VI. The position of “king cod” in the ecosystem

ICES mar. Sei. Symp., 198:553-575.1994

A review of the trophic interactions of cod stocks in the North Atlantic

Ölafur K. Pâlsson

Pâlsson, O. K. 1994. A review of the trophic interactions of cod stocks in the North Atlantic. - ICES mar. Sei. Symp., 198: 553-575.

Trophic interactions of the cod stocks in the waters of Newfoundland, Iceland, the Barents Sea, and the North Sea are described on the basis of the available literature and some unpublished material. This includes the feeding habits of the cod stocks and their role as prey of a variety of predators through development stages of the cod, i.e. : (1) the food composition of the cod stocks with respect to major prey groups (fish, crustaceans, other food), as well as stomach content weight; (2) predation by invertebrates (medusae, cephalopods, crustaceans, and chaetognaths) on eggs, lar­ vae, and juveniles of cod; (3) predation by fish, including cod, on cod; (4) predation by seals; (5) predations by whales; and (6) predation by seabirds. In general, predation on cod has been recorded for a number of predators in the taxonomic groups of invertebrates, fish, birds, and marine mammals. In most cases the predatory impact appears to be fairly limited. However, marked predation has been recorded by some predators in most of the taxonomic groups covered. Among these are species like the scyphomedusa Aurelia aurita, herring, cod, thorny skate, kittiwake, grey seal, and minke whale.

Ôlafur K. Pâlsson: Marine Research Institute, Skulagata 4, PO Box 1390, 121 Reykjavik, Iceland.

Introduction Materials and methods Studies on the food and feeding of cod and other marine For the evaluation of predation by cod with respect to fishes have been part of fisheries research during all of major prey groups, existing databases have been used. this century and even longer. However, quantitative For Newfoundland, the data were collected during studies specifically aimed at multispecies analysis have autumn 1981-1983 and 1985-1989 in NAFO areas 2J been carried out only during one or two decades. The 3KL (Lilly, pers. comm.). The Icelandic data were predation by cod with respect to some major prey groups collected in 1979-1992, mainly during March and is briefly summarized in the first section of the paper. September-November, on the Icelandic continental The main part reviews available information on the shelf. The Barents Sea data cover the period 1984-1992 predatory impact on cod by other species of the marine and the waters of the Barents Sea and Spitsbergen fauna in the Arctic-boreal regions of Newfoundland, (Mehl, pers. comm.). The North Sea data used are Iceland, and the Barents Sea as well as in the North Sea. described by Daan (1983). The purpose of this review is to describe the trophic The existing literature has been scanned for infor­ interactions of the cod stocks, and to identify trophic mation on predation on cod by marine invertebrates, interactions of particular importance in an ecological fish, mammals, and birds. In most cases predation is context or in terms of management implications. This quantified as frequency of occurrence of the prey in review will also focus on the shortcomings in the present either the total number of stomachs analysed or only in state of knowledge and, it is hoped, give an impetus to those stomachs containing food. When available, the further research. former measure has been selected, since this can be 554 Ô. K. Pâlsson ICES mar. Sei. Symp., 198 (1994) regarded as an index of the proportion of the predator Stomach content weight stock preying on cod. When available, the percentage Double logarithmic plots of average weight of total weight of cod in the stomach content is preferred above stomach content versus the median of predator length frequency of occurrence. As a rule the percentage groups generally follow straight lines for all stocks, weight is given on a length group basis. An average indicating power relationships (Fig. 2). The power is across predator length group is evaluated as an index of 3.32, 2.79, 2.86, and 3.09 for Newfoundland, Icelandic, predation based on percentage weight of cod in stomach Barents Sea, and North Sea cod, respectively. The value content. In a few cases the proportion of the number of for Newfoundland cod is the only one significantly cod as prey against total number of prey (% by number) different from 3 (p < 0.01). Thus, in general the weight has been evaluated. Although this procedure of averag­ of the stomach content appears to be linearly related to ing may blur some important detail, it draws attention to the weight of the predator. the main features in the predator-prey interaction.

Predation by cod Predation on cod Food composition Invertebrates Average values of food composition of cod in the four Medusae and ctenophores areas have been calculated by predator length groups for Meile (1985) studied the predation induced by the cteno- three groups of prey, i.e. fish, crustaceans, and other phore Bolinopsis infundibulum and the scyphomedusa food (Fig. 1). The contribution of fish as food is distinctly Aurelia aurita in Lofoten. Both species were identified lower for North Sea cod compared with the other stocks as predators of cod eggs and larvae, in particular A. and somewhat higher for Icelandic cod. The proportion aurita (Table 1). Furthermore, one example of the of fish shows a general increase with predator length for scyphomedusa Tiaropsis multicirrata was observed con­ all stocks. The increase follows basically a straight line taining one cod larva. for North Sea cod. For Barents Sea and, especially, Laboratory and field studies of the predation by Newfoundland cod there is a sharp increase in the medusae and ctenophores on eggs and larvae of marine proportion of fish in the lower predator length range fishes have identified at least 34 species of piscivorous (<40 cm), but a much slower increase for the larger medusae and 5 species of ctenophores according to a predators. For Iceland cod the proportion of fish is review by Hunter (1984). Attempts have been made to relatively high in the smallest predators (<20 cm). roughly estimate the consumption by these predators. The contribution of crustaceans in the stomach con­ Fraser (1969) estimates a probable consumption of 50- tent weight is highest for North Sea cod and lowest for 250 larval fish per hydromedusa during its lifetime, Iceland cod, but intermediate and similar for Newfound­ about 450-500 by Aurelia, and in the order of 15 000 by land and Barents Sea cod. The overall trend with respect Cyanea. to predator length is the opposite to the proportion of Möller (1980) studied the predation by A. aurita on fish for all stocks. herring larvae in Kiel Bight and identified this scypho­ The highest level of other food is observed for North medusa both as a competitor for food and as a predator Sea cod, lowest for Barents Sea cod, and intermediate of the larvae. The estimated predation was 2-5% of the for the other two stocks. The trend generally decreases total stock of yolk-sac larvae per day. The author con­ with predator length. However, the proportion of this cludes that his findings support Fraser’s (1969) estimates group in Barents Sea cod is fairly constant except for the of predation by medusae. largest and the smallest length groups. Based on enclosure experiments, Øiestad (1983) Overall, fish clearly dominates the food constituting suggested predation by hydromedusae as the most likely more than 50% of the stomach content weight already in cause of the rapid decline in abundance of cod larvae. In the predator length range of 20-39 cm for the Arcto- addition, he identified medusae as important competi­ boreal stocks. For North Sea cod, however, this level is tors with larvae for food. not reached until length group 50-69 cm. The overall contribution of crustaceans is higher than 50% for the Cephalopods Newfoundland, Barents Sea, and North Sea stocks in the predator length range below 20 cm. For Icelandic cod the The abundance of cephalopods in the waters of New­ proportion of crustaceans below 20 cm predator length is foundland, Iceland, and Norway is subject to large reduced in correspondence with high values of fish prey. fluctuations from year to year. In the Northwest Atlantic Clearly, other food is the least important prey group for the short-finned squid (Illex illecebrosus) and the long- all stocks, with maximum proportions around 15%. finned squid (Loligo pealei) are most abundant and of ICES mar. Sei. Symp., 198 (1994) Trophic interactions of cod stocks 555

Fish prey

8

O CO

s Newfoundland 5 North Sea o Barents Sea Iceland

o

20 40 60 80 100 Predator length (cm)

Crustacean prey

8 Newfoundland North Sea Barents Sea O Iceland CO

o CO

o •«r

o CM

o

20 40 60 80 100 Predator length (cm)

Other prey

in Newfoundland CM North Sea Barents Sea Iceland o CM

o

O

20 40 60 80 100 Predator length (cm)

Figure 1. Average composition of the food (% weight of stomach content) of cod: (a) fish prey, (b) crustacean prey, (c) other prey, in four areas. 556 Ô. K. Pâlsson ICES mar. Sei. Symp., 198 (1994)

O O Newfoundland North Sea Barents Sea Iceland

O O

O) '© £

o o -C o cd E o

/ /

~ r~ 10 50 100 log (Predator length (cm))

Figure 2. Average stomach-content weight of cod by areas with respect to predator length (log-log scale).

