Fishing vs. natural recruitment variation in sandeels as a cause of seabird breeding failure at Shetland: a modelling approach Elvira S. Poloczanska, Robin M. Cook, Graeme D. Ruxton, and Peter J. Wright Poloczanska, E. S., Cook, R. M., Ruxton, G. D., and Wright, P. J. 9999. Fishing vs. natural recruitment variation in sandeels as a cause of seabird breeding failure at Shetland: a modelling approach. e ICES Journal of Marine Science, 61: 788e797. Sandeels represent a major component in the diet of fish, bird, and mammal predators as well as supporting a large industrial fishery. The availability of young sandeels in coastal waters around Shetland is generally considered a key factor influencing the breeding success of many seabird species in the area, but the risk to the populations as a direct consequence of the fishery is unknown. Low exploitation rates coupled with high natural mortality rates make assessment of the Shetland sandeel stock problematic and safe biological limits have not yet been defined. We use stochastic models to evaluate the likely effect of varying fishing mortality on kittiwake breeding success. The models consider some main sources of uncertainty about natural processes, such as recruitment and natural mortality, which may affect the design of robust management strategies. The type of model tested had a stronger influence on sandeel recruitment than the level of fishing pressure. Even with low exploitation rates, poor years for seabird breeding were inevitable. �� 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. Keywords: kittiwake, sandeel, seabird breeding, Shetland. Received 19 June 2003 accepted 23 March 2004. E. S. Poloczanska and G. D. Ruxton: Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, Scotland, UK. Present address of E. S. Poloczanska: Scottish Association for Marine Science, Dunstaffnage Marine Laboratory, Oban, Argyll PA37 1QA, Scotland, UK. R. M. Cook and P. J. Wright: Fisheries Research Services, Marine Laboratory, Aberdeen AB11 9DB, Scotland, UK. Correspondence to E. S. Poloczanska: e-mail: elvira.poloczanska@ sams.ac.uk. Introduction Sandeels (Ammodytes sp.) are small, shoaling fish that are ubiquitous throughout the North Sea, including shallow coastal waters over sandbanks (Macer, 1966 Reay, 1970). The industrial fishery for sandeels in the North Sea is the largest single-species fishery in this area. Sandeels are an important part of the marine foodweb, forming a major component in the diets of many fish, marine mammal, and seabird species (Furness, 1990 Hammond et al., 1994 Tollit and Thompson, 1996 Wright and Tasker, 1996 Greenstreet et al., 1998 Doyle and Greenstreet, 1999). The availability of young sandeels in the coastal waters around Shetland appears to be a crucial factor influencing local breeding success of many seabirds such as the kitti- wake Rissa tridactyla (Danchin, 1992 Hamer et al., 1993), Arctic skua Stercorarius parasiticus (Phillips et al., 1996) and Arctic tern Sterna paradisea (Monaghan et al., 1989, 1992 Monaghan, 1992). The dependence of seabird breeding on sandeels has resulted in conflict between the fishing and environmental interests, most notably in the Shetland area in the 1990s. Around Shetland, juvenile sandeels recruit to the fishery as 0-group fish (Wright, 1996). The fishing grounds are close inshore and often adjacent to major breeding seabird colonies (Monaghan, 1992). During the late 1980s, the breeding success of the local seabird populations declined concurrently with a decline in the sandeel population and landings. At the time, there was considerable controversy about the relationship between the fishery and the availabil- ity of sandeels to breeding birds. Environmental groups argued for a closure of the fishery as a precautionary measure. Subsequent research indicated that the decrease in the sandeel population was not caused by fishing but by environmentally induced fluctuations in recruitment (Kunzlik, 1989 Wright, 1996). Compared with the total North Sea sandeel catch of 0.5 million to 1 million tonnes per year, the fishery around ICES Journal of Marine Science, 61: 788e797 (2004) doi:10.1016/j.icesjms.2004.03.030 1054-3139/$30.00 �� 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.

