ICES mar. Sei. Symp., 193: 1. 1991

Multispecies Models Relevant to Management of Living Resources

Preface

Scientific quality is undoubtedly the most important bers of the Steering Committee. In addition, they would aspect of a contribution to a symposium, but the value of like to thank the referees of the papers selected for a contribution is also greatly heightened by a vivid and publication for their invaluable contribution and ex­ stirring presentation, and the discussion it stimulates. In pertise in formulating many suggestions for improve­ order to underline the importance of the latter in com­ ment. It seems only appropriate that the names of these municating scientific results, it was decided to give scientists be listed here: R. S. Bailey, N. J. Bax, W. awards for the “best presentations”. On the basis of a Brugge, S. Clark, E. B. Cohen, W. Dekker, W. Gabriel, plenary vote, the awards were presented to H. Gislason S. Garcia, H. Gislason, J. Gulland, T. Helgason, J. R. (paper) and to M. Tasker, R. Furness, M. Harris, and G. Hislop, M. Holden, E. Houde, G. R. Lilly, J. R. S. Bailey (poster) for their excellent use of audio­ McGlade, G. Magnusson, R. Marasco, B. M. van der visual aids. Meer, S. Mehl, B. Mesnil, S. A. Murawski, W. J. The Co-conveners would like to express their grati­ Overholtz, O. K. Pâlsson, D. Pauly, E. K. Pikitch, J. G. tude to J. Harwood (UK), A. Laurec (France), J. G. Pope, J. E. Powers, J. C. Rice, A. Rosenberg, B. J. Pope (UK), and H. Sparholt (Denmark), who put great Rothschild, K. J. Sainsbury, F. M. Serchuk, T. Smith, effort into the organization of the Symposium as mem­ H. Sparholt, W. Stobo, K. J. Sullivan, and C. Tucker.

1 ICES mar. Sei. Symp., 193: 209-216. 1991

Recent changes in the population of the sandeel {Ammodytes marinus Raitt) at Shetland in relation to estimates of seabird predation

R. S. Bailey, R. W. Furness, J. A. Gauld, and P. A. Kunzlik

Bailey, R. S., Furness, R. W., Gauld, J. A. and Kunzlik, P. A. 1991. Recent changes in the population of the sandeel (Ammodytes marinus Raitt) at Shetland in relation to estimates of seabird predation. - ICES mar. Sei. Symp., 193: 209-216.

Recent changes in the Shetland population of the lesser sandeel (Ammodytes marinus Raitt) have been investigated using data from commercial catches and research-vessel surveys using small-mesh midwater trawls. Both recruitment and total stock size have decreased since the early 1980s. Over the period 1981-1988 there has also been a decrease in consumption of sandeels by seabirds. On the assumption that the natural mortality rate has not changed, the predation mortality caused by seabirds (i.e. the fraction of the population taken) has not decreased significantly. These findings indicate that the switching of seabirds from sandeels to other prey is in approximate proportion to the abundance of sandeels, and that there is no evidence of a non-linear functional response. The estimates on which this analysis is based are subject to considerable uncertainty, however, and annual data on the consumption of sandeels and other prey (in terms of numbers at age) by each of the main groups of predators would be needed to refine the analysis significantly. The importance of incorporating consumption by seabirds and other predators in future assessments of this stock is stressed.

R. S. Bailey, J. A. Gauld, and P. A. Kunzlik: The Scottish Office Agriculture and Fisheries Department, Marine Laboratory, P.O. Box 101, Victoria Road, Aberdeen AB9 8DB, Scotland. R. W. Furness: Applied Ornithology Unit, Department of Zoology, University of Glasgow, Glasgow G12 8QQ, Scotland.