Table 1. Predation by invertebrates on cod eggs and larvae in the Lofoten area indicated as average number of eggs and larvae per 100 predators (n.a. = not available).

Eggs Larvae Year of Reference Predator /100 pred. /100 pred. n sampling

B. infundibulum 0.7 0.3 4666 1983-1984 Meile (1985) Melle (1985) A. aurita 2.4 3.9 461 1983-1984 T. multicirrata l a n.a. 1983-1984 Melle (1985)

a One stomach containing 1 larva recorded. ICES mar. Sei. Symp., 198 (1994) Trophic interactions of cod stocks 557 commercial importance, with annual catches of 2000- that pre-recruit cod (0-group) are preyed upon by cepha­ 87 000 t for lllex and 11 000-25 000 t for Loligo during lopods in all areas. In view of the regularity and apparent the last decade (NAFO Stat. Bull.). Short-finned squid intensity of cephalopod migrations, the cod stocks of the migrate northwards to Newfoundland in summer, Northwest Atlantic and northern Norway are probably whereas long-finned squid migrate to shallow waters most affected by these predators, whereas their effect on from Cape Cod to Chesapeake Bay in spring and sum­ cod in the North Sea and, particularly, in Icelandic mer (Maurer and Bowman, 1985). waters should be regarded as negligible. In Icelandic waters the main species is flying squid (Todarodes sagittatus), which migrates occasionally to Crustaceans the southwestern grounds during summer and autumn. It has rarely been recorded since 1966. However, dur­ No direct information is available on predation by crus­ ing 1958-1966 the flying squid was more frequently taceans on eggs or larvae of cod in the field or in recorded although annual nominal catches were less experiments. However, consumption of other marine than 1000 t (Jönsson, 1980). fish larvae by a variety of crustacean groups, e.g. cope- Flying squid is also the most abundant species in the pods, euphausiids, and hyperiids, has been observed in Barents Sea and the Norwegian Sea, with annual catches field as well as laboratory studies (Hunter, 1984). Few of up to 18000 t during the last decade (Bulletin Statis­ crustaceans have been identified as predators of pelagic tique and ICES Fisheries Statistics). In the North Sea, fish eggs, but very few species have been studied so far cephalopods appear to be less abundant, judging by (Hunter, 1984). Among the predators of fish larvae, the annual catches, which were mostly less than 1000 t for euphausiid shrimp Euphausia pacifica (Theilacker and squid and less than 500 t for cuttlefish during the last Lasker, 1974), the hyperiid amphipod Hyperoche medu- decade (Bulletin Statistique and ICES Statistics). In sarum (Westernhagen and Rosenthal, 1976; Western­ groundfish surveys in the North Sea (IYFS and EGFS), hagen, 1976), the hyperiid amphipod, Parathemisto gau- catches of cephalopods have also been very small (ICES, dichaudi (Shaeder and Evans, 1975), and marine 1987). copepods (Lillelund and Lasker, 1971) have been identi­ Dawe (1992) analysed 11562 stomachs of short- fied as important invertebrate predators of fish larvae. finned squid at eight coastal Newfoundland localities in Thus, field studies indicate that fish larvae are vulner­ 1980-1990, finding that most otoliths occurring in the able to predation by marine crustaceans such as cope­ squid stomachs were from 0-group cod. The average pods and hyperiid amphipods. This is supported by frequency of occurrence of cod was 8.0%. This author observations in freshwater lakes (Hunter, 1984). In view also measured almost 4000 cod as prey of short-finned of these findings the predatory impact by crustaceans on squid at Newfoundland. The size range was 6-175 mm cod should be classified as a potentially important source (total length), but only a few specimens were larger than of mortality requiring further research. 85 mm. It was recognized by Dawe that the squid may reject the head of 0-group cod larger than 80 mm. Chaetognaths Maurer and Bowman (1985) calculated the consump­ No information is available on chaetognath predation on tion by squid (lllex and Loligo) off the Northeastern cod. An experiment on the feeding behaviour of Sagitta United States in 1979 and 1980, concluding that preda­ setosa and 5. elegans (Kuhlmann, 1977) indicated no tion by squid on fish of several species, including Atlan­ predation on fish eggs. Predation on fish larvae was tic cod, may be a significant source of pre-recruit mor­ tality. Jönsson (1980) analysed the stomach content of found to be limited, since copepods are the preferred prey and fish larvae were only preyed on in significant flying squid in Icelandic waters in 1979. Fish were the numbers after a starvation period of more than 24 h. most abundant prey (42% by volume of stomach con­ These findings suggest that chaetognaths of the genus tent), whereas herring was the only fish species quanti­ Sagitta are not important predators of fish larvae in fied (12% by volume). Of other fish species, 0-group cod and haddock were the most frequently recorded as prey. general. Breiby and Jobling (1985) analysed the food of flying squid in North Norwegian waters in 1982-1983 and identified 11 fish species. Pelagic species were more Fish frequently recorded than gadoid species. The approxi­ Some pelagic fish species have been identified as pred­ mate size range of cod as prey was 7-13 cm. ators of cod eggs and larvae (Table 2). Jespersen (1932) In view of the limited observations available on preda­ analysed stomach contents of 4900 herring (Clupea har- tion on cod by cephalopods, a quantitative analysis of engus) around Iceland during 1926-1931 and identified their predatory impact is not feasible. However, the approximately 50 postlarval cod, 1.5-3.0 cm in length, in studies carried out in the different areas clearly show one sample of herring stomachs. 558 Ô. K. Pâlsson ICES mar. Sei. Symp.. 198 (1994)

Table 2. Predation by fish on cod eggs and larvae by areas indicated as average number of eggs and larvae per 100 predators and percent of eggs eaten per day of the total egg production (% predation).

Eggs Larvae o//o Year of Area Predator /100 pred. /100 pred. predation n sampling Reference

Lofoten Herring 185000 0 1.4 81 1983 Meile (1985) Lofoten Norway pout 0 a 0 n.a. 20 1983 Melle (1985) Lofoten Cod 0 0 0 13 1983 Melle (1985)

Southern Bight Herring 360 n.a. 311 1976 Daan 1976 North Sea Herring 30 0.04-0.19 5 408 1980-1983 Daan et al. (1985) Southern Bight Sprat 200 n.a. 254 1976 Daan et al. (1985) German Bight Three spined 20 n.a. 15 1976 Daan et al. (1985) stickleback

North Sea Anchovy 70 363 1976 Garrod and Harding (1981) North Sea Sprat 0.1 1377 1976 Garrod and Harding (1981) North Sea Herring 3 81 1976 Garrod and Harding (1981) North Sea Whiting 0.2 592 1976 Garrod and Harding (1981) North Sea Sandeels 2 394 1976 Garrod and Harding (1981) North Sea Grey gurnard 0 283 1976 Garrod and Harding (1981) North Sea Dab 0 362 1976 Garrod and Harding (1981)

11 One stomach contained 37 fish eggs.

Meile (1985) studied the predation by fish on cod eggs Garrod and Harding (1981) examined the frequency at and larvae in the Lofoten area during 4 days in April which eggs and larvae of plaice and other fishes occurred 1983. He identified the herring as a heavy predator of in the diets of 3721 fish belonging to 27 species spawning cod eggs. The predatory impact by a herring population in the west central North Sea in 1976. Fish eggs, other of 47 million fish on cod eggs was estimated at 1.4% per than of the plaice, were found in the stomachs of eight day of the total egg production in that area and period predator species, but not identified to species level. (66 x 109 eggs). Thus, it can be concluded that at least 19 of the 27 species More fish species have been investigated in this re­ did not prey on cod eggs. However, for most of the 19 spect in the North Sea. Cod eggs have mainly been species the number of stomachs analysed was very low recorded in stomachs of herring and sprat (Fig. 3). (<10 stomachs). Of the seven predator species analysed

8 i

Herring Herring Sprat T.s.stickleb (S. Bight)

