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No. 19. The Role of Ctenophores and Salps in Zooplankton Production and Standing Crop By

J. H. F r a s e r Marine Laboratory, Aberdeen

Swarms of zooplankton have effects on the plankton sides of the North Atlantic, but it is rarely taken in the community as a whole, which may be more drastic open ocean. Mertensia is arctic in its distribution. than is generally realized. Two contrasting examples Bolinopsis is arctic and boreal and is more widespread are given ; the carnivorous ctenophores and the herbi­ than Mertensia, it occurs round the British Isles, though vorous salps. less numerous there than in more northern latitudes. Beroë is usually regarded as oceanic but it spreads into Ctenophores coastal areas often in great numbers. It is most Taxonomically these are divided into two classes: abundant in boreal regions but is nevertheless a wide­ Class Tentaculata and Class Nuda. The former in­ spread species. All of these can be very abundant, cludes the genera Pleurobrachia, Mertensia, Hormiphora, particularly during the summer and into autumn, but Bolinopsis, and Mnemiopsis; Class Nuda includes Beroë. they sink to deeper levels or die out in shallow water This classification is based on structural differences during the winter. which are linked with the feeding mechanisms so that Bolinopsis can reach 400 per m3 in summer off Mur­ the taxonomic classification is thus also an ecological mansk (Kamshilov, 1960 b); although there do not one. appear to be any similar figures for Pleurobrachia many The Tentaculata spread their tentacles through a authors stress the abundance of this species in the considerable area, up to 20 cm or more in Pleurobrachia North Sea, Irish Sea and in other localitites. Beroë, (Kühl, 1932), feeding largely on what is available, but being a much larger species, does not reach such high especially copepods, young euphausids, decapod figures (Kamshilov, 1960b) but nevertheless can be larvae, chaetognaths, fish eggs, and young fish - see abundant (Kamshilov 1960 a; Manteufel, 1941; Lebour (1922, 1923), M ayer (1912), Bigelow (1910, Bigelow, 1924). 1924), Mortensen (1912), Nelson (1925), Main (1928), The dry weight of ctenophores is small compared to Russell (1935), Kamshilov (1958). wet weight and their food value is correspondingly The Nuda, represented by Beroë, feed by engulfing small, but as they occur in such swarms they are eaten their food through the large mouth by a sudden suc­ by fish, sometimes perhaps because there is little else tion and the individual organisms preyed on are much available at the time. Hansen (1949) observed that larger than in the Tentaculata. Although they will take cod west of Greenland often feed on Beroë, Bolinopsis, Calams and other copepods (Lebour, 1923), Beroë Mertensia, and Pleurobrachia even to gorging. Russian feeds mainly on other ctenophores, especially the workers have confirmed the liking of cod and also Tentaculata - Mayer (1912), Bigelow (1924), Nelson haddock for Beroë in particular (Kamshilov, 1959, (1925), Kamshilov (1960 a) - but will also take other 1960 b) but Kieselev (1960) states that haddock may specimens of Beroë (Steuer, 1910). Kamshilov (1960 b) not be as partial to it as cod. Ctenophores are part of is of the opinion that Beroë cannot digest crustacea or the normal diet of Molva molva, and Acanthias vulgaris fish taken accidentally, and that such organisms found and Cyclopterus lumpus also sometimes feed on them. in Beroë are usually the undigested remnants of the Pleurobrachia was the dominant food of mackerel for food of other ctenophores. about three weeks in the Irish Sea in 1913 (Scott, Pleurobrachia is a neritic form, very common on both 1924). Medusae also feed on ctenophores (Lebour, 122