Introduction seabirds, fisheries, and sandeel stocks in this area are of considerable interest to both fisheries scientists and Sandeels (Ammodytidae) are numerically among the ornithologists (Heubeck, 1989). most abundant fish in the North Sea (Yang, 1982). As In recent years, there has been a decrease in the well as supporting large fisheries, they are important in breeding success of several species of seabirds at Shet­ food chain dynamics, and many predators (fish, sea­ land which has been attributed to a shortage or non­ birds, and marine mammals) prey heavily upon them availability of sandeels (Heubeck, 1989). In addition, (Harwood and Croxall, 1988; Daan, 1989; Furness, while historical data indicate large increases in several 1990). Since 1974 there has been a sandeel fishery in seabird species to unprecedented numbers in the late inshore waters around Shetland which takes almost 1970s (Thom, 1986), the numbers of breeding pairs have exclusively the lesser sandeel (A m m odytes marinus recently decreased in some species (Furness, 1989). Raitt). Landings rose to a peak of 52000 t in 1982 and These findings imply that the quantity of sandeels taken have subsequently decreased to a much lower level annually by seabirds may vary. Correspondingly, it is (Anon., 1989). also possible that the fraction of the sandeel population Sandeels form one of the most important items of the taken by seabirds varies as stock size changes. In the food of many species of seabirds at Shetland, especially absence of prey-switching, seabirds might be expected during the breeding season (Heubeck, 1989). The esti­ to show increased predation rates (i.e. take a greater mated quantity of sandeels consumed by seabirds at percentage of the available prey) as stock declines owing Shetland in 1981-1983 was about 49 000 t yr~1 (Furness, to their rather stable food requirements. Alternatively, 1990), that is approximately the same as that taken by if seabirds switch diet as the sandeel stock declines then the fishery. Thus the potential interactions between the predation rate by seabirds might fall or remain the

209 same. At present, there is no recorded information January-June: about the functional response of seabirds to changes in 1.0 and 0.4 for 1-group and older fish, respectively; sandeel abundance. July-December: The purpose of this paper is to summarize the evi­ 0.8 and 0.2 for 0-group and older fish, respectively. dence for the recent changes in Shetland sandeel popu­ lation size and to examine the influence of these changes It is now known whether these values based on the entire upon the predation rate by seabirds, with particular North Sea are appropriate for the local Shetland stock, regard to the implications for the value of natural mor­ although values of total mortality calculated from catch tality rate used in fish stock assessment. Since the rele­ per unit effort data obtained during the first few years of vant data on seabird food consumption are not available the Shetland fishery indicate that M cannot be appre­ for all years, the approach taken has been to compare ciably higher than the values given above (A non., 1982). the data from 1981 and 1988, years contrasting in the Values of M are assumed to be constant from year to stock size of sandeels and in the quantity of sandeels year. consumed by seabirds. Additional data on the abundance of 0-group sandeels in the Shetland area have been obtained from an annual midwater trawling survey of the northwestern North Sea carried out from 1969 to 1988. During these surveys, a pelagic trawl especially designed to catch small gadoid Methods fish and fitted with a knotless codend of 11 mm stretched For assessment purposes the Shetland sandeel popu­ mesh was towed in a series of stepped hauls fishing close lation is treated as a