Predator species

Figure 3. Predation by fish on eggs of North Sea cod. ICES mar. Sei. Symp., 198 (1994) Trophic interactions o f cod stocks 559

CO

Anchovy Herring Sandeels Whiting Sprat

Predator species

Figure 4. Predation by fish on larvae of North Sea cod. in the highest numbers (anchovy Engraulis encrasicolus, skate (Raja radiata), Greenland halibut (Reinhardtius sprat, Spratussprattus, herring, whiting Merlangius mer- hippoglossoides), and cod were identified as relatively langus, sandeels Ammodytidae, grey gurnard Eutrigla outstanding predators of cod, but redfish (Sebastes spp.) gurnardus, and dab Limanda limanda), five contained and spotted wolffish (Anarh.ich.as minor) as of very cod larvae (Fig. 4); the largest number (24 larvae) was limited importance. Of 12 demersal species examined in found in the anchovy. Iceland waters, 7 were found to be eating cod. Among Stomach content studies of demersal fish are relatively these, cod and long rough dab (Hippoglossoides plates- frequent in the four areas covered in this review (Table soides) were more pronounced as cod predators than 3, Fig. 5). Of nine species examined in Newfoundland saithe (Pollachius virens), haddock (Melanogrammus waters, five were found to prey on cod. Of these, thorny aeglefinus), Greenland halibut, catfish, and redfish. Of

Table 3. Predation by fish on cod by area waters measured as average (over years and length groups) percent weight of stomach content (% weight) and percent occurrence of cod in stomachs by samples (% occurr.). (+ indicates a very low or an uncertain value of occurrence or weight, n = number of stomachs examined; n.a. = not available.

% % Year of Area Predator weight occurr. n sampling Reference

Newfoundland Cod 1.1 0.3 1898 1979 Lilly and Rice (1983) Newfoundland Cod n.a. 0.6 n.a. 1980-1991 Lilly pers. comm. Newfoundland Haddock 0 0 452 1963-1975 Podrazhanskaya and Shestov (1981) Newfoundland Redfish + + 2 669 n.a. Lambert (1960) Newfoundland Atlantic wolffish 0 0 149 n.a. Templeman (1985) Newfoundland Atlantic wolffish 0 0 n.a. 1981 Albikovskaya (1983) Newfoundland Spotted wolffish + + n.a. 1981 Albikovskaya (1983) Newfoundland Northern wolffish 0 0 n.a. 1981 Albikovskaya (1983) Newfoundland Halibut 0 0 5 1950 McIntyre (1953) Newfoundland Greenland halibut 5.7 0.5 10 309 1981-1984 Bowering and Lilly (1992) Newfoundland Greenland halibut n.a. 0.8 26426 1969-1981 Chumakov and Podrazhanskaya 1986 Newfoundland Thorny skate 4.1 1.5 446 1947-1967 Templeman (1982)

Iceland Cod 6.0 2.5 43143 1979-1992 Pâlsson (1983) Iceland Haddock 0.7 0.8 3 048 1979-1981 Pâlsson (1983) Iceland Saithe 3.0 0.8 1755 1979-1981 Pâlsson (1983) Continued overleaf. 560 Ô. K. Pâlsson ICES mar. Sei. Symp.. 198 (1994)

Table 3 continued

O/ 0 / /o /o Year of Area Predator weight occurr. n sampling Reference

Iceland Redfish 0.03 0.3 1614 1979-1981 Pâlsson (1983) Iceland Catfish 0.1 0.5 2 182 1979-1981 Pâlsson (1983) Iceland Long rough dab 1.6 1.7 438 1979-1981 Pâlsson (1983) Iceland Megrim 0 0 205 1976-1977 Steinarsson (1979) Iceland Witch 0 0 153 1976-1977 Steinarsson (1979) Iceland Lemon sole 0 0 119 1976-1977 Steinarsson (1979) Iceland Halibut 0 0 630 1948-1950 McIntyre (1953) Iceland Megrim 0 0 428 1938-1960 Rae (1963) Iceland Witch 0 0 105 1949-1952 Rae (1969) Iceland Greenland halibut 0.4 0.2 1 478 1991-1992 Sölmundsson 1993 Iceland Black grenadier 0 0 132 1967 Podrazhanskaya 1968

Barents Sea Cod 3.9 1.4 57 126 1949-1992 Bogstade/a/. (1993) Barents Sea Haddock 0 0 1984 1984-1986 Burgos and Mchl (1987) Barents Sea Greenland halibut 0 0 87 1982 Haug and Gulliksen (1982) Barents Sea Greenland halibut n.a. 1.3 43 304 1980-1989 Shvagzhdis (1990) Barents Sea Witch 0 0 355 1975-1976 Mattson (1981) Barents Sea Fourbeard rockling 0 0 329 1975-1976 Mattson (1981) Barents Sea Norway pout 0 0 268 1975-1976 Mattson (1981) Barents Sea Silvery pout 0 0 468 1975-1976 Mattson (1981) Barents Sea Galeus melastomus 0 0 59 1975-1976 Mattson (1981) Barents Sea Thorny skate 8.8 8.2 1352 1983-1987 Berestovsky (1989) Barents Sea Round skate 0 0 108 1983-1987 Berestovsky (1989) North Sea L.-sp. dogfish 0 613 1921-1963 Rae and Shelton (1982) North Sea Bl.-m. dogfish 0 200 1928-1961 Rae and Shelton (1982) North Sea Cuckoo ray 0 430 1924—1961 Rae and Shelton (1982) North Sea Shagreen ray 0 130 1928-1960 Rae and Shelton (1982) North Sea Blonde ray 0 56 1928-1959 Rae and Shelton (1982) North Sea Skate 0 255 1928-1959 Rae and Shelton (1982) North Sea Starry ray 0 253 1928-1959 Rae and Shelton (1982) North Sea Thornback ray 0 334 1928-1959 Rae and Shelton (1982) North Sea Spotted ray 0 172 1928-1959 Rae and Shelton (1982) North Sea Angler fish 0.4 1 630 1921-1958 Rae and Shelton (1982) North Sea Catfish 0 437 1921-1959 Rae and Shelton (1982) North Sea Hake 0 416 1923-1959 Rae and Shelton (1982) North Sea Brill 0 178 1948-1959 Rae and Shelton (1982) North Sea Ling 2a 45 h 1951-1959 Rae and Shelton (1982) North Sea Lythe 0 56 b 1951-1959 Rae and Shelton (1982) North Sea Tusk 0 20 b 1951-1959 Rae and Shelton (1982) North Sea Conger eel 0 16 b 1951-1959 Rae and Shelton (1982) North Sea Halibut 0 13 1949-1951 McIntyre (1953) North Sea Megrim 0.1 2 503 1938-1960 Rae (1963) North Sea Witch 0 1751 1938-1953 Rae (1969) North Sea Lemon sole 0 4 987 1935-1955 Rae (1956) North Sea Norway pout 0 1129 1960-1962 Raitt and Adams (1965) North Sea Cod 4 11418 1981 Daan (1989) North Sea Cod 1.6 9 723 1991 Kikkert (1993) North Sea Haddock 0 17 396 1981 Daan (1989) North Sea Whiting 0.3 9 217 1981 Daan (1989) North Sea Saithe 0.1 2190 1981 Daan (1989) North Sea Mackerel 0.1 4 945 1981 Daan (1989) North Sea Horse mackerel 4 395 1986 Dahl and Kirkegård (1987) North Sea Starry ray 0 1838 1983-1986 Vinther (1989) North Sea Starry ray 0.6 3 201 1991 Daan el al. (1993) North Sea Raja naevus 0 192 1991 Daan et al. (1993) North Sea R. montagui 0 133 1991 Daan et al. (1993) North Sea R. clavata 0 206 1991 Daan et al. (1993) North Sea Grey gurnard 1.8 11700 1991 Gee and Kikkert (1993)

a Of stomachs containing food. b Stomachs containing food. L.-sp. dogfish = Lesser-spotted dogfish, Bl.-m. dogfish = Black-mouthed dogfish. CSmr e.Sm. 198(1994) Symp., Sei. mar. ICES Figure 5. Predation by fish on cod by areas, indicated as % weight (black columns) or % occurrence (whitecolumns). occurrence %weightby (blackfish %or columns) as Predation indicated bycodareas, on 5.Figure

