André W. Visser

Plankton motility patterns and encounter rates.

Many planktonic organisms have motility patterns with correlation run lengths (distances traversed before direction changes) of the same order as their reaction distances regarding prey, mates and predators (distances at which these organisms are remotely detected). At these scales, the relative measure of run length to reaction distance determines whether the underlying encounter is ballistic or diffusive. Since ballistic interactions are intrinsically more efficient than diffusive, we predict that organisms will display motility with long correlation run lengths compared to their reaction distances to their prey, but short compared to the reaction distances of their predators. We show motility data for planktonic organisms ranging from bacteria to copepods that support this prediction. We also present simple ballistic and diffusive motility models for estimating encounter rates, which lead to radically different predictions, and we present a simple criterion to determine which model is the more appropriate in a given case.

Characteristic Sizes of Life in the Oceans, from Bacteria to Whales

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.

Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic

Significance Every autumn across the North Atlantic, large numbers of zooplankton copepods migrate from the surface waters into the oceans interior to hibernate at depths of 600–1,400 m. Through this migration, they actively transport lipid carbon to below the permanent thermocline, where it is metabolized at a rate comparable to the carbon delivered by sinking detritus. This “lipid pump” has not been included in previous estimates of the deep-ocean carbon sequestration, which are based on either measurements of sinking fluxes of detritus, or estimates of new primary production. Unlike other components of the biological pump, the lipid pump does not strip the surface ocean of nutrients, and decouples carbon sequestration from nutrient replenishment, a process we term the “lipid shunt.” Estimates of carbon flux to the deep oceans are essential for our understanding of global carbon budgets. Sinking of detrital material (“biological pump”) is usually thought to be the main biological component of this flux. Here, we identify an additional biological mechanism, the seasonal “lipid pump,” which is highly efficient at sequestering carbon into the deep ocean. It involves the vertical transport and metabolism of carbon rich lipids by overwintering zooplankton. We show that one species, the copepod Calanus finmarchicus overwintering in the North Atlantic, sequesters an amount of carbon equivalent to the sinking flux of detrital material. The efficiency of the lipid pump derives from a near-complete decoupling between nutrient and carbon cycling—a “lipid shunt,” and its direct transport of carbon through the mesopelagic zone to below the permanent thermocline with very little attenuation. Inclusion of the lipid pump almost doubles the previous estimates of deep-ocean carbon sequestration by biological processes in the North Atlantic.

Capital versus income breeding in a seasonal environment

The allocation of resources between growth, storage, and reproduction is a key trade-off in the life-history strategies of organisms. A central dichotomy is between capital breeders and income breeders. Capital breeders build reserves that allow them to spawn at a later time independently of food availability, while income breeders allocate ingested food directly to reproduction. Motivated by copepod studies, we use an analytical model to compare the fitness of income with capital breeding in a deterministic seasonal environment. We analyze how the fitness of breeding strategies depend on feeding season duration and size at maturity. Small capital breeders perform better in short feeding seasons but fall behind larger individuals when the length of the feeding season increases. Income breeding favors smaller individuals as their short generation time allows for multiple generations within a year and thereby achieve a high annual growth rate, outcompeting capital breeders in long feeding seasons. Therefore, we expect to find a dominance of small income breeders in temperate waters, while large capital breeders should dominate high latitudes where the spring is short and intense. This pattern is evident in nature, particularly in organisms with a generation time of a year or less.

Analysis of self-overlap reveals trade-offs in plankton swimming trajectories.

Movement is a fundamental behaviour of organisms that not only brings about beneficial encounters with resources and mates, but also at the same time exposes the organism to dangerous encounters with predators. The movement patterns adopted by organisms should reflect a balance between these contrasting processes. This trade-off can be hypothesized as being evident in the behaviour of plankton, which inhabit a dilute three-dimensional environment with few refuges or orienting landmarks. We present an analysis of the swimming path geometries based on a volumetric Monte Carlo sampling approach, which is particularly adept at revealing such trade-offs by measuring the self-overlap of the trajectories. Application of this method to experimentally measured trajectories reveals that swimming patterns in copepods are shaped to efficiently explore volumes at small scales, while achieving a large overlap at larger scales. Regularities in the observed trajectories make the transition between these two regimes always sharper than in randomized trajectories or as predicted by random walk theory. Thus, real trajectories present a stronger separation between exploration for food and exposure to predators. The specific scale and features of this transition depend on species, gender and local environmental conditions, pointing at adaptation to state and stage-dependent evolutionary trade-offs.

