In hot water: zooplankton and climate change

An overview is provided of the observed and potential future responses of zooplankton communities to global warming. I begin by describing the importance of zooplankton in ocean ecosystems and the attributes that make them sensitive beacons of climate change. Global warming may have even greater repercussions for marine ecosystems than for terrestrial ecosystems, because temperature influences water column stability, nutrient enrichment, and the degree of new production, and thus the abundance, size composition, diversity, and trophic efficiency of zooplankton. Pertinent descriptions of physical changes in the ocean in response to climate change are given as a prelude to a detailed discussion of observed impacts of global warming on zooplankton. These manifest as changes in the distribution of individual species and assemblages, in the timing of important life-cycle events, and in abundance and community structure. The most illustrative case studies, where climate has had an obvious, tangible impact on zooplankton and substantial ecosystem consequences, are presented. Changes in the distribution and phenology of zooplankton are faster and greater than those observed for terrestrial groups. Relevant projected changes in ocean conditions are then presented, followed by an exploration of potential future changes in zooplankton communities from the perspective of different modelling approaches. Researchers have used a range of modelling approaches on individual species and functional groups forced by output from climate models under future greenhouse gas emission scenarios. I conclude by suggesting some potential future directions in climate change research for zooplankton, viz. the use of richer zooplankton functional groups in ecosystem models; greater research effort in tropical systems; investigating climate change in conjunction with other human impacts; and a global zooplankton observing system.

Global latitudinal variations in marine copepod diversity and environmental factors

Latitudinal gradients in diversity are among the most striking features in ecology. For terrestrial species, climate (i.e. temperature and precipitation) is believed to exert a strong influence on the geographical distributions of diversity through its effects on energy availability. Here, we provide the first global description of geographical variation in the diversity of marine copepods, a key trophic link between phytoplankton and fish, in relation to environmental variables. We found a polar-tropical difference in copepod diversity in the Northern Hemisphere where diversity peaked at subtropical latitudes. In the Southern Hemisphere, diversity showed a tropical plateau into the temperate regions. This asymmetry around the Equator may be explained by climatic conditions, in particular the influence of the Inter-Tropical Convergence Zone, prevailing mainly in the northern tropical region. Ocean temperature was the most important explanatory factor among all environmental variables tested, accounting for 54 per cent of the variation in diversity. Given the strong positive correlation between diversity and temperature, local copepod diversity, especially in extra-tropical regions, is likely to increase with climate change as their large-scale distributions respond to climate warming.

Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments

Recent changes in the seasonal timing (phenology) of familiar biological events have been one of the most conspicuous signs of climate change. However, the lack of a standardized approach to analysing change has hampered assessment of consistency in such changes among different taxa and trophic levels and across freshwater, terrestrial and marine environments. We present a standardized assessment of 25 532 rates of phenological change for 726 UK terrestrial, freshwater and marine taxa. The majority of spring and summer events have advanced, and more rapidly than previously documented. Such consistency is indicative of shared large scale drivers. Furthermore, average rates of change have accelerated in a way that is consistent with observed warming trends. Less coherent patterns in some groups of organisms point to the agency of more local scale processes and multiple drivers. For the first time we show a broad scale signal of differential phenological change among trophic levels; across environments advances in timing were slowest for secondary consumers, thus heightening the potential risk of temporal mismatch in key trophic interactions. If current patterns and rates of phenological change are indicative of future trends, future climate warming may exacerbate trophic mismatching, further disrupting the functioning, persistence and resilience of many ecosystems and having a major impact on ecosystem services.