separate stock (Anon., 1989). This to the bottom, roughly in the middle of the water column is justified on the grounds that the fishing areas around and within about 10-15 m of the sea surface (Holden, Shetland are close inshore (Fig. 1) and therefore isolated 1981), and provided samples of sandeels as well as other from sandeel fishing grounds in other parts of the North small fish. Sea, and that growth rates at Shetland are much lower Numbers of breeding pairs of seabirds in Shetland than in other areas of the northern North Sea where over the years 1981-1983 and in 1988 have been taken sandeel fisheries take place (Anon., 1979). While this from compilations of census data (Tasker et al., 1987; does not necessarily mean that the Shetland population Heubeck, 1989). Decreases in numbers of each species is totally isolated from other populations, it is likely that from 1981-1988 have been estimated to the nearest 10% sandeel population dynamics at Shetland are governed as census data and variations between colonies within principally by local events rather than by immigration or Shetland do not allow a more precise treatment. The emigration, at least after the juveniles have recruited to breeding success of seabirds in 1981 and 1988 was the population at around six months of age. The bound­ recorded in colonies at Foula as well as in several other aries of the Shetland area used for stock assessment colonies in Shetland (Heubeck, 1989). purposes and the fishing grounds at Shetland are shown Seabird feeding data are available from various colon­ in Figure 1. ies for the period 1975-1983 and for 1988. For some Throughout the sandeel fishing season at Shetland, species, dietary data have been collected by indepen­ which usually lasts from April to September, samples of dent studies at two or more colonies. Thus, puffins sandeels were taken every month from a random sample Fraterculu arctica have been studied at Unst (Martin, of vessels landing at the fishmeal plant on Bressay and at 1989), at Foula (Furness, 1990), at Fetlar (Harris and Scalloway. From half-yearly landings in numbers at age Hislop, 1978), and at Fair Isle (Harris and Riddiford, (Anon., 1989), estimates of stock size were made by 1989). In general, dietary variation between Shetland virtual population analysis (VPA; Gulland, 1983). To colonies has been found to be small and so studies at a allow for fish dying from natural causes, estimates of the single colony are taken to represent Shetland as a whole. instantaneous natural mortality coefficient (M) were Over the period 1975-1983, there were no clear changes derived from a multispecies model for the whole North between years in breeding success or diets except for a Sea (Anon., 1988). Values of M were based on estimates declining prevalence of sandeels in gannet Sula bassana of the numbers of sandeels eaten by the main fish diet as herring Clupea harengus increased (Martin, predators and rough estimates of quantities eaten by 1989) and a declining frequency of sandeels in the diet of other predators and of quantities that die from other non-breeding great skuas Catharacta skua (Furness, causes. The estimates of consumption by other fish were 1987). Thus, dietary data for all the years 1975-1983 based on extensive stomach sampling in 1981 (Daan, have been pooled (except for gannet) to represent diets 1989) and on a multispecies virtual population analysis of breeding seabirds and chicks in 1981. Further infor­ in which it was assumed that the suitability of different mation on this compilation of dietary data is given in prey organisms remained the same over the period Furness (1990). 1981-1988 (Anon., 1988). The values of M (yr~H'5) Daily consumption of sandeels by each seabird species obtained were was estimated by multiplying breeding numbers by their

