International Council for the ICES CM 2007/D: 08 Exploration of the Sea Theme Session D: Comparative marine ecosystem structure and function: Descriptors and characteristics

Trophic structure of the Barents Sea fish community with the special reference to the cod stock recovery ability by

A.V. Dolgov Polar Research Institute of Marine Fisheries and Oceanography (PINRO) 6 Knipovich Street, Murmansk 183038 Russia Tel: +7 (8152) 47 24 69 Fax: +7 (8152) 47 33 31 e-mail:[email protected]

Abstract The trophic structure of the Barents Sea fish community is considered based on the data of different species diets. Some trophic groups were revealed. Their composition, ratio of different trophic groups and their inter-annual dynamics are analyzed. Besides, trophic structure of fish community in the Barents Sea and in some other areas is compared. Special attention was paid to the recovery ability of cod stock with consideration for trophic interrelations in fish communities from different North Atlantic seas. Analysis of trophic structure of the Barents Sea and other areas (North Sea, Western Greenland, Newfoundland-Labrador shelf) showed that only the Barents Sea cod stock ability to recover cannot be restricted by trophic relations among fishes due to lack of other abundant predatory species and low competition level caused by spatial-temporal changes.

Introduction Atlantic cod is one of the most commercially important fish and simultaneously an ecologically key species in various areas of the North Atlantic. Last decades depression of cod stocks was registered in a number of these areas. In late 1980s the cod stocks off Canadian coast from southern Labrador to Scotian shelf had sharply decreased by unknown causes. It was the reason for imposition of moratorium on fishery for six cod populations in that area since 1992-1993 (Myers et al., 1996а). The cod stocks declines were also observed off western Greenland (ICES, 2006c) and in the North Sea (ICES, 2006d) at the end of the 20th century. The Barents Sea cod stock is one of few stocks which recently are on the rather high level and provide the highest cod catches in the North Atlantic (ICES, 2006a). Some peculiarities of biology and fisheries of cod were recognized as possible reasons of such cod stocks depression and factors which prevent its recovering – fisheries impact (Hutchings and Myers, 1994; Myers and Cadigan, 1995; Myers et al., 1996ab; Rose, 2004), increased natural mortality (Fu et al, 2001), decreased resilience to fisheries impact (Rose and Kulka, 1999), changes in cod distribution (Rose et al., 1994, 2000), low recruitment (de Young and Rose, 1993; Shelton and Healy, 1999) and some others (e.g., Myers and Cadigan, 1995; Hutchings, 1996; Walters and Maguire, 1996; Myers et al., 1997; Brander, 2007). Other authors assigned the ability of cod to recover to trophic relationships between cod and other species in the ecosystem – harp seal predation (Sinclair and Murawski, 1997) or impact of pelagic fishes (herring and mackerel) on juvenile cod (Swain and Sinclair, 2000). Many cited authors noted complex impact of various environmental factors and cod biology aspects on cod recovery. It has been also suggested that cod stock recovery could be restricted by predation on cod juveniles and food competition between cod juveniles and other fish species. (Bundy, 2005; Bundy and Fanning, 2005). In our opinion, three factors are the most important reasons for successful recovery of any fish species: 1) availability of food resources; 2) lack of abundant food competitors which can occupy food niche and decrease available food supply, and 3) lack of abundant predators which can prey on juveniles and decrease probability of stock recovery even after very strong year classes of such species. So, species composition and structure of fish community as well as trophic relationships should be considered when we study the ability of any species to recover in any ecosystem. Main objectives of this paper were to study the species composition and trophic structure of the Barents Sea fish community as well as the trophic relations of demersal fishes, compare these peculiarities to other areas of the North Atlantic and consider how these factors can influence on the Barents Sea cod stock ability to recover.

Material and methods

Three large marine ecosystems (the Barents Sea, the North Sea and the Newfoundland-Labrador shelf) were chosen for comparison of the composition and trophic structure of fish community where large cod stocks inhabit. In addition, some data from western Greenland and Iceland were used. Data on species composition of fish communities and ecological characteristics of the fish species were taken from FishBase (2006). For the analysis of the trophic structure of the Barents Sea fish community data on total stock biomass of the most important commercial fishes were used (ICES, 2006ab). Data on total stock biomass of the most important fishes of the North Sea and the Newfoundland-Labrador shelf were taken from literature (Hislop, 1996; Harding et al., 1986; NAFO, 2006). For analysis of food relationships in the fish community of the Barents Sea the quantitative data on diets of the most abundant fish species from the joint Russian-Norwegian data base (cod 1984-2006 and haddock1 1984-1991) (Mehl and Yaragina, 1992) and Polar Institute (PINRO, Murmansk, Russia) (haddock and other species 1994-2006) were used. According to information on stomach content the number of stomachs analysed was as follows: 260 577 stomachs of cod, 40 962 stomachs of haddock, 3980 stomachs of saithe, 4588 stomachs of thorny skate, 263 stomachs of Arctic skate, 122 stomachs of round skate, 31 stomachs of spiny-tail skate, 79 stomachs of blue skate, 7969 stomachs of capelin , 6944 stomachs of polar cod, 2881 stomachs of Atlantic herring, 918 stomachs of striped wolffish, 1791 stomachs of spotted wolfish, 699 stomachs of blue wolffish, 352 stomachs of roughhead grenadier, 7171 stomachs of deepwater redfish, 1314 stomachs of golden redfish, 54 stomachs of halibut, 26 726 stomachs of Greenland halibut, 17 292 stomachs of long rough dab, 3306 stomachs of plaice and 243 stomachs of dab. Similarity of food composition of various fishes was estimated using the index of food similarity (FSI) (Shorygin, 1952), calculated as follows:

FSI = ∑ m i min , %

2 where minimal value of weight percent of prey “i” in compared fish species are used. The range of this index is from 0 % (no similarity) to 100 % (full similarity). Separation of trophic groups of the Barents Sea fishes was conducted using cluster analysis of the average data on food composition in the period of 1984-2006.