Accuracy and precision in the calculation of phenology metrics

Phytoplankton phenology (the timing of seasonal events) is a commonly used indicator for evaluating responses of marine ecosystems to climate change. However, phenological metrics are vulnerable to observation-(bloom amplitude, missing data, and observational noise) and analysis-related (temporal resolution, preprocessing technique, and phenology metric) processes. Here we consider the impact of these processes on the robustness of four phenology metrics (timing of maximum, 5% above median, maximum growth rate, and 15% of cumulative distribution). We apply a simulation-testing approach, where a phenology metric is first determined from a noise- and gap-free time series, and again once it has been modified. We show that precision is a greater concern than accuracy for many of these metrics, an important point that has been hereto overlooked in the literature. The variability in precision between phenology metrics is substantial, but it can be improved by the use of preprocessing techniques (e.g., gap-filling or smoothing). Furthermore, there are important differences in the inherent variability of the metrics that may be crucial in the interpretation of studies based upon them. Of the considered metrics, the 15% of cumulative distribution metric best satisfies the precision criteria. However, the 5% above median metric is comparable in terms of precision and exhibits more inherent variability. We emphasize that the choice of phenology metric should be determined by the specific nature of the question being asked. We believe these findings to be useful to the current discussion on phenology metrics of phytoplankton dynamics.

Diel vertical migration arising in a habitat selection game

Predator and prey react to each other, adjusting their behavior to maximize their fitness and optimizing their food intake while keeping their predation risk as low as possible. In a pelagic environment, prey reduce their predation mortality by adopting a diel vertical migration (DVM) strategy, avoiding their predator during their peak performance by finding refuge in deep layers during daylight hours and feeding at the surface during the night. Due to the duality of the interaction between prey and predator, we used a game theory approach to investigate whether DVM can be a suitable strategy for the predator as well as the prey. We formulated three scenarios in plankton ecology in order to address this question. A novel finding is that mixed strategies emerge as optimal over a range of the parameter space, where part of the predator or prey population adopts a DVM while the rest adopt one or other “sit and wait” strategies.

Size structures sensory hierarchy in ocean life.

Survival in aquatic environments requires organisms to have effective means of collecting information from their surroundings through various sensing strategies. In this study, we explore how sensing mode and range depend on body size. We find a hierarchy of sensing modes determined by body size. With increasing body size, a larger battery of modes becomes available (chemosensing, mechanosensing, vision, hearing and echolocation, in that order) while the sensing range also increases. This size-dependent hierarchy and the transitions between primary sensory modes are explained on the grounds of limiting factors set by physiology and the physical laws governing signal generation, transmission and reception. We theoretically predict the body size limits for various sensory modes, which align well with size ranges found in literature. The treatise of all ocean life, from unicellular organisms to whales, demonstrates how body size determines available sensing modes, and thereby acts as a major structuring factor of aquatic life.

Adaptive behaviour, tri-trophic food-web stability and damping of chaos

We examine the effect of adaptive foraging behaviour within a tri-trophic food web with intra-guild predation. The intra-guild prey is allowed to adjust its foraging effort so as to achieve an optimal per capita growth rate in the face of realized feeding, predation risk and foraging cost. Adaptive fitness-seeking behaviour of the intra-guild prey has a stabilizing effect on the tri-trophic food-web dynamics provided that (i) a finite optimal foraging effort exists and (ii) the trophic transfer efficiency from resource to predator via the intra-guild prey is greater than that from the resource directly. The latter condition is a general criterion for the feasibility of intra-guild predation as a trophic mode. Under these conditions, we demonstrate rigorously that adaptive behaviour will always promote stability of community dynamics in the sense that the region of parameter space in which stability is achieved is larger than for the non-adaptive counterpart of the system.

A trait-based approach to ocean ecology

Trait-based ecology merges evolutionary with classical population and community ecology and is a rapidly developing branch of ecology. It describes ecosystems as consisting of individuals rather than species, and characterizes individuals by few key traits that are interrelated through trade-offs. The fundamental rationale is that the spatio-temporal distribution of organisms and their functional role in ecosystems depend on their traits rather than on their taxonomical affiliation. The approach respects that interactions are between individuals, not between species or populations, and in trait-based models ecosystem structure emerges as a result of interactions between individuals and with the environments, rather than being prescribed. It offers an alternative to classical species-centric approaches and has the potential to describe complex ecosystems in simple ways and to assess the effects of environmental change on ecosystem structure and function. Here, we describe the components of the trait-based approach and apply it to describe and model marine ecosystems. Our description is illustrated with multiple examples of life in the ocean from unicellular plankton to fish.