Predicting future thermal habitat suitability of competing native and invasive fish species: from metabolic scope to oceanographic modelling

Global increase in sea temperatures has been suggested to facilitate the incoming and spread of tropical invaders. The increasing success of these species may be related to their higher physiological performance compared with indigenous ones. Here, we determined the effect of temperature on the aerobic metabolic scope (MS) of two herbivorous fish species that occupy a similar ecological niche in the Mediterranean Sea: the native salema (Sarpa salpa) and the invasive marbled spinefoot (Siganus rivulatus). Our results demonstrate a large difference in the optimal temperature for aerobic scope between the salema (21.8°C) and the marbled spinefoot (29.1°C), highlighting the importance of temperature in determining the energy availability and, potentially, the distribution patterns of the two species. A modelling approach based on a present-day projection and a future scenario for oceanographic conditions was used to make predictions about the thermal habitat suitability (THS, an index based on the relationship between MS and temperature) of the two species, both at the basin level (the whole Mediterranean Sea) and at the regional level (the Sicilian Channel, a key area for the inflow of invasive species from the Eastern to the Western Mediterranean Sea). For the present-day projection, our basin-scale model shows higher THS of the marbled spinefoot than the salema in the Eastern compared with the Western Mediterranean Sea. However, by 2050, the THS of the marbled spinefoot is predicted to increase throughout the whole Mediterranean Sea, causing its westward expansion. Nevertheless, the regional-scale model suggests that the future thermal conditions of Western Sicily will remain relatively unsuitable for the invasive species and could act as a barrier for its spread westward. We suggest that metabolic scope can be used as a tool to evaluate the potential invasiveness of alien species and the resilience to global warming of native species.

Evaluating machine-learning techniques for recruitment forecasting of seven North East Atlantic fish species

The effect of different factors (spawning biomass, environmental conditions) on recruitment is a subject of great importance in the management of fisheries, recovery plans and scenario exploration. In this study, recently proposed supervised classification techniques, tested by the machine-learning community, are applied to forecast the recruitment of seven fish species of North East Atlantic (anchovy, sardine, mackerel, horse mackerel, hake, blue whiting and albacore), using spawning, environmental and climatic data. In addition, the use of the probabilistic flexible naive Bayes classifier (FNBC) is proposed as modelling approach in order to reduce uncertainty for fisheries management purposes. Those improvements aim is to improve probability estimations of each possible outcome (low, medium and high recruitment) based in kernel density estimation, which is crucial for informed management decision making with high uncertainty. Finally, a comparison between goodness-of-fit and generalization power is provided, in order to assess the reliability of the final forecasting models. It is found that in most cases the proposed methodology provides useful information for management whereas the case of horse mackerel is an example of the limitations of the approach. The proposed improvements allow for a better probabilistic estimation of the different scenarios, i.e. to reduce the uncertainty in the provided forecasts.

An innovative statistical approach to constructing a readily comprehensible food web for a demersal fish community

Many food webs are so complex that it is difficult to distinguish the relationships between predators and their prey. We have therefore developed an approach that produces a food web which clearly demonstrates the strengths of the relationships between the predator guilds of demersal fish and their prey guilds in a coastal ecosystem. Subjecting volumetric dietary data for 35 abundant predators along the lower western Australia coast to cluster analysis and the SIMPROF routine separated the various species x length class combinations into 14 discrete predator guilds. Following nMDS ordination, the sequence of points for these predator guilds represented a 'trophic' hierarchy. This demonstrated that, with increasing body size, several species progressed upwards through this hierarchy, reflecting a marked change in diet, whereas others remained within the same guild. A novel use of cluster analysis and SIMPROF then identified each group of prey that was ingested in a common pattern across the full suite of predator guilds. This produced 12 discrete groups of taxa (prey guilds) that each typically comprised similar ecological/functional prey, which were then also aligned in a hierarchy. The hierarchical arrangements of the predator and prey guilds were plotted against each other to show the percentage contribution of each prey guild to the diet of each predator guild. The resultant shade plot demonstrates quantitatively how food resources are spread among the fish species and revealed that two prey guilds, one containing cephalopods and teleosts and the other small benthic/epibenthic crustaceans and polychaetes, were consumed by all predator guilds.

Future fish distributions constrained by depth in warming seas

European continental shelf seas have experienced intense warming over the past 30 years1. In the North Sea, fish have been comprehensively monitored throughout this period and resulting data provide a unique record of changes in distribution and abundance in response to climate change2, 3. We use these data to demonstrate the remarkable power of generalized additive models (GAMs), trained on data earlier in the time series, to reliably predict trends in distribution and abundance in later years. Then, challenging process-based models that predict substantial and ongoing poleward shifts of cold-water species4, 5, we find that GAMs coupled with climate projections predict future distributions of demersal (bottom-dwelling) fish species over the next 50 years will be strongly constrained by availability of habitat of suitable depth. This will lead to pronounced changes in community structure, species interactions and commercial fisheries, unless individual acclimation or population-level evolutionary adaptations enable fish to tolerate warmer conditions or move to previously uninhabitable locations.