% % weight % weight % weight % weight o H mcee Wiig akrl ate ig nlrfs Megrim fish Angler Ling Saithe Mackerel Whiting mackerel H. Cod hrysae Gr.halibut skate Thorny rhlbt hrysae Gr.halibut skate Thorny Gr.halibut Saithe Newfoundland Barents Sea Barents Predator species Predator North Sea North Iceland Haddock Trophic interactions o f cod stocks f cod o interactions Trophic Gr.halibutCatfish Redfish

% occurr % occurr % occurr % occurr 561 562 Ô. K. Pâlsson ICES mar. Sei. Symp., 198 (1994)

10 species examined in Norwegian waters only three Results of feeding studies on the three seal species in were found to prey on cod, i.e. thorny skate, cod, and different areas are summarized in Table 5 and shown in Greenland halibut. Of 33 species in the North Sea, 10 Figure 6. In recent years, the method of recalculated were identified as predators of cod. Most pronounced as weight of the stomach content has mainly been applied, predators were cod, horse mackerel (Trachurus trachur- although the less quantitative method of frequency of us), and grey gurnard, where starry ray, whiting, saithe, occurrence is still in use. In the former method, undi­ and mackerel (Scomber scombrus) were of relatively gested parts, such as otoliths, are used to recalculate the minor importance in this respect. size of the prey. Cannibalism in cod appears to be a relatively import­ In general, the predation on cod is most intense in the ant source of predation compared with predation by case of the grey seal (% by weight 19-42%; % by other demersal fish in most of the areas considered occurrence 11-41%), intermediate for the harbour seal (Table 3, Fig. 5). In Icelandic waters cannibalism (% by weight <24%; % by occurrence <9%), and occurred in 2.5% of the samples examined and com­ relatively limited for the harp seal (% by weight <14%). prised 6% of the average stomach content. Using the There is a marked difference in predation by areas. correction procedure described in Bogstad et al. (1994) it The harbour seals prey more intensively on cod off can be calculated that, on an individual fish basis, 0.6% Iceland and in the Skagerrak-Kattegat than in the North of the cod had consumed cod. Cannibalism in cod in the Sea, Norway, and eastern Canada. The grey seals, on Barents Sea is analysed by Bogstad et al. The incidence the other hand, seem to prey more heavily on cod in the of cannibalism in this analysis was 3.9% by weight and Gulf of St Lawrence than in the North Sea or off Iceland. 1.4% by occurrence. In the North Sea, cannibalism was For harp seals, increased predation on cod was observed more pronounced in 1981 than in 1991 in terms of in 1986-1988 during migrations from the Barents Sea to average weight of stomach content or 4% and 1.6%, the Norwegian coast. In their Arctic habitats (Canadian respectively. The incidence of cannibalism in cod in the arctic, West Greenland, Barents Sea) the predation by waters of Newfoundland has been found to be low, or harp seals on cod is negligible. 0.6% by frequency of occurrence in divisions 2J 3KL in Length measurements and age analyses of cod as the 1980-1991, (Lilly, pers. comm.), and 1.1% by weight in prey of seals indicate that the bulk of the cod belong the northern Grand Bank in 1979 (Lilly and Rice, 1983). within the youngest age groups (0—II) and the length range 10-50 cm, although older and larger fish are also recorded. For North Sea grey seals, predation has been Seals recorded on age groups 0-IV, but mainly on the age The most important stocks of seals in the context of fish groups 0—III (Sea Mammal Research Unit, 1988). Cod predation are probably the harbour seal (Phoca vitu- as prey of grey seals at Anticosti Island, Gulf of St lina), the grey seal (Halichoerus grypus), and the harp Lawrence, were mainly (>90%) in this length range seal (Phoca groenlandica). These stocks differ greatly in (Benoit and Bowen, 1990b). Age analyses of cod as the population sizes with respect to the various areas. In prey of harbour seals and grey seals in Icelandic waters areas where all three stocks are found (Northwest Atlan­ have shown that approximately 90% or more of the cod tic and Barents Sea/Norwegian coast) the harp seal belong within age groups 0—II. Age groups III- and IV stocks are the largest. In Icelandic waters and in the were also recorded (Hauksson, 1984) and even cod up to Baltic, the harbour seal population is larger than the 6 years old on occasion (Hauksson, pers. comm.). Cod grey seal population, whereas grey seals outnumber eaten by harbour seals in the Moray Firth, Northeast harbour seals in the North Sea. Estimates of seal stock Scotland were virtually all 0-group fish (Thompson et al., sizes in the different areas are summarized in Table 4. 1991). Length distribution of cod recorded in harp seal

Table 4. Approximate ranges of seal population sizes for various areas as indicated by available information (total population in thousands).

Area Harbour seal Grey seal Harp seal Reference

Eastern Canada 10-20 50-100 1000-2500 Templeman (1990) Iceland 40-50 10-20 Hauksson (1989) Barents Sea 800-1000 Benjaminsen and Christensen (1979) Norwegian coast 4.5+ 3+ Thompson et al. (1990) North Sea 25 + 100 Thompson et al. (1990) Baltic 2 2 Almkvist et al. (1980) CSmr Si yp. 198(1994) Symp.. Sei. mar. ICES Figure 6. Predation by seals on cod by areas, indicated as % weight (black columns) or % occurrence (whitecolumns). occurrence % weightor (blackcolumns)as %by indicated seals by Predation cod onareas, 6.Figure

% weight % weight % weight ufS.ar N.ufLw. cl Sol Sol Es.a. NW.Gulf.Lawr. East.Can. Scotl. Scotl. Icel. NW.Gulf.Lawr. Gulf.St.Lawr. Can.Arc. W.Greenl. Bar.Sea N.Norw.(wint.) N.Norw. NW Atlant. NW N.Norw. N.Norw.(wint.) Bar.Sea W.Greenl. Can.Arc. owy .it kg-atg Sa. kg Wde. atCn Sol Sol Skag. Scotl. Scotl. East.Can. Wadden. Skag. Skag. Skag.-Katteg. M.Firth Norway Harbour Seal Harbour Grey Seal Grey Harp Seal Harp Trophic interactions o f cod stocks f cod o interactions Trophic

% % occurr % occurr % occurr 564 Ô. K. Pâlsson ICES mar. Sci. Symp.. 198(19V4)

Table 5. Predation by seals on cod by areas measured as percent recalculated weight or percent frequency of occurrence of cod in stomach or faecal samples.

°//o % Year of Predator Area weight occurr. n sampling Reference

Harbour seal Eastern Canada n.a. 2.1 602 1968-1973 Boulva and McLaren (1979) Harbour seal Iceland 23.9 n.a. 140 1979-1982 Hauksson (1984) Harbour seal Norway coast 5.4 3.4 238 1978-1982 Bjørge et al. (1993) Harbour seal Scotland n.a. 4.9 78 1967-1971 Rae (1973) Harbour seal Scotland n.a. 3.4 508 1986-1988 Pierce et al. (1990) Harbour seal Moray F. (NE Scotland) 1.9 n.a. 4 0 a 1988-1989 Thompson et al. (1991) Harbour seal Skagerrak-Kattegat 16.0 n.a. 103“ 1980 Härkönen (1988) Harbour seal Skagerrak 20.0 n.a. 314a 1977-1979 Härkönen (1987) Harbour seal Skagerrak 23.0 n.a. n.a. 1989 Härkönen et al. (1991) Harbour seal Skagerrak n.a. 8.8 193 a 1990-1991 Olsen and Björge ( 1992) Harbour seal Wadden Sea (North Sea) 5.1 n.a. 138 1981-1984 Sievers (1989)