Results

Species composition and structure of fish community Recently 207 fish species can occur in the Barents Sea and 90-95 of these species regularly occur in the catches in the Russian research surveys (Dolgov, 2004). Based on the data from the Russian autumn-winter survey, which were conducted in October- December 1998-2006, long rough dab, cod, thorny skate, haddock, Greenland halibut and lumpsucker were the most abundant species in terms of abundance. The mean catches of these species exceeded 50 individuals per 1 hour tow (Table 1). It should be noted that all species from this group are demersal species. Two following groups combined 9 and 10 species respectively. The mean catches of species from these two groups were considerably lower - 25- 50 and 10-25 individuals per 1 hour tow respectively. The first from these groups combined all mass pelagic species (blue whiting, polar cod, capelin and Atlantic herring) together with demersal species. The mean catches of following 34 species consisted from 1 to 10 individuals per 1 hour tow, whereas the catches of rest of species didn’t exceed 1 individual per 1 hour tow.

Ratio of cod biomass and biomasses of other demersal fishes During the period 1946-2005 the cod stock biomass in the Barents Sea varied from 739 to 4169 thousand tons (on average 1988 thousand tons) (Table 3). But in the same period the biomass of each other fish species (even the maximal biomass) was much lower than the cod biomass. For example, the haddock stock biomass varied from 68 to 582 thousand tons (on average 348 thousand tons). Probably the saithe stock biomass in the Barents Sea is similar to the haddock stock biomass or lower as the estimation of total saithe biomass was conducted for both the Norwegian and Barents Seas and it is rather difficult to estimate what part of saithe stock distributed in the Barents Sea. The mean stock biomasses of other demersal fishes were much lower and varied from 50 thousand tons for plaice to 194 thousand tons for deepwater redfish. On average, the cod stock biomass amounted for approximately 57 % of total biomass of the commercially important demersal fishes in the Barents Sea (Table 3). The portion of other fish species didn’t exceed 10 %.

Trophic groups The cluster analysis of data on food composition of the most abundant fish species in the Barents Sea during 1984-2006 showed that 3 large groups could be separated (Figure 1). The first group combines planktivore fishes (Atlantic herring and capelin), which feed mainly on copepods and euphausids. The second group includes saithe and golden redfish, which diet consists of euphausids and fish. The third, most numerous group falls into two distinct subgroups, and besides two species (cod and blue skate) are not included in any subgroup. The first subgroup consists of three species of wolfish, which prey on mainly benthic organisms (mollusks and echinoderms) and additionally on fisheries wastes. The second subgroup combines Greenland halibut, long rough dab, and thorny and arctic skates. Various fishes, shrimps as well as fisheries wastes and lesser bottom organisms dominate in the diets of these species. Other fish species don’t join any group. It can be related to relatively small number of studied stomachs (e.g. dab, halibut) or food habit peculiarities (haddock, plaice).

3 Similarity of diet of cod and other fishes According to the revealed trophic groups long rough dab, Greenland halibut, thorny, Arctic and blue skates and wolffishes can be considered as the species with the similar food composition and possible food competitors in the Barents Sea. But the analysis of food similarity of these species based on data on average food composition in 1984-2006 demonstrated the following results (Table 2). The highest values of the index of food similarity (FSI) were observed between cod and long rough dab and deepwater redfish (53-54 %). The values of FSI between cod and saithe, thorny skate and golden redfish accounted for 41-47 %, and between cod and Greenland halibut, Arctic and blue skates for 31-34 %. The food similarity between cod and other species was much lower and didn’t exceed 24 %. The minimal values of FSI were observed between cod and capelin, Atlantic herring and plaice (3-8 %). So, the most important species, which can be food competitors for cod, are long rough dab, two species of redfishes, saithe, Greenland halibut and thorny skate.