Future fish distributions constrained by depth in warming seas

European continental shelf seas have experienced intense warming over the past 30 years1. In the North Sea, fish have been comprehensively monitored throughout this period and resulting data provide a unique record of changes in distribution and abundance in response to climate change2, 3. We use these data to demonstrate the remarkable power of generalized additive models (GAMs), trained on data earlier in the time series, to reliably predict trends in distribution and abundance in later years. Then, challenging process-based models that predict substantial and ongoing poleward shifts of cold-water species4, 5, we find that GAMs coupled with climate projections predict future distributions of demersal (bottom-dwelling) fish species over the next 50 years will be strongly constrained by availability of habitat of suitable depth. This will lead to pronounced changes in community structure, species interactions and commercial fisheries, unless individual acclimation or population-level evolutionary adaptations enable fish to tolerate warmer conditions or move to previously uninhabitable locations.

Impacts of fisheries on plankton community structure

There has been much debate on the extent to which resource availability (bottom-up) versus predation pressure from fish (top-down) modulates the dynamics of plankton in marine systems. Physico/chemical bottom-up forcing has been considered to be the main mechanism structuring marine ecosystems, although some field observations and empirical correlations support top-down modulation. Models have indicated possible feedback loops to the plankton and other studies have interpreted a grazing impact from long-term changes in fish stocks. In freshwater systems, evidence for top-down forcing by fish and trophic cascading is well documented. First, evidence for equivalent top-down effects in the marine environment is presented, with an overview of relevant publications. In the second part, time series, averaged for the North Sea (when possible from 1948 to 1997), of fish catch, recruitment, and spawning stock biomass are related to the abundance of species or larger groupings of zooplankton and phytoplankton from the Continuous Plankton Recorder survey and selected environmental parameters. Preliminary analysis suggests that there is strong interaction between different fish species and the plankton and that the fishery, through top-down control, may at times be an important contributor to changes in the North Sea ecosystem.

Ranking of length-class seasonal and regional effects on dietary compositions of the co-occurring Pagrus auratus (Sparidae) and Pseudocaranx georgianus (Carangidae)

Using an effective combination of multivariate testing and ordination analyses, this study compares the extents to which the diets of two co-occurring fish species (Pagrus auratus and Pseudocaranx georgianus) are related to body size (length class), season and region and the rank order importance of those effects. Thus, volumetric dietary compositions were determined for these species on the lower west coast of Australia, where both are abundant, and for P. auratus from the mid west coast and P. georgianus from the south coast. The diet of P. auratus on the lower west coast was strongly related to body size and slightly less to season. With increasing body size, its diet shifted from predominantly ophiuroids to larger prey, such as brachyuran crabs, teleosts, echinoids and ultimately asteroids, probably reflecting a shift from foraging over soft sediments to areas over and around reefs. Seasonal changes on the lower west coast were restricted mainly to small P. auratus, while larger fish underwent seasonal changes further north. Analyses using a common size range of medium to larger P. auratus demonstrated that dietary composition differed more between regions than seasons. The relationships between diet and length class of P. georgianus on both the lower west and south coasts were less pronounced than for P. auratus and seasonal changes were restricted to the south coast, where amphipod consumption increased markedly in summer. The diet of P. georgianus was related far more to region than length class and season, with more small teleosts, small crabs, carideans and littorinids and less amphipods, isopods and small bivalves being ingested on the lower west than south coasts. Although crabs and teleosts were important typifying prey of P. auratus and P. georgianus, when co-occurring, the former predator tended to ingest greater volumes of larger and often less mobile prey. This reflects differences in dentition, jaw morphology and feeding behaviour and reduces the potential for competition for food resources. The results imply that P. auratus and P. georgianus are opportunistic feeders and that the effects of length class, season and region on dietary composition and their rank orders can vary markedly between species and for length class and season between regions for the same species.

