Within the context of oceanography, the term regime shift is used to describe changes in abundance and composition of biomass; principally plankton and fish over decadal timescales, signifying an 'abrupt shift' from one dynamic ecological regime to another (Reid et al., 2001; Scheffer et al., 2001). First scientifically recognised in the mid-1970s in the northern Pacific (Venrick et al., 1987), a regime shift is predominantly driven by modifications of the atmospheric and oceanic circulations (Stenseth et al., 2002). The 'shift' was primarily seen in phytoplankton biomass increase after this episode, indicating that some major change had occurred. This was attributed to adjustment of spatial gradients of atmospheric pressure at sea level which increased strength and frequency of storms - notably westerly winds - which allowed deeper mixing and greater transfer of nutrient rich water to the surface (Venrick et al., 1987). As a result, the North Pacific Gyre exhibited greater plankton bloom biomass thus enhancing the carrying capacity, contributing to increased abundance of cod and salmon, with a decrease in shrimp (Botsford et al., 1997).
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A similar regime shift in the North Sea was identified involving changes within all trophic levels of the ecosystem and validated using a three dimensional hydrodynamic model (Reid et al., 2001). Similarities drawn between Pacific and Atlantic examples have given rise to understanding of connectivity throughout the marine environment (Beaugrand, 2004). Alheit et al. (2005) found synchronous ecological change in the Baltic Sea, identifying the importance of the shifting North Atlantic Oscillation (NAO) between negative and positive phases. The NAO is a measure of basin scale alterations in atmospheric mass (pressure) between the subtropical and arctic Atlantic Ocean (Hurrell, 1995). Beaugrand (2004) emphasises the importance of identifying 'stepwise changes' within the pelagic ecosystem, and highlights the significance of changes both within and out of trophic levels, dynamics of species diversity, population characteristics of key species, and of hydro-climatic variability.
This paper uses this broad framework to identify evidence of changes within the physical and biological characteristics of the North Sea.
2. Methods of analysis
2.1 Biological data
Biological data has been accumulated for over 60 years at approximately monthly intervals utilising continuous plankton recorders (CPRs) towed by merchant ships (Figure 1), maintaining regular and consistent coverage of plankton and copepod growth in the Northeast Atlantic (Warner & Hays, 1994; Reid et al., 2001).
Figure 1 - Continuous Plankton Recorder (CPR) sample distribution in the North East Atlantic during the period 1960-1995. Source: Edwards et al., 2001.
The International Council for the Exploration of the Sea (ICES) compiles fish catch statistics yearly within standard areas in the North Sea. This is accumulated from national submissions of catches from member states of ICES which is used to assess fish stocks in the North Sea (ICES, 2001).
2.2 Physical data
Consideration of physical attributes of the marine and atmospheric environments is vital to the understanding of ecological interactions within them, and to the development of models to simulate change under various scenarios.
Measured and remotely sensed physical and meteorological data was used in the formation of statistical models. This typically utilises calculations of six-hourly pressure field, wind stress, tidal ranges and freshwater inflow hindcasts were provided from the Norwegian Meteorological Institute (Reid et al., 2001); temperature and salinity (bottom and surface) data from ICES (ICES, 2001); COADS (Comprehensive Ocean-Atmosphere Data Set) from the National Oceanic and Atmospheric Administration research centre (NOAA) and the Cooperative Institute for Research in Environmental Sciences (CIRES) (Woodruff et al., 1987). Sea Surface Temperature (SST) anomalies and winter NAO index are obtained from the Hadley Centre, Meteorological Office, London (Hurrell, 1995).
2.3 Statistical analyses
Various statistical analyses are applied to identify and quantify regime shifts in CPR data sets. Principal Component Analysis (PCA) is generally used to reveal dominant yearly changes in the relative abundances of zooplankton and phytoplankton whilst Split Moving-Window Boundary Analysis identifies temporal discontinuities in multivariate time-series (e.g. Beaugrand, 2003). Cluster analysis reduces the influence of episodic events and high frequency variability.