Grey seal Eastern Canada n.a. 18.5 1878 1950-1987 Benoit and Bowen (1990a) Grey seal Gulf St Lawrence 41.5 n.a. 744 1982-1987 Benoit and Bowen (1990b) Grey seal NW Gulf St Lawrence 36.0 41.0 82 1983 Murie and Lavigne (1992) Grey seal Iceland 30.5 n.a. 215 1990-1991 Hauksson (pers. comm.) Grey seal Iceland 22.0 n.a. 89 1979-1982 Hauksson (1984) Grey seal Scotland n.a. 10.8 241 1967-1971 Rae (1973) Grey seal Scotland 18.7 n.a. 1401 1983-1988 Hammond and Prime (1990) Grey seal SW North Sea 17.6 n.a. 481 1985 Prime and Hammond (1990)

Harp seal NW Atlantic 7h n.a. 1949-1971 Sergeant(1973) Harp seal Canadian Arctic 0 n.a. 157 1978-1979 Finley et al. (1990) Harp seal W Greenland 4 n.a. 818 1986-88 Kapel and Angantyr (1989) Harp seal Barents Sea (summer) 0 n.a. 58 1987 Lydersen et al. (1991) Harp seal N Norway (winter) 14.0 n.a. 59 1986, 1988 Nilssen et al. (1992) Harp seal N Norway 13.5 n.a. 153 1986-1988 Haug et al. (1991)

"Faecal samples. b % numbers.

stomachs off North Norway covered the length range 5- natural mortality by age caused by this predation was in 70 cm, but was mainly (>90%) in the range of 10-55 cm the range 0.0034—0.1259. (Nilssener al., 1992). Hammond and Prime (1990) concluded that a great Boulva and McLaren (1979) estimated that a harbour deal of information is required to assess the impact of seal population of 12700 in eastern Canada in 1973 seal consumption on commercial fish stocks and fish­ could have consumed about 8500 t, mainly fish, and eries. In addition to consumption of fish and seal popu­ classified the overall economic impact of such a take as lation size, data are needed on the local distribution and negligible. movements of the fish prey and on the distribution of Hauksson (1989) estimated the consumption of har­ grey seal feeding effort. bour seal and grey seal in Icelandic waters based on population sizes of 43000 and 12000 animals, respect­ Whales ively. The calculated total fish consumption by harbour seal and grey seal was 20 4311 and 15 8441, respectively; The stomach content of minke whales (Balaenoptera the consumption by cod was 6680 and 4145 t respect­ acutorostrata) in various areas of the North Atlantic has ively. Clearly, such an impact would have major impli­ been described (Table 6 and Fig. 7). Sergeant (1963) and cations for fisheries management. Mitchell (1974a) analysed the stomach contents of The annual amount of cod consumed by grey seals in minke whales in the Northwest Atlantic and identified the North Sea has been estimated based on data col­ capelin as the predominant food. Cod was the second lected in 1985 (ICES, 1988, Table 2.5.4; Sea Mammal most important prey with 9% and 12% frequency of Research Unit, 1988). The number of cod consumed at occurrence, respectively. The material (32 animals) ana­ ages 1-4 was 14.3 million or 4.8% of the size of this stock lysed by Sergeant (1963) was sampled in June-July. component (299.2 million). The partial coefficient of However, the occurrence of cod in the food of 338 minke ic e s mar. sd. Symp., 198 (1994) Trophic interactions of cod stocks 5 6 5

Table 6. Predation by minke whale on cod by areas measured as percent frequency of occurrence of cod in stomach samples.

°//o Year of Area occurr. n sampling Reference

Barents Sea 0 13 1950 Jonsgârd (1982) Bear Island 0 53 1950 Jonsgärd (1982) Spitsbergen 4 26 1950 Jonsgård (1982) Coast of Norway 13 107 1943-1950 Jonsgård (1982) Coast of Norway 21 34 1988, 1990 Nordöy and Blix (1992) Spitsbergen 0 17 1989 Nordöy and Blix (1992) W Spitsbergen 6 16 1992 Haug et al. (1993) Bear Island 5 19 1992 H auge/al. (1993) Kola coast 47 19 1992 Haug et al. (1993) Finnmark coast 15 20 1992 Haug et al. (1993) Lofoten/Vesterålen 16 18 1992 Haug et al. (1993) Iceland 2 58 1977-1978 Sigurjönsson and Galan (1990) Newfoundland 9 32 n.a. Sergeant(1963) Newfoundland 1 338 1948,1951-1961 Sergeant(1963) Newfoundland 12 172 1966,1969-1972 Mitchell (1974a) Greenland 0 36 1968 Jonsgård (1982)

whales, as reported in whaling statistics from 1948 and stomachs of minke whales sampled in coastal north 1951-1961, was markedly lower (approximately 1%), Norwegian waters during summer 1992 (Haug et al., (Sergeant, 1963). 1993) and in 1990 (Nordøy and Blix, 1992). Jonsgård Of 237 minke whales from several areas, 15 animals (1982) reported one minke whale caught off Spitsbergen caught in Lofoten and at Spitsbergen contained cod as with its stomach half full of small fish, probably cod. prey. Some stomachs were completely full of cod and Furthermore, 14 minke whales from Lofoten contained one stomach contained 40 large fresh cod (Jonsgård, large cod; one stomach contained 40 large, fresh cod. 1982). In material sampled off the Norwegian coast in According to these findings, “large” cod seem to be 1988 and 1990, 6 animals out of 29 contained cod more frequent as the prey of minke whales than “small” (Nordøy and Blix, 1992). In the most recent study of the cod. feeding habits of minke whales caught during scientific In one analysis of 58 minke whales from Icelandic whaling operations in the Northeast Atlantic in the waters, one stomach was almost full of cod and another summer of 1992, a higher level of predation on cod was with cod or a cod-like species (Sigurjönsson and Galan, recorded in all areas (Haug et al., 1993). 1990). Limited information is available on the size of cod as Thus, the minke whale has been identified as a pred­ the prey of whales. “Large” cod were recorded in the ator of cod in some areas. This stock is one of the largest

Norway coast Spitsbergen Bear Island Newf.ld. Iceland

Figure 7. Predation by minke whale on cod by areas, indicated as % occurrence (average values of available results. Table 6). 566 Ô. K. Pâlsson ICES mar. Sei. Symp., 198 (1994) whale stocks in the North Atlantic. The stock has been Newfoundland and Nova Scotia in 1969-1971. No cod estimated at 27 000 animals in Icelandic and adjacent were identified in the stomachs, but capelin was the prey waters (Sigurjönsson and Vfkingsson, 1992) and at found in most stomachs containing food. Similar results about 80000 animals in Norwegian waters (Inter­ were found in the case of the sei whale (Balaenoptera national Whaling Commission, 1991). The annual con­ borealis) in the Northwest Atlantic (Mitchell, 1974b) sumption by minke whales of fish in Icelandic waters has and in the Norwegian Sea (Hjort and Ruud, 1929). The been estimated at about 200000 t (Sigurjönsson and same is true for blue whale (Balaenoptera musculus) in Vfkingsson, 1992). The impact of minke whale preda­ the Norwegian Sea (Hjort and Ruud, 1929) and in the tion on cod obviously depends on the reliability of the Northwest Atlantic, where several hundred stomachs of stomach data. The Icelandic material indicates mark­ blue whale from the region of Newfoundland were edly lower predation by minke whale on cod than analysed (Tomilin, 1967). Thus, the highly specialized observed off Norway and Newfoundland. In general, foraging of the large baleeen whales on zooplanktonic however, the predator-prey interaction of minke whale prey has been recognized for more than a century. Cod and cod must be considered as one of the major whale- has very rarely been identified as prey. The predatory cod interactions in the North Atlantic. impact of these whale stocks on cod must therefore be Jonsgård (1966) reviewed observations on the food of regarded as virtually zero. fin whales (Balaenoptera physalus) in Norwegian, Ice­ Roe (1969) examined 57 sperm whales (Physeter landic, and western North Atlantic waters as well as off macrocephalus) caught off the west coast of Iceland in the British Isles. The fish prey found in stomachs con­ 1967. Cod was identified in the stomach of three animals sisted almost exclusively of pelagic species such as her­ (Table 7). Martin and Clarke (1986) examined 221 ring, capelin, and blue whiting. Cod as prey was sperm whales captured between Iceland and Greenland recorded only from southwest Greenland waters, where in 1977-1981, finding that cod was commonly rep­ 600 cod were found in one fin whale and 800 in another resented by otoliths but rarely, if ever, by flesh. They (Brown, 1875; cited in Jonsgård, 1966). However, this concluded that it would seem reasonable to classify cod, information is considered doubtful (Allen, 1916; cited in along with a number of other fish species, as of second­ Jonsgård, 1966). In an analysis of the food of 435 fin ary importance in the fish biomass consumed by sperm whales caught off the Norwegian coast in 1952-1953, whales, whereas lumpfish (Cyclopterus lumpus) pro­ none was found to contain cod, whereas pelagic fish vided at least 50% of the fish biomass. Stomach content species (capelin, herring, blue whiting (Micromeristius analyses of northern bottlenose whale (Hyperoodon pontasson), and mackerel) were found in 22 stomachs ampullatus) and pilot whale (Globicephala melas) indi­ (Jonsgård, 1966). This author concluded “that the North cate that these species do not prey on cod (Table 7). Atlantic fin whales do not seem to feed on large fish”. More limited information is available on the food of Comparable results were reported by Mitchell ( 1974) for other toothed whales, such as the killer whale (Orcinus fin whales in the Northwest Atlantic (Table 7). orca), the white-beaked dolphin (Lagenorhynchus albir- Mitchell (1973) reported on the stomach content of 41 ostris), the white-sided dolphin (L. acutus), and the humpback whales (Megaptera novaeangliae) caught off harbour porpoise (Hyperoodon ampullatus). According