210 f r ~

59°30' J ____

Figure 1. Map showing the position of the Shetland sandeel fishing grounds (filled circles). The inset shows: (a) the Shetland sandeel assessment area used by ICES (Anon.. 1989); and (b) the survey area referred to in Table 2.

estimated daily food requirement during chick-rearing been shown to contribute little to the total population and by the proportion of sandeels intheirdiet.Thedaily budget (Furness, 1978) and diets of non-breeders tend to energy requirement was taken as 3.5 times the basal differ from, and contain less sandeels than, diets of metabolic rate (BMR) with a 30% increase for food breeders or chicks (Hudson, 1986; Furness, 1987). requirements of chicks (Furness, 1978). The factor of 3.5 represents the mean of some 20 studies of daily energy Results budgets of seabirds measured using labelled water (Fur­ ness, 1990). No allowance was made for food require­ The numbers at age and biomass of the sandeel popu­ ments of non-breeders, as these have previously lation as estimated by the ICES Industrial Fisheries

211 Tabic 1. Estimated numbers of sandeels at age (millions) in the Shetland assessment area (Fig. 1 ) at 1 July and total stock biomass (tonnes) at 1 January (TBM) from 1974 to 1988 (from Anon., 1989).

1974 1975 1976 1977 1978

0 13 898 32076 41 765 48257 36663 1 4015 1973 3459 4186 4 372 2 451 1242 866 1 085 1 119 3 136 126 600 339 452 3=4 167 97 82 282 275

TBM 41 770 34 566 50640 66 954 78 845

1979 1980 1981 1982 1983

0 30605 42 783 76083 81180 74 926 1 3528 4426 4264 6240 8090 2 1794 1363 1 405 1 147 2626 3 538 653 397 428 402 &4 373 274 311 193 194

TBM 65 389 68 725 77 152 102117 109895

1984 1985 1986 1987 1988

0 29 188 21 343 19451 2208 20 750 1 10 144 3067 2742 2398 253 2 3088 5022 1 247 I 405 1 126 3 1066 1467 2396 641 674 147 566 868 1721 1205