Coupled physical, chemical, biological modelling systems are developed to recognise interactions between ocean circulation, primary production, transport of nutrients and dispersion of particles (e.g. Skogen et al., 1995). The Norwegian Ecological Model (NORWECOM) utilises North Sea data to create a circulation model; allowing calculation of oceanic inflow from the north east Atlantic to be calculated daily (Reid et al., 2001).
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3. Evidence of North Sea ecosystem regime shift
Biological indicators observed by Reid et al. (2001) showed the first signs that a regime shift may have occurred in the North Sea. This was primarily driven my observations in phytoplankton abundance and species assemblage and on fish catches, in addition to suggestions of similar changes in the benthos (Beaugrand, 2004). Some debate whether regime shift occurred remains (e.g. Reid & Beaugrand, 2002; Taylor, 2002), however it is postulated that a regime or climate shift may be best determined by biological monitoring of marine organism rather than climate (Hare & Mantuna, 2001) and that slight changes in physical forcing has profound effects on complex and interactive food webs (Taylor et al., 2002). This section reviews evidence for a regime shift in the North Sea.
Although CPR monitoring has identified over 100 phytoplankton species, relatively few have been formally studied. Edwards et al. (2001) present a broad 'phytoplankton colour' index based on relative quantities of chlorophyll-É‘ from CPR samples which reflects phytoplankton biomass. They provide data indicating increasing phytoplankton biomass in the North Sea after the mid-1980s (Figs. 2a-b). PCA (Fig. 2d) signifies the magnitude of the shift seen in
Figure 2 - Long term phytoplankton 'colour' changes in the North Sea. (a) Long term monthly changes in phytoplankton colour. (b) Long term monthly anomalies in phytoplankton colour. (c) Split Window Moving Boundary Analysis. (d) Axis 1 from standard PCA applied to CPR data set - shift indicated between dashed lines. Source: Beaugrand, 2004; data from Edwards et al., 2001).
phytoplankton biomass in the North Sea, reinforced by discontinuities seen during the onset of the shift (Fig. 1c). These results are conclusive evidence of change occurring in the flora of the North Sea. Future phytoplankton research would benefit from assessing relative species abundance in CPR samples.
Research on zooplankton is more abundant; many studies focusing on individual species (e.g. Beaugrand et al., 2003), and diversity and species assemblage (Beaugrand, 2002a; Beaugrand, 2003) have yielded conclusive results of regime shift in the North Sea.
Fig. 3 shows further planktonic evidence for regime shift. Axis 1 of PCA for calanoid copepod CPR data for the North Sea reveals a clear stepwise change from a cold to warm dynamic equilibrium (Beaugrand et al., 2002b).
Figure 3 - Long term changes (1958-1999) in calanoid copepod community structure. Axis 1 of PCA (32.46% total variance). Source: Beaugrand et al., 2002b.
Indices to monitor plankton responses to climate change using calanoid copepod community structures are being developed (e.g. Beaugrand, 2005). Beaugrand and Ibañez identified 'pronounced changes' in ecosystem communities; Fig. 4 illustrates a shift from high species abundance indicative of colder environs to one of lower abundance after the period 1984-1999 (Beaugranad & Ibañez, unpublished data; diagram reproduced in Beaugrand, 2004).
Flatfish and gadoid fish (those of Gadidae) have an inverse relationship to each other after the shift seen at ~1980 (Figs. 4a-b). This is indicative of a stepwise change prior to the regime shift (1983-1989, Beaugrand, 2004). Although not related to calanoid assemblage changes in the Norh Sea, this shift is linked to salinity (Fig. 4c) and Sea Surface Temperature (SST) (Fig. 4.d). A slight relationship between westerly wind strength (NAO derived) and fish recruitment can be seen, however longer trends in NAO phase shifts suggest this is probable (Fig. 7) and correlates with northern hemisphere temperature (NHT) anomalies.
