Present Status And Future Of The North Sea Pelagic Food Web

The North Sea, considered one of the most heavily fished areas in the world, dramatic changes in abundance, community composition and phenology of plankton at lower trophic levels have been documented and linked to climate change (Beaugrand, 2004). Delicate, yet intensive, research has been wandering for decades around the correlations between the trophic levels and the effects they dictate on one another. One argument that is almost out of discussion now is the fact that climate-driven changes in plankton communities affect higher trophic levels depending on the structure and function of the ecosystem mode of regulation (Frederiksen et al., 2006). Many species of seabirds in the North Sea reply intensively on a single species of fish, the lesser sandeel Ammodytes marinus (hereafter 'sandeel) in order to rear their young (Pearson, 1968). In other North-east Atlantic areas as Shetland, however, there appears to be no alternative high-energy prey, i.e. sandeels, and if these were not available, breeding of seabirds would be poor or even cease (Wright, 1996). On the contrary, birds that breed to the south of the North Sea have potentially various pelagic prey species, especially the energy rich sprat Sprattus sprattus.

The lesser sandeels, mentioned above, play one of the most important roles in the structure and functionality of the marine ecosystem of the North Sea. In fact, these species are abundant mid-trophic pelagic fish that act as links between zooplankton and top predators as well as being principal fishery targets. Sandeel abudance may be regulated 'bottom-up' or 'top-down' controls. Specifically, understanding the relative importance of both mechanisms will be critical for predicting impacts on top predators, notably seabirds. Top-down effects imply control through predation, including fishery, while bottom-up effects designate control through food abundance, almost usually driven by climate or nutrient load (Furness, 2004). Temperate marine environments may be particularly vulnerable to these changes- be them affecting the first tropic level or the closing parameter denoted by the top predators- because the recruitment success of higher trophic levels is considerably dependent upon synchronization with pulsed planktonic production (Cushing, 1990). Hereby, we find it crucial to deal with phenology, the study of annually recurring life cycle events of different species assuming various functions in successive trophic groups, and consequently assess to the match/mismatch hypothesis that would, by far, affect the breeding and prosperity of a certain lineage of species, namely North Sea seabirds in our current report (Edwards and Richardson, 2004). ????

"Why use seabirds as indicators of marine ecosystem changes?"

There exists a substantial policy-driven need to find accurate and reliable indicators of the ecological state of marine environment on the road to manage and sustain living resources (Rice and Rochet, 2005). In an attempt to manage these resources, delicate and extensive timely information on crucial fluctuations in the ecosystem should be obtained (Botsford et al., 1997). By analyzing time series data of the North Sea among many other ecosystems, it was proven that biological data are more reliable for use than physical ones to assess the ecological fluctuations in a certain area as they tend to vary less on annual basis. Even so, biological time-series may also be confusing when they coexisting marine species respond in a different manner to ecosystem variability (Hare and Mantua, 2000). In terms of marine species, seabirds represent the perfect indicators of marine ecological changes, no matter what the reasons behind such variabilities are. Seabirds offer many advantages namely:

- They are highly visible animals in an environment in which most other plants and animals are hidden underwater. - They are smoothly enumerated as they travel or forage in productive marine hotspots (Sydeman et al., 2006). - Seabirds are mostly colonial species that gather annually in large numbers at relatively few locations for the sake of reproduction. - They are sensitive to variation in food supply, relatively easy to study and have a high public profile (Montevecchi, 1993).

Heretofore, assessing the contributory role of seabirds to the energy flow chain across the trophic levels of the North Sea is fundamental to draw a far more detailed picture as to what controls the balance of the North Sea pelagic food web, how seabird breeding success or failure might affect other species coexistence- be them in higher or lower trophic levels- and to what extent do the anthropogenic activities, namely those leading to climate change, play a role in creating a match/mistmatch correlation in predator-prey relationships.

"Changes in the North Sea pelagic food web"

