From plankton to top predators: bottom‐up control of a marine food web across four trophic levels

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Abstract
Summary: Abundant mid‐trophic pelagic fish often play a central role in marine ecosystems, both as links between zooplankton and top predators and as important fishery targets. In the North Sea, the lesser sandeel occupies this position, being the main prey of many bird, mammal and fish predators and the target of a major industrial fishery. However, since 2003, sandeel landings have decreased by > 50%, and many sandeel‐dependent seabirds experienced breeding failures in 2004. Despite the major economic implications, current understanding of the regulation of key constituents of this ecosystem is poor. Sandeel abundance may be regulated ‘bottom‐up’ by food abundance, often thought to be under climatic control, or ‘top‐down’ by natural or fishery predation. We tested predictions from these two hypotheses by combining unique long‐term data sets (1973–2003) on seabird breeding productivity from the Isle of May, SE Scotland, and plankton and fish larvae from the Continuous Plankton Recorder survey. We also tested whether seabird breeding productivity was more tightly linked to sandeel biomass or quality (size) of individual fish. The biomass of larval sandeels increased two‐ to threefold over the study period and was positively associated with proxies of the abundance of their plankton prey. Breeding productivity of four seabirds bringing multiple prey items to their offspring was positively related to sandeel larval biomass with a 1‐year lag, indicating dependence on 1‐year‐old fish, but in one species bringing individual fish it was strongly associated with the size of adult sandeels. These links are consistent with bottom‐up ecosystem regulation and, with evidence from previous studies, indicate how climate‐driven changes in plankton communities can affect top predators and potentially human fisheries through the dynamics of key mid‐trophic fish. However, the failing recruitment to adult sandeel stocks and the exceptionally low seabird breeding productivity in 2004 were not associated with low sandeel larval biomass in 2003, so other mechanisms (e.g. predation, lack of suitable food after metamorphosis) must have been important in this case. Understanding ecosystem regulation is extremely important for predicting the fate of keystone species, such as sandeels, and their predators.