1923). There is some evidence that Pleurobrachia acts as and is consequently more widespread in the north­ a secondary host to a trematode parasite of mackerel east Atlantic. It frequently occurs in dense shoals off and other fish (Lebour, 1916; Mortensen, 1912) - the west of the British Isles, entering the Faroe-Shet- see also Van Cleave (1927). land Channel to affect the northern North Sea ac­ Because of the voracious feeding of tentaculate cording to the hydrographic conditions. Years of peak ctenophores in particular and their great abundance abundance were 1920, 1921, 1925, 1926, 1955, and at times they tend to deplete the plankton of other 1958. They also reach the southern part of the Nor­ species. This has been commented on by many wegian Sea, one of the peak years being 1954 (Rae, workers, for example, Bigelow (1915), Bigelow and 1956) and on one occasion - 1957 -shoals extended Leslie (1928), Russell (1931), Fraser (1961), to quote north to Iceland and continued west of Iceland to just a few, but we are indebted to recent Russian work reach as far as the North Cape (Fraser, 1959). They for a more precise evaluation of the position, see in generally reach these limits of their distribution by particular Kamshilov (1958, 1959, 1960 b), and Kam- about September. shilov, Zelikman and Roukhiyainen (1958). Ihlea asymmetrica is less tolerant to cold water and it Bolinopsis in the environs of Murmansk can reach sometimes occurs in numbers west of the British Isles, but 120 or even 400 individuals per m3. Experiments as it is a delicate species it soon disintegrates as the con­ showed that one individual, 2-5-3 cm, can digest a ditions become cooler and it rarely forms dense swarms. Calanus, St. V, in one hour and can swallow 10-11 Thalia democratica, probably the most abundant salp copepods in two hours, digesting half in a day and in the world, very occasionally reaches as far north as expelling the rest dead. A larval capelin can be the British Isles, or the ICES area, in sufficient num­ digested in seven hours. Feeding does not stop until bers to be called a swarm, and this has only been re­ the entire digestive cavity is filled with food. Russian corded once — in 1958 — since the close of the last calculations show that with Calanus at 300 per m 3 two century. No other species of salp can be considered as Bolinopsis are sufficient to eliminate the entire popul­ occurring in swarms in the ICES area. ation in a month. Kamshilov (1959) was able to show These swarms of salps, especially Salpa fusiformis, that in years of abundance of Bolinopsis and Pleuro­ m ay cover large areas - Fraser (1961) quotes 20,000 brachia, the numbers of Calanus and young euphausids square miles off the British Isles - and he says they were low, and in years when zooplankton, particularly filter out the phytoplankton to such an extent that Calanus, was rich the plankton feeding ctenophores there is little food left for other herbivorous species. were scarce. Such differences may be vital for herring Copepods in particular are markedly scarce when and other plankton-eating fish. Swarms of ctenophores salps are abundant, and this is especially so when the have been shown, too, to have serious effects on the salps have continued to thrive for several months as a survival of shellfish larvae and spat production in community in a moving water mass. It is less evident oysters (Nelson, 1925). under mixed conditions when salps rarely dominate Beroë, however, feeds on tentaculate ctenophores the plankton. and keeps their numbers down. A Beroë growing at When such denuded oceanic water masses invade the rate of 0-442 mm per day would require to eat one the continental shelf areas in the summer the effect Bolinopsis 10 mm long every 18-3 hours (Kamshilov, on the local communities may be serious. Herring are 1960 b); and in experimental conditions one Beroë scarce in such patches, possibly because of the lack 3-5 cm long swallowed and digested 31 Bolinopsis of food there or because of some distasteful product of (average 2 cm) in one month and increased in size to the salp’s metabolism (Fraser, 1961) - see also Koma­ 4-9 cm (Kamshilov, 1959). When cod approach the rovsky, 1959. The lack of phytoplankton and of herbi­ coast in numbers they feed on Beroë thus reducing the vorous zooplankton may affect in turn the carnivorous predation of Beroë on Bolinopsis and Pleurobrachia. These species which are then also in short supply. Such con­ then increase in number, resulting in a marked re­ ditions are likely to be poor for autumn spawned duction in the numbers of Calanus. In years when cod invertebrate larvae and this, together with a poor food stocks were poor Jieroë increased and so did the total supply of planktonic origin could affect the bottom biomass of zooplankton. fauna, and so too the demersal fish. Not many species of fish are reported to eat salps Salps though it may be that fish which take ctenophores will Salps, on the other hand, are herbivorous and feed also take salps. Information on this point is scarce, by filtering off the phytoplankton which is then passed which supports the impression that they do not form to the stomach by ciliary action. any valuable source of fish food, but cod were reported Salps are all oceanic, mostly warm water forms, but feeding on salps west of Orkney in September 1958, Salpa fusiformis is more cosmopolitan than the others a year of peak salp abundance (Fraser, 1960). 123

