Synergistic Effects of Climate and Fishing in a Marine Ecosystem

Current climate change and overfishing are affecting the productivity and structure of marine ecosystems. This situation is unprecedented for the marine biosphere and it is essential to understand the mechanisms and pathways by which ecosystems respond. We report that climate change and overfishing are likely to be responsible for a rapid restructuring of a highly productive marine ecosystem with effects throughout the pelagos and the benthos. In the mid-1980s, climate change, consequent modifications in the North Sea plankton, and fishing, all reduced North Sea cod recruitment. In this region, production of many benthic species respond positively and immediately to temperature. Analysis of a long-term, spatially extensive biological (plankton and cod) and physical (sea surface temperature) dataset suggests that synchronous changes in cod numbers and sea temperature have established an extensive trophic cascade favoring lower trophic level groups over economic fisheries. A proliferation of jellyfish that we detect may signal the climax of these changes. This modified North Sea ecology may provide a clear indication of the synergistic consequences of coincident climate change and overfishing. The extent of the ecosystem restructuring that has occurred in the North Sea suggests we are unlikely to reverse current climate and human-induced effects through ecosystem resource management in the short term. Rather, we should understand and adapt to new ecological regimes. This implies that fisheries management policies will have to be fully integrated with the ecological consequences of climate change to prevent a similar collapse in an exploited marine ecosystem elsewhere. Author Contributions  RRK conceived the project and GB analysed the data. RRK, GB and JAL co-wrote the paper.     

How small can the difference among competitors be for coexistence to occur

Closely related competitors comprising ofEscherichia coli strains having the same metabolic system and differing only with a few bases on the glutamine synthetase gene in the plasmid pKGN were previously shown to coexist in a chemostat. The differences among these closely related competitors can be considered large enough to allow coexistence as the level of enzyme activity is different. To bring the difference among competitors to the slightest possible, the mutation was introduced on the noncoding region of the plasmid pKGN harbored in the wild-type strain (strain W). The new strain, strain W’, carries the plasmid pKGN’ with a 4-base insertion at theHind III site in the polycloning site of pKGN. As the noncoding region is a nucleotide segment that is not translated into amino acids, the relatedness between strains W and W’ is the closest possible from the genetic point of view. Interestingly, though both strains are almost identical, they can coexist stably in a chemostat irrespective of the initial population size. These experimental results suggest that in the natural ecosystem, no matter how akin competitors are, coexistence is not impossible.     

Hutchinson revisited: Patterns of density regulation and the coexistence of strong competitors

Ecologists have long been searching for mechanisms of species coexistence, particularly since G.E. Hutchinson raised the ‘paradox of the plankton’. A promising approach to solve this paradox and to explain the coexistence of many species with strong niche overlap is to consider over-compensatory density regulation with its ability to generate endogenous population fluctuations.Previous work has analysed the role of over-compensation in coexistence based on analytical approaches. Using a spatially explicit time-discrete simulation model, we systematically explore the dynamics and conditions for coexistence of two species. We go beyond the analytically accessible range of models by studying the whole range of density regulation from under- to very strong over-compensation and consider the impact of spatial structure and temporal disturbances. In particular, we investigate how coexistence can emerge in different types of population growth models.We show that two strong competitors are able to coexist if at least one species exhibits over-compensation. Analysing the time series of population dynamics reveals how the differential responses to density fluctuations of the two competitors lead to coexistence: The over-compensator generates density fluctuations but is the inferior competitor at strong amplitudes of those fluctuations; the competitor, therefore, becomes frequent and dampens the over-compensator's amplitudes, but it becomes inferior under dampened fluctuations.These species interactions cause a dynamic alternation of community states with long-term persistence of both species. We show that a variety of population growth models is able to reproduce this coexistence although the particular parameter ranges differ among the models. Spatial structure influences the probability of coexistence but coexistence is maintained for a broad range of dispersal parameters.The flexibility and robustness of coexistence through over-compensation emphasize the importance of nonlinear density dependence for species interactions, and they also highlight the potential of applying more flexible models than the classical Lotka-Volterra equations in community ecology.     