Spatial and temporal disaggregating of cod and other fishes Data of the Russian trawl surveys showed the considerable spatial disaggregating of concentrations of cod and other demersal fishes. So, based on the data from the joint Russian- Norwegian ecosystem survey of the Barents Sea in August-September 2006, different patterns of overlapping of cod and other demersal fishes were observed (Figure 2). This period is characterized by active migrations of cod to the northern and eastern borders of its feeding grounds in the Barents Sea. Cod occurred in 72 % of all trawl stations in the area covered by the survey. One more species (Long rough dab) distributed very wide too (69 % of all trawl stations). In contrast, other demersal species were registered in the catches not so often – from 9 % of trawls (saithe) to 33 % of trawls (Greenland halibut).Therefore, the highest overlapping was observed between cod and long rough dab ((76 % of the trawls with cod). Greenland halibut, thorny skate and deepwater redfish occurred in 30-40 % of the trawls with cod, and saithe – only in 11 % of trawls with cod. In addition to spatial disaggregating between cod and demersal fishes, different vertical distribution patterns were observed (Figure 3). So, based on the data from the Russian autumn- winter survey in October-December 1998-2006, despite the fact that cod occurred in the depth range from 30 to 700 m, maximal catches of were registered at the depths of 50-350 m. Long rough dab and thorny skate had the similar depth distribution patterns, but the catches of these species were rather higher in the deeper depths too. Though saithe occurred at the same depths as cod (30-700 m), its maximal catches were observed at shallower depths than cod (50-200 m) and sharply decreased in deeper waters. Deepwater redfish and Greenland halibut distribute mainly in larger depth range than cod and its maximal catches were observed at depths of 400- 600 m and 500-850 m respectively.

Discussion

Species composition and structure of fish community A higher portion of demersal fish species was observed in the Barents Sea (44 % of all fish species) (Table 4) while this parameter did not exceed 20-30 % in other areas of the North Atlantic. The similar but a slightly higher portion of demersal species was registered only in the North Sea (49 %). According to the data from English bottom surveys (Harding et al., 1986), cod biomass made up only 6-9 % of the total fish biomass on the shelf and in the central and south-eastern North Sea. Besides, the total biomass of the potential cod food competitors (saithe, whiting and, to a lesser extent, haddock, plaice, dab etc) was 4-6 times higher than cod biomass.

4

The similar relatively low portion of cod probably occurred in the North Sea ecosystem at the beginning of the 20th century even at lower fishery intensity. According to the data from Rijnsdorp et al. (1996) based on the results of the bottom surveys using beam and otter trawl, the cod portion was rather low both during 1906-1909 and 1990-1995 and didn’t exceed 0,2-3,5 % of the total species abundance. Similarly, during 1901-1907 mean catches of cod were 2-3 times higher than during 1989-1997, but they came to only 2-3 % of the total demersal fish abundance (Rogers and Ellis, 2000). According to the data from the Spanish bottom surveys on Grand Bank during 2002-2005 (Gonzalez et al., 2006), cod accounted for only 0,8-6,8 % of the total catch, while long rough dab, yellow-tail flounder and deepwater redfish dominated in the catches (from 8 to 34 % for each species). In addition, the abundance of additional 3 species (thorny skate, roughhead grenadier and Greenland halibut) was similar to the cod abundance. On the Georges Bank during 1991-1997, the cod biomass in the catches in the different local areas of this bank varied from 2,2-5,2 % in spring to 10,4-13,8 % in autumn (Garrison, 2000). In contrast to this, cod is the dominant demersal species in the Barents Sea, and not only adult cod. So, according to the data from the Russian ichthyoplankton surveys during 1959-1990 (Mukhina, 1992, unpublished data), cod was also one of the dominant species in the egg and larval stage. The mean cod egg abundance ran up to 64,1 %, and the mean cod larva abundance – 26,7 % of the total eggs and larva abundance respectively in April-May. For comparison, on the Scotian shelf during 1978-1982 the mean cod larva abundance amounted to only 4,39 % of the total larva abundance (Shackel and Frank, 2000). Thus, cod is the dominant or one of the dominant demersal fish species in the Barents Sea in all life stages from eggs to adult fish.

Ratio between cod biomass and biomasses of other demersal fishes Analysis of the cod stock biomasses in various areas of the North Atlantic has demonstrated that in contrast to the North Sea and the Newfoundland-Labrador shelf the Barents Sea cod biomass is much higher than the biomass of other demersal predatory and benthophagous fishes. In the North Sea among the most abundant demersal species (cod, haddock, whiting and saithe) combined into the demersal piscivores trophic guild (Heat, 2005), the highest stock biomass during 1970-1995 was observed in haddock (from 500 to 2000 thousand tons). The stock biomasses of other species were rather similar and varied approximately from 300 to 1400 thousand tons for each species (Hislop, 1996). According to the data of bottom surveys off western Greenland (Sunksen et al., 2006), Greenland halibut and deepwater redfish dominated in the catches (47 and 37 % of the total catch weight respectively). The portion of cod was equal to only 4 % of the total demersal fish biomass and corresponded to the weight portions of some other demersal fishes (thorny skate, striped and spotted wolffish, long rough dab) (1,1-4,0 %). Similar ratio of the demersal fish biomasses was observed on the Newfoundland-Labrador shelf (NAFO, 1996). On average during 1988-2005 cod biomass accounted for approximately 18 % of the total demersal fishes biomass, while the portions of fishes with similar food habits (Greenland halibut and thorny skate) amounted to 53 and 21 % respectively. According to the results from the ECOPATH model for the Scotian shelf ecosystem (Bundy, 2005), the cod relative biomass (in terms tons per km-1) varied from 15 % in the early 1980s to 18 % of total fish biomass in the late 1990s.

5 Obviously, the number of fish species, whose food habits and habit of life are similar to those of cod, is considerably higher in other areas of the North Atlantic than in the Barents Sea and the abundance of these species is higher than the cod abundance.