Figure 4 - Long term changes in fish abundance in relation to zooplankton assemblage composition and hydro-climatological forcing. Source: Beaugrand & Ibañez, unpublished data; reproduced in Beaugrand, 2004.
Reid et al. provide further evidence for fish abundance changes during the regime shift period (2001). SST fluctuation and oceanic inflow are attributed to this shift (Fig. 5). Catches in the northern North Sea increase after ~1980 whilst catches in the south fall (Figs. 5a-b), catches in the English Channel and Skagerrak/Kattegat areas remain low (Fig. 5c), suggesting change is driven by cooler waters entering the North Sea basin from the north (Reid et al., 2001); catches through the north east Atlantic were high 1988-1994 (Fig. 5.d).
This correlates with rapid rises in summer SST (Fig. 4c) in the North Sea (55-60Â°N) which is likely to drive primary production in planktonic groups (Beaugrand, 2003). Large inflows to
the North Sea during winter months after 1988 (Fig. 6) across a northsouth/eastwest boundary coincide with positive NAO index (Fig. 7), driving planktonic shifts (Reid et al., 2003).
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Figure 5 - Horse mackerel (Trachurus trachurus) catches (tonnes) for the period 1965-1994. (a) Western catches, 46-65Â°N (upper curve), northern catches (lower curve). (b) Southern catches, south of 45Â°N. (c) Combined catches for the eastern English Channel, south-central North Sea and Skagerrak/Kattegat. (d) Total north east Atlantic catches. Source: Reid et al., 2001.
Figure 6 - Modelled inflow into the North Sea across a section between Orkney, Shetland and Norway. (a) Contour plot of monthly mean inflow January 1976 - December 1994. (b) The same data as annual means 1976-1994. Source: Reid et al., 2001.
The NAO index is a major variability in the northern hemisphere atmosphere where it is has major control over northern hemisphere climate during the winter (Osborn, 2010), and is thought to have major affects on ocean currents. Oceanic flow into the North Sea basin is considered to be of major importance to the ecological maintenance of the marine environment (Skogen & Soiland, 1998). Modelling reveals a relationship between primary productivity and intensity of wind speed, driven by positive winter NAO phases (Reid et al., 2003). Fig. 7 illustrates the oscillation of the NAO and shows positive winter phases increasing in frequency and strength ~1974. Whilst not in the North Sea, but geographically close, Soay sheep populations exhibit similar trends in phase with positive NAO (Coulson et al., 2001). Freshwater algal assemblages from Scotland and Norway also indicate responses to the NAO during the time of the North Sea regime shift (Monteith & Shilland, 2007). The NAO impact is therefore also seen in terrestrial ecosystems in the north east Atlantic region, furthering the hypothesis that global climate changes alter the dynamics of basin scale ecosystems and is the main driver for ecosystem change in the North Sea.
Figure 7 - Temporal variability in Winter North Atlantic Oscillation index (December-March average) 1823-2010. Source: Osborn, T. (2010) University of East Anglia Climatic Research Unit.
4. The North Sea Cod Fishery - regime shifts, impacts and implications
The regime shift observed in the North Sea ecosystems appears unique in recorded memory (Reid et al., 2001), however anecdotal evidence suggests similar changes have happened before. During the 16th to 19th centuries Dutch fishermen sailed to Iceland to exploit cod (Gadus morhua) fisheries there; suggesting stocks in the North Sea were not worth utilising during this period (Brander, 1994). However, fishing pressure increased during this time as European countries developed maritime exploitation during periods of low agricultural productivity and shifting areas of productive fishing grounds associated with the Little Ice Age (Lamb, 1995).
A recent large increase was observed in the North Sea cod population in the 1960s, (an occurrence seen in many gadoids at the time) and was dubbed the 'gadoid outburst' (Holden, 1981). As discussed in section 3 this can be largely attributed to hydro-climatological forcing associated with the NAO, however overfishing of herring (Clupea harengus) (a planktonivorous species) may have exaggerated the natural increase in cod recruitment (Daan et al., 1985). Since 1981 there has been a steady decline in the population; cod biomass in the 1990s was at the 1960s level (Brander, 1994). The 'gadoid outburst' was characterised by strong year classes in gadoid species, which led to huge and unsustainable landings of fish during this period (Hislop, 1996).