Colourful coexistence of red and green picocyanobacteria in lakes and seas

Hutchinson's paradox of the plankton inspired many studies on the mechanisms of species coexistence. Recent laboratory experiments showed that partitioning of white light allows stable coexistence of red and green picocyanobacteria. Here, we investigate to what extent these laboratory findings can be extrapolated to natural waters. We predict from a parameterized competition model that the underwater light colour of lakes and seas provides ample opportunities for coexistence of red and green phytoplankton species. To test this prediction, we sampled picocyanobacteria of 70 aquatic ecosystems, ranging from clear blue oceans to turbid brown peat lakes. As predicted, red picocyanobacteria dominated in clear waters, whereas green picocyanobacteria dominated in turbid waters. We found widespread coexistence of red and green picocyanobacteria in waters of intermediate turbidity. These field data support the hypothesis that niche differentiation along the light spectrum promotes phytoplankton biodiversity, thus providing a colourful solution to the paradox of the plankton.     

Balancing yield with resilience and conservation objectives in harvested predator–prey communities

The global overexploitation of fish stocks is endangering many marine food webs. Scientists and managers now call for an ecosystem‐based fisheries management, able to take into account the complexity of marine ecosystems and the multiple ecosystem services they provide. By contrast, many fishery management plans only focus on maximizing the productivity of harvested stocks. Such practices are suggested to affect other ecosystem services, altering the integrity and resilience of natural communities. Here we show that while yield‐maximizing policies can allow for coexistence and resilience in predator–prey communities, they are not optimal in a multi‐objective context. We find that although total prey and predator maximum yields are higher with a prey‐oriented harvest, focusing on the predator improves species coexistence. Also, moderate harvesting of the predator can enhance resilience. Furthermore, increasing maximum yields by changing catchabilities improves resilience in predator‐oriented systems, but reduces it in prey‐oriented systems. In a multi‐objective context, optimal harvesting strategies involve a general tradeoff between yield and resilience. Resilience‐maximizing strategies are however compatible with quite high yields, and should often be favored. Our results further suggest that balancing harvest between trophic levels is often best at maintaining simultaneously species coexistence, resilience and yield.     

Population size dependence, competitive coexistence and habitat destruction

1. Spatial dynamics can lead to coexistence of competing species even with strong asymmetric competition under the assumption that the inferior competitor is a better colonizer given equal rates of extinction. Patterns of habitat fragmentation may alter competitive coexistence under this assumption.
2. Numerical models were developed to test for the previously ignored effect of population size on competitive exclusion and on extinction rates for coexistence of competing species. These models neglect spatial arrangement.
3. Cellular automata were developed to test the effect of population size on competitive coexistence of two species, given that the inferior competitor is a better colonizer. The cellular automata in the present study were stochastic in that they were based upon colonization and extinction probabilities rather than deterministic rules.
4. The effect of population size on competitive exclusion at the local scale was found to have little consequence for the coexistence of competitors at the metapopulation (or landscape) scale. In contrast, population size effects on extinction at the local scale led to much reduced landscape scale coexistence compared to simulations not including localized population size effects on extinction, especially in the cellular automata models. Spatially explicit dynamics of the cellular automata vs. deterministic rates of the numerical model resulted in decreased survival of both species. One important finding is that superior competitors that are widespread can become extinct before less common inferior competitors because of limited colonization.
5. These results suggest that population size–extinction relationships may play a large role in competitive coexistence. These results and differences are used in a model structure to help reconcile previous spatially explicit studies which provided apparently different results concerning coexistence of competing species.     