Trophic groups and similarity of diet of cod and other fishes The analysis of the trophic groups composition in the Barents Sea showed that the number of species in the trophic groups with the similar food habits to cod is rather small (approximately 9- 10 species). Besides, cod is distinct in food composition from other species in this group. In other areas of the North Atlantic the number of species with similar food habits considerably differs from the Barents Sea. So, during spring and autumn period of 1991-1997 on the Grand Bank the species number in the trophic group, cod over 20 cm long included, was equal to 6 and 2 species respectively (Garrison, 2000). But in the North Sea the number of species from the demersal piscivores guild exceeds 40 (Heat, 2005). Our data on the high food similarity between cod and other demersal fishes in the Barents Sea during 1990s correspond to earlier published results. During 1960s-1970s the highest level of food similarity was registered between cod and Greenland halibut (Nizovtsev, 1978). Thus, the food similarity coefficient FSC (based on the qualitative data) between cod and this species was 46.1 % in 1964-1970 and varied according to various seasons and local areas. The highest food similarity was observed in the southern and north-western Barents Sea in 1st, 2nd and 3rd quarters and in the Kopytov area and the western slope of the Bear Island bank in 3rd and 4th quarters. Rather high food similarity (FSC up to 50 %) may occur between cod and long rough dab for several seasons (Berestovsky, 1996). But this author noted that seasonal dynamics of feeding intensity of these species was different. During very intensive feeding of cod on pre-spawning and spawning capelin in the spring, long rough dab practically did not feed. For this reason the maximal food similarity between cod and long rough dab was registered only during the summer-autumn period. Comparative analysis of feeding of cod and haddock in 1930s showed that despite the fact that on average the food similarity between these species was considerable (FSI 40 %), the high spatial and temporal variability took place (Petrova-Grinkevich, 1944). Additionally this author revealed that the capelin and euphausids were the main objects of food competition between cod and haddock. In other areas of the North Atlantic food similarity levels could be higher than in the Barents Sea. So, on the Grand Bank coefficient of food niche overlapping (which varies from 0 (no similarity) to 1 (complete similarity)) between cod and thorny skate was equal to 0.94 in the upper 200 m, to 0.69 between 200 and 399 m depth and to 0.89 between 400 and 599 m depth (Gonzalez et al., 2006).

Spatial and temporal disaggregating of cod and other fishes The feeding area of adult cod in the Barents Sea is considerably larger than feeding areas for other adult demersal fishes. According to literature data during warm years the northern border of the cod distribution area can reach the Hope Island and the eastern border – the Novaya Zemlya archipelago (Yaragina et al., 2003). In contrast, distribution area of haddock is located mainly in the southern Barents Sea, even though in some years dense concentrations can be found near the southern Spitsbergen (Sonina, 1969; Berestovsky and Mukhina, 1986). The distribution area of saithe is confined to waters near the Norwegian and Murman coasts (Lukmanov, 1986), and Greenland halibut dwell mainly the continental slope deepwater area along the western border of the Barents Sea (Nizovtsev, 1978, Kovtsova, 1986). Besides, the distribution area of cod in the Barents Sea is the largest one in the North Atlantic (592 thousand km2 vs. 36-250 thousand km2) and is only comparable to the North Sea cod (539 thousand km2 ) (Myers et al., 2001). It allowed using food resources that are unavailable for other demersal fishes in the Barents Sea.

6 The disaggregating of cod and other demersal fishes in the Barents Sea in relation to depths also contributed to decrease in the potential food competition. The densest concentrations of demersal fishes with the similar food habits usually occurred in deeper (Greenland halibut, deepwater redfish) or shallower (saithe) waters than cod. Only two species (long rough dab and thorny skate) distribute at the same depths as cod. In addition, reduction in potential food competition in the Barents Sea is related to differences in seasonal variations of feeding intensity of different species. Thorny skate practically doesn’t feed during summer period in the southern Barents Sea (Antipova and Nikiforova, 1990), while cod traditionally prey intensively on euphausids (Zatsepin and Petrova, 1939). In contrast, the feeding intensity of long rough dab is the highest during summer period and the lowest during winter period (Berestovsky, 1996). Thus, despite the high level of food similarity between cod and its potential food competitors, food competition between these species considerably decreases since available food resources are separated in time and space.

Conclusions

The analysis of the composition and structure of demersal fish communities in the Barents Sea and in some other regions of the North Atlantic showed that cod is the dominant demersal species in the Barents Sea in all life stages and the cod biomass makes up 57 % of the total biomass of demersal fishes. Relatively small number of fish species with similar food habits which could occupy the cod feed niche after cod stock decline, considerably lower biomass of the possible cod food competitors and wider distribution of cod due to long distance migrations are typical for the Barents Sea. These factors provide more preferable conditions for successfully and fast recovery even after any drastic stock decline for cod in the Barents Sea compared to other areas of North Atlantic. Besides, despite the relatively high level of food similarity, food competition level between cod and its possible food competitors still more decreases due to spatial and temporal separation of food resources.

