To predict shifts in phenology and distribution of organisms we need to understand how survival through early life stages depends on environmental conditions. Here, we present a mechanistic model of ...development, feeding and bioenergetics of early life stages in bluefin tuna and predict the optimal time of the year for them to be born. We find that the availability of prey, particularly nauplii, is sufficient for fast growth in tuna larvae while temperature is moderate during midsummer, but not when temperatures increase later in summer. High temperatures benefit egg and yolk‐sac stages, but the metabolic needs of feeding larvae are hard to sustain during the warmest periods. Heatwaves, such as the one in 2003, increase larval survival potential, but shorten the viable part of the season for the larvae. Atlantic bluefin tuna is a large, highly migratory marine top predator that spawns while temperatures are rising, but before the heat leads to a metabolic meltdown in larvae. This means that food resources modulate how temperature change shifts optimal phenology.
Predatory fish structure communities through prey pursuit and consumption and, in many marine systems, the gadoids are particularly important. These predators have flexible feeding behaviours and ...often feed on large prey items. Digestion times of large prey are usually longer than handling times, and gut processing limits feeding rate at high prey density. Optimizing the gut content mix can therefore be an important behavioural strategy. Here, we develop a foraging model that incorporates gut processing and use the model to disentangle internal and external limitations on feeding in the omnivorous cod (Gadus morhua, Gadidae). We extend the traditional definition of prey profitability to consider prey digestive quality, which we quantify for prey of Northeast Atlantic cod populations. We find an important role for gut limitation; within a range of ecologically relevant temperatures and prey densities, predicted feeding rates were strongly reduced compared to feeding constrained by external factors only, and the optimal diet composition under gut limitation differed from predictions from traditional foraging theory. Capelin, a main prey of Northeast Arctic cod, had the highest digestive quality of all prey across ecosystems, but the cold temperatures in the Barents Sea strongly limited feeding rate by slowing down digestion. Baltic cod fed on a higher proportion of poor‐quality prey compared to the other populations, contributing to its slow growth in relation to water temperature. Gut limitation is particularly important to consider in foraging models for fish with many alternative prey species or fish occupying cold waters where digestion is slow.
Intra‐cohort cannibalism is an example of a size‐mediated priority effect. If early life stages cannibalize slightly smaller individuals, then parents face a trade‐off between breeding at the best ...time for larval growth or development and predation risk from offspring born earlier. This game‐theoretic situation among parents may drive adaptive reproductive phenology toward earlier breeding. However, it is not straightforward to quantify how cannibalism affects seasonal egg fitness or to distinguish emergent breeding phenology from alternative adaptive drivers. Here, we devise an age‐structured game‐theoretic mathematical model to find evolutionary stable breeding phenologies. We predict how size‐dependent cannibalism acting on eggs, larvae, or both changes emergent breeding phenology and find that breeding under inter‐cohort cannibalism occurs earlier than the optimal match to environmental conditions. We show that emergent breeding phenology patterns at the level of the population are sensitive to the ontogeny of cannibalism, that is, which life stage is subject to cannibalism. This suggests that the nature of cannibalism among early life stages is a potential driver of the diversity of reproductive phenologies seen across taxa and may be a contributing factor in situations where breeding occurs earlier than expected from environmental conditions.
Cannibalism introduces a trade‐off between breeding at the optimal time in the season and increased predation risk from offspring born earlier. We predict how size‐dependent cannibalism on eggs, larvae, or both changes emergent breeding phenology and find breeding that occurs earlier than the optimal match to environmental conditions. We show that emergent breeding phenology patterns at the level of the population are sensitive to the ontogeny of cannibalism.
Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another ...predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.