Interactive effects of builders and exploiters on environmental quality and the outcome of competition between the two

The implications of spatial and temporal structure for the maintenance of mutualism, altruism, and niche construction or ecosystem engineering have been explored by many theoretical models. Part of what these models have shown is that organisms that give up some amount of potential short-term gain in order to improve the quality of their environment can, in a variety of scenarios, persist in the face of more exploitative competitors if structure in environmental quality allows the former to preferentially benefit from their investments. The models presented here consider the additional implications of interactions between competitors in their effects on their environment (recently documented in multiple systems). Relative to when competitor types were additive, synergistic effects promoted coexistence and antagonistic effects promoted founder effects (but favored the less exploitative type when both had equal initial frequencies). Spatial and temporal patterns of patch quality and occupancy also differed markedly between scenarios, even where all three scenarios generated the same qualitative outcome. These models show that understanding both the scale over which organisms affect their environment and the degree to which organisms interact in such effects are important for interpreting patterns in environmental quality, predicting the effects of organism-environment feedback on competition, and explaining the persistence of mutualistic traits.     

Fusing spatial resource heterogeneity with a competition–colonization trade-off in model communities

Two commonly cited mechanisms of multispecies coexistence in patchy environments are spatial heterogeneity in competitive abilities caused by variation in resources and a competition–colonization trade-off. In this paper, a model that fuses these mechanisms together is presented and analyzed. The model suggests that spatial variation in resource ratios can lead to multispecies coexistence, but this mechanism by itself is weak when the number of resources for which species compete is small. However, spatial resource heterogeneity is a powerful mechanism for multispecies coexistence when it acts synergistically with a competition–colonization trade-off. The model also shows how resource supply can control the competitive balance between species that are weak competitors but superior colonizers and strong competitors/inferior colonizers. This provides additional theoretical support for a possible explanation of empirically observed hump-shaped relationships between species diversity and ecological productivity.     

Structure and functioning of two pelagic communities in the North Chilean Patagonian coastal system

The size composition of primary producers is important for how energy is channeled through a food web and on to the higher trophic levels and eventually to fisheries. To evaluate this, we studied the productive patterns for large (micro) versus small (nano) phytoplankton in two south marine Patagonian ecosystems: The Inner Sea of Chiloe—ISCh and, Moraleda Channel—MCh. We built Ecopath models (EwE), and evaluated the hypothesis that the overall primary productivity—rather than the ratio of large to small primary producers—constitutes an adequate proxy for predicting the amount of secondary and tertiary production and biomass (up to the fisheries). The EwE model included four small-scale fisheries and 36 functional groups. The functioning of both ecosystems was similar but the ecosystem parameters (biomass, energy transfer efficiencies from primary producers, secondary, and tertiary production) were twice as much in the basin with more microphytoplankton biomass. Overall, the hypothesis was rejected, albeit it was possible to highlight the importance of the quality and size spectrum of plankton on the structure of marine ecosystem, and to demonstrate the key role of the microbial loop over traditional food web in the functioning of the carbon biological pump in Patagonia ecosystems.     

Mixing of supersaturated assemblages and the precipitous loss of species

Mechanisms influencing species richness are many. Recent theoretical research revealed additional mechanisms that involved neutral and lumpy coexistence and alternating assemblage states. These mechanisms can lead to conditions where the number of coexisting species is greater than the number of limiting resources, that is, species supersaturation. Our research focused on the role of disturbances (migration and pulsed through-flows) in supersaturated plankton systems. Our simulations employed 30 different supersaturated assemblages generated by using various ecological principals. Our findings indicated that immigration rates as low as 0.1% of total biomass per day generally led to regional homogenization of species and dramatic extinction events, with assemblages characteristic of lumpy coexistence being more resilient than those characteristic of neutral coexistence or alternating states. Generally, pulsed through-flows tended to offset, to some extent, the negative effects of migration. The precipitous loss of species with the onset of migration is observed in other systems as well, for example, cichlid fish communities of East Africa rift lakes and songbird assemblages from Indian Ocean islands. While many explanations have been offered to explain postimmigration extinctions in species-rich systems, another explanation might be that the assemblages in these systems are in a fragile state of supersaturated coexistence.     