Beaugrand et al. (2003) provide evidence that unfavourable changes in the plankton assemblage has exacerbated impacts of overfishing by reducing North Sea cod recruitment since the mid-1980s, and that shifts in the planktonic ecosystem are the probable causes of increased recruitment during the gadoid outburst (Cook et al., 1997). This leads to suggest that a combination of factors working in synergy led to the 'boom and bust' nature of the gadoid outburst, and that whilst it started as a purely natural phenomenon, anthropogenic pressures led to the recent and nearly ultimate demise of gadoid fish in the North Sea.
Regime shifts have implications for fish stocks and their associated fishery industries. Fish stocks have been over exploited in the North Sea since the 1960s, which has been exacerbated by natural pressures driven by the NAO and wider climatic forcing (Clover, 2004). The majority of the fish biomass decline can be attributed to fishing, a major restraint on recovery of and replenishment of fisheries is the deficiency in brood stock; repeatedly removed and preventing natural recruitment (Shaefer, 1954). This explains why gadoid populations have been at a historical low since the 1990s, where overfishing cut through a natural 'restocking phase' driven by the NAO (Reid et al., 2001). The function of adult fish is to reproduce, with larger, older female fish spawning greater numbers of eggs over a longer period than younger females (Harris, 1998). Fishing mortality since the 1960s has removed large fish, and prevented many more from reaching maturation (Christensen, 2001), thus initiatives aiming to rebuild stocks must focus on reinstating large healthy females.
To restore gadoid brood stock to a sufficient point at which population recovery would begin, a reduction in the fishing mortality rate by 30-40% was required (Cook, 1998), and in 2001 40,000 square miles of the North Sea were closed to fishing between February and April to help mitigate mortality of reproducing fish during the breeding season (Christensen, 2001). Levels of fishing has more impact on fitness and yield of cod stocks than capture length, thus stressing the importance of lowering fishing effort rather than net mesh sizes for example (Bridson, 2001). Additionally, spatial modelling suggests that the institution of no take zones or Marine Protected Areas (MPAs) should be thoughtfully undertaken so as to not encourage decreased growth rates, as persistent fishing pressure creates an artificial 'fitness' in smaller fish (Bridson, 2001). Recovery is also increasingly impacted by anthropogenic disturbances including chemical pollution, dredging, engineering works, and damage from fishing gear to the sea bed (Worm et al., 2006). Current fishing practices also waste large quantities of fish, as fishing is practiced through a quota system (ICES, 2005). Bycatch from other North Sea fisheries (and others) will inevitably include juvenile cod, which are commonly thrown back dead or dying (Hall et al., 2000).
Closure of fishing grounds must also take in to account geography and predicted climatic trends since, as discussed in section 3, natural forcing is the major driver in ocean circulation and environmental change. Cod stocks in the northern Atlantic are at an all time low, largely due to overfishing (ICES, 2005), however it is likely environmental factors are actively hampering growth and recovery of the remaining population. As discussed (e.g. Beild et al., 2001; Beaugrand et al., 2002b; Beaugrand, 2004), water temperature, salinity and water transit are importance factors in the production of phytoplankton, upon which the ecosystem depends. Cod begin to spawn in March (Conover et al., 1995), thus the spring water conditions depend on the NAO which will impact influx of freshwater from melting glaciers and pack ice, and temperature affecting primary productivity (Edwards et al., 2001). In the Grand Banks area of the Atlantic overfishing has been constantly intense for centuries (ICES, 2005), leading to the collapse of the fishery in the early 1990s forcing a moratorium on fishing. Spawning biomass had decreased by at least 75% in all cod stocks, by 90% in three of the six Grand Banks stocks, and by 99% in the case of 'northern' cod, which had previously been the largest cod fishery in the world (Ryan, 1990), and after an 18 year moratorium on fishing the cod had still not returned (ICES, 2005).