TBM 138 177 99893 86 755 72421 47315

Working Group using VPA are shown in Table 1 Combining estimates of BMR (Table 5) with the (Anon., 1989). This analysis indicates that the total population and dietary data in Table 4 yields daily stock biomass at 1 January increased over the period consumption of sandeels during the chick-rearing period 1974-1984. Subsequently, recruitment has been below in 1981-1983 and 1988 as shown in Table 5. Sandeel average and stock biomass has fallen. Densities of sandeels expressed as the number caught per unit time in ICES statistical rectangles adjacent to Table 2. Geometric mean numbers of sandeels (all age groups) Shetland (Fig. 1) are given in Table 2. A high proportion caught in small mesh midwater trawls around Shetland (cf. of these fish were 0-group, so this provides an indication Fig. 1.). of the abundance of each year's recruiting age group in Mid-date No. of offshore waters. A marked decrease in the abundance of Geometric Year of survey hauls mean 0-group sandeels is indicated after 1982. The estimated total biomass of sandeels on 1 July, 1969 8 July 23 12.20 commercial catch, and total production of the stock, 1970 27 June 3 279.00 defined as biomass dying plus change in biomass, are 1971 24 July 17 5.80 1972 27 July 14 0.93 given for each year 1974-1988 in Table 3. These data 1973 20 July 4 242.00 indicate a pronounced decrease in total production from 1974 18 June 6 25.80 1983 to 1987. In fact, production in 1987 is estimated to 1975 1 July 6 1301.00 have been less than the 490001 of sandeels estimated to 1976 23 June 3 744.00 1977 26 J une have been taken by seabirds in the years 1981-1983 9 208.00 1978 1 July 7 1368.00 (Furness, 1990). 1979 16 June 7 115.00 Most breeding seabirds in Shetland fed themselves 1980 21 June 6 6.40 and their chicks predominantly on sandeels in June-July 1981 14 June 5 75.80 1975-1983, but several species had changed diet in 1988 1982 28 June 6 14.90 1983 27 June 4 0.41 (Table 4). Populations of several species declined be­ 1984 No survey -- tween 1981 and 1988 and several (an overlapping subset) 1985 22 June 5 0.43 suffered breeding failures in 1988 (Table 4). There is, 1986 5 July 5 0.00 however, no direct correlation between these two 1987 17 June 4 0.50 1988 effects. 15 June 6 0.86

212 Table 3. Estimated total biomass at 1 July, annual change in biomass, biomass dying by all causes, commercial catch, and total production of A. marinus in the Shetland assessment area (Fig. 1) for each calendar year from 1974 to 1988 (data from Anon., 1989). All figures in tonnes.

Total Change in Biomass Commercial Total Year biomass biomass dying catch1 production

1974 49 900 -7200 48100 8 540 40900 1975 75400 + 16100 68 400 13 500 84500 1976 100600 + 16300 83400 17 800 99700 1977 116600 + 11900 103 900 25 100 115 800 1978 99400 -13400 104 500 32400 91 100 1979 92100 +3300 77800 13 700 81 100 1980 113 600 +8400 97000 22100 105 400 1981 167400 +25 000 147 100 44 500 172100 1982 182600 +7800 177 100 57500 184 900 1983 191500 +28300 159500 27900 187 800 1984 133 300 -38300 134 500 28 700 96200 1985 108 6(M) -13100 84800 14100 71700 1986 89500 -14300 73 000 12000 58700 1987 54 100 -25 100 45 400 5 300 20300 1988 68400 +7 100 45300 3 900 52400

1 For comparability, these are estimated by multiplying the numbers caught at each age by mean wcights-at-agc in the catches. They may not therefore equate exactly to the reported annual catches.

Table 4. Average number of breeding pairs in 1981-1983 (N), percentage decrease in 1988 compared to 1981-1983, breeding success and percentage of sandeels in the diets of breeding adult seabirds and their chicks in June-July for study periods 1981-1983 and 1988 in Shetland.