Spatial overlap between predator and prey is a prerequisite for predation, but the degree of overlap is not necessarily proportional to prey consumption. This is because many of the behavioural ...processes that precede ingestion are non‐linear and depend on local prey densities. In aquatic environments, predators and prey distribute not only across a surface, but also vertically in the water column, adding another dimension to the interaction. Integrating and simplifying behavioural processes across space and time can lead to systematic biases in our inference about interaction strength. To recognise situations when this may occur, we must first understand processes underlying variation in prey consumption by individuals. Here we analysed the diet of a major predator in the Barents Sea, the Atlantic cod Gadus morhua, aiming to understand drivers of variation in cod's feeding on its main prey capelin Mallotus villosus. Cod and capelin only partly share habitats, as cod mainly reside near the seafloor and capelin inhabit the free water masses. We used data on stomach contents from ~2000 cod individuals and their surrounding environment collected over 12 years, testing hypotheses on biological and physical drivers of variation in cod's consumption of capelin, using generalized additive models. Specifically, effects of capelin abundance, capelin depth distribution, bottom depth and cod abundance on capelin consumption were evaluated at a resolution scale of 2 km. We found no indication of food competition as cod abundance had no effect on capelin consumption. Capelin abundance had small effects on consumption, while capelin depth distribution was important. Cod fed more intensively on capelin when capelin came close to the seafloor, especially at shallow banks and bank edges. Spatial overlap as an indicator for interaction strength needs to be evaluated in three dimensions instead of the conventional two when species are partly separated in the water column.
Most mesopelagic fish are small planktivores that migrate up at nightfall to feed in the safety of darkness and descend to depth at dawn to escape visual predators. However, the trophic roles can ...reverse since mesopelagic fishes also predate eggs and larvae of their predators. We use the Atlantic bluefin tuna as a model species to test the hypothesis that fishes in the open ocean synchronize spawning to moon‐lit nights (when mesopelagic fishes avoid near‐surface waters) to increase offspring fitness. Our analysis over two decades of field observations shows that tuna spawn most intensively the week before full moon. This fits predictions from a mechanistic model where spawning around full moon increases offspring fitness by two orders of magnitude due to low predation from mesopelagic fishes. Circalunar patterns of food availability can also favor fitness of offspring spawned the days before full moon. Our findings suggest that mesopelagic fishes may have an important impact on pelagic fish through predation of early life stages and cause an evolutionary drive to synchronize spawning to the lunar cycle.
When prey and predator are seasonal migrants, encounters depend on migration phenologies and environmental constraints on predation. Here we investigate the relative contribution of seasonality in ...irradiance and prey abundance in shaping the rapid seasonal body condition increase of a migrating predator searching visually for its prey: the Norwegian spring-spawning herring, Clupea harengus, feeding on the copepod Calanus finmarchicus. Two main seasonal pulses of prey are available to herring: (1) the parent generation of C. finmarchicus, with peak abundance in March—April, which appear too early to cause the main increase in herring condition; and (2) the abundant offspring generation of C. finmarchicus, with peak abundance in June—July, too late to explain the main increase in body condition. However, a mechanistic model of ingestion rate, including both solar irradiance and prey abundance, predicted seasonal food intake in good accordance with observed herring body condition. This suggests that the seasonality in herring foraging and energy storage is closely linked to the return of longer days in spring, and less dependent on a match or mismatch with seasonal peaks in abundance of their zooplankton prey. Consequently, light related constraints on foraging may make visually searching predators at high latitudes resilient to changes and fluctuations in prey phenology and abundance, but vulnerable to changes in the light regime, such as water clarity.
Caught in broad daylight Aarflot, Johanna M.; Aksnes, Dag L.; Opdal, Anders F. ...