Climate change and food safety: A review

Climate change and variability may have an impact on the occurrence of food safety hazards at various stages of the food chain, from primary production through to consumption. There are multiple pathways through which climate related factors may impact food safety including: changes in temperature and precipitation patterns, increased frequency and intensity of extreme weather events, ocean warming and acidification, and changes in contaminants’ transport pathways among others. Climate change may also affect socio-economic aspects related to food systems such as agriculture, animal production, global trade, demographics and human behaviour which all influence food safety. This paper reviews the potential impacts of predicted changes in climate on food contamination and food safety at various stages of the food chain and identifies adaptation strategies and research priorities to address food safety implications of climate change. The paper concludes that there is a need for intersectoral and international cooperation to better understand the changing food safety situation and in developing and implementing adaptation strategies to address emerging risks associated with climate change.

1H NMR metabolomics reveals contrasting response by male and female mussels exposed to reduced seawater pH, increased temperature and a pathogen

Human activities are fundamentally altering the chemistry of the world's oceans. Ocean acidification (OA) is occurring against a background of warming and an increasing occurrence of disease outbreaks, posing a significant threat to marine organisms, communities, and ecosystems. In the current study, (1)H NMR spectroscopy was used to investigate the response of the blue mussel, Mytilus edulis, to a 90-day exposure to reduced seawater pH and increased temperature, followed by a subsequent pathogenic challenge. Analysis of the metabolome revealed significant differences between male and female organisms. Furthermore, males and females are shown to respond differently to environmental stress. While males were significantly affected by reduced seawater pH, increased temperature, and a bacterial challenge, it was only a reduction in seawater pH that impacted females. Despite impacting males and females differently, stressors seem to act via a generalized stress response impacting both energy metabolism and osmotic balance in both sexes. This study therefore has important implications for the interpretation of metabolomic data in mussels, as well as the impact of environmental stress in marine invertebrates in general.

Can we trust simple marine DMS parameterisations within complex climate models?

Dimethylsulphide (DMS) is a globally important aerosol precurser. In 1987 Charlson and others proposed that an increase in DMS production by certain phytoplankton species in response to a warming climate could stimulate increased aerosol formation, increasing the lower-atmosphere's albedo, and promoting cooling. Despite two decades of research, the global significance of this negative climate feedback remains contentious. It is therefore imperative that schemes are developed and tested, which allow for the realistic incorporation of phytoplankton DMS production into Earth System models. Using these models we can investigate the DMS-climate feedback and reduce uncertainty surrounding projections of future climate. Here we examine two empirical DMS parameterisations within the context of an Earth System model and find them to perform marginally better than the standard DMS climatology at predicting observations from an independent global dataset. We then question whether parameterisations based on our present understanding of DMS production by phytoplankton, and simple enough to incorporate into global climate models, can be shown to enhance the future predictive capacity of those models. This is an important question to ask now, as results from increasingly complex Earth System models lead us into the 5th assessment of climate science by the Intergovernmental Panel on Climate Change. Comparing observed and predicted inter-annual variability, we suggest that future climate projections may underestimate the magnitude of surface ocean DMS change. Unfortunately this conclusion relies on a relatively small dataset, in which observed inter-annual variability may be exaggerated by biases in sample collection. We therefore encourage the observational community to make repeat measurements of sea-surface DMS concentrations an important focus, and highlight areas of apparent high inter-annual variability where sampling might be carried out. Finally, we assess future projections from two similarly valid empirical DMS schemes, and demonstrate contrasting results. We therefore conclude that the use of empirical DMS parameterisations within simulations of future climate should be undertaken only with careful appreciation of the caveats discussed.