7 References

Antipova, T.V., and Nikiforova, T.B. 1990. Peculiarities of feeding of thorny skate in the Barents Sea. In : Food resources and trophic relationships of fishes in the North Atlantic. Murmansk, PINRO Press. Pp.167-172. (in Russian) Berestovsky, E.G. 1996. Feeding of long rough dab in the Barents and Norwegian Seas. Ph.D. thesis. Dalnye Zelentsy. 118 pp. (in Russian) Berestovsky, E.G., Mukhina, N.V. 1986. Haddock. In : Ichthyofauna and its habitat conditions. Apatity, Kola Scientific Center of the Russian Academy of Sciences. Pp. 32-33. (in Russian) Brander, K. M. 2007. The role of growth changes in the decline and recovery of North Atlantic cod stocks since 1970. – ICES Journal of Marine Science, 64: 211–217. Bundy A. 2005. Structure and functioning of the eastern Scotian Shelf ecosystem before and after the collapse of ground fish stocks in the early 1990s Can. J. Fish. Aquat. Sci. 62: 1453– 1473. Bundy A. and L. P. Fanning. 2005. Can Atlantic cod (Gadus morhua) recover? Exploring trophic explanations for the non-recovery of the cod stock on the eastern Scotian Shelf, Canada. Can. J. Fish. Aquat. Sci. 62: 1474–1489. de Young B., and Rose, G.A. 1993. On recruitment distribution of Atlantic cod (Gadus morhua) off Newfoundland. Can. J. Fish. Aquat. Sci. 50: 2729–2741. Dolgov A. V. 2004. Species composition of ichthyofauna and the structure of ichthyocenoses of the Barents Sea. Izvestia TINRO 137 : 177–195. (in Russian). Fu C., Mohn R., and Fanning L. P. 2001. Why the Atlantic cod (Gadus morhua) stock off eastern Nova Scotia has not recovered? Can. J. Fish. Aquat. Sci. 58: 1613–1623. Garrison L.P. 2000. Spatial and dietary overlap in the Georges Bank ground fish community. Can. J. Fish. Aquat. Sci. 57: 1679–1691 Gonzalez, C., Paz, X., Roman, E., and Hermida, M. 2006. Feeding Habits of Fish Species Distributed on the Grand Bank (NAFO Divisions 3NO, 2002-2005). NAFO SCR Doc. 06/31. Serial No. N5251. 22 pp. Harding, D., Woolner, L., and Dann, J. 1986. The English groundfish surveys in the North Sea, 1977–85. ICES CM 1986/G:13. 8 pp. Heath, M. R. 2005. Changes in the structure and function of the North Sea fish foodweb, 1973-2000, and the impacts of fishing and climate. ICES Journal of Marine Science, 62: 847- 868. Hislop, J. R. G. 1996. Changes in North Sea gadoid stocks. – ICES Journal of Marine Science, 53: 1146–1156. Hutchings, J.A. 1996. Spatial and temporal variation in the density of northern cod and a review of hypotheses for the stock’s collapse. Can. J. Fish. Aquat. Sci. 53: 943–962. Hutchings, J.A., and Myers, R.A. 1994. What can be learned from the collapse of a renewable resource? Atlantic cod, Gadus morhua, of Newfoundland and Labrador. Can. J. Fish. Aquat. Sci. 51: 2126–2146. ICES. 2006a. Report of the Arctic Fisheries Working group. ICES CM 2006/ACFM:25. – 594 рp. ICES. 2006b. Report of the Northern Pelagic and Blue Whiting Fisheries Working Group. ICES C.M. 2006/ACFM:05. 241 pp. ICES. 2006c. Report of the North Western Working Group. ICES CM 2006/ACFM: 26. 612 pp. ICES. 2006d Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak. ICES CM 2006/ACFM:09 . 971 pp. Kovtsova, M.V. 1986. Greenland halibut. In: Ichthyofauna and its habitat conditions. Apatity, Kola Scientific Center of the Russian Academy of Sciences. Pp. 46-48. (in Russian)