The North Sea is a shelf sea of the North Atlantic Ocean where relatively shallow water and high nutrient inputs sustain a highly productive ecosystem. Copepods comprise up to 90% of mesozooplankton (referred to hereafter as zooplankton) biomass in both shallow-mixed and summer-stratified regions (Williams et al., 1994). The abundance of zooplankton in the central and northern regions of the North Sea is directly related to the inflow of North Atlantic water, which re-introduces species such as Calanus finmarchicus, Calanus heldolandicus and Candacia armata each spring from overwintering stocks off the North Atlantic shelf (Fransz et al., 1994). The distributions of such species within the shallow pelagic North Sea waters are determined by currents and atmospheric features including seasonal forcing. For example, C. armata's abundance has increased after 1997 with increasing inflow of North Atlantic water into the northern North Sea (Ku''rten et al., 2012). ?????? ???As mentioned in the first section of this report, various trophic levels coexist in the North Sea marine ecosystem and they aid in the interplay of energy flow and biomass distribution. In North Atlantic shelf seas as the North Sea, calanoid copepods such as Calanus spp., Temora spp. and Centropages spp. play major roles in transferring energy mainly in the form of (essential) fatty acids to higher trophic levels such as cod and herring (Beaugrand et al., 1993). In a research paper by Michael Heath over the changes in the structure and function of the North Sea fish foodweb, Heath indicates that the latitudinal ranges of Subarctic zooplankton taxa and temperate copepod species in the northeastern Atlantic have both shifted northwards over the last 40 years, in concert with warming sea temperatures and changes in climate indices such as the North Atlantic Oscillation index (NAO) (Heath, 2005). This, by his evidence, has resulted in a fundamental change in species compostion of zooplankton in the North Sea, particularly the substitution of Calanus finmarchicus by smaller temperate copepod species (Beaugrand et al., 2002). In the same vein, correlations between phytoplankton and zooplankton abundances over large spatial and temporal domains indicate a tight "bottom-up" control of the planktonic foodweb. In Heath's study, it was shown that the pelagic side of the fish foodweb was controlled by production processes (bottom-up), while the demersal part was under the mercy of predation pressure (top-down control). The study period spans almost 30 years, but it begins in 1973 during the "gadoid outburst" in the North Sea. If zooplankton production was controlled by predation pressure, an inverse relationship must have existed between consumption and production, but this was not the case. A lack of inverse relationship between planktivore production and consumption by piscivores; fish feeding on other smaller fish, stands as a mere conclusion that planktivorous fish production is not limited by predation. This production is mostly controlled by bottom-up processes such as new primary production, physical oceanographic, and climate-related phenomena (Heath, 2005). In yet another vein, macrobenthos production showed an inverse trend to the consumption of benthos by demersal (benthic) fish, a clear suggestion that predation is the major control on macrobenthos production.

"Dynamical relationships between the benthic and pelagic foodwebs of the North Sea"

Even though the interest in our report is based on unveiling the trends, changes, and consequences of dymanic relationships between species in the pelagic side of a trophic level, one should bare in mind that the marine ecosystem, as any other terrestrial ecosystem is a multidisciplinary and multivariate one. What happens in the far benthic parts of the North Sea almost always affects the interrelations coexisting in the more pelagic regions of the sea. The main feature of the modern system is the near absence of large fish (<4kg), which would be principally demersal piscivores and benthivores (Heath, 2005). Depletion of benthos-consuming fish, through a combination of fishing and climate (discussed later), has shifted the structure of the secondary production demand at the base of the foodweb towards zooplankton, and released the benthos from predation pressure, causing an increase in macrobenthos production. This brings up the fact that planktivorous fish production correlates directly to that of the zooplankton, thereby assuming that the shift in structure in the benthos will have made the system as a whole more vulnerable to climatic fluctuations. For our purpose, we'll be focusing on the causes of low breeding success in seabird species and their long-term changes in phenological trends in the North Sea.

"Causes of low breeding success and survival of seabirds"

A study by Frederiksen on the reasons behind the decline of North Sea black- legged kittiwakes, breeding success at the Isle of May was shown to be high during the late 1980s, very low during the 1990s and showed a partial recovery in 2000-02 (figure 1). Many similar patterns occurred at various British kittiwake colonies along the North Sea during this period (Mavor et al., 2003). The period of low breeding success coincided with the activity of the Wee Bankie sandeel fishery, but when the 2 years with very low catches (1990 and 1998) were excluded the correlation was less strong. When all fishery years were included, the presence or absence of a fishery explained 70% of the observed between-year variation in breeding. Nevertheless, when winter sea surface temperature ???(SST) during the previous year was included in the model, a very large part of the variation; in fact 81% of it, was explained (Frederiksen et al., 2004). Figure 1. Kittiwake breeding success on the Isle of may 1986-2002, expressed as the number of fledged chicks per completed nest. Weighted means and 95% confidence limits of 15 monitoring plots (10 in 1986) are shown. It seems obvious that the effect of sea surface temperature on kittiwake breeding success and survival must be mediated by the sandeel availability. A possible scenario embraced and proved highly possible by figure 3 is the following: warm winters lead to low sandeel recruitment, perhaps by reducing the food supplies available to larval sandeels (Arnott and Ruxton, 2002). Kittiwakes from the same year start feeding on that weak class of growing sandeels during chick rearing in June. This, however, is insufficient to affect the breeding success of the seabirds in that certain year, yet it will have abrupt effects on the adults, and presumably fledgings, at the end of the breeding season and so the overwinter survival of adult kittiwakes is correspondingly low. Because sandeels older than 1 group constitute a relatively small proportion of kittiwake diet (Lewis et al., 2001), breeding adults in the next spring will be poorly fed by the same weak year class as the previous one. ? ??? 1. FISHING

Low trophic-level (LTL) fish species in marine ecosystems comprise species that are generally plankton feeders for the larger part of their life cycle. These species play a fundamental role in marine food webs because they are the principal means of transferring production from plankton to larger predatory fish and to marine mammals and seabirds (Smith et al., 2011). Several studies have raised concerns over the future of seabirds in times where forage fish are being seriously depleted. Sandeels in North Sea, Anchovy in Peru, and sardines in South Africa are all being threathened by overfishing and so are the seabirds depending on them for their survival. The impacts of harvesting a certain LTL species had different impact in each ecosystem; for our concern, the fishing sandeels had the highest impact in the North Sea.

