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The Ups and Downs of Trophic Control in Continental Shelf Ecosystems

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The Ups and Downs of Trophic Control in Continental Shelf Ecosystems Opinion TRENDS in Ecology and Evolution Vol.22 No.5 The ups and downs of trophic control in continental shelf ecosystems Kenneth T. Frank, Brian Petrie and Nancy L. Shackell Ocean Sciences Division, Bedford Institute of Oceanography, Dartmouth, NS, B2Y 4A2, Canada Traditionally, marine ecosystem structure was thought to were areas before the onset of significant commercial be determined by phytoplankton dynamics. However, an exploitation. The accumulation of knowledge on trophic integrated view on the relative roles of top-down (con- dynamics could be used to formulate ecosystem guidelines sumer-driven) and bottom-up (resource-driven) forcing in to regulate and manage fisheries in a sustainable fashion. large-scale, exploited marine ecosystems is emerging. Long time series of scientific survey data, underpinning Support for top-down dynamics the management of commercially exploited species such During the early 1990s, Parsons et al. [9] drew attention to as cod, are being used to diagnose mechanisms that could the effects of top predator removal by marine fisheries, affect the composition and relative abundance of species using examples from the Atlantic, Pacific and Antarctic in marine food webs. By assembling published data from Oceans. The effects ranged from replacement by alternate studies in exploited North Atlantic ecosystems, we found predators, increased production at lower trophic levels, pronounced geographical variation in top-down and bot- and/or long-term ecosystem-level change. More recently, tom-up trophic forcing. The data suggest that ecosystem Reid et al. [10] concluded that, although there were few susceptibility to top-down control and their resiliency to convincing examples of top-down control, particularly in exploitation are related to species richness and oceanic the well-studied North Sea, the Barents Sea ecosystem temperature conditions. Such knowledge could be used provided a clear example of top-down and size-selective to produce ecosystem guidelines to regulate and manage predation by fish on zooplankton. fisheries in a sustainable fashion. The Barents Sea is a relatively simple, low-diversity arctic system in contrast to the species-rich, temperate The structure of marine ecosystems North Sea. By analyzing time series of cod Gadus morhua The traditional view of how marine ecosystems are (predator) and shrimp Pandalus borealis (prey) abun- structured is based on resource control, where phytoplank- dances from several North Atlantic continental shelf ton dynamics determines the production and biomass locations, Worm and Myers [11] revealed precipitous variability of the upper trophic level [1–5]. The alternative declines in cod stocks followed by large increases in shrimp viewpoint of consumer or top-down control, where preda- populations in most areas examined. The authors con- tion determines the abundance and composition of prey, cluded that predation was a strong structuring force in was considered limited to nearshore or intertidal commu- the North Atlantic, with a few exceptional areas mainly nities involving one or two dominant predator and prey near the southern limit of the species where bottom-up species [6,7]. Until recently, continental shelf ecosystems processes dominated [11]. were thought immune to top-down control, because of their relatively large spatial scales, high species diversity and Unexpected impacts of overfishing food-web complexity. Steele [8] contended that he knew of The slow recovery (in several instances, their failure to no cases where large changes in predatory marine fish recover [12,13]) of several collapsed North Atlantic cod stocks had affected their food supplies, in other words no populations has also fueled an interest in trophic forcing, top-down control. particularly as it relates to the formation of alternate Here, our viewpoint is based on recent studies of heavily ecosystem states [14,15]. Top-down forcing can lead to a exploited ecosystems in the North Atlantic Ocean whose ‘quasi-permanent’ ecosystem change (i.e. a regime shift type of trophic forcing was assessed from correlations typified by fundamentally different structural and func- between time series of the relative abundances of succes- tional attributes from the one preceding it). Strong [16] sive trophic levels (or species). The response (correlation) maintains that top-down structuring is not the norm for varies temporally and spatially, with a geographical distri- ecosystems but instead represents a form of biological bution that is statistically related to species richness and instability. When larger predator species are depleted ocean temperature. We suggest that species-rich, warmer