2 Breeding pairs Chicks per pair1 % sandeels

N % decrease Species 1981-1983 1988 1981-1983 1988 1975-1983 1988

Red-throated diver 700 10 0.6 0.3 95 17 Gavia srellata (62) (41) Fulmar 200000 0 0.6 0.3 70 5 Fulmarus glacialis (177) (28) Gannet 20000 0 0.6 0.6 80 5 Sula bassana (137) (111) Shag 8300 30 1.4 1.4 100 100 Phalacrocorax aristotelis (500) (35) Arctic skua 1 900 40 1.1 <0.1 100 100 Stercorarius parasiticus (200) (20) Great skua 5 600 10 1.2 0.0 70 5 Catharacta skua (>900) (322) Herring gull 4 500 20 0.5 nd 20 0 Larus argentatus (50) (10) Great black-backed gull 2800 0 2.1 2.2 45 0 Larus marinus (100) (20) Kittiwake 54500 10 1.3 0.0 100 65 Rissa tridactyla (106) (6) Arctic tern 32000 70 0.5 0.0 100 20 Sterna paradisaea (>500) (42) Guillemot 110000 30 (0.7) (0.7) 100 95 Uria aalge (230) (91) Razorbill 12000 30 (0.7) (0.6) 1(X) 45 Alca tor da (128) (7) Black guillemot 6000 10 0.9 (0.7) 60 5 Cepphus grylle (164) (31) Puffin 125 000 30 0.7 0.1 95 40 Fratercula arctica (315) (121)

^Values in parentheses indicate only very approximate estimates; n.d. = no data available. -Dietary data from Furness (unpubl.), Hudson (1986), and Martin (1989); sample sizes are given in parentheses.

213 Table 5. Estimates of basal metabolic rate (BMR) from allometric equations of Lasiewski and Dawson corrected to 60° latitude (Ellis, 1984) or, where available, from direct measurements for the species (see Furness. 1990); estimates of sandeel consumption per day by the Shetland breeding population during chick-rearing in 1981-1983 and 1988. In the status columns species showing a marked decline in breeding population between 1981 and 1988 (D) and/or a pronounced breeding failure in 1988 (F) are indicated.

Sandeels consumed (tonnes day-1) BMR Species (kj day- ') 1981-1983 1988 Status

Red-throated diver 850 0.9 0.2 Fulmar 330 77.6 5.5 Gannet 1230 33.1 2.1 Shag 855 11.9 8.3 D Arctic skua 220 0.7 0.4 D F Great skua 710 4.7 0.3 F Herring gull 390 0.6 0.0 Great black-backed gull 780 1.7 0.0 Kittiwake 285 26.1 15.3 F Arctic tern 105 5.6 0.3 D F Guillemot 550 101.6 67.6 D Razorbill 395 8.0 2.5 D Black guillemot 295 1.8 0.1 Puffin 280 55.5 15.4 D F

All seabirds 330 118

consumption in 1988 was less for all species studied, and 1981 1988 varied from ()—70% of the 1981-1983 level. The consumption of sandeels by seabirds is expressed Number (10‘') dying due to all causes" 66.10 14.80 Biomass (t) dying due to all causes 147 100 45 300 in terms of weight and data are not available to convert Equivalent total mortality rateb 2.16 1.28 this to numbers of each age group. Comparisons with sandeel stock size and production have therefore been Biomass (t) eaten by seabirds 49000 17500 made using the biomasses directly, making the assump­ Equivalent seabird predation 0.72 0.50 tion that the mean weights of sandeels taken by seabirds mortality rate were the same as those in the commercial catch. Biomass (t) taken in fishery 44500 3 900 The daily rates of consumption can be totalled over Equivalent value of fishing mortality 0.65 0.11 the breeding season (see Furness, 1990) to give esti­ rate mates that can be expressed as a proportion of sandeel Estimated production of sandeels (t) 172 100 52400 stock size. However, the stock size at the beginning of Seabird consumption: production 0.28 0.33 the year in question is not the appropriate value for ratio comparison because 0-group sandeels recruit to the stock in the summer. Instead, from VPA estimates of ‘‘Assuming that the mortality of 0-group sandeel begins on 1 the numbers and biomass of sandeels dying during the July. bFrom VPA; Anon., 1989. year, the estimated biomass of sandeels eaten by sea­ birds has been converted to approximate estimates of predation mortality rate. The text table here shows the The interpretation of the above results in terms of results for 1981 and 1988 based on the assumption that prey switching is more difficult, largely because the natural mortality due to all causes did not differ between analysis is constrained by the assumption that natural years, even though the component due to seabird preda­ mortality from all causes remains constant from year to tion may have done. Estimated fishing mortality rates year. Ideally, one would wish to incorporate changes in calculated in the same way are also given for compari­ M in the VPA using estimates of the annual consump­ son. These estimates suggest that seabirds may have tion in terms of numbers at age by each of the main exerted a slightly greater mortality on sandeels in 1981 predator groups. Annual series of appropriate data, than they did on the reduced stock in 1988. The esti­ however, are available for neither seabirds nor other mated difference is not great, however, and may well be groups of predators. To explore the possibility of prey within the confidence limits of the data. There is no firm switching, it has therefore been assumed that compensa­ evidence that the consumption of sandeels as a pro­ tory changes in consumption take place within the com­ portion of sandeel production changed over the same munity of predators such that the annual rate of natural period. mortality remains constant. This does not of course

