Unanticipated biological changes and global warming

Evidence of global warming is now unequivocal, and studies suggest that it has started to influence natural systems of the planet, including the oceans. However, in the marine environment, it is well-known that species and ecosystems can also be influenced by natural sources of large-scale hydro-climatological variability. The North Atlantic Oscillation (NAO) was negatively correlated with the mean abundance of one of the subarctic key species Calanus finmarchicus in the North Sea. This correlation was thought to have broken down in 1996, however, the timing has never been tested statistically. The present study revisits this unanticipated change and reveals that the correlation did not break down in 1996 as originally proposed but earlier, at the time of an abrupt ecosystem shift in the North Sea in the 1980s. Furthermore, the analyses demonstrate that the correlation between the NAO and C. finmarchicus abundance is modulated by the thermal regime of the North Sea, which in turn covaries positively with global temperature anomalies. This study thereby provides evidence that global climate change is likely to alter some empirical relationships found in the past between species abundance or the ecosystem state and large-scale natural sources of hydro-climatological variability. A theory is proposed to explain how this might happen. These unanticipated changes, also called ‘surprises’ in climatic research, are a direct consequence of the complexity of both climatic and biological systems. In this period of rapid climate change, it is therefore hazardous to integrate meteo-oceanic indices such as the NAO in models used in the management of living resources, as it has been sometimes attempted in the past.

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.

Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios

The long-term effects of ocean warming on prokaryotic communities are unknown because of lack of historical data. We overcame this gap by applying a retrospective molecular analysis to the bacterial community on formalin-fixed samples from the historical Continuous Plankton Recorder archive, which is one of the longest and most geographically extensive collections of marine biological samples in the world. We showed that during the last half century, ubiquitous marine bacteria of the Vibrio genus, including Vibrio cholerae, increased in dominance within the plankton-associated bacterial community of the North Sea, where an unprecedented increase in bathing infections related to these bacteria was recently reported. Among environmental variables, increased sea surface temperature explained 45% of the variance in Vibrio data, supporting the view that ocean warming is favouring the spread of vibrios and may be the cause of the globally increasing trend in their associated diseases.

Quantifying ecosystem-level consequences of ocean acidification and warming by scaling up individual level responses of a predator snail and its trophic interactions

Understanding long‐term, ecosystem‐level impacts of climate change is challenging because experimental research frequently focuses on short‐term, individual‐level impacts in isolation. We address this shortcoming first through an interdisciplinary ensemble of novel experimental techniques to investigate the impacts of 14‐month exposure to ocean acidification and warming (OAW) on the physiology, activity, predatory behaviour and susceptibility to predation of an important marine gastropod (Nucella lapillus). We simultaneously estimated the potential impacts of these global drivers on N. lapillus population dynamics and dispersal parameters. We then used these data to parameterize a dynamic bioclimatic envelope model, to investigate the consequences of OAW on the distribution of the species in the wider NE Atlantic region by 2100. The model accounts also for changes in the distribution of resources, suitable habitat and environment simulated by finely resolved biogeochemical models, under three IPCC global emissions scenarios. The experiments showed that temperature had the greatest impact on individual‐level responses, while acidification had a similarly important role in the mediation of predatory behaviour and susceptibility to predators. Changes in Nucella predatory behaviour appeared to serve as a strategy to mitigate individual‐level impacts of acidification, but the development of this response may be limited in the presence of predators. The model projected significant large‐scale changes in the distribution of Nucella by the year 2100 that were exacerbated by rising greenhouse gas emissions. These changes were spatially heterogeneous, as the degree of impact of OAW on the combination of responses considered by the model varied depending on local‐environmental conditions and resource availability. Such changes in macro‐scale distributions cannot be predicted by investigating individual‐level impacts in isolation, or by considering climate stressors separately. Scaling up the results of experimental climate change research requires approaches that account for long‐term, multiscale responses to multiple stressors, in an ecosystem context.

Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem

Understanding long-term, ecosystem-level impacts of climate change is challenging because experimental research frequently focuses on short-term, individual-level impacts in isolation. We address this shortcoming first through an inter-disciplinary ensemble of novel experimental techniques to investigate the impacts of 14-month exposure to ocean acidification and warming (OAW) on the physiology, activity, predatory behaviour and susceptibility to predation of an important marine gastropod (Nucella lapillus). We simultaneously estimated the potential impacts of these global drivers on N. lapillus population dynamics and dispersal parameters. We then used these data to parameterise a dynamic bioclimatic envelope model, to investigate the consequences of OAW on the distribution of the species in the wider NE Atlantic region by 2100. The model accounts also for changes in the distribution of resources, suitable habitat and environment simulated by finely resolved biogeochemical models, under three IPCC global emissions scenarios. The experiments showed that temperature had the greatest impact on individual level responses, while acidification has a similarly important role in the mediation of predatory behaviour and susceptibility to predators. Changes in Nucella predatory behaviour appeared to serve as a strategy to mitigate individual level impacts of acidification, but the development of this response may be limited in the presence of predators. The model projected significant large-scale changes in the distribution of Nucella by the year 2100 that were exacerbated by rising greenhouse gas emissions. These changes were spatially heterogeneous, as the degree of impact of OAW on the combination of responses considered by the model varied depending on local environmental conditions and resource availability. Such changes in macro-scale distributions cannot be predicted by investigating individual level impacts in isolation, or by considering climate stressors separately. Scaling up the results of experimental climate change research requires approaches that account for long-term, multi-scale responses to multiple stressors, in an ecosystem context.

Flexible C : N ratio enhances metabolism of large phytoplankton when resource supply is intermittent

Phytoplankton cell size influences particle sinking rate, food web interactions and biogeographical distributions. We present a model in which the uptake, storage and assimilation of nitrogen and carbon are explicitly resolved in different-sized phytoplankton cells. In the model, metabolism and cellular C :N ratio are influenced by the accumulation of carbon polymers such as carbohydrate and lipid, which is greatest when cells are nutrient starved, or exposed to high light. Allometric relations and empirical data sets are used to constrain the range of possible C : N, and indicate that larger cells can accumulate significantly more carbon storage compounds than smaller cells. When forced with extended periods of darkness combined with brief exposure to saturating irradiance, the model predicts organisms large enough to accumulate significant carbon reserves may on average synthesize protein and other functional apparatus up to five times faster than smaller organisms. The advantage of storage in terms of average daily protein synthesis rate is greatest when modeled organisms were previously nutrient starved, and carbon storage reservoirs saturated. Small organisms may therefore be at a disadvantage in terms of average daily growth rate in environments that involve prolonged periods of darkness and intermittent nutrient limitation. We suggest this mechanism is a significant constraint on phytoplankton C :N variability and cell size distribution in different oceanic regimes.

The impact of ocean acidification and warming on the skeletal mechanical properties of the sea urchin Paracentrotus lividus from laboratory and field observations

Increased atmospheric CO2 concentration is leading to changes in the carbonate chemistry and the temperature of the ocean. The impact of these processes on marine organisms will depend on their ability to cope with those changes, particularly the maintenance of calcium carbonate structures. Both a laboratory experiment (long-term exposure to decreased pH and increased temperature) and collections of individuals from natural environments characterized by low pH levels (individuals from intertidal pools and around a CO2 seep) were here coupled to comprehensively study the impact of near-future conditions of pH and temperature on the mechanical properties of the skeleton of the euechinoid sea urchin Paracentrotus lividus. To assess skeletal mechanical properties, we characterized the fracture force, Young's modulus, second moment of area, material nanohardness, and specific Young's modulus of sea urchin test plates. None of these parameters were significantly affected by low pH and/or increased temperature in the laboratory experiment and by low pH only in the individuals chronically exposed to lowered pH from the CO2 seeps. In tidal pools, the fracture force was higher and the Young's modulus lower in ambital plates of individuals from the rock pool characterized by the largest pH variations but also a dominance of calcifying algae, which might explain some of the variation. Thus, decreases of pH to levels expected for 2100 did not directly alter the mechanical properties of the test of P. lividus. Since the maintenance of test integrity is a question of survival for sea urchins and since weakened tests would increase the sea urchins' risk of predation, our findings indicate that the decreasing seawater pH and increasing seawater temperature expected for the end of the century should not represent an immediate threat to sea urchins vulnerability.