Severe tissue damage in Atlantic cod larvae under increasing ocean acidification

Ocean acidification, caused by increasing atmospheric concentrations of CO2 (refs 1-3), is one of the most critical anthropogenic threats to marine life. Changes in seawater carbonate chemistry have the potential to disturb calcification, acid-base regulation, blood circulation and respiration, as well as the nervous system of marine organisms, leading to long-term effects such as reduced growth rates and reproduction(4,5). In teleost fishes, early life-history stages are particularly vulnerable as they lack specialized internal pH regulatory mechanisms(6,7). So far, impacts of relevant CO2 concentrations on larval fish have been found in behaviour(8,9) and otolith size(10,11), mainly in tropical, non-commercial species. Here we show detrimental effects of ocean acidification on the development of a mass-spawning fish species of high. commercial importance. We reared Atlantic cod larvae at three levels of CO2, (1) present day, (2) end of next century and (3) an extreme, coastal upwelling scenario, in a long-term (2; months) mesocosm experiment. Exposure to CO2 resulted in severe to lethal tissue damage in many internal organs, with the degree of damage increasing with CO2 concentration. As larval survival is the bottleneck to recruitment, ocean acidification has the potential to act as an additional source of natural mortality, affecting populations of already exploited fish stocks.

Biodiversity and ecosystems: Change at the community level

Some commercial fish species of the northeast Atlantic Ocean have relocated in response to warming. The impact of warming on marine assemblages in the region may already be much greater than appreciated, however, with over 70% of common demersal fish species responding through changes in abundance, rather than range. The northeast Atlantic Ocean is one of the most productive marine ecoregions in the world with a substantial commercial fishery. It is also a region that has undergone particularly rapid warming over the past 50 years, up to four times faster than the global average1. Compared with other marine regions worldwide, the biological response in the northeast Atlantic Ocean has been particularly dramatic, reflecting this rapid warming. Studies have documented biogeographical movements in marine plankton of over 1,000 km northwards2 and advances in the onset of key life-history events by six to eight weeks3. In addition, there has been limited evidence of distributional shifts in some fish species along latitudinal and depth gradients in response to warming4, 5. Writing in Current Biology, Stephen Simpson and colleagues6 present the most comprehensive analysis so far of the impact of warming on commercially important European continental-shelf fish species in the region, and in doing so show that there has been a profound reorganization of local communities.

Transient dynamics of an altered large marine ecosystem

Overfishing of large-bodied benthic fishes and their subsequent population collapses on the Scotian Shelf of Canada’s east coast1, 2 and elsewhere3, 4 resulted in restructuring of entire food webs now dominated by planktivorous, forage fish species and macroinvertebrates. Despite the imposition of strict management measures in force since the early 1990s, the Scotian Shelf ecosystem has not reverted back to its former structure. Here we provide evidence of the transient nature of this ecosystem and its current return path towards benthic fish species domination. The prolonged duration of the altered food web, and its current recovery, was and is being governed by the oscillatory, runaway consumption dynamics of the forage fish complex. These erupting forage species, which reached biomass levels 900% greater than those prevalent during the pre-collapse years of large benthic predators, are now in decline, having outstripped their zooplankton food supply. This dampening, and the associated reduction in the intensity of predation, was accompanied by lagged increases in species abundances at both lower and higher trophic levels, first witnessed in zooplankton and then in large-bodied predators, all consistent with a return towards the earlier ecosystem structure. We conclude that the reversibility of perturbed ecosystems can occur and that this bodes well for other collapsed fisheries.

Organ damage in Atlantic herring larvae as a result of ocean acidification

The dissolution of anthropogenically emitted excess carbon dioxide lowers the pH of the world's ocean water. The larvae of mass spawning marine fishes may be particularly vulnerable to such ocean acidification (OA), yet the generality of earlier results is unclear. Here we show the detrimental effects of OA on the development of a commercially important fish species, the Atlantic herring (Clupea harengus). Larvae were reared at three levels of CO2: today (0.0385 kPa), end of next century (0.183 kPa), and a coastal upwelling scenario (0.426 kPa), under near-natural conditions in large outdoor tanks. Exposure to elevated CO2 levels resulted in stunted growth and development, decreased condition, and severe tissue damage in many organs, with the degree of damage increasing with CO2 concentration. This complements earlier studies of OA on Atlantic cod larvae that revealed similar organ damage but at increased growth rates and no effect on condition.

Within-Otolith Variability in Chemical Fingerprints: Implications for Sampling Designs and Possible Environmental Interpretation

