Land use change and coastal water darkening drive synchronous dynamics in phytoplankton and fish phenology on centennial timescales.

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.

Trade-offs between risks of predation and starvation in larvae make the shelf break an optimal spawning location for Atlantic bluefin tuna.

Atlantic bluefin tuna (ABT) (Thunnus thynnus) travel long distances to spawn in oligotrophic regions of the Gulf of Mexico (GoM) which suggests these regions offer some unique benefit to offspring survival. To better understand how larval survival varies within the GoM a spatially explicit, Lagrangian, individual-based model was developed that simulates dispersal and mortality of ABT early life stages within realistic predator and prey fields during the spawning periods from 1993 to 2012. The model estimates that starvation is the largest cumulative source of mortality associated with an early critical period. However, elevated predation on older larvae is identified as the main factor limiting survival to late postflexion. As a result, first-feeding larvae have higher survival on the shelf where food is abundant, whereas older larvae have higher survival in the open ocean with fewer predators, making the shelf break an optimal spawning area. The modeling framework developed in this study explicitly simulates both physical and biological factors that impact larval survival and hence could be used to support ecosystem based management efforts for ABT under current and future climate conditions.

Atlantic bluefin tuna spawn early to avoid metabolic meltdown in larvae.

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.

Optimal reproductive phenology under size-dependent cannibalism.

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.

The emotion system promotes diversity and evolvability.

Studies on the relationship between the optimal phenotype and its environment have had limited focus on genotype-to-phenotype pathways and their evolutionary consequences. Here, we study how multi-layered trait architecture and its associated constraints prescribe diversity. Using an idealized model of the emotion system in fish, we find that trait architecture yields genetic and phenotypic diversity even in absence of frequency-dependent selection or environmental variation. That is, for a given environment, phenotype frequency distributions are predictable while gene pools are not. The conservation of phenotypic traits among these genetically different populations is due to the multi-layered trait architecture, in which one adaptation at a higher architectural level can be achieved by several different adaptations at a lower level. Our results emphasize the role of convergent evolution and the organismal level of selection. While trait architecture makes individuals more constrained than what has been assumed in optimization theory, the resulting populations are genetically more diverse and adaptable. The emotion system in animals may thus have evolved by natural selection because it simultaneously enhances three important functions, the behavioural robustness of individuals, the evolvability of gene pools and the rate of evolutionary innovation at several architectural levels.

Effects of the emotion system on adaptive behavior.

A central simplifying assumption in evolutionary behavioral ecology has been that optimal behavior is unaffected by genetic or proximate constraints. Observations and experiments show otherwise, so that attention to decision architecture and mechanisms is needed. In psychology, the proximate constraints on decision making and the processes from perception to behavior are collectively described as the emotion system. We specify a model of the emotion system in fish that includes sensory input, neuronal computation, developmental modulation, and a global organismic state and restricts attention during decision making for behavioral outcomes. The model further includes food competition, safety in numbers, and a fluctuating environment. We find that emergent strategies in evolved populations include common emotional appraisal of sensory input related to fear and hunger and also include frequency-dependent rules for behavioral responses. Focused attention is at times more important than spatial behavior for growth and survival. Spatial segregation of the population is driven by personality differences. By coupling proximate and immediate influences on behavior with ultimate fitness consequences through the emotion system, this approach contributes to a unified perspective on the phenotype, by integrating effects of the environment, genetics, development, physiology, behavior, life history, and evolution.

Seasonal plankton-fish interactions: light regime, prey phenology, and herring foraging.

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.

Size-selective fishing gear and life history evolution in the Northeast Arctic cod.

Industrial fishing has been identified as a cause for life history changes in many harvested stocks, mainly because of the intense fishing mortality and its size-selectivity. Because these changes are potentially evolutionary, we investigate evolutionarily stable life-histories and yield in an energy-allocation state-dependent model for Northeast Arctic cod Gadus morhua. We focus on the evolutionary effects of size-selective fishing because regulation of gear selectivity may be an efficient management tool. Trawling, which harvests fish above a certain size, leads to early maturation except when fishing is low and confined to mature fish. Gillnets, where small and large fish escape, lead to late maturation for low to moderate harvest rates, but when harvest rates increase maturation age suddenly drops. This is because bell-shaped selectivity has two size-refuges, for fish that are below and above the harvestable size-classes. Depending on the harvest rate it either pays to grow through the harvestable slot and mature above it, or mature small below it. Sustainable yield on the evolutionary time-scale is highest when fishing is done by trawling, but only for a small parameter region. Fishing with gillnets is better able to withstand life-history evolution, and maintains yield over a wider range of fishing intensities.

The evolution of spawning migrations: state dependence and fishing-induced changes.

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.

Meta-ecosystems and biological energy transport from ocean to coast: the ecological importance of herring migration.

Ecosystems are not closed, but receive resource subsidies from other ecosystems. Energy, material and organisms are moved between systems by physical vectors, but migrating animals also transport resources between systems. We report on large scale energy transport from ocean to coast by a migrating fish population, the Norwegian spring-spawning (NSS) herring Clupea harengus. We observe a rapid body mass increase during parts of the annual, oceanic feeding migration and we use a bioenergetics model to quantify energy consumption. The model predicts strong seasonal variation in food consumption with a marked peak in late May to July. The copepod Calanus finmarchicus is the most important prey and 23 x 10(6) tones (wet weight) of C. finmarchicus is consumed annually. The annual consumption-biomass ratio is 5.2. During the feeding migration 17% of consumed energy is converted to body mass. The biomass transported to the coast and left as reproductive output is estimated from gonad weight and is about 1.3 x 10(6) tones for the current population. This transport is to our knowledge the world's largest flux of energy caused by a single population. We demonstrate marked temporal variation in transport during the last century and discuss the effects of NSS herring in the ocean, as a major consumer, and at the coast, where eggs and larvae are important for coastal predators. In particular, we suggest that the rapid decline of lobster Homarus gammarus landings in Western Norway during the 1960s was related to the collapse of NSS herring. We also discuss spatial variation in energy transport caused by changed migration patterns. Both climate and fisheries probably triggered historical changes in the migration patterns of NSS herring. New migration routes emerge at the level of individuals, which in turn determines where resources are gathered and delivered, and therefore, how meta-ecosystems function.