Toxic phytoplankton as a keystone species in aquatic ecosystems: stable coexistence to biodiversity

The effect of allelochemicals released by toxic species in plankton community is often taken into account to reveal plankton biodiversity. Using a minimal chemostat model we show that the interaction between toxic and non‐toxic phytoplankton species with changing competitive effects among species due to allelopathy helps to promote the stable coexistence of many species on a single resource and hence can solve the paradox of plankton. We emphasize toxic phytoplankton as a keystone species that strongly uncovers its allelochemicals on other non‐toxic phytoplankton and enhances the species persistence and diversity in aquatic ecosystems. In addition, we analyze the consistency of ecosystem functioning and species diversity using a number of approaches, such as sampling hypothesis with selection and complementarity effects, cascading extinction–reinvasion, and examining system dynamics at different enrichment levels and toxicity. Our results suggest that chemostats with one toxic and one or more nontoxic phytoplankton species can be used for the experimental verification of the stable coexistence of many species on a single resource in aquatic ecology.     

Trophic amplification of climate warming

Ecosystems can alternate suddenly between contrasting persistent states due to internal processes or external drivers. It is important to understand the mechanisms by which these shifts occur, especially in exploited ecosystems. There have been several abrupt marine ecosystem shifts attributed either to fishing, recent climate change or a combination of these two drivers. We show that temperature has been an important driver of the trophodynamics of the North Sea, a heavily fished marine ecosystem, for nearly 50 years and that a recent pronounced change in temperature established a new ecosystem dynamic regime through a series of internal mechanisms. Using an end-to-end ecosystem approach that included primary producers, primary, secondary and tertiary consumers, and detritivores, we found that temperature modified the relationships among species through nonlinearities in the ecosystem involving ecological thresholds and trophic amplifications. Trophic amplification provides an alternative mechanism to positive feedback to drive an ecosystem towards a new dynamic regime, which in this case favours jellyfish in the plankton and decapods and detritivores in the benthos. Although overfishing is often held responsible for marine ecosystem degeneration, temperature can clearly bring about similar effects. Our results are relevant to ecosystem-based fisheries management (EBFM), seen as the way forward to manage exploited marine ecosystems.     

Spatial mechanisms for coexistence of species sharing a common natural enemy

We examine the conditions under which spatial structure can mediate coexistence of apparent competitors. We use a spatially explicit, host-parasitoid metapopulation model incorporating local dynamics of Nicholson-Bailey type and global dispersal. Depending on the model parameters, the resulting system displays a plethora of asynchronous dynamical behaviors for which permanent or transient coexistence is observed. We identify a number of spatially mediated tradeoffs which apparent competitors can utilize and demonstrate that the dynamics of spatial coexistence can typically be understood from consideration of two and three patch systems. The phase relationships of species abundances are different for our model than for some other mechanisms of spatial coexistence. We discuss the implications of our findings relative to issues of community organization and biological conservation.     

Functional responses and scaling in predator-prey interactions of marine fishes: contemporary issues and emerging concepts

Predator-prey interactions are a primary structuring force vital to the resilience of marine communities and sustainability of the world's oceans. Human influences on marine ecosystems mediate changes in species interactions. This generality is evinced by the cascading effects of overharvesting top predators on the structure and function of marine ecosystems. It follows that ecological forecasting, ecosystem management, and marine spatial planning require a better understanding of food web relationships. Characterising and scaling predator-prey interactions for use in tactical and strategic tools (i.e. multi-species management and ecosystem models) are paramount in this effort. Here, we explore what issues are involved and must be considered to advance the use of predator-prey theory in the context of marine fisheries science. We address pertinent contemporary ecological issues including (1) the approaches and complexities of evaluating predator responses in marine systems; (2) the 'scaling up' of predator-prey interactions to the population, community, and ecosystem level; (3) the role of predator-prey theory in contemporary fisheries and ecosystem modelling approaches; and (4) directions for the future. Our intent is to point out needed research directions that will improve our understanding of predator-prey interactions in the context of the sustainable marine fisheries and ecosystem management.     