Largely used as a natural biological tag in studies of dispersal/connectivity of fish, otolith elemental fingerprinting is usually analyzed by laser ablation-inductively coupled plasma-mass spectrometry (LA-ICP-MS). LA-ICP-MS produces an elemental fingerprint at a discrete time-point in the life of a fish and can generate data on within-otolith variability of that fingerprint. The presence of within-otolith variability has been previously acknowledged but not incorporated into experimental designs on the presumed, but untested, grounds of both its negligibility compared to among-otolith variability and of spatial autocorrelation among multiple ablations within an otolith. Here, using a hierarchical sampling design of spatial variation at multiple scales in otolith chemical fingerprints for two Mediterranean coastal fishes, we explore: 1) whether multiple ablations within an otolith can be used as independent replicates for significance tests among otoliths, and 2) the implications of incorporating within-otolith variability when assessing spatial variability in otolith chemistry at a hierarchy of spatial scales (different fish, from different sites, at different locations on the Apulian Adriatic coast). We find that multiple ablations along the same daily rings do not necessarily exhibit spatial dependency within the otolith and can be used to estimate residual variability in a hierarchical sampling design. Inclusion of within-otolith measurements reveals that individuals at the same site can show significant variability in elemental uptake. Within-otolith variability examined across the spatial hierarchy identifies differences between the two fish species investigated, and this finding leads to discussion of the potential for within-otolith variability to be used as a marker for fish exposure to stressful conditions. We also demonstrate that a 'cost'-optimal allocation of sampling effort should typically include some level of within-otolith replication in the experimental design. Our findings provide novel evidence to aid the design of future sampling programs and improve our general understanding of the mechanisms regulating elemental fingerprints.

DIESE Final Report

The DIESE program (Determination of relevant Indicators for Environmental monitoring: A Strategy for Europe) brought together seven French and British research teams, a private company and the agencies responsible for the management of water bodies of the two countries (ONEMA and the Environmental Agency) in a joint effort to document the ecotoxicological effects related to the presence of chemicals in the environment. To contribute to a better understanding and management of the environment, the program has expanded its efforts to (1) use existing knowledge, or new information acquired during the research program, to identify important biological problems affecting wildlife, (2) increase our understanding of toxicological mechanisms involved and thus be able to identify the causes of the identified dysfunctions and (3) to hone our expertise and vigilance systems in order to better monitor changes in the environment and make appropriate diagnoses. The first part of the program identified clear biological effects, and using biological tests representative of the mechanisms of action of compounds, identified the responsible compounds present in the environment. In connection with the feminization observed in many fish species in European streams, a search for estrogenic and anti-androgenic compounds was conducted. A new test identifying estrogenic compounds has been developed in roach and the ER-Calux test for anti-androgenic effects has been implemented. The results showed that, in addition to biocides such as triclosan and chlorophène, many aromatic hydrocarbon compounds are likely to disturb the physiology of living organisms by interacting with the androgen receptor. Six of these were identified in sediment extracts: benzanthrone, fluoranthene, 1,2- benzodiphenylene sulfide, benzo[a]pyrene, benz[a] anthracene, and 9-phenylcarbazole. The second part of the program aimed at documenting and understanding the mechanisms of action of chemicals leading to physiological changes. This work represents a particular challenge when dealing with molluscs, as knowledge about their physiology and endocrinology is still fragmentary. Thus, new technologies including metabolomic and transcriptomic analyses have been implemented in order to obtain a comprehensive picture of the effects on molluscs. Metabolomic research demonstrated that estrogenic compounds are able to alter the metabolism of eicosanoids and amines, while transcriptomic strategies identified genes whose expression is altered in intersex clams. Because these genes mainly appear as “male” genes, the results suggest that these profound physiological changes result from demasculinisation of male clams. Proteomic studies have also been carried out to elucidate the mechanisms of action of pollutants on fish physiology. These studies generally included a set of molecular marker measurements in an integrative and ecological perspective. The results showed that not only male fish physiology is altered but also female reproductive status is impaired. Moreover, it appeared that other alterations of the fish endocrine system, such as androgenic effects, are at work and that the immune system is also subject to chemical pressure including effects from environmental estrogens. Notably, the immune system, like the endocrine system, seems to show periods of particular sensitivity during development. Measurements on growth and on the general metabolism emphasize the importance of environmental conditions in the physiology of aquatic organisms and in particular the inter-site variability due to temperature,hypoxic conditions, and fish development strategies. They thus provide a unique perspective that allow us to better understand the context and consequences of natural conditions on the population. In a third part of the program, the research conducted had the objective of developing and testing a biomarker strategy to support the environmental management methodologies. Two lanes of specific studies have been followed. The first was to implement, over all or part of the study area, robust biomarkers to establish maps that highlight the water bodies at risk and provide information on sources of compounds and associated disturbances. The second part of the work aimed at exploring methodologies to take advantage of biomarker measurements and to integrate them in a very simple and clear index. Partial or comprehensive maps of the Channel area were produced to report the presence of mutagenic or anti-androgenic compounds in the sediments, intersex fish and clams, and imposex. These maps may remain to be completed and work will be necessary to confront this information in order to learn relevant lessons for management of the environment, a goal that the DIESE program has contributed to by providing some necessary and original information.