoms is approximately inversely proportional to their silica content, both within and among diatom species. While a sixfold increase in silica content leads to a fourfold decrease in copepod grazing, silicification provides no protection against protozoan grazers that directly engulf their prey. We also found that the wall provides limited protection to cells ingested by copepods, since less than 1% of consumed cells were alive in the faecal pellets. Moreover, silica deposition in diatoms decreases with increasing growth rates, suggesting a possible cost of defence. Overall, our results demonstrate that thickening of silica walls is an effective defence strategy against copepods. This suggests that the plasticity of silicification in diatoms may have evolved as a response to copepod grazing pressure, whose specialized tools to break silicified walls have coevolved with diatoms.

The two parameters of the Michaelis-Menten model, the maximum uptake rate and the half-saturation constant, are not stochastically independent, and the half-saturation constant is not a measure of nutrient affinity, as commonly assumed. Failure to realise their interdependence and mechanistic interpretation may lead to the emergence of false trade-offs., (© 2019 John Wiley & Sons Ltd/CNRS.)

Marine plankton have been conspicuously affected by recent climate change, responding with profound spatial relocations and shifts in the timing of their seasonal occurrence. These changes directly affect the global carbon cycle by altering the transport of organic material from the surface ocean to depth, with consequences that remain poorly understood. We investigated how distributional and abundance changes of copepods, the dominant group of zooplankton, have affected biogenic carbon cycling. We used trait-based, mechanistic models to estimate the magnitude of carbon transported downward through sinking faecal pellets, daily vertical migration and seasonal hibernation at depth. From such estimates for over 200,000 community observations in the northern North Atlantic we found carbon flux increased along the northwestern boundary of the study area and decreased in the open northern North Atlantic during the past 55 years. These changes in export were primarily associated with changes in copepod biomass, driven by shifting distributions of abundant, large-bodied species. Our findings highlight how recent climate change has affected downward carbon transport by altering copepod community structure and demonstrate how carbon fluxes through plankton communities can be mechanistically implemented in next-generation biogeochemical models with size-structured representations of zooplankton communities.

Our traditional view of the interactions between marine organisms is conceptualized as food webs where species interact with one another mainly via direct consumption. However, recent research suggests that understudied non-consumptive interactions, such as behaviourally mediated indirect interactions (BMIIs), can influence marine ecosystems as much as consumptive effects. Here, we show, to our knowledge, the first experimental evidence and quantification of bottom-up BMIIs in plankton food webs. We used observational, modelling and experimental approaches to investigate how behavioural responses to resource availability influence predation mortality on grazers with different foraging strategies (ambushing versus active foraging). A three-level food chain was used: phytoplankton as resource, copepod nauplii as grazers of phytoplankton and a large copepod as a predator. Ambushers showed little change in foraging activity with resource availability, whereas active foragers decreased their foraging activity with increasing resources, which led to a decrease (24-50%) in predation mortality. Therefore, an increase in resources ('initiator') causes behavioural changes in active grazers ('transmitter'), which ultimately negatively affects predator ('receiver') consumption rates. Consequently, increase in resource abundance may result in decreasing energy transfer to higher trophic levels. These results indicate that behaviourally mediated interactions drive marine food web dynamics differently from that predicted by only density-mediated or consumptive interactions.

Choanoflagellates are unicellular eukaryotes that are ubiquitous in aquatic habitats. They have a single flagellum that creates a flow toward a collar filter composed of filter strands that extend from the cell. In one common group, the loricate choanoflagellates, the cell is suspended in an elaborate basket-like structure, the lorica, the function of which remains unknown. Here, we use Computational Fluid Dynamics to explore the possible hydrodynamic function of the lorica. We use the choanoflagellate Diaphaoneca grandis as a model organism. It has been hypothesized that the function of the lorica is to prevent refiltration (flow recirculation) and to increase the drag and, hence, increase the feeding rate and reduce the swimming speed. We find no support for these hypotheses. On the contrary, motile prey are encountered at a much lower rate by the loricate organism. The presence of the lorica does not affect the average swimming speed, but it suppresses the lateral motion and rotation of the cell. Without the lorica, the cell jiggles from side to side while swimming. The unsteady flow generated by the beating flagellum causes reversed flow through the collar filter that may wash away captured prey while it is being transported to the cell body for engulfment. The lorica substantially decreases such flow, hence it potentially increases the capture efficiency. This may be the main adaptive value of the lorica.