Limnology and oceanography,
05/2019, Volume:
64, Issue:
3
Journal Article
Peer reviewed
Open access
For visual predators, sufficient light is critical for prey detection and capture. Because light decays exponentially with depth in aquatic systems, vertical movement has become a widespread strategy ...among zooplankton for avoiding visual predation. However, topographical features such as seamounts have been shown to block their descent, trapping them in illuminated waters with potential feeding benefits for visually searching fish. Here, we present an extensive and previously unpublished dataset on the vertical distribution of zooplankton in the topographically rugged Barents Sea, a continental shelf region hosting some of the largest fish stocks in the world. By modeling the ambient light exposure of zooplankton in relation to the bathymetry, we find support for a similar blockage mechanism. During daytime, zooplankton are exposed to four orders of magnitude more light above shallow banks than in the deeper water surrounding the banks. We show that zooplankton depth distributions are highly related to zooplankton size and that the bottom constrains the vertical distributions. Consequently, zooplankton remain in the planktivores’ visual feeding habitat over the banks but not in deeper areas. Bottom topography and light absorbance are significant determinants of the seascape ecology across continental shelves with heterogeneous bathymetry.
At high latitudes, the suitable window for timing reproductive events is particularly narrow, promoting tight synchrony between trophic levels. Climate change may disrupt this synchrony due to ...diverging responses to temperature between, for example, the early life stages of higher trophic levels and their food resources. Evidence for this is equivocal, and the role of compensatory mechanisms is poorly understood. Here, we show how a combination of ocean warming and coastal water darkening drive long‐term changes in phytoplankton spring bloom timing in Lofoten Norway, and how spawning time of Northeast Arctic cod responds in synchrony. Spring bloom timing was derived from hydrographical observations dating back to 1936, while cod spawning time was estimated from weekly fisheries catch and roe landing data since 1877. Our results suggest that land use change and freshwater run‐off causing coastal water darkening has gradually delayed the spring bloom up to the late 1980s after which ocean warming has caused it to advance. The cod appear to track phytoplankton dynamics by timing gonadal development and spawning to maximize overlap between offspring hatch date and predicted resource availability. This finding emphasises the importance of land–ocean coupling for coastal ecosystem functioning, and the potential for fish to adapt through phenotypic plasticity.
In temperate and Arctic areas, land‐use change together with a warmer and wetter climate promote plant and forest growth making freshwaters browner as more degraded plant‐litter end up as coloured dissolved organic matter. Although freshwater drain to the coast, the downstream consequences in coastal marine ecosystems are poorly understood. Here, we propose that a century of afforestation in Northern Europe has caused more than a month delay in spawning time for the Northeast Atlantic cod. The two are connected through a cascade of physical and biological processes, starting with plant growth on land moving through browner lakes and rivers causing decreased light penetration in coastal waters that postpone the phytoplankton spring bloom and culminate in an adaptive adjustment of spawning time for the cod.
Individuals migrate to exploit heterogeneities between spatially separated environments to modulate growth, survival, or reproduction. We devised a bioenergetics model to investigate the evolution of ...migration distance and its dependence on individual states. Atlantic cod Gadus morhua ranges from sedentary populations to stocks that migrate several thousand kilometers annually. We focused on the Northeast Arctic cod stock, which migrates south to spawn. A linear relationship between migration distance and the expected survival of offspring was assumed, here understood as the prospects for future survival and development that a fertilized egg faces at a particular spawning location. Reasons for why it may increase southward include warmer water that increases development rates, and thereby survival, along the pelagic drift trajectory. In the model, ingested energy can either be allocated to growth or stored for migration and reproduction. When migrating, individuals forgo foraging opportunities and expend energy. Optimal energy allocation and migration strategies were found using state-dependent optimization, with body length, age, condition, and current food availability as individual states. For both a historical and contemporary fishing regime we modeled two behaviors: (1) homing cod returning to the same spawning site each year and (2) roaming cod with no such constraints. The model predicted distinct regions of locally high spawning stock biomass. Large individuals in good condition migrated farthest, and these also tended to mature later in life. The roaming cod spread farther south as they grew larger and older. Homing cod did not have this freedom, and spawning was generally concentrated along a narrower stretch of the coastline. Under contemporary fishing, individuals matured earlier at a smaller size, had shorter migrations, spawned over a contracted geographical range, and tended to be in poorer condition. The effects were most pronounced for the homing behavior.
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