8 Lukmanov, E.G. 1986. Saithe. In : Ichthyofauna and its habitat conditions. Apatity, Kola Scientific Center of the Russian Academy of Sciences. Pp. 29-31. (in Russian) Mehl S. and Yaragina N.A. 1992. Methods and results in the joint PINRO-IMR stomach sampling program. In : B.Bogstad and S.Tjelmeland (eds.). Interrelations between fish populations in the Barents Sea. 1992. Proceedings of the Fifth PINRO-IMR Symposium, Murmansk, 12-16 August 1991. P.5-16. Mukhina. N.V. 1992. Results of ichthyoplankton surveys conducted in the Norwegian and Barents Seas in 1959-1990. In : Ecological problems of the Barents Sea. Murmansk, PINRO Press. – P.62-102 (in Russian) Myers, R. A., MacKenzie, B. R., Bowen, K. G., and Barrowman, N. J. 2001. What is the carrying capacity for fish in the ocean? A meta-analysis of populations dynamics of North Atlantic cod. Canadian Journal of Fisheries and Aquatic Sciences, 58: 1464–1476. Myers, R.A., and Cadigan, N.G. 1995. Was an increase in natural mortality responsible for the collapse of northern cod? Can. J. Fish. Aquat. Sci. 52: 1274–1285. Myers, R.A., Barrowman, N.J., Hoenig, J.M., and Qu, Z. 1996b. The collapse of cod in Eastern Canada: the evidence from tagging data. ICES J. Mar. Sci., 53 : 629-640. Myers, R.A., Hutchings, J.A., and Barrowman, N.J. 1996a. Hypotheses for the decline of cod in the North Atlantic. Mar. Ecol. Prog. Ser. 138: 293–308. Myers, R.A., Hutchings, J.A., and Barrowman, N.J. 1997. Why do fish stocks collapse? The example of cod in Atlantic Canada. Ecol. Appl. 7: 91–106. NAFO 2006. Report of Scientific Council meeting, 1-15 June 2006. NAFO SCS Doc. 06/22 Serial No. N5282. – 207 pp. Nizovtsev, G.P. 1978. Biology and fisheries of Greenland halibut from the Norwegian- Barents Sea stock. Ph.D. thesis. Murmansk. 225 pp. (in Russian) Petrova-Grinkevich. 1944. On food competition between cod and haddock in the Barents Sea. Trudy PINRO, v.8. Pp.416-428. (in Russian) Rijnsdorp, A. D., Van Leeuwen, P. I., Daan, N., and Heessen, H. J. L. 1996. Changes in abundance of demersal fish species in the North Sea between 1906–1909 and 1990–1995. – ICES Journal of Marine Science, 53: 1054–1062. Rogers, S. I., and Ellis, J. R. 2000. Changes in the demersal fish assemblages of British coastal waters during the 20th century. – ICES Journal of Marine Science, 57:866–881. Rose G.A. 2004. Reconciling overfishing and climate change with stock dynamics of Atlantic cod (Gadus morhua) over 500 years Can. J. Fish. Aquat. Sci. 61: 1553–1557. Rose, G.A., and Kulka, D.W. 1999. Hyperaggregation of fish and fisheries: how catch- per-unit-effort increased as the northern cod (Gadus morhua) declined. Can. J. Fish. Aquat. Sci. 56(Suppl. 1): 118–127. Rose, G.A., Atkinson, B.A., Baird, J., Bishop, C.A., and Kulka, D.W. 1994. Changes in distribution of Atlantic cod and thermal variations in Newfoundland waters, 1980–1992. ICES Mar. Sci. Symp. 198: 542–552. Rose, G.A., de Young, B., Kulka, D.W., Goddard, S.V., and Fletcher, G.L. 2000. Distribution shifts and overfishing the northern cod (Gadus morhua): a view from the ocean. Can. J. Fish. Aquat. Sci. 57: 644–663. Shackel, N.I., and Frank, K.T. 2000. Larval fish diversity on the Scotian Shelf. Can. J. Fish. Aquat. Sci. 57: 1747–1760 Shelton P.A. and B.P. Healey. 1999. Should depensation be dismissed as a possible explanation for the lack of recovery of the northern cod (Gadus morhua) stock? Can. J. Fish. Aquat. Sci. 56: 1521–1524. Shorygin, A.A. 1952. Feeding and food relations of fishes of the Caspian Sea. Moscow, Pistchepromizdat. 268 pp. (in Russian) Sinclair, A.F., and Murawski, S.A. 1997. Why have groundfish stocks declined? Chapter 3. In Northwest Atlantic groundfish: perspectives on a fishery collapse. Edited by J. Boreman,

9 B.S. Nakashima, J.A. Wilson, and R.L. Kendall. American Fisheries Society, Bethesda, Maryland. pp. 71–93. Sonina, M.A. 1969. Migrations of haddock and impacted factors. Trudy PINRO, v.26. 126 pp. (in Russian) Sunksen, K., Storr-Paulsen, M. and Jorgensen, O.A. 2006. Biomass and Abundance of Demersal Fish Stocks off West Greenland Estimated from the Greenland Shrimp Survey, 1988- 2005. NAFO SCR Doc. 06/28 Serial No. N5247. 30 pp. Swain D.P. and A.F. Sinclair. 2000. Pelagic fishes and the cod recruitment dilemma in the Northwest Atlantic. Can. J. Fish. Aquat. Sci. 57: 1321–1325. Walters, C., and Maguire, J.-J. 1996. Lessons for stock assessment from the northern cod collapse. Rev. Fish Biol. Fish. 6: 125–137. Yaragina, N.A., Ponomarenko, V.P., and Shevelev, M.S. 2003. Migrations. In : Cod of the Barents Sea: biology and fisheries (2nd ed.). Murmansk, PINRO Press. Pp.20-29. (in Russian) Zatsepin, V.I., and Petrova, N.S. 1939. Feeding of commercial concentrations of cod in the southern Barents Sea (based on the observations in 1934-1936). Trudy PINRO, v.5. 170 pp. (in Russian)

10

Table 1. Catches of common fish species in the Barents Sea based on the data from the Russian autumn-winter survey in October-December 1998-2006, individuals per 1 hour tow.