214 mean that the total quantity of sandeels consumed Discussion remains constant, only that the proportion of the avail­ able stock consumed by predators does so. Two independent sets of data indicate a substantial Under this assumption, the extent of prey switching decrease in sandeel abundance in the Shetland area can be evaluated by comparing the effectiveness of during the last few years. Using the VPA estimates, total seabirds in generating mortality on sandeels in 1981 and biomass decreased from 77 000 t in 1981 to 47 0001 in 1988. Just as in the case of fishing, a measure of effective­ 1988 after rising to a peak of 138 000 t in 1984. Over the ness is given by the catchability coefficient q, i.e. the same period, estimated recruitment of 0-group sandeels mortality rate generated by a unit of fishing effort, in this to the Shetland stock dropped from 76 billion in 1981 to 2 case a pair of seabirds. Taking all species of seabirds billion in 1987 and 21 billion in 1988 with a peak of 81 together the relevant estimates are given in the accom­ billion in 1982. From the midwater trawling survey, the panying text table. These figures indicate no significant ratio of 0-group sandeel abundance in waters adjacent to Shetland between 1981 and 1988 was 90:1. There is thus a considerable difference in the timing and magnitude of events in the two data sets. Peak abundance of 0-group Predation Catchability in the research vessel surveys occurred in the mid-1970s, Year mortality No. of pairs coefficient whereas VPA results suggest an increase in recruitment 1981 0.72 583000 0.00123 up to 1982 and then a decline. The difference could be 1988 0.50 476000 0.00105 due to a change in the distribution of the 0-group, since the research vessel hauls at Shetland were made further offshore than the areas trawled by the commercial trawlers. change in catchability even though the stock of sandeels The validity of the VPA results depends inter alia on decreased. Seabirds as a group consist of diverse species, the applicability of the values of M, which have been however, which may have changed their feeding prefer­ derived from studies of the total North Sea sandeel stock ences differentially. A full analysis of this is not possible including Shetland and which are assumed to remain because different species specialize on different size constant. The VPA estimates for 1988 are further de­ groups of sandeels. Making the broad assumption that pendent on the validity of the estimates of fishing mor­ all seabirds take the same sizes, there are indications tality rate (F) which are based on a regression of F using the data in Tables 4 and 5 that, among the against nominal fishing effort (Anon., 1989). Both M commonest birds, fulmars, gannets, the two gulls and and F are undoubtedly subject to considerable impre­ arctic terns may have actively switched away from sand- cision, which adds to the imprecision of the seabird data. eels between 1981 and 1988. Shags, and guillemots, on Nevertheless, both sets of data indicate a pronounced the other hand, may have created a higher proportional decrease in sandeel recruitment in recent years. Preda­ mortality by retaining a high proportion of sandeels in tion rates on sandeels by seabirds in Shetland are high, their diet even though the sandeel stock had decreased. accounting for 30-40% of total mortality. The estimated For kittiwakes, razorbills, and puffins there is no indi­ 49 0001 of sandeels consumed annually in 1981-1983 is cation of a change in catchability. Even though the almost the same as the industrial fishery catch in the proportion of sandeels in their diet diminished, this was years of peak landings. Seabird consumption represents in proportion to the change in sandeel stock size, indi­ 27% of the estimated production of sandeels in the years cating that these species had not actively switched from 1981-1983 (Table 3). Since the present VPA analysis sandeels to another prey. of the Shetland sandeel stock uses natural mortality The above findings suggest that seabirds treated rates based on those estimated from studies of the together reduced their intake of sandeels but that this combined North Sea sandeel stocks and ignores the was roughly in proportion to the decrease in stock size. high concentration of non-fish predators at Shetland, The data do not reveal any non-linearities in the re­ the possibility cannot be excluded that M is different sponse of seabirds to a decrease in the abundance of in this area. In this case stock biomass and production sandeels. may not have been estimated accurately. The high Changes in catchabilities strictly show the change in mortality due to seabirds, and possible variation at efficiency with which seabirds create predation mor­ different stock densities due to ecological responses of tality. To evaluate switching as such, one also needs seabirds, should be taken into account in the assessment information on compensatory changes in predation mor­ of this stock. tality on alternative prey. While some seabird species The analyses contained in this paper are subject to may actively have switched their preference, it is also considerable uncertainty largely because the natural possible that a decrease in catchability simply represents mortality rate cannot at present be quantified in terms of the extent to which that species failed to catch enough the different age groups of sandeels consumed by differ­ food to meet its full requirements. ent groups of predators. The exercise should therefore