Table 7. Predation by baleen whales, other than minke whale and toothed whales, on cod by areas measured as percent frequency of occurrence of cod in stomach samples.

% Year of Predator Area occurr. n sampling Reference

Blue whale Norwegian Sea 0 n.a. n.a. Hjort and Ruud (1929) Blue whale NW Atlantic 0 n.a. n.a. Tomilin (1967) Fin whale Coast of Norway 0 435 1952-1953 Jonsgârd (1966) Fin whale NW Atlantic <1 n.a. 1967-1972 Mitchell (1974b) Humpback whale NW Atlantic 0 41 1969-1971 Mitchell (1973) Sei whale Norwegian Sea 0 n.a. n.a. Hjort and Ruud (1929) Sei whale NW Atlantic 0 n.a. 1967-1972 Mitchell (1974b)

Sperm whale Iceland 5 57 1967 Roe (1969) Northern bottlenose Labrador 0 108 1971 Benjaminsen and Northern bottlenose Iceland 0 46 1967 Christensen ( 1979) Pilot whale Faroe Is. 0 720 1986-1987 Desportes and Mouritsen 1988 ICES mar. Sei. Symp.. 198 (1994) Trophic interactions of cod stocks 567 to Tomilin (1967), cod have been identified in the seabirds have been carried out in the Barents Sea (Table stomachs of three of these species, i.e., killer whale, 8). Erikstad (1990) studied the feeding of four seabird white-beaked dolphin, and harbour porpoise. Accord­ species in the open water of the southeastern Barents ing to Lepektin (1805, cited by Tomilin 1967), a killer Sea, near the ice edge. 1-group cod were recorded in all whale which ran aground in Norway contained “600 species, most frequently in Brünnich’s guillemot (58.3% codfishes, numerous birds and an enormous quantity of frequency of occurrence) and kittiwake (Rissa tridac- still undigested herrings”. tyla) (57.7%), followed by glaucous gull (18.2%) and Sigurjönsson and Vfkingsson (1992) have estimated northern fulmar. the annual consumption of whales in Icelandic and Barrett et al. (1990) studied the diets of shags (Phala- adjacent waters. The total fish consumption by toothed crocorax aristotelis) and cormorants (P. carbo) along the whales was estimated to be 850000 t. Thereof, the fish Norwegian coast through analyses of regurgitated pel­ consumption by the four cod predator species (sperm lets. Cod was recorded in cormorants, and unidentified whale, killer whale, white-beaked dolphin, and harbour gadoids (cod or saithe), mainly 0- and 1-group, occurred porpoise) was about 300 000 t. Killer whales consumed frequently in both bird species. almost 50% of this amount, or 140000 t, and the other Cod as the prey of fulmar, kittiwake, glaucous gull, three species 46000 to 68000 t each. Further stomach and Briinnich’s guillemot in the Barents Sea in March content analyses of the toothed whales are needed to 1987, were 1-group fish in the length range 1.9-13.6 cm, identify the prey species composition of the fish con­ but differing between species (Erikstad, 1990). Cormor­ sumed by these predators. ants and shags in coastal Norwegian waters were found to prey on 0—II group gadoids (cod and saithe) in the length range 2-36 cm (Barrett et al., 1990). Seabirds In the North Sea, numerous studies have covered the Few studies are available of predation by seabirds on cod predatory aspects of seabirds (Table 8). Pearson (1968) in the Northwest Atlantic (Table 8). Studies of the studied the diet of nine seabird species through analysis feeding habits of three species of seabirds, mainly in the of regurgitated food. Ammodytidae and Clupeidae were high Arctic, indicate limited predation on cod. Briin- the commonest food of most species. Cod were recorded nich’s guillemot (thick-billed murre, Uria lomvia), in four species, i.e., kittiwake, lesser black-backed gull northern fulmar (Fulmarusglacialis), and little auk (Alle (Larus fuscus), shag, and cormorant, but their quantity alle), taken off Baffin Island and Northwest Greenland, was not measured. However, the percentage by weight did not prey on cod (Roby et al., 1981 ; Bradstreet, 1982; of Gadidae in the diet of the four species were 21%, Bradstreet and Cross, 1982). Stomachs of Brünnich’s 52%, 30%, and 19%, respectively. guillemot sampled in Ungava Bay, Hudson Strait, con­ Harris and Hislop (1978) and Hislop and Harris tained many otoliths of Atlantic cod (Tuck and Squires, (1985) analysed fish dropped by puffins (Fratercula arc- 1955). tica) feeding youngs at colonies around the coast of In Icelandic waters studies in this field are also limited Scotland. Cod were recorded in the diet on the Isle of (Table 8). Tåning (1930) described the food of auks in May. Gadoids were recorded on the Isle of May and on Icelandic waters in a popular article. His findings, based Hermaness. Furness and Hislop ( 1981) studied pellets of on an unknown number of stomachs, indicated post- the great skua (Catharacta skua) in Shetland and did not larval fish as an important food, especially haddock as record cod as prey. Blake et al. (1985), in studying the well as cod and also whiting, Norway pout (Trisopterus feeding ecology of guillemots off North and East Scot­ esmerkii) and capelin (Mallotus villosus). land, recorded cod only occasionally, whereas gadoids Ingölfsson (1976), in analysing the stomach contents (mainly saithe and Trisopterus sp.) were more abundant of great black-backed gulls (Larus marinus) and glau­ and sandeel the commonest prey. Blake (1984) studied cous gulls (L. hyperboreus), found that the fish prey the diet of auks in the North Sea. Cod were not identi­ were mostly sand lance and capelin. Other fish, usually fied but some other gadoids occurred occasionally. Gal­ young gadoids, were recorded from 28 great black- braith (1983) examined chick regurgitations of backed gulls (13.4% occurrence) and 11 glaucous gulls kittiwakes on the Isle of May, Firth of Forth, Scotland, (4.6% occurrence). Cod were not identified as a species. identifying mainly sand-eels but no cod as prey. Com­ Lilliendahl (1990) studied the feeding of two guille­ parable results were obtained by Furness and Todd mot species and razorbill in three fjords (Faxaflöi, Eyja- (1984) for the diet of fulmars at Foula, Shetland. Harris fjöröur, and Skjâlfandi) during September-May and and Wanless (1991) analysed regurgitated food and recorded no predation on cod. However, four gadoid pellets from shags on the Isle of May. Sandeels domi­ fish were recorded in one Briinnich's guillemot in Eyja- nated in the diet but cod were recorded in 18.2% of the fjöröur in April 1983. pellets although in low numbers. Cod were not recorded A large number of studies on the feeding habits of in the regurgitations. 568 Ô. K. Pâlsson ICES mar. Sei. Symp., 198 (1994)

Table 8. Predation by marine birds on cod by areas measured as percent by numbers of prey and percent frequency of occurrence.