?The primary effect of fishing on a population is an increase in total mortality because the removals by fishing are added to the other sources of mortality. Increased post-juvenile mortality obviously results in reduced survival and a decline in the numbers of old fish. Fishing can also manipulate the size of smaller fish from lower trophic levels on which large piscivorous fish feed; when large fish are removed, the natural mortality of their smaller prey is lowered. ?Figure 3. Effects of level of depletion of LTL species on the proportion of other trophic groups whose biomass varied by more than 40% relative to their level where the LTL species was not fished. Results are shown for a variety of LTL species fished in each modeled ecosystem.

Results from a study by Daan et. al in 2005 show that considerable time lags would be involved in the responses of the fish community to fishing, though the interpretation of a scenario remains complicated. Small and medium class size fish reflect increased survivorship owing to reduced predation as a result of fishing activities, so the delays suggest accumulation of effects across several years (Daan el al., 2005). Fish having low maximal length (Lmax) would spend long times in the smallest size classes experiences low predation pressure so their abundance is keen to increase. This goes without mentioning that if exploitation of fisheries persists, the number of large fish would still vastly decline and intensify the previous scenario. Size-dependent predation would most possibly shrink as a result of increase in absolute numbers of small fish, yet these facts seem to be somehow generalized and might not account for time lags exceeding a dozen years (Daan et al., 2005). Since seabirds and other piscivorous fish depend on smaller fish for their survival, breeding success and adult survival were low when the sandeel fishery was active (1991-1998) and experienced a relative recovery in 2000-2002 after the fishery was closed. The large increase in 1+ group abundance (sandeels aged 1 year or older) was likely to be the combined effects of a substantial decline in fishery removals of sandeels of this age group in 1999 and recruitment of stronger 0 group cohort in 1999 compared with that in 1998 (Greenstreet etl al., 2006). The latter phenomenon, however, was proved to be the effect of environmental factors that can affect sandeel growth during early larval stages in the breeding season. Hereby, one finds it crucial to assess the environmental conditions aiding in the interplay over the breeding success of seabirds through influencing the sandeel abundances in the North Sea.

2. CLIMATE AND ENVIRONMENTAL IMPACT

Climate influences a population through a variety of processes, including reproduction, growth, migration patterns and phenology. Climate may operate either directly through metabolic and reproductive processes or indirectly through prey, predators, and competitors (Durant et al., 2007). In the North Sea, scientists believe that a ?'regime shift', a term used to describe large, decadal-scale switches in the abundance and composition of plankton and fish (Reid, Borges, and Svendsen, 2001), has altered the mechanisms by which species from different trophic groups interact. This regime shift was a result of increase in oceanic inflow into the North Sea due to intensified wind and the state of North Atlantic Oscillation. As a consequence of different species reacting dissimilarly to such phenomena, even minor changes in climate state may invoke non- linear responses unbalancing established patterns of synchrony. Put in simple words, all components of a food chain cannot be expected to shift their phenology at the same rate, and thus are unlikely to remain synchronous (Durant et al., 2007). Other local short-term environmental causes as the sea surface temperature (SST) proved to have an effect on resident species (shag) more than the widely dispersing species (Kittiwakes and guillemots), which are influenced merely by the large-scale NAO (Frederiksen et al., 2004). Other anthropogenic as pollution and oil spills also account for the reduction of the total abundance of seabirds that are induced to immigrate or are doomed in the North Sea. Oil pollution may impact upon seabirds directly via fouling or ingestion, or indirectly by reducing the availability of key food species (Votier et al., 2005).

"Future Scenarios and Prospects"

Evaluation of the findings from the existing scheme thus indicate that the 2004 failure in seabirds breeding had a complex causation- a combination of industrial overfishing and climatic change- and that, while monitoring kittiwake reproductive success was useful, data from a single species with a specialized feeding method and a correlative approach were not sufficient to identify the mechanism(s) involved. This highlights the urgent need for more detailed research that integrates monitoring, targeted data collection (including experiments) and modeling. We must quantify trophic interactions better and come to understand the impacts of environmental influences and the contexts in which they occur. This will improve the quality of advice available to fishery managers, conservationists and policy makers (Wanless et al., 2007).