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.

Variation in ocean colour may help predict cod and haddock recruitment

Characteristics of the spring and fall phytoplankton blooms in spawning areas on the Scotian Shelf, Canada, were estimated from remote sensing data. These blooms, along with anomalies in the North Atlantic Oscillation, were used to explain variation in the recruitment of 4 populations of cod and haddock. We tested the effects of the timing of the bloom using the chlorophyll a (chl a) signal, the maximum amount of chl a, the timing of the diatom bloom, and the maximum relative dominance of diatoms on the recruitment (to Age 1) of cod and haddock on the Scotian Shelf. Models were run separately for the effects of the spring and fall blooms. Only 3 of 10 models tested (0-lag) explained significant (80 to 92%) variation in recruitment. However, the performance of these models was not consistent across populations or species, suggesting that generalities about how spring and fall phytoplankton blooms affect recruitment cannot yet be made. The differences among models suggest that fish larvae are probably adapted locally to food production and thus indirectly to the characteristics of the phytoplankton bloom, which in turn are influenced by regional (meso-scale) oceanographic conditions.

Spatial changes in the sensitivity of Atlantic cod to climate-driven effects in the plankton

Recent strategies to sustain fish stocks have suggested a move towards an ecosystem based fisheries management (EBFM) approach. While EBFM considers the effect of fishing at the ecosystem level, it generally struggles with climate-driven environmental variability. In this study we show that the position of a fish stock within its distributional range or thermal niche (we use Icelandic and North Sea cod as examples of stocks at the centre and edge of their niche, respectively) will influence the relative importance of fishing and climate on abundance. At the warmer edge of the thermal niche of cod in the North Sea, we show a prominent influence of climate on the cod stock that is mediated through temperature effects on the plankton. In contrast, the influence of climate through its effects on plankton appears much less important at the present centre of the niche around Iceland. Recognising the potentially strong effect of climate on fish stocks, at a time of rapid global climate change, is probably an important prerequisite towards the synthesis of a cod management strategy.

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.

A synthesis of large-scale patterns in the planktonic prey of larval and juvenile cod (Gadus morhua)

Data from 40 published studies of the diet composition of larval and juvenile cod (Gadus morhua) from around the northern North Atlantic were summarized to assess generic patterns in ontogenetic and regional variability in the key prey. The results showed that larvae at the northern edge of the latitudinal range of cod depend primarily on development stages of the copepod Calanus finmarchicus, whilst those at the southern edge depend on Para- and Pseudocalanus species. Juvenile cod preyed on a wider range of taxa than larvae, but euphausiids were the main target prey. Analysis of regional variations in the relative abundances of C. finmarchicus and Para/Pseudocalanus spp. in the plankton, as estimated by the continuous plankton recorder (CPR) surveys, showed a similar geographical pattern to the larval cod stomach contents. Comparison of CPR data from the 1960s and 70s with data from the 1990s showed that the boundary between C. finmarchicus and Para/Pseudocalanus spp. dominance has shifted northwards on both sides of the Atlantic, whilst the abundance of euphausiids in the southern cod stock regions has declined. The results are discussed in relation to regional differences in the response of cod stocks to climate variability.

Spatio-Temporal Variability of the North Sea Cod Recruitment in Relation to Temperature and Zooplankton

The North Sea cod (Gadus morhua, L.) stock has continuously declined over the past four decades linked with overfishing and climate change. Changes in stock structure due to overfishing have made the stock largely dependent on its recruitment success, which greatly relies on environmental conditions. Here we focus on the spatio-temporal variability of cod recruitment in an effort to detect changes during the critical early life stages. Using International Bottom Trawl Survey (IBTS) data from 1974 to 2011, a major spatio-temporal change in the distribution of cod recruits was identified in the late 1990s, characterized by a pronounced decrease in the central and southeastern North Sea stock. Other minor spatial changes were also recorded in the mid-1980s and early 1990s. We tested whether the observed changes in recruits distribution could be related with direct (i.e. temperature) and/or indirect (i.e. changes in the quantity and quality of zooplankton prey) effects of climate variability. The analyses were based on spatially-resolved time series, i.e. sea surface temperature (SST) from the Hadley Center and zooplankton records from the Continuous Plankton Recorder Survey. We showed that spring SST increase was the main driver for the most recent decrease in cod recruitment. The late 1990s were also characterized by relatively low total zooplankton biomass, particularly of energy-rich zooplankton such as the copepod Calanus finmarchicus, which have further contributed to the decline of North Sea cod recruitment. Long-term spatially-resolved observations were used to produce regional distribution models that could further be used to predict the abundance of North Sea cod recruits based on temperature and zooplankton food availability.

Empirically modelling the potential effects of changes in temperature and prey availability on the growth of cod larvae in UK shelf seas

It has been hypothesized that changes in zooplankton community structure over the past four decades led to reduced growth and survival of prerecruit Atlantic cod (Gadus morhua) and that this was a key factor underlying poor year classes, contributing to stock collapse, and inhibiting the recovery of stocks around the UK. To evaluate whether observed changes in plankton abundance, species composition and temperature could have led to periods of poorer growth of cod larvae, we explored the effect of prey availability and temperature on early larval growth using an empirical trophodynamic model. Prey availability was parameterized using species abundance data from the Continuous Plankton Recorder. Our model suggests that the observed changes in plankton community structure in the North Sea may have had less impact on cod larval growth, at least for the first 40 days following hatching, than previously suggested. At least in the short term, environmental and prey conditions should be able to sustain growth of cod larvae and environmental changes acting on this early life stage should not limit stock recovery.

Have climate induced changes in zooplankton communities led to poor conditions for larval fish growth? A test on cod larvae on the UK shelf

Climate effects have been shown to be at least partly responsible for the reorganisation in the plankton ecosystem on the shelf seas of NW Europe over the last 50 years. Most fish larvae feed primarily on zooplankton, so changes in zooplankton quantity, quality and seasonal timing have been hypothesized to be a key factor affecting their survival. To investigate this we have implemented a 1-dimensional trophodynamic growth model of cod larvae for the waters around the UK covering the period 1960 to 2003. Larval growth is modelled as the difference between the amount of food absorbed by the larva and its various metabolic costs. Prey availability is based upon the biomass and size of available preys (i.e. adults and nauplii copepods and cladocerans) taken from the Continuous Plankton Recorder dataset. Temperature and wind forcing are also taken into account. Results suggest that observed changes in plankton community structure may have had less impact than previously suggested. This is because changes in prey availability may be compensated for by increased temperatures resulting in little overall impact on potential larval growth. Stock recovery, at least in the short term is likely to be more dependent upon conserving the year classes recruited to allow spawning stock biomass to rebuild. If as our model suggests, the larvae are still able to survive in the changing environment, reduction in fishing on the adults is needed to allow the stock to recover.