through overfishing, the balance between predator and water areas are more resilient to exploitation than are prey populations is disrupted. The imbalance can impede relatively species-poor, colder regions. It also appears that the recovery of predators by increased predation and/or undisturbed areas are structured from the bottom up, as competition for food from their prey during the early life stages of the predators [17,18]. This predator–prey role Corresponding author: Frank, K.T. ([email protected]). reversal has been implicated for cod and herring in the lack Available online 12 March 2007. of recovery of cod in the southern Gulf of St Lawrence [19]. www.sciencedirect.com 0169-5347/$ – see front matter . Crown Copyright ß 2007 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2007.03.002 Opinion TRENDS in Ecology and Evolution Vol.22 No.5 237 In the North Sea, populations of grey gurnard Eutrigla The bottom-up versus top-down controversy gurnardus (an early maturing benthic fish species of no Hunt and McKinnell [24] discuss the complexity of commercial value) have increased dramatically and occupy unraveling the effects of trophic forcing within ecosystems an ecological niche similar to that filled by the once domi- and contend that the necessary data to test hypotheses nant cod. The habit of gurnards of feeding on juveniles of about predator effects on trophic structuring in marine commercially exploited species and their greatly expanded systems are generally lacking. Other investigators have spatial distribution have also been implicated in the lack of lamented that studies involving exploited marine ecosys- recovery of North Sea cod and whiting stocks [20]. tems have reached no consensus on how animal abun- Cury and Shannon [21] discussed how overfishing has dances and productivities are controlled, with apparent initiated and maintained a regime shift within the Ben- demonstrations of both top-down and bottom-up controls guela upwelling system off South Africa through tightly [25]. Still others believe that the tendency for interpreting coupled predation processes, including predator–prey role all marine pelagic food webs from a resource perspective reversals. This suggests that top-down processes are cas- alone has resulted in limited understanding and poor cading to lower trophic levels, resulting in conspicuous predictability of the processes influencing the structure indirect effects that lead to a reorganization of the entire and function of these ecosystems [26]. Unfortunately, stu- food-web. Such a condition (i.e. a trophic cascade) has been dies that have given balanced attention to top-down and repeatedly documented for several freshwater systems bottom-up processes are rare, owing in part to the lack of [22], although infrequently for large marine ecosystems. data sets that include time series of multiple trophic levels An examination of trophic forcing was made within a within and among years [27]. A previous study of a rela- single geographical area, the eastern half of the continen- tively data-rich region (the western North Atlantic) tal shelf off Nova Scotia, Canada, where the resident cod has addressed the spatial and temporal aspects of these population, which had been subject to ongoing heavy processes [28]. exploitation, collapsed during the early 1990s and has failed to recover, despite the cessation of fishing for over The importance of context (where and when) a decade [23]. Analysis of time series spanning several Where decades revealed top-down control and a trophic cascade Frank et al. [28] examined abundance time series of several emanating from the top predator level, resulting in alter- species of predators and prey from nine heavily exploited nating changes (i.e. negative correlations between adjacent regions in the western North Atlantic. The data were tropic levels) in abundance from planktivorous fish species derived from fishery-independent surveys that collect all to herbivorous zooplankton and then to phytoplankton fish species at all life stages (except eggs and larvae). The (Figure 1 [23]). The cascade further penetrated to the basal resultant estimates of numerical abundances are generally nutrient level, as nitrate concentrations were negatively reliable from age 1 onward and diminish the need to correlated with phytoplankton abundance. This study introduce time lags into the correlation analysis because clearly demonstrated that strong, possibly irreversible, the expression of change in abundance of the components cascading effects can occur in marine systems. species making up a trophic level occurs relatively rapidly. Figure 1. Geographical location of the assembled data on trophic forcing. Dot colour refers to the type of trophic forcing and the number on the dot refers to the data source (Table 1). Green dots represent correlation coefficients
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