°//o % Year Area Predator number occurr. n sampling Reference

NW Atlantic Briinnich’s guillemot + + 34“ 1954 Tuck and Squires (1955) NW Atlantic Briinnich’s guillemot 0 0 n.a. h 1954 Tuck and Squires (1955) NW Atlantic Briinnich's guillemot 0 0 115 1978-1979 Bradstreet and Cross (1982) NW Atlantic Northern fulmar 0 0 115 1978-1979 Bradstreet and Cross (1982) NW Atlantic Little auk 0 0 410 1976-1979 Bradstreet (1982) NW Atlantic Little auk 0 0 204 1978 Roby et al. (1981)

Iceland Great black-backed gull 0 0 223 1964-1965 Ingölfsson (1976) Iceland Glaucous gull 0 0 244 1964-1965 Ingölfsson (1976) Iceland Briinnich’s guillemot 0 0 37c 1982-1983 Liiliendah! (1990) Iceland Razorbill 0 0 101 1982-1983 Lilliendahl (1990) Iceland Common guillemot 0 0 123 1982-1983 Lilliendahl (1990)

Barents Sea Kittiwake 29 58 26 1987 Erikstad (1990) Barents Sea Kittiwake + + 34 1985 Lønne and Gabrielsen (1992) Barents Sea Kittiwake 0 0 20 1984 Lydersen et al. (1989) Barents Sea Kittiwake 0 0 72 1983 Furness and Barnett (1985) Barents Sea Glaucous gull 15 18 11 1987 Erikstad (1990) Barents Sea Glaucous gull 0 0 18 1984 Lydersen et al. (1989) Barents Sea Great black-backed gull 0 0 12 1983 Furness and Barnett (1985) Barents Sea Herring gull 0 0 45 1983 Furness and Barnett (1985) Barents Sea Northern fulmar 8 17 30 1987 Erikstad (1990) Barents Sea Northern fulmar 0 0 20 1984 Lydersen et al. ( 1989) Barents Sea Puffin 0 0 14 1984 Lydersen et al. (1989) Barents Sea Puffin 0 0 193 1983 Furness and Barnett (1985) Barents Sea Black guillemot 0 0 20 1984 Lydersen et al. (1989) Barents Sea Black guillemot 0 0 13 1985 Lønne and Gabrielsen (1992) Barents Sea Black guillemot 0 0 20 1983 Furness and Barnett (1985) Barents Sea Common guillemot 0 0 1580 1983 Furness and Barnett (1985) Barents Sea Briinnich's guillemot 81 58 24 1987 Erikstad (1990) Barents Sea Briinnich’s guillemot 0 0 50 1983 Furness and Barnett (1985) Barents Sea Briinnich’s guillemot 0 0 34 1985 Lønne and Gabrielsen (1992) Barents Sea Briinnich's guillemot 0 0 21 1984 Lydersen et al. (1989) Barents Sea Shag 0 0d 204 1985-1986 Barrett et al. (1990) Barents Sea Shag 0 0 9 1983 Furness and Barnett (1985) Barents Sea Cormorant 14 3e 100 1989 B arrette!al. (1990) Barents Sea Eider 0 0 20 1984 Lydersen etal. (1989) Barents Sea Little auk 0 0 11 1984 Lydersen et al. (1989) Barents Sea Razorbill 0 0 24 1983 Furness and Barnett (1985)

North Sea Common guillemot + + 750 1982-1983 Blake et al. (1985) North Sea Common guillemot 0 0 403 1983 Blake (1984) North Sea Razorbill 0 0 503 1983 Blake (1984) North Sea Kittiwake 0 0 147f 1982 Galbraith (1983) North Sea Kittiwake + + 218 1961-1963 Pearson (1968) North Sea Lesser black-backed gull + + 68 1961-1963 Pearson (1968) North Sea Fulmar 0 0 177f 1978-1982 Furness and Todd (1984) North Sea Shag + + 24 1961-1963 Pearson (1968) North Sea Shag 0.2 18.2 1476 1985-1990 Harris and Wanless (1991) North Sea Cormorant + + 100 1961-1963 Pearson (1968) North Sea Puffin 0 + 638 s 1971-1976 Harris and Hislop (1978) North Sea Puffin 0.9 n.a. 1062h 1973-1982 Hislop and Harris (1985) North Sea Great skua 0 0 n.a. 1975-1976 Furness and Hislop (1981)

“Stomachs of adults. hFood to young. 'Gadoid fish in one stomach. dUnid. gadoids 20-71% occurrence. eUnid. gadoids 9-17% occurrence, th ic k regurgitations. gSampling on Isle of May, Fair Isle and Hermaness. hNumber of loads to young, Isle of May. ICES mar. Sei. Symp., 198 (1994) Trophic interactions of cod stocks 569

Kittiwake G.gull N.fulmar B.guillemot Cormorant

Figure 8. Predation by marine birds on cod in the Barents Sea, indicated as % occurrence.

considerable uncertainty in view of the differences in Conclusions and discussion methods, data treatment, time of studies, predator species studied in the different areas, and other aspects. The main findings regarding life-stage, size, and age of The findings should, therefore, be regarded as a first cod falling prey to other marine animals, based on the indication of relevant trophic interactions of the cod studies mentioned earlier, are summarized in Figure 9. stocks in question. The absolute predatory impact is Cod eggs were identified in relatively few predators, and obviously very much dependent upon the size of the were mainly preyed on by invertebrates and pelagic fish, respective predator stock, which is only occasionally especially herring. Cod larvae were also primarily ident­ dealt with in this review. ified as the prey of invertebrates and pelagic fish. Two species of marine invertebrates have been ident­ 0-group cod appear to be the life-stage most vulner­ ified as relatively important, i.e. A. aurita as a predator able to predation and were identified as the prey of most of eggs and larvae in the Barents Sea and short-finned predators, the exceptions being invertebrates and small squid as a predator of 0-group cod in Newfoundland pelagic fish. 1-group cod were identified as the prey of waters. The scarcity of invertebrate predators can hardly predators other than invertebrates and pelagic fish. be interpreted as an indication of the limited predatory Older cod were only found as the prey of cod, seals, and impact of this predator group on cod. Studies of the minke whale as well as cormorants (2-group). The predation of marine invertebrates on fish as prey as well length range of the prey varies accordingly, the largest as laboratory experiments suggest interesting and rele­ prey, up to 70 cm, being found in cod, seals, and minke vant trophic interactions between marine invertebrates whale, whereas for other predators the prey length was and eggs and larvae of fish. Intensive studies are obvi­ usually less than 20 cm. ously required in this field. The food composition of cod on a prey group basis Predation by fish on cod has been recorded for various indicates a similar trophic level for the four cod stocks, in groups, e.g., pelagic and demersal fish, flatfish, and particular of the three Arcto-boreal stocks. Fish prey is elasmobranch fish. The predation covers all life-stages clearly the main level of food. However, it is well known of cod as prey, from eggs and larvae to medium-sized that prey species are different between North Sea cod fish, although the main predatory impact seems to be on and the other stocks, capelin being the main fish prey for the pre-recruit phase. However, predation by pelagic the northern cod stocks and various demersal and pela­ fish has only been recorded on eggs, larvae, and 0-group gic species for the North Sea cod. The crustacean group cod. Most noticeable is the predation by herring on eggs is most important for the smallest cod (<30 cm), but in the Lofoten area, by anchovy in the North Sea on cod contributes also markedly to the diet of small and larvae, and by horse mackerel in the North Sea on 0- medium-sized cod (30-70 cm). Other food contributes group cod. Among demersal fish, cod is apparently the the least to the diet of cod in all areas. most important predator of juvenile cod, especially age The trophic interactions of the cod stocks are summar­ groups 0—II, in three of the four areas, followed by ized in Table 9. Clearly, this information is subject to thorny skate and Greenland halibut. 570 Ô. K. Pâlsson ICES mar. Sei. Symp., 198 (1994)

Life-stage Age group Predator Area Eggs Larvae 0 12 3 4

B.infundibulum NC

A.aurita NC

Short-finned squid NF

Flying squid IC/BS

Herring NC/NS

Herring IC

Sprat NS

Three sp.stickleback NS

Anchovy NS

Sandeels NS

Horse mackerel NS

Mackerel NS

Whiting NS

Saithe NS

Cod NF

Cod BS

Cod NS

Cod IC

Haddock IC

Saithe IC

Redfish IC

Catfish IC

Long rough dab IC

Greenland halibut IC

Harbour seal IC

Grey seal IC

Grey seal GL

Harp seal BS

Kittiwake IC

Kittiwake BS

Glaucous gull BS

Northern fulmar BS

Brunnich’s guillemot BS

Cormorant NC

Shag NC

0 10 20 30 40 50 60 70

Prey length (cm)

Figure 9. Predation on cod with respect to life-stage, age, or length range of cod as prey. BS = Barents Sea, IC = Iceland, NF = Newfoundland, NS = North Sea, NC = Norway coast, GL = Gulf of St Lawrence.