Many species of phytoplankton produce toxins that may provide protection from grazing. In that case one would expect toxin production to be costly; else all species would evolve toxicity. However, experiments have consistently failed to show any costs. Here, we show that costs of toxin production are environment dependent but can be high. We develop a fitness optimization model to estimate rate, costs, and benefits of toxin production, using PST (paralytic shellfish toxin) producing dinoflagellates as an example. Costs include energy and material (nitrogen) costs estimated from well-established biochemistry of PSTs, and benefits are estimated from relationship between toxin content and grazing mortality. The model reproduces all known features of PST production: inducibility in the presence of grazer cues, low toxicity of nitrogen-starved cells, but high toxicity of P-limited and light-limited cells. The model predicts negligible reduction in cell division rate in nitrogen replete cells, consistent with observations, but >20% reduction when nitrogen is limiting and abundance of grazers high. Such situation is characteristic of coastal and oceanic waters during summer when blooms of toxic algae typically develop. The investment in defense is warranted, since the net growth rate is always higher in defended than in undefended cells.

Many phytoplankton species produce toxic substances, but their functional role is unclear. Specifically, it remains uncertain whether these compounds have a toxic or deterrent effect on grazers; only, the latter is consistent with toxins as defensive tools. Here, we show that 10 of 12 species or strains of toxic dinoflagellates were consumed at lower rates than a similarly sized nontoxic dinoflagellate by a copepod. Through video observations of individual prey-grazer interactions, we further demonstrate that the dominating mechanism is through capture, examination, and subsequent rejection of vital cells, that is, a true deterrent effect that offers a straightforward explanation to its evolution. We argue that the diversity of grazer responses to toxic phytoplankton reported in the literature, including toxic effects, and the high diversity of toxin profiles between strains of the same phytoplankton species reflect different stages of an ever-ongoing evolutionary arms race, facilitated by rapid adaptation of grazers to toxic substances. We further argue that defensive toxicity requires a chemical signal exterior to the cell that informs the grazer about the toxicity of the cell. The signal can be the toxin itself or just an aposematic signal of toxicity. In the former case, allelochemical effects may emerge at high cell concentrations as a nonadaptive side effect of a predator defenses., (© 2018 by the Ecological Society of America.)

Diatoms and copepods are main actors in marine food webs. The prey-predator interactions between them affect bloom dynamics, shape marine ecosystems and impact the energy transfer to higher trophic levels. Recently it has been demonstrated that the presence of grazers may affect the diatom prey beyond the direct effect of grazing. Here, we investigated the response of the chain-forming centric diatom Skeletonema marinoi to grazer cues, including changes in morphology, gene expression and metabolic profile. S. marinoi cells were incubated with Calanus finmarchicus or with Centropages typicus and in both cases responded by reducing the chain length, whereas changes in gene expression indicated an activation of stress response, changes in the lipid and nitrogen metabolism, in cell cycle regulation and in frustule formation. Transcripts linked to G protein-coupled receptors and to nitric oxide synthesis were differentially expressed suggesting involvement of these signalling transduction pathways in the response. Downregulation of a lipoxygenase in the transcriptomic data and of its products in the metabolomic data also indicate an involvement of oxylipins. Our data contribute to a better understanding of the gene function in diatoms, providing information on the nature of genes implicated in the interaction with grazers, a crucial process in marine ecosystems.

