Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles.

Nitrogen ([Formula: see text]) fixation by heterotrophic bacteria associated with sinking particles contributes to marine N cycling, but a mechanistic understanding of its regulation and significance are not available. Here we develop a mathematical model for unicellular heterotrophic bacteria growing on sinking marine particles. These bacteria can fix [Formula: see text] under suitable environmental conditions. We find that the interactive effects of polysaccharide and polypeptide concentrations, sinking speed of particles, and surrounding [Formula: see text] and [Formula: see text] concentrations determine the [Formula: see text] fixation rate inside particles. [Formula: see text] fixation inside sinking particles is mainly fueled by [Formula: see text] respiration rather than [Formula: see text] respiration. Our model suggests that anaerobic processes, including heterotrophic [Formula: see text] fixation, can take place in anoxic microenvironments inside sinking particles even in fully oxygenated marine waters. The modelled [Formula: see text] fixation rates are similar to bulk rates measured in the aphotic ocean, and our study consequently suggests that particle-associated heterotrophic [Formula: see text] fixation contributes significantly to oceanic [Formula: see text] fixation.

Co-adaptive behavior of interacting populations in a habitat selection game significantly impacts ecosystem functions.

Individuals of different interacting populations often adjust to prevailing conditions by changing their behavior simultaneously, with consequences for trophic relationships throughout the system. While we now have a good theoretical understanding of how individuals adjust their behavior, the population dynamical consequences of co-adaptive behaviors are rarely described. Further, mechanistic descriptions of ecosystem functions are based on population models that seldom take behavior into account. Here, we present a model that combines the population dynamics and adaptive behavior of organisms of two populations simultaneously. We explore how the Nash equilibrium of a system - i.e. the optimal behavior of its constituent organisms - can shape population dynamics, and conversely how population dynamics impact the Nash equilibrium of the system. We illustrate this for the case of diel vertical migration (DVM), the daily movement of marine organisms between food-depleted but safe dark depths and more risky nutrition-rich surface waters. DVM represents the archetypal example of populations choosing between a foraging arena (the upper sunlit ocean) and a refuge (the dark depths). We show that population sizes at equilibrium are significantly different if organisms can adapt their behavior, and that optimal DVM behaviors within the community vary significantly if population dynamics are considered. As a consequence, ecosystem function estimates such as trophic transfer efficiency and vertical carbon export differ greatly when fitness seeking behavior is included. Ignoring the role of behavior in multi-trophic population modeling can potentially lead to inaccurate predictions of population biomasses and ecosystem functions.

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.

Predator-Prey Games in Multiple Habitats Reveal Mixed Strategies in Diel Vertical Migration.

Prey and predators continuously react to each other and to their environment, adjusting their behavior to maximize their fitness. In a pelagic environment, organisms can optimize their fitness by performing diel vertical migrations. We applied a game-theoretic approach to investigate the emergent patterns of optimal habitat selection strategies in a multiple-habitat arena. Our setup allows both players to choose their position at day and at night in the water column. The model reproduces features of vertical migrations observed in nature, including residency at depth or at the surface, vertical migrations, mixed strategies, and bimodal distributions within a population. The mixed strategies appear as a consequence of frequency-dependent processes and not of any intraspecies difference between individuals. The model also reveals a curious feature where natural selection on individuals can provoke distinct regime shifts and precipitate an irreversible collapse in fitness. In the case presented here, the increasing voracity of the predator triggers a behavioral shift in the prey, reducing the fitness of all members of the predator population.

Climate change has altered zooplankton-fuelled carbon export in the North Atlantic.

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.

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

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 cycling­a "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.

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.

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.