Biomass changes and trophic amplification of plankton in a warmer ocean

Ocean warming can modify the ecophysiology and distribution of marine organisms, and relationships between species, with nonlinear interactions between ecosystem components potentially resulting in trophic amplification. Trophic amplification (or attenuation) describe the propagation of a hydroclimatic signal up the food web, causing magnification (or depression) of biomass values along one or more trophic pathways. We have employed 3-D coupled physical-biogeochemical models to explore ecosystem responses to climate change with a focus on trophic amplification. The response of phytoplankton and zooplankton to global climate-change projections, carried out with the IPSL Earth System Model by the end of the century, is analysed at global and regional basis, including European seas (NE Atlantic, Barents Sea, Baltic Sea, Black Sea, Bay of Biscay, Adriatic Sea, Aegean Sea) and the Eastern Boundary Upwelling System (Benguela). Results indicate that globally and in Atlantic Margin and North Sea, increased ocean stratification causes primary production and zooplankton biomass to decrease in response to a warming climate, whilst in the Barents, Baltic and Black Seas, primary production and zooplankton biomass increase. Projected warming characterized by an increase in sea surface temperature of 2.29 ± 0.05 °C leads to a reduction in zooplankton and phytoplankton biomasses of 11% and 6%, respectively. This suggests negative amplification of climate driven modifications of trophic level biomass through bottom-up control, leading to a reduced capacity of oceans to regulate climate through the biological carbon pump. Simulations suggest negative amplification is the dominant response across 47% of the ocean surface and prevails in the tropical oceans; whilst positive trophic amplification prevails in the Arctic and Antarctic oceans. Trophic attenuation is projected in temperate seas. Uncertainties in ocean plankton projections, associated to the use of single global and regional models, imply the need for caution when extending these considerations into higher trophic levels.

Indications of a climate effect on Mediterranean fisheries

Using the Food and Agriculture Organization’s (FAO) Mediterranean capture fisheries production dataset in conjunction with global and Mediterranean sea surface temperatures, we investigated trends in fisheries landings and landings per unit of effort of commercially important marine organisms, in relation to temperature oscillations. In addition to the overall warming trend, a temperature shift was detected in the Mediterranean Sea in the late 1990s. Fisheries landings fluctuations were examined for the most abundant commercial species (59 species) and showed significant year-to-year correlations with temperature for nearly 60 % of the cases. From these, the majority (~70 %) were negatively related and showed a reduction of 44 % on average. Increasing trends were found, mainly in the landings of species with short life spans, which seem to have benefited from the increase in water temperature. Τhe effect of oceanic warming is apparent in most species or groups of species sharing ecological (e.g. small and medium pelagic, demersal fish) or taxonomic (e.g. cephalopods, crustaceans) traits. A landings-per-unit-of-effort (LPUE) proxy, using data from the seven Mediterranean European Union member states, also showed significant correlation with temperature fluctuations for six out of the eight species examined, indicating the persistence of temperature influence on landings when the fishing effect is accounted for. The speed of response of marine landings to the warming of the Mediterranean Sea possibly shows both the sensitivity and the vulnerable state of the fish stocks and indicates that climate should be examined together with fisheries as a factor shaping stock fluctuations.

The future of the northeast Atlantic benthic flora in a high CO2 world

Seaweed and seagrass communities in the northeast Atlantic have been profoundly impacted by humans, and the rate of change is accelerating rapidly due to runaway CO2 emissions and mounting pressures on coastlines associated with human population growth and increased consumption of finite resources. Here, we predict how rapid warming and acidification are likely to affect benthic flora and coastal ecosystems of the northeast Atlantic in this century, based on global evidence from the literature as interpreted by the collective knowledge of the authorship. We predict that warming will kill off kelp forests in the south and that ocean acidification will remove maerl habitat in the north. Seagrasses will proliferate, and associated epiphytes switch from calcified algae to diatoms and filamentous species. Invasive species will thrive in niches liberated by loss of native species and spread via exponential development of artificial marine structures. Combined impacts of seawater warming, ocean acidification, and increased storminess may replace structurally diverse seaweed canopies, with associated calcified and noncalcified flora, with simple habitats dominated by noncalcified, turf-forming seaweeds.