Swarms of salps, however, are not usually long-lived Kamshilov, M. M., 1960b. “Biology of Ctenophores off Mur- in the inshore areas and they die off with the onset man”. ICES, C.M. 1960, Doc. No. 157 (mimeo.). Kamshilov, M. M., Zelikman, E. A., & Roukhiyainen, M. I., of cooler conditions. 1958. “Plankton of Murman coastal waters”. In “Collected Ctenophores (except Beroë) and salps both occur in papers on regularities in concentration and migrations of food swarms and the general evidence suggests that both fishes” . Izd. Akad. Nauk S.S.S.R .: 59-102. may severely reduce the zooplankton standing crop Kieselev, O. N., 1960. “ Observations on behaviour of fishes in the Barents Sea with the aid of submarine apparatus”. Sov. with its consequent effect on the food cycle. The Fish. Invest. N. Europ. Seas, Moscow, pp. 457-61. effects of both can, however, be regarded as relatively Komarovsky, B., 1959. “ A study of the food of Sardinella aurita V. shortlived, even though they are not as transient as off the Mediterranean coast of Israel during a peak season phytoplankton blooms, and the products of their (May-June 1958)”. Proc. Tech. Pap., 5 (42), F.A.O., 1959. Kühl, W., 1932. “Rippenquallen beim Beutefang”. Natur u. disintegration may be expected to enrich the local Mus., 62: 130-33. waters, helping to produce better conditions for phyto­ Lebour, M. V., 1916. “Medusae as hosts for larval trematodes”. plankton growth the following spring. We need, how­ J. mar. biol. Ass. U.K., 11: 57-59. ever, more precise determinations of their effects, Lebour, M. V., 1922. “The food of plankton organisms”. J. mar. biol. Ass. U.K., 12: 644-77. particularly those of the salps, so that we may evaluate Lebour, M. V., 1923. “The food of plankton organisms, II”. them better as competitors with the fish for the zoo­ J. mar. biol. Ass. U.K., 13: 70-92. plankton crop, and we need more positive evidence Main, R.J., 1928. “Observations on the feeding mechanism of a cte­ of the effects of their disintegration on the regeneration nophore, Mnemiopsis leidyi”. Biol. Bull. Woods Hole, 5 5 (2) : 69-78. Manteufel, B. P., 1941. “Plankton and herring in the Barents of nutrients. Sea” . Trudy PIN RO , 7: 125-218. R eferences Mayer, A. G., 1912. “Ctenophores of the Atlantic coast of North Bigelow, H. B., 1910. “ Coelenterates from Labrador” . Proc. U.S. America”. Publ. Carneg. Instn., 162: 1-58. nat. Mus., 37: 301-20. Mortensen, T. L., 1912. “Ctenophora”. Dan. Ingolf-Exped., 5(2): Bigelow, H. B., 1924. “Plankton of the offshore waters of the 1-95. Gulf of Maine”. Bull. U.S. Bur. Fish., 40 (2): 1-509. Nelson, T. C., 1925. “ On the occurrence and food habits of Bigelow, H. B., & Leslie, M., 1928. “ Plankton in Monterey Bay” . ctenophores in New Jersey inland coastal waters” . Biol. Bull. Bull. Mus. Comp. Zool. Harv., 70 (5) : 429-581. Woods Hole, 48 (2) : 92-111. Fraser, J. H., 1959. “Plankton investigations from Aberdeen in Rae, K .M ., 1956. “The continuous plankton recorder survey: 1957”. Ann. biol., Copenhague, 14: 29-30. Plankton around the British Isles during 1954” . Ann. biol., Fraser, J. H., 1960. “Plankton investigations from Aberdeen in Copenhague, 11: 54-58. 1958”. Ann. biol., Copenhague, 15: 57-58. Russell, F. S., 1931. “The study of copepods as a factor in oceanic Fraser, J. H., 1961. “The oceanic and bathypelagic plankton of economy” . 5 th Pacif. Sei. Congr., p. 2023. the north-east Atlantic and its possible significance to fisheries” . Russell, F. S., 1935. “ Seasonal abundance and distribution of the Mar. Res. Scot. 1961, No. 4: 1-48. young of teleostean fishes caught in the ring trawl in offshore Hansen, P. M., 1949. “Studies on cod”. Rapp. Cons. Explor. water in the Plymouth area. Pt. II.” J. mar. biol. Ass. U.K., Mer, 123: 1-77. 20 (2 ): 147-79. Kamshilov, M. M., 1959. “Interrelations between organisms and Scott, A., 1924. “ Food of the Irish Sea herring in 1923” . Proc. the part they play in evolution”. Zh. Obshch. Biol., 20 (5) : Lpool biol. Soc., 38: 115-19. 370-78. (In Russian). Steuer, A., 1910. “ Planktonkunde” . Leipzig, 723 pp. Kamshilov, M. M., 1960a. “Feeding of Ctenophore, Beroë cucumis van Cleave, H. J., 1927. “Ctenophores as the host of a cestode”. (Fabr.)”. Dokl. Akad. Nauk, 130 (5): 1138-40. Trans. Amer. Micr. Soc., 46: 214-15.

D iscussion In presenting his paper Dr. Fraser said that at the pre­ populations of Beroë in North American inshore waters vious week’s Herring Symposium there had been discus­ when there were no tentaculate ctenophores for them sion on the loss of broods in the early stages : in the nor­ to feed on. thern North Sea a very poor brood year could be produced Several speakers referred to observations of fish and by each Pleurobrachia eating only one more herring larva. birds feeding on salps, viz. : - flying fish feeding on During the discussion examples of ctenophore and Thalia democratica (Mr. Wickstead), espada off Madeira salp swarms were described from various parts of the feeding on Pyrosoma (Mr. Currie) and Antarctic birds world, viz. : salps of west Algeria in 1958 (Dr. Bernard) feeding on solitary forms of salps (Mr. Currie). Dr. and between the Faroes and south-west Iceland in the Curl thought that salps and ctenophores are only summer of 1957 (Mr. Vagn Hansen) and Pleuro­ eaten by fish as a last resort since they supply little brachia in the North Sea (Dr. Kramp), in English nutrient: the test is made of mucopolysaccharids and estuaries from May to July (Professor Raymont) and is indigestible. He said that ctenophores respire at the in Galway Bay (Dr. Ö Ceidigh). In all these swarms same rate as copepods but eliminate 90 °/0 of the other zooplankton was sparse. assimilated nitrogen, mainly as ammonia. Dr. Yentsch Dr. Kramp said that Pleurobrachia in the North Sea commented that by their excretion ctenophores and feed on cod larvae, and Dr. Curl mentioned large salps keep nutrients in the photic zone.