Organismal trade-offs and the pace of planktonic life.

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.

Foraging mechanisms in excavate flagellates shed light on the functional ecology of early eukaryotes.

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.

The fluid dynamics of barnacle feeding.

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.

Predation in a Microbial World: Mechanisms and Trade-Offs of Flagellate Foraging.

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.

The function of the feeding groove of 'typical excavate' flagellates.

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.

Gelatinous larvacean zooplankton can enhance trophic transfer and carbon sequestration.

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.

Machine learning techniques to characterize functional traits of plankton from image data.

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.

Evolution of toxins as a public good in phytoplankton.

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.

Costs and benefits of predator-induced defence in a toxic diatom.

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.

The effect of external flow on the feeding currents of sessile microorganisms.

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.

Predator-induced defence in a dinoflagellate generates benefits without direct costs.

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.

Foraging trade-offs, flagellar arrangements, and flow architecture of planktonic protists.

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.

The effect of tethering on the clearance rate of suspension-feeding plankton.

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).

Hydrodynamics of sponge pumps and evolution of the sponge body plan.

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.

Heterotrophic eukaryotes show a slow-fast continuum, not a gleaner-exploiter trade-off.

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.

The 2020 motile active matter roadmap.

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.

Trophic interactions drive the emergence of diel vertical migration patterns: a game-theoretic model of copepod communities.

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.