Catches, ind. per 1 hour tow Scientific name English name min. max. mean Hippoglossoides platessoides Long rough dab 87.5 96.1 91.9 Gadus morhua Cod 89.2 94.6 91.8 Amblyraja radiata Thorny skate 53.2 85.3 70.9 Melanogrammus aeglefinus Haddock 56.5 82.2 69.6 Reinhardtius hippoglossoides Greenland halibut 48.4 59.1 52.8 Cyclopterus lumpus Lumpsucker 47.2 59.9 52.3 Micromesistius poutassu Blue whiting 27.0 65.6 47.5 Boreogadus saida Polar cod 32.1 59.3 46.0 Sebastes mentella Deepwater redfish 31.6 48.0 40.6 Anarhichas denticulatus Blue wolfish 22.8 48.6 37.6 Mallotus villosus Capelin 31.6 49.3 37.5 Sebastes marinus Golden redfish 26.9 46.9 36.0 Clupea harengus Atlantic herring 10.0 43.7 29.4 Anarhichas minor Spotted wolfish 22.1 44.2 28.5 Artediellus atlanticus Atlantic hookear sculpin 16.0 40.2 28.4 Careproctus reinhardti Sea tadpole 15.5 34.8 23.5 Anarhichas lupus Striped wolfish 17.2 30.1 22.1 Trisopterus esmarki Norway pout 15.3 32.1 21.8 Leptagonus decagonus Atlantic poacher 10.2 26.7 18.7 Triglops murrayi Moustache sculpin 12.7 22.6 17.9 Lycodes vahli gracilis Vahl’s eelpout 5.3 25.7 14.4 Cottunculus microps Polar sculpin 6.2 21.6 13.5 Lycodes esmarki Greater eelpout 4.8 24.0 11.7 Pleuronectes platessa Plaice 8.3 15.7 10.9 Pollachius virens Saithe 6.7 15.9 10.5 Eumicrotremus spinosus Atlantic spiny lumpsucker 7.9 10.5 9.0 Leptoclinus maculatus Daubed shanny 0.8 17.8 8.9 Macrourus berglax Roughhead grenadier 4.6 12.9 8.8 Liparis gibbus Variegated snailfish 2.8 10.7 6.7 Triglops nybelini Bigeye sculpin 1.5 13.5 6.4 Amblyraja hyperborea Arctic skate 3.1 10.3 6.4 Lycodes reticulatus Arctic eelpout 1.5 9.5 6.3 Lycodes rossi Threespot eelpout + 11.2 6.3 Notolepis risso Ribbon barracudine 2.3 11.1 6.3 Sebastes viviparous Norway haddock 1.0 9.4 6.0 Lycodes seminudis Longear eelpout 1.0 10.1 5.9 Lycodes pallidus Pale eelpout 0.2 18.7 5.2 Rajella fyllae Round skate 0.8 7.7 4.4 Argentina silus Greater argentine 1.2 5.6 3.8 Liparis fabricii Gelatinous snailfish 0.3 7.7 3.5 Lumpenus fabricii Slender eelblenny + 9.5 3.4 Cottunculus sadko Sadko sculpin 0.3 9.2 3.4 Myoxocephalus scorpius Shorthorn sculpin 1.6 5.9 3.4 Lycodes eudipleurostictus Doubleline eelpout 1.0 4.9 2.7 Brosme brosme Tusk 1.1 3.8 2.6 Gasterosteus aculeatus Three-spined stickleback 0.2 5.3 2.6 Limanda limanda Dab + 4.6 2.4 Triglops pingelii Ribbed sculpin 1.0 4.7 2.3 Lumpenus lampretaeformis Snake blenny 0.3 3.9 2.2 Gaidropsarus argentatus Arctic rockling 0.5 4.7 2.0

11 Gymnacanthus tricuspis Arctic staghorn sculpin 0.8 3.3 1.9 Icelus bicornis Twohorn sculpin + 4.2 1.9 Clupea pallasi suwurowi Chosa herring + 5.2 1.6 Dipturus batis Blue skate 0.3 4.5 1.6 Glyptocephalus cynoglossus Witch 1.0 2.3 1.6 Bathyraja spinicauda Spiny-tail skate + 2.7 1.3 Gymnelis spec Fish doctor + 3.4 1.2 Icelus spatula Spatulate sculpin + 4.8 1.0 Lycodes polaris Canadian eelpout + 3.3 1.0 Hippoglossus hippoglossus Halibut + 2.4 0.9 Benthosema glacialis Glacier lanternfish + 2.2 0.9 Gadiculus argenteus thori Silvery pout + 2.1 0.7 Merlangius merlangus Whiting + 2.9 0.7 Ulcina olrikii Arctic alligatorfish + 2.7 0.6 Eumicrotremus derjugini Leatherfin lumpsucker + 1.3 0.5 Maurolicus muelleri Pearlsides + 1.5 0.5 Enchelyopus cimbrius Fourbeard rockling + 1.3 0.5 Liparis tunicatus Kelp snailfish + 2.2 0.4 Microstomus kitt Lemon sole + 1.0 0.4 Somniosus microcephalus Greenland shark 0.2 0.5 0.3 Dipturus linteus Sail ray + 0.8 0.3 Clupea pallasi maris-albi White Sea herring + 1.5 0.3 Hyperoplus lanceolatus Great sandeel + 1.0 0.2 Chimaera monstrosa Rabbit fish + 0.4 0.2 Molva molva Ling + 0.6 0.2 Careproctus ranula Scotian snailfish + 0.7 0.2 Liopsetta glacialis Arctic flounder + 1.4 0.2 Coryphaenoides rupestris Roundnose grenadier + 0.7 0.2 Anisarchus medius Stout eelblenny + 0.6 0.2 Agonus cataphractus Hooknose + 0.5 0.1 Eutrigla gurnardus Grey gurnard + 0.4 0.1 Careproctus micropus - + 0.3 0.1

+ - less than 0.1 %

12

Table 2. Diet similarity index (DSI) of cod and other most abundant fishes of the Barents Sea based on averaged data during 1984-2006.