In aquatic ecosystems, unicellular algae form the basis of the food webs. Theoretical and experimental studies have demonstrated that one of the mechanisms that maintain high diversity of phytoplankton is through predation and the consequent evolution of defence mechanisms. Proposed defence mechanisms in phytoplankton are diverse and include physiological (e.g. toxicity, bioluminescence), morphological (e.g. silica shell, colony formation), and behavioural (e.g. escape response) traits. However, the function of many of the proposed defence mechanisms remains elusive, and the costs and benefits (trade-offs) are often unquantified or undocumented. Here, we provide an overview of suggested phytoplankton defensive traits and review their experimental support. Wherever possible we quantify the trade-offs from experimental evidence and theoretical considerations. In many instances, experimental evidence suggests that defences are costless. However, we argue that (i) some costs materialize only under natural conditions, for example, sinking losses, or dependency on the availability of specific nutrients, and (ii) other costs become evident only under resource-deficient conditions where a rivalry for limiting resources between growth and defence occurs. Based on these findings, we suggest two strategies for quantifying the costs of defence mechanisms in phytoplankton: (i) for the evaluation of defence costs that are realized under natural conditions, a mechanistic understanding of the hypothesized component processes is required; and (ii) the magnitude of the costs (i.e. growth reduction) must be assessed under conditions of resource limitation., (© 2018 Cambridge Philosophical Society.)

Species establishing outside their natural range, negatively impacting local ecosystems, are of increasing global concern. They often display life-history features characteristic for r-selected populations with fast growth and high reproduction rates to achieve positive population growth rates (r) in invaded habitats. Here, we demonstrate substantially earlier maturation at a 2 orders of magnitude lower body mass at first reproduction in invasive compared to native populations of the comb jelly Mnemiopsis leidyi. Empirical results are corroborated by a theoretical model for competing life-history traits that predicts maturation at the smallest possible size to optimize r, while individual lifetime reproductive success (R 0 ), optimized in native populations, is near constant over a large range of intermediate maturation sizes. We suggest that high variability in reproductive tactics in native populations is an underappreciated determinant of invasiveness, acting as substrate upon which selection can act during the invasion process., (© 2017 John Wiley & Sons Ltd.)

Copepods can respond to predators by powerful escape jumps that in some surface-dwelling forms may propel the copepod out of the water. We studied the kinematics and energetics of submerged and out-of-water jumps of two neustonic pontellid copepods, Anomalocera patersoni and Pontella mediterranea , and one pelagic calanoid copepod, Calanus helgolandicus ( euxinus ). We show that jumping out of the water does not happen just by inertia gained during the copepod's acceleration underwater, but also requires the force generated by the thoracic limbs when breaking through the water's surface to overcome surface tension, drag and gravity. The timing of this appears to be necessary for success. At the moment of breaking the water interface, the instantaneous velocity of the two pontellids reached 125 cm s -1 , while their maximum underwater speed (115 cm s -1 ) was close to that of similarly sized C. helgolandicus (106 cm s -1 ). The average specific power produced by the two pontellids during out-of-water jumps (1700-3300 W kg -1 muscle mass) was close to that during submerged jumps (900-1600 W kg -1 muscle mass) and, in turn, similar to that produced during submerged jumps of C. helgolandicus (1300 W kg -1 muscle mass). The pontellids may shake off water adhering to their body by repeated strokes of the limbs during flight, which leads to a slight acceleration in the air. Our observations suggest that out-of-water jumps of pontellids are not dependent on any exceptional ability to perform this behavior but have the same energetic cost and are based on the same kinematic patterns and contractive capabilities of muscles as those of copepods swimming submerged., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

Microbial filter feeders are an important group of grazers, significant to the microbial loop, aquatic food webs, and biogeochemical cycling. Our understanding of microbial filter feeding is poor, and, importantly, it is unknown what force microbial filter feeders must generate to process adequate amounts of water. Also, the trade-off in the filter spacing remains unexplored, despite its simple formulation: A filter too coarse will allow suitably sized prey to pass unintercepted, whereas a filter too fine will cause strong flow resistance. We quantify the feeding flow of the filter-feeding choanoflagellate Diaphanoeca grandis using particle tracking, and demonstrate that the current understanding of microbial filter feeding is inconsistent with computational fluid dynamics (CFD) and analytical estimates. Both approaches underestimate observed filtration rates by more than an order of magnitude; the beating flagellum is simply unable to draw enough water through the fine filter. We find similar discrepancies for other choanoflagellate species, highlighting an apparent paradox. Our observations motivate us to suggest a radically different filtration mechanism that requires a flagellar vane (sheet), something notoriously difficult to visualize but sporadically observed in the related choanocytes (sponges). A CFD model with a flagellar vane correctly predicts the filtration rate of D. grandis , and using a simple model we can account for the filtration rates of other microbial filter feeders. We finally predict how optimum filter mesh size increases with cell size in microbial filter feeders, a prediction that accords very well with observations. We expect our results to be of significance for small-scale biophysics and trait-based ecological modeling., Competing Interests: The authors declare no conflict of interest.