Long-term annual primary production in the Ulleung Basin as a biological hot spot in the East/Japan Sea

Although the Ulleung Basin is an important biological hot spot in East/Japan Sea (hereafter the East Sea), very limited knowledge for seasonal and annual variations in the primary productivity exists. In this study, a recent decadal trend of primary production in the Ulleung Basin was analyzed based on MODIS-derived monthly primary production for a better annual production budget. Based on the MODIS-derived primary production, the mean daily primary productivity was 766.8 mg C m-2 d-1 (SD=+/- 196.7 mg C m-2 d-1) and the annual primary productivity was 280.2 g C m-2 yr-1 (SD=+/- 14.9 g C m-2 yr-1) in the Ulleung Basin during the study period. The monthly contributions of primary production were not largely variable among different months, and a relatively small interannual production variability was also observed in the Ulleung Basin, which indicates that the Ulleung Basin is a sustaining biologically productive region called as hot spot in the East Sea. However, a significant recent decline in the annual primary production was observed in the Ulleung Basin after 2006. Although no strong possibilities were found in this study, the current warming sea surface temperature and a negative phase PDO index were suggested for the recent declining primary production. For a better understanding of subsequent effects on marine ecosystems, more intensive interdisciplinary field studies will be required in the Ulleung Basin.

Long-term iceshelf-covered meiobenthic communities of the Antarctic continental shelf resemble those of the deep sea

Since strong regional warming has led to the disintegration of huge parts of the Larsen A and B ice shelves east of the Antarctic Peninsula in 1995 and 2002, meiofaunal communities covered by ice shelves for thousands of years could be investigated for the first time. Based on a dataset of more than 230,000 individuals, meiobenthic higher taxa diversity and composition of Larsen continental shelf stations were compared to those of deep-sea stations in the Western Weddell Sea to see whether the food-limiting conditions in the deep sea and the food-poor shelf regime at times of iceshelf coverage has resulted in similar meiobenthic communities, on the premises that food availability is the main driver of meiobenthic assemblages. We show here that this is indeed the case; in terms of meiobenthic communities, there is greater similarity between the deep sea and the inner Larsen embayments than there is similarity between the deep sea and the former Larsen B iceshelf edge and the open continental shelf. We also show that resemblance to Antarctic deep-sea meiofaunal communities was indeed significantly higher for communities of the innermost Larsen B area than for those from intermediate parts of Larsen A and B. Similarity between communities from intermediate parts and the deep sea was again higher than between those of the ice-edge and the open shelf. Meiofaunal densities were low at the inner parts of Larsen A and B, and comparable to deep-sea densities, again likely owing to the low food supply at both habitats. We suggest that meiobenthic communities have not yet recovered from the food-limiting conditions present at the time of iceshelf coverage. Meiofaunal diversity on the other hand seemed driven by sediment structure, being higher in coarser sediments.

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.

Interaction Effects of Light, Temperature and Nutrient Limitations (N, P and Si) on Growth, Stoichiometry and Photosynthetic Parameters of the Cold-Water Diatom Chaetoceros wighamii

Light (20-450 μmol photons m^-2 s^-1), temperature (3-11°C) and inorganic nutrient composition (nutrient replete and N, P and Si limitation) were manipulated to study their combined influence on growth, stoichiometry (C:N:P:Chl a) and primary production of the cold water diatom Chaetoceros wighamii. During exponential growth, the maximum growth rate (~0.8 d^-1) was observed at high temperture and light; at 3°C the growth rate was ~30% lower under similar light conditions. The interaction effect of light and temperature were clearly visible from growth and cellular stoichiometry. The average C:N:P molar ratio was 80:13:1 during exponential growth, but the range, due to different light acclimation, was widest at the lowest temperature, reaching very low C:P (~50) and N:P ratios (~8) at low light and temperature. The C:Chl a ratio had also a wider range at the lowest temperature during exponential growth, ranging 16-48 (weight ratio) at 3°C compared with 17-33 at 11°C. During exponential growth, there was no clear trend in the Chl a normalized, initial slope (α*) of the photosynthesis-irradiance (PE) curve, but the maximum photosynthetic production (P_m) was highest for cultures acclimated to the highest light and temperature. During the stationary growth phase, the stoichiometric relationship depended on the limiting nutrient, but with generally increasing C:N:P ratio. The average photosynthetic quotient (PQ) during exponential growth was 1.26 but decreased to <1 under nutrient and light limitation, probably due to photorespiration. The results clearly demonstrate that there are interaction effects between light, temperature and nutrient limitation, and the data suggests greater variability of key parameters at low temperature. Understanding these dynamics will be important for improving models of aquatic primary production and biogeochemical cycles in a warming climate.

