Get up early: Revealing behavioral responses of sandeel to ocean warming using commercial catch data.

Warming of the oceans and shifts in the timing of annual key events are likely to cause behavioral changes in species showing a high degree of site fidelity. While this is well studied in terrestrial systems, there are fewer examples from the marine environment. Sandeel (Ammodytes marinus) is a small eel-shaped teleost fish with strong behavioral attachment to sandy habitats in which they are buried from late summer through winter. When spring arrives, the sandeel emerge to feed during the day for several of months before returning to the sand for overwintering refuge.Using fisheries data from the North Sea, we investigated whether catch rates reflect the timing of emergence and if seasonal patterns are related to temperature and primary production.Catch per unit effort (CPUE) was used to describe sandeel emergence. We developed indicators of the relative timing of the emergence from the winter sand refuge and the subsequent growth period. Different modeling approaches were used to investigate the relationship with bottom temperature and primary production.Variation in emergence behavior was correlated with variation in sea bottom temperature. Warmer years were characterized by earlier emergence. Significant warming over the last three decades was evident in all sandeel habitats in the North Sea throughout most of their adult life history, though no net shift in the phenology of emergence was detected. Minimum temperature during spring was a better predictor of emergence behavior than, for example, degree days.This study emphasizes how temperature-induced changes in behavior may have implications for predators and fisheries of sandeel. The method can be applied to other species for which the timing of exploitation (i.e., fisheries) and species life history are well matched.

Personality-dependent inter- and intraspecific foraging competition in the invasive round goby, Neogobius melanostomus.

This study examines the impact of boldness on foraging competition of the highly invasive round goby Neogobius melanostomus Pallas 1815. Individual risk tolerance, or boldness, was measured as the time to resume movement after a simulated predation strike. Fish that resumed movement faster were categorized as "bold," fish that took more time to resume movement were categorized as "shy" and those that fell in between these two categories were determined to have "intermediate" boldness. Competitive impacts of boldness in N. melanostomus were determined in a laboratory foraging experiment in which interspecific (juvenile Atlantic cod Gadus morhua Linnaeus 1758) and intraspecific (intermediate N. melanostomus) individuals were exposed to either bold or shy N. melanostomus competitors. G. morhua consumed fewer prey when competing with bold N. melanostomus than when competing with shy N. melanostomus, whereas intermediately bold N. melanostomus foraging was not affected by competitor boldness. Bold and shy N. melanostomus consumed similar amounts of prey, and the number of interactions between paired fish did not vary depending on the personality of N. melanostomus individuals. Therefore, intraspecific foraging competition was not found to be personality dependent. This study provides evidence that individual differences in boldness can mediate competitive interactions in N. melanostomus; nonetheless, results also show that competition is also governed by other mechanisms that require further study.

Effects of temperature on physiological performance and behavioral thermoregulation in an invasive fish, the round goby.

Invasive species exert negative impacts on biodiversity and ecosystems on a global scale, which may be enhanced in the future by climate change. Knowledge of how invasive species respond physiologically and behaviorally to novel and changing environments can improve our understanding of which traits enable the ecological success of these species, and potentially facilitate mitigation efforts. We examined the effects of acclimation to temperatures ranging from 5 to 28°C on aerobic metabolic rates, upper temperature tolerance (critical thermal maximum, CTmax), as well as temperature preference (Tpref) and avoidance (Tavoid) of the round goby (Neogobius melanostomus), one of the most impactful invasive species in the world. We show that round goby maintained a high aerobic scope from 15 to 28°C; that is, the capacity to increase its aerobic metabolic rate above that of its maintenance metabolism remained high across a broad thermal range. Although CTmax increased relatively little with acclimation temperature compared with other species, Tpref and Tavoid were not affected by acclimation temperature at all, meaning that round goby maintained a large thermal safety margin (CTmax-Tavoid) across acclimation temperatures, indicating a high level of thermal resilience in this species. The unperturbed physiological performance and high thermal resilience were probably facilitated by high levels of phenotypic buffering, which can make species readily adaptable and ecologically competitive in novel and changing environments. We suggest that these physiological and behavioral traits could be common for invasive species, which would only increase their success under continued climate change.

Weak genetic structure despite strong genomic signal in lesser sandeel in the North Sea.