Zooplankton responses to toxic algae are highly variable, even towards taxonomically closely related species or different strains of the same species. Here, the individual level feeding behavior of a copepod, Temora longicornis, was examined which offered 4 similarly sized strains of toxic dinoflagellate Alexandrium spp. and a non-toxic control strain of the dinoflagellate Protoceratium reticulatum. The strains varied in their cellular toxin concentration and composition and in lytic activity. High-speed video observations revealed four distinctly different strain-specific feeding responses of the copepod during 4h incubations: (i) the 'normal' feeding behavior, in which the feeding appendages were beating almost constantly to produce a feeding current and most (90%) of the captured algae were ingested; (ii) the beating activity of the feeding appendages was reduced by ca. 80% during the initial 60min of exposure, after which very few algae were captured and ingested; (iii) capture and ingestion rates remained high, but ingested cells were regurgitated; and (iv) the copepod continued beating its appendages and captured cells at a high rate, but after 60min, most captured cells were rejected. The various prey aversion responses observed may have very different implications to the prey and their ability to form blooms: consumed but regurgitated cells are dead, captured but rejected cells survive and may give the prey a competitive advantage, while reduced feeding activity of the grazer may be equally beneficial to the prey and its competitors. These behaviors were not related to lytic activity or overall paralytic shellfish toxins (PSTs) content and composition and suggest that other cues are responsible for the responses., (Copyright © 2016 Elsevier B.V. All rights reserved.)

Many unicellular flagellates are mixotrophic and access resources through both photosynthesis and prey capture. Their fitness depends on those processes as well as on swimming and predator avoidance. How does the flagellar arrangement and beat pattern of the flagellate affect swimming speed, predation risk due to flow-sensing predators, and prey capture? Here, we describe measured flows around two species of mixotrophic, biflagellated haptophytes with qualitatively different flagellar arrangements and beat patterns. We model the near cell flows using two symmetrically arranged point forces with variable position next to a no-slip sphere. Utilizing the observations and the model we find that puller force arrangements favour feeding, whereas equatorial force arrangements favour fast and quiet swimming. We determine the capture rates of both passive and motile prey, and we show that the flow facilitates transport of captured prey along the haptonema structure. We argue that prey capture alone cannot fulfil the energy needs of the observed species, and that the mixotrophic life strategy is essential for survival.

Functional traits, rather than taxonomic identity, determine the fitness of individuals in their environment: traits of marine organisms are therefore expected to vary across the global ocean as a function of the environment. Here, we quantify such spatial and seasonal variations based on extensive empirical data and present the first global biogeography of key traits (body size, feeding mode, relative offspring size and myelination) for pelagic copepods, the major group of marine zooplankton. We identify strong patterns with latitude, season and between ocean basins that are partially (c. 50%) explained by key environmental drivers. Body size, for example decreases with temperature, confirming the temperature-size rule, but surprisingly also with productivity, possibly driven by food-chain length and size-selective predation. Patterns unrelated to environmental predictors may originate from phylogenetic clustering. Our maps can be used as a test-bed for trait-based mechanistic models and to inspire next-generation biogeochemical models., (© 2016 John Wiley & Sons Ltd/CNRS.)

Competition between large jellyfish and forage fish for zooplankton prey is both a possible cause of jellyfish increases and a concern for the management of marine ecosystems and fisheries. Identifying principal factors affecting this competition is therefore important for marine management, but the lack of both good quality data and a robust theoretical framework have prevented general global analyses. Here, we present a general mechanistic food web model that considers fundamental differences in feeding modes and predation pressure between fish and jellyfish. The model predicts forage fish dominance at low primary production, and a shift towards jellyfish with increasing productivity, turbidity and fishing. We present an index of global ecosystem susceptibility to shifts in fish-jellyfish dominance that compares well with data on jellyfish distributions and trends. The results are a step towards better understanding the processes that govern jellyfish occurrences globally and highlight the advantage of considering feeding traits in ecosystem models., (© 2016 The Author(s).)