Managing fisheries involving predator and prey species

Several management strategies for ecosystems with biological interaction are discussed, including predator removal, predator-prey coexistence, prey exploitation, overexploitation, and introduction of sanctuaries. Some case studies related to ecosystem management are briefly presented; these describe Lakes Victoria and Tanganyika, discarding from shrimp trawl fisheries and the development in the North Sea that led to introduction of multispecies analysis. The concept of fishing down the food web is discussed and the average trophic levels at which the fisheries operate in different ecosystem types are estimated based on quantified trophic flow models. On a global level, while on average fisheries operate around two trophic levels above the primary producers, still one third of the catch of the 70 major fish species caught in the world is of piscivorous fish. Using exploitation-predation rate indices for different ecosystem types, the amount of finfish consumed globally by finfish is roughly estimated to be three times the catches of finfish. Finally some implications for the management of ecosystems are drawn up. It makes little difference if short-term prognoses are based on single-species or multispecies considerations. Multispecies models may, however, give the better long-term advice, and adaptive management may facilitate the move towards such long-term goals.     

Complex wasp-waist regulation of pelagic ecosystems in the Pacific Ocean

‘Wasp-waist’ control of marine ecosystems is driven by a combination of top-down and bottom-up forcing by a few abundant short-lived species occupying intermediate trophic levels that form a narrow ‘waist’ through which energy flow from low to high trophic levels is controlled. It has been assumed that wasp-waist control occurs primarily in highly productive and species-poor systems (e.g. upwelling regions). Two large, species-rich, pelagic ecosystems in the relatively oligotrophic eastern and western Pacific Ocean also show wasp-waist-like structure, in that short-lived and fast-growing cephalopods and fishes at intermediate trophic levels comprise the vast majority of the biomass. Possible forcing dynamics of these systems were examined using ecosystem models by altering the biomass of phytoplankton (bottom-up forcing), large pelagic predators (top-down forcing), and intermediate ‘wasp-waist’ functional groups independently and observing how these changes propagated throughout the ecosystem. The largest effects were seen when altering the biomass of mid trophic-level epipelagic and mesopelagic fishes, where dramatic trophic cascades occurred both upward and downward in the system. We conclude that the high productivity and standing biomass of animals at intermediate trophic levels has a strong top-down influence on the abundance of primary producers. Furthermore, their importance as prey for large predators results in bottom-up controls on populations at higher trophic levels. We show that these tropical pelagic ecosystems possess a complex structure whereby several waist groups and alternate trophic pathways from primary producers to apex predators can cause unpredictable effects when the biomasses of particular functional groups are altered. Such models highlight the possible structuring mechanisms in pelagic systems, which have implications for fisheries that exploit these wasp-waist groups, such as squid fisheries, as well as for fisheries of top predators such as tunas and billfishes that prey upon wasp-waist species.     

The competition-colonization trade-off is dead; long live the competition-colonization trade-off

When applied at the individual patch level, the classic competition-colonization models of species coexistence assume that propagules of superior competitors can displace adults of inferior competitors (displacement competition). But if adults are invulnerable to displacement by propagules (as trees are to seeds), and propagules compete to replace adults that die for reasons independent of the outcome of juvenile competition (a lottery system), a competition-colonization trade-off alone is not able to produce coexistence. However, we show that coexistence is possible if patch density varies spatially, such that it becomes a niche axis. We also show how a dispersal-fecundity trade-off can partition variation in patch density. We discuss the application of these models to empirical systems. An important implication of communities coexisting via variation in patch density is that the amount of habitat loss necessarily interacts with the pattern of loss in affecting extinctions, invasions, and coexistence, in contrast to displacement competition models, for which the spatial pattern of loss is not important or is less important. Finally, with respect to mechanisms promoting coexistence, we suggest that trade-offs between different stages of colonization could be far more common in nature than a trade-off between competitive ability and colonization ability.     

