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No. 19.

The Role o f Ctenophores and Salps in Zooplankton Production andStanding Crop

By

J . H . F r a s e rM arine Laboratory, A berdeen

Swarms of zooplankton have effects on the plankton community as a whole, which m ay be more drastic than is generally realized. Two contrasting examples are given ; the carnivorous ctenophores and the herbivorous salps.

Ctenophores

Taxonomically these are divided into two classes: Class T entaculata and Class N uda. T he former in cludes the genera Pleurobrachia, Mertensia, Hormiphora, Bolinopsis, and Mnemiopsis; Class N uda includes Beroë. This classification is based on structural differences which are linked with the feeding mechanisms so tha t the taxonomic classification is thus also an ecological one.

The T entaculata spread their tentacles through a considerable area, up to 20 cm or more in Pleurobrachia (Kühl, 1932), feeding largely on w hat is available, bu t especially copepods, young euphausids, decapod larvae, chaetognaths, fish eggs, and young fish - see Lebour (1922, 1923), M ayer (1912), Bigelow (1910, 1924), M ortensen (1912), Nelson (1925), M ain (1928), Russell (1935), Kamshilov (1958).

T he N uda, represented by Beroë, feed by engulfing their food through the large m outh by a sudden suction and the individual organisms preyed on are much larger than in the Tentaculata. Although they will take Calams and other copepods (Lebour, 1923), Beroë feeds mainly on other ctenophores, especially the Tentaculata - M ayer (1912), Bigelow (1924), Nelson (1925), Kamshilov (1960 a) - bu t will also take other specimens o f Beroë (Steuer, 1910). Kamshilov (1960 b) is of the opinion tha t Beroë cannot digest crustacea or fish taken accidentally, and tha t such organisms found in Beroë are usually the undigested remnants of the food o f other ctenophores.

Pleurobrachia is a neritic form, very common on both

sides of the N orth Atlantic, bu t it is rarely taken in the open ocean. Mertensia is arctic in its distribution. Bolinopsis is arctic and boreal and is more widespread than Mertensia, it occurs round the British Isles, though less numerous there than in more northern latitudes. Beroë is usually regarded as oceanic bu t it spreads into coastal areas often in great numbers. I t is most abundan t in boreal regions bu t is nevertheless a widespread species. All of these can be very abundant, particularly during the summer and into autum n, but they sink to deeper levels or die out in shallow water during the winter.

Bolinopsis can reach 400 per m 3 in summer off M urmansk (Kamshilov, 1960 b ); although there do not appear to be any similar figures for Pleurobrachia m any authors stress the abundance of this species in the North Sea, Irish Sea and in other localitites. Beroë, being a m uch larger species, does not reach such high figures (Kamshilov, 1960b) b u t nevertheless can be abundant (Kamshilov 1960 a ; M anteufel, 1941; Bigelow, 1924).

T he dry weight of ctenophores is small com pared to wet weight and their food value is correspondingly small, bu t as they occur in such swarms they are eaten by fish, sometimes perhaps because there is little else available a t the time. Hansen (1949) observed that cod west of Greenland often feed on Beroë, Bolinopsis, Mertensia, and Pleurobrachia even to gorging. Russian workers have confirmed the liking of cod and also haddock for Beroë in particular (Kamshilov, 1959, 1960 b) bu t Kieselev (1960) states tha t haddock may not be as partia l to it as cod. Ctenophores are p a rt of the norm al diet of Molva molva, and Acanthias vulgaris and Cyclopterus lumpus also sometimes feed on them. Pleurobrachia was the dom inant food of mackerel for about three weeks in the Irish Sea in 1913 (Scott, 1924). M edusae also feed on ctenophores (Lebour,

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1923). There is some evidence tha t Pleurobrachia acts as a secondary host to a trem atode parasite of mackerel and other fish (Lebour, 1916; Mortensen, 1912) - see also Van Cleave (1927).

Because of the voracious feeding of tentaculate ctenophores in particular and their great abundance a t times they tend to deplete the plankton o f other species. This has been commented on by m any workers, for example, Bigelow (1915), Bigelow and Leslie (1928), Russell (1931), Fraser (1961), to quote just a few, bu t we are indebted to recent Russian work for a more precise evaluation of the position, see in particular Kamshilov (1958, 1959, 1960 b), and Kam- shilov, Zelikman and Roukhiyainen (1958).

Bolinopsis in the environs o f M urm ansk can reach 120 or even 400 individuals per m 3. Experiments showed tha t one individual, 2-5-3 cm, can digest a Calanus, St. V, in one hour and can swallow 10-11 copepods in two hours, digesting half in a day and expelling the rest dead. A larval capelin can be digested in seven hours. Feeding does not stop until the entire digestive cavity is filled with food. Russian calculations show tha t with Calanus a t 300 per m 3 two Bolinopsis are sufficient to eliminate the entire population in a month. Kamshilov (1959) was able to show that in years of abundance o f Bolinopsis and Pleurobrachia, the numbers of Calanus and young euphausids were low, and in years when zooplankton, particularly Calanus, was rich the plankton feeding ctenophores were scarce. Such differences may be vital for herring and other plankton-eating fish. Swarms of ctenophores have been shown, too, to have serious effects on the survival of shellfish larvae and spat production in oysters (Nelson, 1925).