Effects of elevated CO2 and temperature on an intertidal meiobenthic community

In the near future, the marine environment is likely to be subjected to simultaneous increases in temperature and decreased pH. The potential effects of these changes on intertidal, meiofaunal assemblages were investigated using a mesocosm experiment. Artificial Substrate Units containing meiofauna from the extreme low intertidal zone were exposed for 60 days to eight experimental treatments (four replicates for each treatment) comprising four pH levels: 8.0 (ambient control), 7.7 & 7.3 (predicted changes associated with ocean acidification), and 6.7 (CO2 point-source leakage from geological storage), crossed with two temperatures: 12 °C (ambient control) and 16 °C (predicted). Community structure, measured using major meiofauna taxa was significantly affected by pH and temperature. Copepods and copepodites showed the greatest decline in abundance in response to low pH and elevated temperature. Nematodes increased in abundance in response to low pH and temperature rise, possibly caused by decreased predation and competition for food owing to the declining macrofauna density. Nematode species composition changed significantly between the different treatments, and was affected by both seawater acidification and warming. Estimated nematode species diversity, species evenness, and the maturity index, were substantially lower at 16 °C, whereas trophic diversity was slightly higher at 16 °C except at pH 6.7. This study has demonstrated that the combination of elevated levels of CO2 and ocean warming may have substantial effects on structural and functional characteristics of meiofaunal and nematode communities, and that single stressor experiments are unlikely to encompass the complexity of abiotic and biotic interactions. At the same time, ecological interactions may lead to complex community responses to pH and temperature changes in the interstitial environment

Disentangling the impacts of heat wave magnitude, duration and timing on the structure and diversity of sessile marine assemblages

Extreme climatic events, including heat waves (HWs) and severe storms, influence the structure of marine and terrestrial ecosystems. Despite growing consensus that anthropogenic climate change will increase the frequency, duration and magnitude of extreme events, current understanding of their impact on communities and ecosystems is limited. Here, we used sessile invertebrates on settlement panels as model assemblages to examine the influence of HW magnitude, duration and timing on marine biodiversity patterns. Settlement panels were deployed in a marina in southwest UK for ≥5 weeks, to allow sufficient time for colonisation and development of sessile fauna, before being subjected to simulated HWs in a mesocosm facility. Replicate panel assemblages were held at ambient sea temperature (∼17 °C), or +3 °C or +5 °C for a period of 1 or 2 weeks, before being returned to the marina for a recovery phase of 2–3 weeks. The 10-week experiment was repeated 3 times, staggered throughout summer, to examine the influence of HW timing on community impacts. Contrary to our expectations, the warming events had no clear, consistent impacts on the abundance of species or the structure of sessile assemblages. With the exception of 1 high-magnitude long-duration HW event, warming did not alter not assemblage structure, favour non-native species, nor lead to changes in richness, abundance or biomass of sessile faunal assemblages. The observed lack of effect may have been caused by a combination of (1) the use of relatively low magnitude, realistic heat wave treatments compared to previous studies (2), the greater resilience of mature adult sessile fauna compared to recruits and juveniles, and (3) the high thermal tolerance of the model organisms (i.e., temperate fouling species, principally bryozoans and ascidians). Our study demonstrates the importance of using realistic treatments when manipulating climate change variables, and also suggests that biogeographical context may influence community-level responses to short-term warming events, which are predicted to increase in severity in the future.