215 be considered as an exploration of the possible effects of Anon. 1982. Report of the Working Group for Norway Pout, changing prey abundance on a predator community. To Sandeel and Sprat Fisheries in the North Sea and Adjacent Waters, Copenhagen, 16-22 March 1982. ICES CM 1982/ investigate if prey switching occurs, better estimates Assess: 6. would be needed of the local consumption of sandeels Anon. 1988. Report of the Multispecies Assessment Working and of other prey, broken down by age group, by all Group, Copenhagen. 1-8 June 1988. ICES CM 1988/Assess: their main predators over a period of years in which 23. Anon. 1989. Report of the Industrial Fisheries Working stock size changed. Furness (1990) has made provisional Group. Copenhagen, 29 MarclMl April 1989. ICES CM estimates of sandeel consumption by seabirds, sea mam­ 1989/Assess: 13. mals, and other fish for the years 1981-1983, but these Berruti, A., Adams, N. J., and Jackson, S. 1989. The Bcnguela are expressed in terms of biomass rather than numbers ecosystem, pt VI Seabirds. Oceanogr. Mar. Biol. Ann. Rev., at age. The additional data requirements for such an 27: 273-335. Cairns, D. K. 1987. Seabirds as indicators of marine food analysis are clearly formidable. supplies. Biol. Oceanogr., 5: 261-271. With the recent decline in stock size, fishing for Daan, N. (ed.). 1989. Data base report of the stomach sampling sandeels at Shetland has decreased to a low level. project 1981. Coop. Res. Rep. Cons. int. Explor. Mer, 164. Assessment of future changes in stock based on VPA 144 pp. Ellis. H. 1.1984. Energetics of free-ranging seabirds. In Seabird will become increasingly difficult because mortality due energetics, pp. 203-234. Ed. by G. C. Whittow and H. Rahn. to fishing is only a small component of total mortality. Plenum Press, New York. Ecological responses of seabirds may provide a crude Furness, R. W. 1978. Energy requirements of seabird commu­ but simple fishery-independent indication of stock dy­ nities: a bioencrgctics model. J. Anim. Ecol., 47: 39-53. namics. For example, it is clear that different seabirds Furness, R. W. 1987. The Skuas. Poyser, Calton. Furness, R. W. 1989. Declining seabird populations. J. Zool.. respond differently to changes in stock. Arctic terns Lond.,219: 177-180. Sterna paradisaea feed largely on 1-group sandeels early Furness, R. W. 1990. A preliminary assessment of the quan­ in the year and on 0-group in July (Monaghan et al., tities of Shetland sandeels taken by seabirds, seals, predatory 1989). Because they are surface feeders that must forage fish and the industrial fishery in 1981-83. Ibis, 132: 205-217. Gulland, J. A. 1983. Fish stock assessment: a manual of basic close to the colony and make many fishing trips per day, methods. Chichcster, UK. Wiley Inter-Science, FAO/Wilcy they are especially sensitive to reductions in food avail­ series on food and agriculture, vol. 1. 233 pp. ability. This is in agreement with the evidence that they Harris. M. P., and Hislop, J. R. G. 1978. The food of young have shown the earliest and most severe breeding fail­ puffins (Fratercula arctica). J. Zool. Lond.. 185: 213-236. ures at Shetland (Heubeck. 1989). By contrast, some of Harris, M. P., and Riddiford, N. J. 1989. The food of some young seabirds on Fair Isle in 1986-88. Scott. Birds, 15: 119- the larger seabirds with generalist feeding abilities took 125. sandeels when these were abundantly available but Harwood, J., and Croxall, J. P. 1988. The assessment of switched diet as the sandeel stock declined. A further competition between seals and commercial fisheries in the possibility is that the availability of sandeels may have North Sea and the Antarctic. Mar. Mammal Sei., 4: 13-33. Heubeck, M. (ed.) 1989. Seabird and sandeels: Proceedings of changed independently of stock abundance. Any change a seminar held in Lerwick, Shetland, 15-16 October 1988. in vertical distribution, for example, would lead to Shetland Bird Club, Lerwick. changes in availability to seabirds, especially surface Holden, M. J. 1981. The North Sea international 0-group feeding species. This would complicate attempts to gadoid surveys 1969-1978. Coop. Res. Rep. Cons. int. assess changes in fish stock abundance from seabird Explor. Mer, 99. 73 pp. Hudson, A. V. 1986. The biology of seabirds utilising fishery ecology. waste in Shetland. PhD thesis. University of Glasgow. Although similar seabird-fish stock interactions in Martin, A. R. 1989. The diet of Atlantic puffin Fratercula other parts of the world have recently been documented arctica and northern gannet Sula bassana chicks at a Shetland and discussed (Springer etal., 1986; Cairns, 1987; Mon- colony during a period of changing prey availability. Bird Study, 36: 170-180. tevecchi eta l., 1988; Berruti eta l., 1989), the reliability Monaghan, P., Uttley, J. D., Burns. M. D., Thainc, C., and of predictions of fish stock abundance from seabird food Blackwood, J. 1989. The relationship between food supply, consumption remains to be tested. reproductive effort and breeding success in Arctic terns Sterna paradisaea. J. Anim. Ecol., 58: 261-274. Acknowledgements Montevecchi. W. A., Birt, V. L., and Cairns, D. K. 1988. Dietary changes of seabirds associated with local fisheries Fieldwork on seabirds was supported by NERC, failures. Biol. Oceanogr., 5: 153-161. SOTEAG, Earthwatch and its volunteer corps, Springer, A. M., Rosencau, D. G., Lloyd, D. S., McRoy, C. P.. and Murphy. E. C. 1986. Seabird responses to fluctuat­ National Geographic and NATO Scientific Affairs Div­ ing prey availability in the eastern Bering Sea. Mar. Ecol. ision. Prog. Ser., 32: 1-12. Tasker, M. L.. Webb, A., Hall, A. J., Picnkowski, M. W., and References Langslow, D. R. 1987. Seabirds in the North Sea. NCC, Peterborough. Anon. 1979. Report of the Working Group on Norway Pout Thom, V. M. 1986. Birds in Scotland. Poyser, Calton. and Sandeels in the North Sea. Charlottenlund, 23-25 April Yang, J. 1982. An estimate of the fish biomass in the North Sea. 1979. ICES CM 1979/Demersal Fish Comm.: 26. J. Cons. int. Explor. Mer, 40: 161-172.

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