Sandeels are an ecologically important group of fishes; they are a key part of the food chain serving as food for marine mammals, seabirds and fish. Sandeels are further targeted by a large industrial fishery, which has led to concern about ecosystem effects. In the North Sea, the lesser sandeel Ammodytes marinus is by far the most prevalent species of sandeel in the fishery. Management of sandeel in the North Sea plus the Kattegat is currently divided into seven geographical areas, based on subtle differences in demography, population dynamics and results from simulations of larval dispersal. However, little is known about the underlying genetic population structure. In this study, we used 2,522 SNPs derived from restriction site-associated DNA sequencing (RADseq) typed in 429 fish representing four main sandeel management areas. Our main results showed (a) a lack of a clear spatially defined genetic structure across the majority of genetic markers and (b) the existence of a group of at least 13 SNPs under strong linkage disequilibrium which together separate North Sea sandeel into three haplotype clusters, suggestive of one or more structural variants in the genome. Analyses of the spatial distribution of these putative structural variants suggest at least partial reproductive isolation of sandeel in the western management area along the Scottish coast, supporting a separate management. Our results highlight the importance of the application of a large number of markers to be able to detect weak patterns of differentiation. This study contributes to increasing the genetic knowledge of this important exploited species, and results can be used to improve our understanding of population dynamics and stock structure.

Personality- and size-related metabolic performance in invasive round goby (Neogobius melanostomus).

Differences between individuals in behavioral type (i.e. animal personality) are ecologically and evolutionarily important because they can have significant effects on fitness components such as growth and predation risk. In the present study we are used the invasive round goby (Neogobius melanostomus) from an established population in controlled experiments to examine the relationships among personality, metabolic performance, and growth rate (inferred as size-at-age). Boldness was measured as the time to return to normal behavior after a simulated predator attack, where fish with shorter freezing times were categorized as "bold" and fish with longer times were categorized as "shy." We show that bold fish have significantly higher standard metabolic rate (SMR) than their shy conspecifics, whereas there was no difference between personality types in their maximum metabolic rate (MMR) or aerobic scope (AS). Bold fish furthermore had a smaller size-at-age as compared to shy fish. Together this provides evidence of a metabolic underpinning of personality where the high-SMR bold fish require more resources to sustain basic life functions than their low-SMR shy conspecifics, indicating that bold round goby from established populations with high densities (and high competition for food) pay a price of reduced growth rate.

Evaluating dispersal potential of an invasive fish by the use of aerobic scope and osmoregulation capacity.

Non-indigenous species (NIS) can impact marine biodiversity and ecosystem structure and function. Once introduced into a new region, secondary dispersal is limited by the physiology of the organism in relation to the ambient environment and by complex interactions between a suite of ecological factors such as presence of predators, competitors, and parasites. Early prediction of dispersal potential and future 'area of impact' is challenging, but also a great asset in taking appropriate management actions. Aerobic scope (AS) in fish has been linked to various fitness-related parameters, and may be valuable in determining dispersal potential of aquatic invasive species in novel environments. Round goby, Neogobius melanostomus, one of the most wide-ranging invasive fish species in Europe and North America, currently thrives in brackish and fresh water, but its ability to survive in high salinity waters is unknown to date. We show that AS in round goby is reduced by 30% and blood plasma osmolality increased (indicating reduced capacity for osmoregulation) at salinities approaching oceanic conditions, following slow ramping (5 PSU per week) and subsequent long-term acclimation to salinities ranging between 0 and 30 PSU (8 days at final treatment salinities before blood plasma osmolality measurements, 12-20 additional days before respirometry). Survival was also reduced at the highest salinities yet a significant proportion (61%) of the fish survived at 30 PSU. Reduced physiological performance at the highest salinities may affect growth and competitive ability under oceanic conditions, but to what extent reduced AS and osmoregulatory capacity will slow the current 30 km year-1 rate of advance of the species through the steep salinity gradient from the brackish Baltic Sea and into the oceanic North Sea remains speculative. An unintended natural experiment is in progress to test whether the rate of advance slows down. At the current rate of advance the species will reach the oceanic North Sea by 2018/2019, therefore time for taking preventative action is short.

Marine ecosystem connectivity mediated by migrant-resident interactions and the concomitant cross-system flux of lipids.

Accumulating research argues that migrants influence the functioning and productivity of local habitats and ecosystems along migration routes and potentially drive cross-system energy fluxes of considerable magnitude, yet empirical documentation of local ecological effects and descriptions of the underlying mechanisms are surprisingly rare. In this study, we discovered migrant-resident interactions and substantial cross-system lipid transportation in the transition zone between the Baltic Sea and the North Sea where a resident cod population (predators) was found to interact with a herring population (prey) on a seasonal basis. We traced the lipids, using fatty acid trophic markers (FATM), from the herring feeding grounds in the North Sea to the cod livers in the Western Baltic Sea. Time series analysis of population dynamics indicated that population-level production of cod is positively affected by the herring subsidies. However, the underlying mechanisms were more complicated than anticipated. During the herring season, large cod received most of its dietary lipids from the herring, whereas smaller cod were prevented from accessing the lipid pool due to a mismatch in predator-prey size ratio. Furthermore, while the herring were extremely rich in bulk energy, they were surprisingly poor in a specific functional fatty acid. Hence, our study was the first to illustrate how the magnitude cross-system fluxes of subsidies in migrant-resident systems are potentially constrained by the size structure of the resident predator population and the nutritional quality of the migrants.