Whilst overfishing is certainly to blame for the rapid decline, some similarities can be drawn with the North Sea, as a comparable regime shift has appeared to have occurred, complicated by increasing dominance of capelin (Mallotus villosus) which prey upon juvenile cod (Conover et al., 1995). Theories on factors hampering gadoid re-growth and recolonisation in the North Sea, apply to those in the north west Atlantic (Fromentin & Planque, 1996), and governing bodies can learn stern lessons from the fate of the Grand Banks fishery, as only two strong year classes (1996 and 2009) have occurred since the crash of North Sea cod stocks (O'Brian et al., 2000; ICES, 2010), stressing the importance of the cold/warm phases of dynamic equilibrium (Beaugrand et al., 2002b). North Sea cod stock is currently dominated by immature fish and high rates of exploitation up to 2001 reduced recruits from 1996 and prevented reproduction on a large enough scale to make a significant difference (O'Brian et al., 2000). Low rates of spawning success in the North Sea correspond with a general trend in rising water temperature, suggesting the range that the cod traditionally spawn in may be moving northwards. This may be exacerbated by anthropogenic forcing of SST due to the accelerated greenhouse effect (O'Brian et al., 2000; Fogarty et al., 2008).
Regime shift in the North Sea has led to some impacts affecting the decline of the fishing industry during the latter part of the twentieth century (Chavez et al., 2003). The tragedy of the commons is widely discussed as the result of economic factors driving overexploitation and unsustainable resource exploitation throughout the world (Hardin, 1968). Not only has this led to loss of employment and livelihood within the fishing industry, it has ultimately driven what started as a natural cycle of productivity and recruitment into the regime shift we recognise has occurred in the North Sea. If this shift becomes the norm (as has occurred in the Grand Banks cod fishery), it has great potential to lead to the destruction of fisheries resources in the North Sea (Reid et al., 2001). Regime shift has also had knock-on effects on other fisheries, as the loss of productive cod fisheries in the north Atlantic has resulted in widespread exploitation of other white-fish stocks, with some catastrophic affects - the orange roughy (Hoplostethus atlanticus), a long lived and slow growing animal, has been fished in Australian waters to 10% of its total former biomass in under 10 years (Australian Marine Conservation Society, 2010). However, telling fishermen not to fish is generally politically unacceptable and leads to unemployment and degradation of tight knit communities who have relied on fishing for centuries. The impacts of large international fleets and inherent lack of any alternative to fishing complicates fisheries management, particularly in poor or developing areas. This emphasises the requirement for an integrated approach to stock assessment, controls and standards throughout the industry in order to conserve and protect our marine resources (Worm et al., 2009).
This paper has presented sufficient evidence to suggest a regime shift did occur in the North Sea; primarily caused by natural fluctuations in environmental parameters, whilst being push towards a tipping point by excessive detrimental anthropogenic disturbance. The importance of first three trophic levels within the ecosystem and species' dependence on primary productivity is clear. Observations of fish catches correspond in phase and duration to fluctuations in air temperature, atmospheric circulation and ocean temperatures (Chavez et al., 2003), and also show relationships with overfishing of other species.
In addition to natural pressures, overfishing and impacts from industry is progressively reducing the marine environment's ability to provide goods and services and to recover from anthropogenic and naturally forced shifts. Encouragingly however, data suggests that at the current state the damaged marine environment is capable of recovery (Andersen et al., 2009; Worm et al., 2006; Worm et al., 2009). This has been made possible through understanding ecological thresholds in both aquatic and terrestrial ecosystems which provide prospects of revealing patterns, and to model future events using those of the past. The role of political pressure is also becoming stronger, not only from the fishing industry but from the public. Now that the concept of regime shifts and the causes and implications are known, effort must be placed on prediction and management to conserve our precious resource.
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