Climate,plankton and cod

While a few North Atlantic cod stocks are stable, none have increased and many have declined in recent years. Although overfishing is the main cause of most observed declines, this study shows that in some regions, climate by its influence on plankton may exert a strong control on cod stocks, complicating the management of this species that often assumes a constant carrying capacity. First, we investigate the likely drivers of changes in the cod stock in the North Sea by evaluating the potential relationships between climate, plankton and cod. We do this by deriving a Plankton Index that reflects the quality and quantity of plankton food available for larval cod. We show that this Plankton Index explains 46.24% of the total variance in cod recruitment and 68.89% of the variance in total cod biomass. Because the effects of climate act predominantly through plankton during the larval stage of cod development, our results indicate a pronounced sensitivity of cod stocks to climate at the warmer, southern edge of their distribution, for example in the North Sea. Our analyses also reveal for the first time, that at a large basin scale, the abundance of Calanus finmarchicus is associated with a high probability of cod occurrence, whereas the genus Pseudocalanus appears less important. Ecosystem‐based fisheries management (EBFM) generally considers the effect of fishing on the ecosystem and not the effect of climate‐induced changes in the ecosystem state for the living resources. These results suggest that EBFM must consider the position of a stock within its ecological niche, the direct effects of climate and the influence of climate on the trophodynamics of the ecosystem.     

Stability and distribution of predator–prey systems: local and regional mechanisms and patterns

Explaining the coexistence and distribution of species in time and space remains a fundamental challenge. While species coexistence depends on both local and regional mechanisms, it is sometimes unclear which role each mechanism takes in a given ecosystem. Consequently, it is very hard to predict the response of the ecosystem to environmental changes. Here, we develop a model to study spatial patterns of coexistence, focusing on predator–prey and host–parasite populations. We show, both theoretically and empirically, that these systems may exhibit both local and regional patterns and mechanisms of coexistence. Changes in environmental parameters, such as spatial connectivity, may lead to a transition from regional to local coexistence or it may lead directly to extinction, depending on demographic parameters. This demonstrates the importance of simultaneously analysing interacting mechanisms that act at different spatial scales to understand the response of ecosystems to environmental changes.     

Ecosystem response to bivalve density reduction: management implications

Coastal ecosystems are easily overexploited and changed by physical and biological factors. In this paper, we discuss current ideas and arguments for coastal ecosystem management with an emphasis on systems that have large bivalve filter feeder components. For centuries the species or population approach has been utilized in fisheries management. With the growing knowledge base on specific environmental effects and relationships, it has become increasingly evident that a broad or holistic approach to fisheries management in these systems is usually more appropriate. An ongoing ecosystem scale experiment in which oysters are completely removed from tidal creeks is described and used as a case study. The experimental design takes estimates of the systems carrying capacity into account. Using the population or species approach to monitor the oysters, the only observable change after the experimental manipulation was a slight increase in summer somatic growth and elevated recruitment of oysters in creeks with oyster reefs removed. These data are interpreted as an indication that the creeks with oysters present are below or near carrying capacity. However, when nekton, plankton and water chemistry data are also examined a much more complicated picture emerges. During the summer growing season, nekton biomass in all creeks is often greater than oyster biomass. Also, our calculations show that oysters do not produce enough ammonium to satisfy phytoplankton productivity, but nekton, water column remineralization and sediments can account for most of the deficit. Finally, microflagellates, which are a preferred food for the oysters, dominate the phytoplankton during the summer growing season and diatoms dominate the colder months. The timing of the change in phase of phytoplankton dominance seems to mirror the seasonal arrival and departure times of nekton in the creeks. We argue that dense bivalve reefs and beds are indicative of intense positive feedback loops that make their ecosystems susceptible to dramatic changes in structure. Such changes have not been reported for natural systems, but are found in systems influenced by over-fishing, nutrient loading and pollution. Thus, the management of sustainable fisheries in coastal ecosystems requires an understanding of the ecosystem science and the realization that systems dominated by bivalves exhibit complex responses that are not easily explained by linear dynamics.