Statistical species distribution models (SDMs) are increasingly used to project spatial relocations of marine taxa under future climate change scenarios. However, tests of their predictive skill in the real-world are rare. Here, we use data from the Continuous Plankton Recorder program, one of the longest running and most extensive marine biological monitoring programs, to investigate the reliability of predicted plankton distributions. We apply three commonly used SDMs to 20 representative plankton species, including copepods, diatoms, and dinoflagellates, all found in the North Atlantic and adjacent seas. We fit the models to decadal subsets of the full (1958-2012) dataset, and then use them to predict both forward and backward in time, comparing the model predictions against the corresponding observations. The probability of correctly predicting presence was low, peaking at 0.5 for copepods, and model skill typically did not outperform a null model assuming distributions to be constant in time. The predicted prevalence increasingly differed from the observed prevalence for predictions with more distance in time from their training dataset. More detailed investigations based on four focal species revealed that strong spatial variations in skill exist, with the least skill at the edges of the distributions, where prevalence is lowest. Furthermore, the scores of traditional single-value model performance metrics were contrasting and some implied overoptimistic conclusions about model skill. Plankton may be particularly challenging to model, due to its short life span and the dispersive effects of constant water movements on all spatial scales, however there are few other studies against which to compare these results. We conclude that rigorous model validation, including comparison against null models, is essential to assess the robustness of projections of marine planktonic species under climate change., (© 2016 John Wiley & Sons Ltd.)

The purpose of this dataset was to compile adult and offspring size estimates for marine organisms. Adult and offspring size estimates of 408 species were compiled from the literature covering >17 orders of magnitude in body mass and including Cephalopoda (ink fish), Cnidaria ("jelly" fish), Crustaceans, Ctenophora (comb jellies), Elasmobranchii (cartilaginous fish), Mammalia (mammals), Sagittoidea (arrow worms) and Teleost (i.e., Actinopterygii, bony fish). Individual size estimates were converted to standardized size estimates (carbon weight, g) to allow for among-group comparisons. This required a number of size estimates to be converted and a compilation of conversion factors obtained from the literature are also presented., (© 2016 by the Ecological Society of America.)

Copepods are ubiquitous in aquatic habitats. They exude bioactive compounds that mediate mate finding or induce defensive traits in prey organisms. However, little is known about the chemical nature of the copepod exometabolome that contributes to the chemical landscape in pelagic habitats. Here we describe the development of a closed loop solid phase extraction setup that allows for extraction of exuded metabolites from live copepods. We captured exudates from male and female Temora longicornis and analyzed the content with high resolution LC-MS. Chemometric methods revealed 87 compounds that constitute a specific chemical pattern either qualitatively or quantitatively indicating copepod presence. The majority of the compounds were present in both female and male exudates, but nine compounds were mainly or exclusively present in female exudates and hence potential pheromone candidates. Copepodamide G, known to induce defensive responses in phytoplankton, was among the ten compounds of highest relative abundance in both male and female extracts. The presence of copepodamide G shows that the method can be used to capture and analyze chemical signals from living source organisms. We conclude that solid phase extraction in combination with metabolic profiling of exudates is a useful tool to develop our understanding of the chemical interplay between pelagic organisms.

The size of an individual organism is a key trait to characterize its physiology and feeding ecology. Size-based scaling laws may have a limited size range of validity or undergo a transition from one scaling exponent to another at some characteristic size. We collate and review data on size-based scaling laws for resource acquisition, mobility, sensory range, and progeny size for all pelagic marine life, from bacteria to whales. Further, we review and develop simple theoretical arguments for observed scaling laws and the characteristic sizes of a change or breakdown of power laws. We divide life in the ocean into seven major realms based on trophic strategy, physiology, and life history strategy. Such a categorization represents a move away from a taxonomically oriented description toward a trait-based description of life in the oceans. Finally, we discuss life forms that transgress the simple size-based rules and identify unanswered questions.