The grey seal is probably the main predator seal in which are of some relevance as predators of cod. Their most of the areas affecting the juvenile cod stock com­ predatory impact seems to be most pronounced in the ponent, in particular age groups 0—II. In general, the Barents Sea and Newfoundland waters, and more lim­ prey selection of seals and cod on cod as prey appears to ited in Icelandic waters. They are indicated as predators be similar in terms of size and age of the prey. of a broad size spectrum of cod. Minke whales are apparently the only baleen whales Predation by seabirds on cod has been recorded ICES mar. Sei. Symp., 198 (1994) Trophic interactions o f cod stocks 571

Table 9. Trophic interactions of cod stocks in the four areas indicated as average percent weight (w) or percent occurrence (o) of cod as prey. (+ indicates a low or uncertain value).

Area

Predator Newfoundland Iceland Barents Sea North Sea

B. infundibulum + A. aurita 5 (o) T. multicirrata + Short-finned squid 8 (0) Flying squid + +

Herring + + + Sprat + Sandeels + Anchovy + Three sp. stickleback + Horse mackerel 4 (w) Saithe 3 (w) 0.1 (w) Cod 1 (w) 6 (w) 4 (w) 3(w) Haddock 1 (w) Whiting 0.3 (w) Ling 2 (o) Redfish + + Catfish 0.1 (w) Spotted wolffish + Megrim O.l(o) Greenland halibut 6 (w) 0.4 (w) 1 (0) Long rough dab 2 (w) Starry ray 4(o) 9(o) 0.3 (w) Angler fish 0.4 (o) Grey gurnard 2 (w)

Harbour seal 2 (o) 24 (w) 5 (w) 4(o) Grey seal 19(o) 26 (w) 19 (w) Harp seal 7(o) 9 (w) Fin whale + Minke whale 7(o) 2 (o) 12(o) Sperm whale 5(o)

Kittiwake 15(o) + Great black-backed gull + Glaucous gull 9(o) Northern fulmar 9(o) Common guillemot + Briinnich’s guillemot + + 15 (o) Cormorant 3(o) + Shag + “ +

No. of species analysed 21 27 36 46

“Unidentified gadoids (saithe and cod).

mainly in the Barents Sea. Two bird species, kittiwake but gadoids occasionally, e.g., as the prey of gulls in the and Briinnich’s guillemot (thick-billed murre), seem to North Sea and Icelandic waters and kittiwake in the be the major predators, followed by glaucous gull and North Sea. northern fulmar. Cormorants and shags may also be Predation by invertebrates other than cephalopods, is important predators of cod, since cod or unidentified apparently the least studied area of research with respect gadoids (juvenile cod or saithe) were recorded in their to predation on cod. The available results strongly diet in considerable amounts in the Barents Sea and indicate that predators such as ctenophores, medusae, North Sea. However, cod has seldom been recorded in crustacean hyperiids, and euphausiids may constitute the diet of seabirds in the North Sea or Icelandic waters, highly relevant sources of natural mortality during the 572 Ô. K. Pâlsson ICES mar. Sei. Symp., 198 (1994)

early life-stages of cod. Intensified work in this field Bjørge. A.. Olsen. M., and Prime. J. 1993. Food and foraging should be given high priority in marine ecological re­ of the harbour seal, Phoca vitulina L., in Norwegian waters search during the next decade. (ms). Blake, B. F. 1984. Diet and fish stock availability as possible Feeding studies in relation to multispecies consider­ factors in the mass death of auks in the North Sea. J. Exp. ations have focused on fish, as predators and as prey, as Mar. Biol. Ecol., 76: 89-103. well as top predators such as seals. The findings, sum­ Blake, B. F., Dixon, T. J., Jones, P. H., and Tasker, M. L. marized in this review, indicate that relevant predators 1985. Seasonal changes in the feeding ecology of guillemots (Uria aalge) off north and east Scotland. Est. Coast. Shelf of cod may also be found in the lower taxa, i.e., among Sei., 20: 559-568. medusae and crustaceans, and among seabirds. In view Bogstad, B., Lilly, G., Mehl, S., Pâlsson, Ö. K., and Stefâns- of this, it seems appropriate to broaden the ecological son, G. 1994. Cannibalism and year-class strength in Atlantic basis of multispecies research. cod (Gadusmorhua L.) in Arcto-boreal ecosystems (Barents Sea. Iceland, and eastern Newfoundland). ICES mar. Sei. Symp., 198: 576-599. Boulva, J., and McLaren. I. A. 1979. Biology of the harbour Acknowledgments seal Phoca vitulina in eastern Canada. Bull. Fish. Res. Bd Can., 200: 24 pp. Information on the food of cod in areas other than Bowering, W. R., and Lilly, G. R. 1992. Greenland halibut Iceland was kindly provided by George Lilly for eastern (Reinhardtius hippoglossoides) off Southern Labrador and Newfoundland and by Sigbjørn Mehl for the Barents Northeastern Newfoundland (Northwest Atlantic) feed pri­ Sea. Bjarte Bogstad provided valuable information with marily on capelin (Mallotus villosus). Neth. J. Sea Res., 29: 211- 222. respect to the food and feeding of marine animals in the Bradstreet, M. S. W. 1982. Pelagic feeding ecology of dovekies, Barents Sea and Norwegian waters. The contributions Alle alle, in Lancaster Sound and western Baffin Bay. Arctic. by these colleagues are highly appreciated. Further­ 35: 126-140. more, I acknowledge the valuable assistance of Eirikur Bradstreet, M. S. W., and Cross, W. 1982. Trophic relation­ Einarsson, Sigurh'na Gunnarsdottir, Bâra Stefansdöttir, ships at high Arctic ice edges. Arctic, 35: 1-12. Breiby, A., and Jobling, M. 1985. Predatory role of the flying Jön Sölmundsson, and Pâli Enos in preparing this paper squid (Todarodes sagittatus) in North Norwegian waters. and of Hjâlmar Vilhjâlmsson for reading and correcting NAFO Sei. Coun. Stud., 9: 125-132. the manuscript. Finally, the critical and constructive Bulletin Statistique des Pêches Maritimes du Conseil Interna­ review of the manuscript by Professor Niels Daan and tionale pour l’Exploration de la Mer, Vol. no. 65-72 for the years 1980-1987. Dr John Hislop is acknowledged. Burgos, G., and Mehl, S. 1987. Diet overlap between north­ east Arctic cod and haddock in the southern part of the Barents Sea in 1984-1986. ICES CM 1987/G: 50. References Chumakov, A. K., and Podrazhanskaya, S. G. 1986. Feeding of Greenland halibut (Reinhardtius hippoglossoides) in the Albikovskaya, L. K. 1983. Feeding characteristics of wolffishes northwest Atlantic. NAFO Sei. Coun. Stud., 10: 47-52. in the Labrador-Newfoundland region. NAFO Sei., Coun. Daan, N. 1976. Some preliminary investigations into predation Stud., 6: 35-38. on fish eggs and larvae in the southern North Sea. ICES CM Almkvist, L., Olsson, M., and Søderberg, S. 1980. Sälar i 1976/L: 15.11 pp. Sverige. Svenska Naturskyddsføreningen, Stockholm. 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