Shetland is very small, averaging approximately 20 000 tonnes annually before 1991 (ICES, 2000). Following a peak in 1982 (52 000 tonnes), landings and recruitment went into decline and the fishery was closed completely at the end of the fishing season in 1990. After several years of extremely low recruitment, the production of a large year class in 1991 induced a recovery of the stock and the fishery was reopened in 1995. Recruitment to the Shetland stock is highly variable from year to year (ICES, 2000), but the mechanisms behind recruitment variability are poorly understood. At present, the fishery operates with an annual Total Allowable Catch (TAC) of 7000 tonnes and a closed season during June and July to avoid competition with seabirds during the chick-rearing season. However, landings since 1995 have been extremely low with only 1300 tonnes landed in 2001. The low exploitation rate coupled with high natural mortality makes stock assessment problematic and safe biological limits have not been defined for this stock. The ecological interactions between sandeels, their preda- tors, and the fishery remain poorly understood. Currently, the fishery is not regarded as a threat to breed- ing seabirds, but an increase in catch may reduce sandeel availability. It is assumed that high fishing activity would raise the risk of breeding failure for local seabirds. By constructing sandeel population models incorporating func- tional responses for seabird populations, it should be pos- sible to quantify the risk of breeding failure under different exploitation rates and to design suitable fishery manage- ment regimes. However, the processes involved are highly uncertain and parameter estimates have to be based on as- sumptions that are di���cult to verify. To address this problem, we developed a range of alternative population models to reflect the uncertainty about processes such as recruitment and natural mortality. The results of Monte Carlo simulations for different models were compared statistically. The performance of different management regimes was evaluated in terms of consequences for the sandeel stock, for the fishery, and for breeding seabirds. Sandeel population biology Recruitment to the Shetland stock is variable and is posi- tively autocorrelated (n �� 24 r1 �� 0:54 p!0:05) (ICES, 2000 Figure 1). In biological time-series, positive auto- correlations are considered indicative of environmental forcing (Steele, 1985 Petchey et al., 1997). Trends in spawning-stock biomass tend to follow recruitment trends with a two-year lag (Wright, 1996). Sandeels are relatively short-lived fish ( generally up to eight years) compared to most exploited North Sea fish species and become mature at two years (Macer, 1966 Gauld and Hutcheon, 1990). Adults are thought not to undertake extensive spawning migrations and during spawning attach their eggs to sand grains on the seabed (Reay, 1970 Warburton, 1982). At Shetland, larvae emerge during the early spring, when the North Sea circulation is largely wind-driven. Thus, larval transport by currents is likely to vary among years (Wright and Bailey, 1996 Proctor et al., 1998). It has been suggested that the low recruitment around Shetland during the late 1980s was caused by a reduction in the passive transport of pre-recruit sandeels from spawning grounds elsewhere, such as Orkney (Proctor et al., 1998). The size or frequency of potential influx of pre-recruits, or of losses owing to export, remains unquantified. Because fishing mortality is low (F��1e3��!0:3) compared to natural mortality rates (M��1�� �� 1:2, M��2e7�� �� 0:6 ICES, 2000), fluctuations in stock size are driven primarily by natural processes. Seabird breeding biology Seabird populations can respond to food availability in various ways, including changes in adult survivorship, chick growth, fledging success, and colony attendance (Cairns, 1987). Each of these parameters may be sensitive to a 0 50 100 150 200 250 300 1974 1977 1980 1983 1986 1989 1992 1995 Year SSB (000 tonnes) 0 50 100 150 200 250 300 350 Recruits (billions) (a) 0 50 100 150 200 250 300 350 0 50 100 150 200 250 300 SSB Recruitment (b) Figure 1. (a) Time-series of spawning-stock biomass (SSB) and recruitment and (b) stock-recruitment plot (drawn line: Ricker stock-recruitment model estimated from 10 000 bootstrap simu- lations broken lines: 95% confidence interval) for sandeels at Shetland (data from ICES, 2000). 789 A cause of seabird breeding failure at Shetland