Explaining variability in offspring vs. adult size among groups is a necessary step to determine the evolutionary and environmental constraints shaping variability in life history strategies. This is of particular interest for life in the ocean where a diversity of offspring development strategies is observed along with variability in physical and biological forcing factors in space and time. We compiled adult and offspring size for 407 pelagic marine species covering more than 17 orders of magnitude in body mass including Cephalopoda, Cnidaria, Crustaceans, Ctenophora, Elasmobranchii, Mammalia, Sagittoidea, and Teleost. We find marine life following one of two distinct strategies, with offspring size being either proportional to adult size (e.g., Crustaceans, Elasmobranchii, and Mammalia) or invariant with adult size (e.g., Cephalopoda, Cnidaria, Sagittoidea, Teleosts, and possibly Ctenophora). We discuss where these two strategies occur and how these patterns (along with the relative size of the offspring) may be shaped by physical and biological constraints in the organism's environment. This adaptive environment along with the evolutionary history of the different groups shape observed life history strategies and possible group-specific responses to changing environmental conditions (e.g., production and distribution).

Mixotrophy is common, if not dominant, among eukaryotic flagellates, and these organisms have to both acquire inorganic nutrients and capture particulate food. Diffusion limitation favors small cell size for nutrient acquisition, whereas large cell size facilitates prey interception because of viscosity, and hence intermediately sized mixotrophic dinoflagellates are simultaneously constrained by diffusion and viscosity. Advection may help relax both constraints. We use high-speed video microscopy to describe prey interception and capture, and micro particle image velocimetry (micro-PIV) to quantify the flow fields produced by free-swimming dinoflagellates. We provide the first complete flow fields of free-swimming interception feeders, and demonstrate the use of feeding currents. These are directed toward the prey capture area, the position varying between the seven dinoflagellate species studied, and we argue that this efficiently allows the grazer to approach small-sized prey despite viscosity. Measured flow fields predict the magnitude of observed clearance rates. The fluid deformation created by swimming dinoflagellates may be detected by evasive prey, but the magnitude of flow deformation in the feeding current varies widely between species and depends on the position of the transverse flagellum. We also use the near-cell flow fields to calculate nutrient transport to swimming cells and find that feeding currents may enhance nutrient uptake by ≈75% compared with that by diffusion alone. We argue that all phagotrophic microorganisms must have developed adaptations to counter viscosity in order to allow prey interception, and conclude that the flow fields created by the beating flagella in dinoflagellates are key to the success of these mixotrophic organisms.

The optimal allocation of resources to repair vs. reproduction in an organism may depend on the magnitude and pattern of the external mortality it is experiencing, which, in turn, may depend on its feeding and mate-finding behavior. Thus, the fundamental activities of an organism, i.e., to feed, to survive, and to reproduce, are interrelated through trade-offs. Here, we use small planktonic copepods to examine how adult longevity and ageing patterns in a protected laboratory environment relate to the feeding mode (active searching vs. passive ambush feeding), mate-finding behavior, and spawning mode of the species. We show that average adult longevity varies between species by an order of magnitude and is independent of body size. Ambush feeders that carry their eggs have longer average life spans and experience higher mortality later in life relative to active feeders that broadcast their eggs. Males generally have shorter life spans and experience higher mortality earlier in life than females, and this difference may be accentuated in species where dangerous mate-finding is male biased. We finally show a trade-off between longevity and fecundity, with ambush feeders producing eggs at a rate five to 10 times lower than the active feeders, consistent with predictions from optimal resource allocation theory.

The stresslet provides a simple model of the flow created by a small, freely swimming and neutrally buoyant aquatic organism and shows that the far field fluid disturbance created by such an organism in general decays as one over distance squared. Here we discuss a quieter swimming mode that eliminates the stresslet component of the flow and leads to a faster spatial decay of the fluid disturbance described by a force quadrupole that decays as one over distance cubed. Motivated by recent experimental results on fluid disturbances due to small aquatic organisms, we demonstrate that a three-Stokeslet model of a swimming organism which uses breast stroke type kinematics is an example of such a quiet swimmer. We show that the fluid disturbance in both the near field and the far field is significantly reduced by appropriately arranging the propulsion apparatus, and we find that the far field power laws are valid surprisingly close to the organism. Finally, we discuss point force models as a general framework for hypothesis generation and experimental exploration of fluid mediated predator-prey interactions in the planktonic world.