Changes in the North Sea fish community: evidence of indirect effects of fishing?

ICES Journal of Marine Science, 62: 177e188 (2005) doi:10.1016/j.icesjms.2004.08.020 Changes in the North Sea fish community: evidence of indirect effects of fishing? Niels Daan, Henrik Gislason, John G. Pope, and Jake C. Rice Daan, N., Gislason, H., Pope, J. G., and Rice, J. C. 2005. Changes in the North Sea fish community: evidence of indirect effects of fishing? e ICES Journal of Marine Science, 62: 177e188. We investigate changes in the North Sea fish community with particular reference to possible indirect effects of fishing, mediated through the ecosystem. In the past, long-term changes in the slope of size spectra of research vessel catches have been related to changes in fishing effort, but such changes may simply reflect the cumulative, direct effects of fishing through selective removal of large individuals. If there is resilience in a fish community towards fishing, we may expect increases in specific components, for instance as a consequence of an associated reduction in predation and/or competition. We show on the basis of three long-term trawl surveys that abundance of small fish (all species) as well as abundance of demersal species with a low maximum length (Lmax) have steadily and significantly increased in absolute numbers over large parts of the North Sea during the last 30 years. Taking average fishing mortality of assessed commercial species as an index of exploitation rate of the fish community, it appears that fishing effort reached its maximum in the mid-1980s and has declined slightly since. If the observed changes in the community are caused by indirect effects of fishing, there must be a considerable delay in response time, because the observed changes generally proceed up to recent years, although both size and Lmax spectra suggest some levelling off, or even recovery in one of the surveys. Indeed, significant correlations between all community metrics and exploitation rate were obtained only if time lags R 6 years were introduced. Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. Keywords: community metrics, direct and indirect effects of fishing, Lmax spectra, size spectra. Received 4 July 2003; accepted 26 August 2004. N. Daan: Netherlands Institute for Fishery Investigations, PO Box 68, 1970 AB, The Netherlands. H. Gislason: Danish Institute for Fishery Research, Charlottenlund Slot, DK2920 Charlottenlund, Denmark; e-mail: . J. G. Pope: The Old Rectory, Staithe Road, Burgh St. Peter, Beccles, Suffolk NR34 0BT, England, UK. J. C. Rice: DFO Science Advisory Secretariat, Department of Fisheries and Oceans, 200 Kent Street, Ottawa, Ontario, Canada K1A 0E6. Correspondence to N. Daan: tel: +31 255 564646; fax: +31 255 564 644; e-mail: . Introduction 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 (Beverton and Holt, 1957). Increased post-juvenile mortality necessarily results in reduced survival and a decrease in the number of old (large) fish. Fishing may have additional, indirect effects on natural mortality. The removal of large piscivorous fish diminishes predation pressure on the size classes that they eat, thus lowering natural mortality on their prey (Pope, 1991). Similar direct and indirect effects of fishing may also be expected at the fish community level (Rice and Gislason, 1054-3139/$30.00 1996; Shin et al., 2005), because the community simply integrates the accumulated species-specific effects: an increase in exploitation rate of the entire community should lead to a reduction in the abundance of large predators and to an increase in the abundance of small prey. Both responses would make the slope of the log-linear size spectrum of the total fish community steeper, as first demonstrated by Pope and Knights (1982) for survey data. Later investigations indicated that changes in the slope are indeed related to changes in exploitation rate (Pope et al., 1987; Murawski and Idoine, 1992; Gobert, 1994; Bianchi et al., 2000; Zwanenburg, 2000). For the North Sea, Rice and Gislason (1996) showed that, as predicted, spectrum slope had steepened and intercept had increased over time Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. 178 N. Daan et al. both in survey data and in a simulated community of exploited fish stocks. Existing single- and multispecies models clearly provide a theoretical basis for testable predictions of relative effects of exploitation rate on the size spectrum, but the quantitative results depend strongly on assumptions about growth rates and recruitment patterns (Gislason and Rice, 1998). Also, the statistical interpretation of slopes and intercepts is not straightforward, because the two parameters are mutually correlated. Thus, it has remained unclear whether the spectrum changes frequently observed involve only a reduction in the absolute abundance of large fish, an increase in the absolute abundance of small fish released from predation, or a combination of both. Fishing also may directly affect species composition via the relative sensitivity of species to increased mortality (Jennings et al., 1998). As a general rule, species with a low natural mortality (M) should be more sensitive to exploitation than species with a high M, if only because a given fishing mortality (F) represents a greater relative increase in total mortality. Unfortunately, reliable information on M for non-target species is rarely available, except on very coarse scales (Musick, 1999). Therefore, we must reason our way to predictions about patterns to be observed. Even with differences in growth rate, fish must survive a relatively long time to grow large. Therefore, overall M should be inversely correlated with maximum size (Lmax), and changes in Lmax spectra might be expected to provide a measure of the indirect effects of fishing, by reflecting changes in total mortality of the species in the community. Indeed, Rogers and Ellis (2000) reported relative increases between 1901/1907 and 1989/ 1997 in the proportion of demersal fish with Lmax !30 cm in surveys around the British Isles, while Jennings et al. (1999a) showed that the mean (von Bertalanffy) LN of demersal fish in the northern North Sea declined during the twentieth century. However, the metrics used (fractions, means) do not allow clear interpretations and the changes observed might be accounted for entirely by direct effects of fishing, because the number of large fish affects the proportion of fish with large Lmax as well as the mean Lmax (or LN). In interpreting potential impacts of fishing on the community, direct effects have to be separated from indirect effects. Are the direct effects of increased mortality and reduced abundance of larger fish, and the proportionate reduction of fish with the potential to grow large, adequate to explain the observed changes, or is there evidence of indirect, compensatory (...truncated)