Species DSI, % Thorny skate 41,8 Arctic skate 33,0 Round skate 17,6 Blue skate 31,2 Spiny-tail skate 24,6 Atlantic herring 6,4 Capelin 8,2 Roughhead grenadier 23,6 Polar cod 24,2 Saithe 47,8 Haddock 23,7 Deepwater redfish 53,6 Golden redfish 47,7 Striped wolffish 10,5 Spotted wolffish 18,9 Blue wolffish 17,3 Halibut 12,5 Greenland halibut 34,4 Long rough dab 54,6 Plaice 3,6 Dab 15,6

13

Table 3. Ratio of the biomasses of cod and other demersal fishes in the Barents Sea during 1945- 2005.

Stock biomass, thousand tons % of total Species Period demersal fish minimal maximal mean biomass Cod 1946-20051 739 4169 1988 57.3 Haddock 1950-20051 68 582 348 10.0 Saithe 1960-20052 127 628 348 10.0 Deepwater redfish 1992-20013 134 316 194 5.6 Golden redfish 1990-20051 57 179 124 3.6 Greenland halibut 1964-20051 45 312 120 3.5 Wolffishes4 100 2.9 Thorny skate4 100 2.9 Long rough dab4 100 2.9 Plaice4 50 1.4 Total 3472 100

1 – based on the ICES data (2006a) 2 – based on the ICES data (2006a) (as the stock was estimated for whole ICES Subarea I (the Barents and Norwegian Seas) 50 % stock estimate was considered for the Barents Sea. 3 – based on the data of the Russian surveys of deepwater redfish stock in the Barents Sea (ICES, 2006a) 4 – based on the data of the Russian surveys

Table 4. Ratio of species number from different ecological groups in the Barents Sea and other areas of the North Atlantic, % of the total fish number in each area.

Labrador- Scotian Greenland Barents Faroe North Ecological groups Newfoundland Iceland shelf shelf Sea Plateau Sea shelf Bathydemersal 21.6 13.7 26.0 23.3 19.8 23.0 10.1 Bathypelagic 10.5 9.1 23.1 34.2 5.8 13.2 4.3 Benthopelagic 16.4 12.7 13.2 11.4 15.0 16.1 14.4 Demersal 35.1 31.0 24.0 25.6 44.4 31.6 49.5 Pelagic 14.6 20.3 11.6 5.5 12.6 13.8 16.0 Reef-associated 1.8 13.2 2.1 0.0 1.0 2.3 5.9 Total fish number 171 197 242 219 207 174 188

14

Figure 1. Trophic groups of the most abundant fishes of the Barents Sea based on the averaged food composition during 1984-2006.

15 80 80

78 78

76 76

74 74

72 72

70 70

68 68

10 15 20 25 30 35 40 45 50 55 60 10 15 20 25 30 35 40 45 50 55 60 saithe deepwater redfish

80 80

78 78

76 76

74 74

72 72

70 70

68 68

10 15 20 25 30 35 40 45 50 55 60 10 15 20 25 30 35 40 45 50 55 60 long rough dab thorny skate

80

78

76

74

72

70

68

10 15 20 25 30 35 40 45 50 55 60 Greenland halibut

Figure 2. Distribution of cod (circles) and its possible food competitors (crosses) based on data from the joint Russian-Norwegian survey in August-September 2006, individuals per 1 hour tow.

16 140 3.0

120 2.5 100 2.0 80 1.5 60

mean catch catchmean 1.0 40 20 0.5 0 0.0 0-50 0-50 51-100 51-100 101-150 151-200 201-250 251-300 301-350 351-400 401-450 451-500 501-550 551-600 601-650 651-700 701-750 751-800 801-850 101-150 151-200 201-250 251-300 301-350 351-400 401-450 451-500 501-550 551-600 601-650 651-700 701-750 751-800 801-850 depth, m depth, m

cod saithe

140 8 120 7 100 6 5 80 4 60 3 mean catch mean catch 40 2 20 1 0 0 0-50 0-50 51-100 51-100 101-150 151-200 201-250 251-300 301-350 351-400 401-450 451-500 501-550 551-600 601-650 651-700 701-750 751-800 801-850 101-150 151-200 201-250 251-300 301-350 351-400 401-450 451-500 501-550 551-600 601-650 651-700 701-750 751-800 801-850 depth, m depth, m

long rough dab thorny skate

200 600 180 160 500 140 400 120 100 300 80 mean catch mean catchmean 60 200 40 100 20 0 0 0-50 0-50 51-100 51-100 101-150 151-200 201-250 251-300 301-350 351-400 401-450 451-500 501-550 551-600 601-650 651-700 701-750 751-800 801-850 101-150 151-200 201-250 251-300 301-350 351-400 401-450 451-500 501-550 551-600 601-650 651-700 701-750 751-800 801-850 depth, m depth, m

deepwater redfish Greenland halibut

Figure 3. Mean catches of cod and its possible food competitors at different depths in the Barents Sea based on data from the Russian autumn-winter surveys during 1998-2006, individuals per 1 hour tow.

17