Beroë, however, feeds on tentaculate ctenophores and keeps their numbers down. A Beroë growing at the rate o f 0-442 m m per day would require to eat one Bolinopsis 10 m m long every 18-3 hours (Kamshilov, 1960 b ) ; and in experimental conditions one Beroë3-5 cm long swallowed and digested 31 Bolinopsis (average 2 cm) in one m onth and increased in size to4-9 cm (Kamshilov, 1959). W hen cod approach the coast in numbers they feed on Beroë thus reducing the predation of Beroë on Bolinopsis and Pleurobrachia. These then increase in num ber, resulting in a m arked reduction in the numbers of Calanus. In years when cod stocks were poor Jieroë increased and so did the total biomass o f zooplankton.

Salps

Salps, on the other hand, are herbivorous and feed by filtering off the phytoplankton which is then passed to the stomach by ciliary action.

Salps are all oceanic, mostly w arm w ater forms, but Salpa fusiformis is more cosmopolitan than the others

and is consequently more widespread in the northeast Atlantic. I t frequently occurs in dense shoals off the west of the British Isles, entering the Faroe-Shet- land Channel to affect the northern N orth Sea according to the hydrographic conditions. Years of peak abundance were 1920, 1921, 1925, 1926, 1955, and 1958. They also reach the southern part o f the Norwegian Sea, one of the peak years being 1954 (Rae, 1956) and on one occasion - 1957 -sh o a ls extended north to Iceland and continued west of Iceland to reach as far as the N orth Cape (Fraser, 1959). They generally reach these limits of their distribution by about September.

Ihlea asymmetrica is less tolerant to cold water and it sometimes occurs in numbers west of the British Isles, but as it is a delicate species it soon disintegrates as the conditions become cooler and it rarely forms dense swarms.

Thalia democratica, probably the most abundan t salp in the world, very occasionally reaches as far north as the British Isles, or the ICES area, in sufficient num bers to be called a swarm, and this has only been recorded once — in 1958 — since the close of the last century. No other species of salp can be considered as occurring in swarms in the ICES area.

These swarms of salps, especially Salpa fusiformis, m ay cover large areas - Fraser (1961) quotes 20,000 square miles off the British Isles - and he says they filter out the phytoplankton to such an extent that there is little food left for other herbivorous species. Copepods in particular are markedly scarce when salps are abundant, and this is especially so when the salps have continued to thrive for several months as a community in a moving w ater mass. I t is less evident under mixed conditions when salps rarely dominate the plankton.

W hen such denuded oceanic water masses invade the continental shelf areas in the summer the effect on the local communities m ay be serious. H erring are scarce in such patches, possibly because of the lack of food there or because of some distasteful product of the salp’s metabolism (Fraser, 1961) - see also K om arovsky, 1959. T he lack of phytoplankton and of herbivorous zooplankton may affect in turn the carnivorous species which are then also in short supply. Such conditions are likely to be poor for au tum n spawned invertebrate larvae and this, together w ith a poor food supply of planktonic origin could affect the bottom fauna, and so too the demersal fish.

Not m any species of fish are reported to eat salps though it may be tha t fish which take ctenophores will also take salps. Information on this point is scarce, which supports the impression tha t they do not form any valuable source of fish food, bu t cod were reported feeding on salps west of Orkney in September 1958, a year of peak salp abundance (Fraser, 1960).

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Swarms of salps, however, are not usually long-lived in the inshore areas and they die off with the onset o f cooler conditions.

Ctenophores (except Beroë) and salps both occur in swarms and the general evidence suggests tha t both may severely reduce the zooplankton standing crop with its consequent effect on the food cycle. The effects of both can, however, be regarded as relatively shortlived, even though they are not as transient as phytoplankton blooms, and the products of their disintegration may be expected to enrich the local waters, helping to produce better conditions for phytoplankton growth the following spring. We need, however, more precise determinations of their effects, particularly those of the salps, so tha t we may evaluate them better as competitors with the fish for the zooplankton crop, and we need more positive evidence of the effects of their disintegration on the regeneration of nutrients.

R eferen ces

Bigelow, H . B., 1910. “ Coelenterates from Labrador” . Proc. U.S.nat. Mus., 37: 301-20.

Bigelow, H . B., 1924. “ Plankton of the offshore waters of the G ulf of M aine” . Bull. U.S. Bur. Fish., 40 (2): 1-509.

Bigelow, H . B., & Leslie, M ., 1928. “ Plankton in M onterey Bay” .Bull. Mus. Comp. Zool. H arv ., 70 (5) : 429-581.

Fraser, J . H ., 1959. “ Plankton investigations from Aberdeen in 1957” . Ann. biol., Copenhague, 14: 29-30.

Fraser, J . H ., 1960. “ Plankton investigations from Aberdeen in 1958” . Ann. biol., Copenhague, 15: 57-58.

Fraser, J . H ., 1961. “ The oceanic and bathypelagic plankton of the north-east Atlantic and its possible significance to fisheries” . M ar. Res. Scot. 1961, No. 4: 1-48.

Hansen, P. M ., 1949. “ Studies on cod” . R app. Cons. Explor.M er, 123: 1-77.

Kamshilov, M. M ., 1959. “ Interrelations between organisms and the p a rt they play in evolution” . Zh. Obshch. Biol., 20 (5) : 370-78. (In Russian).

Kamshilov, M. M., 1960a. “ Feeding of Ctenophore, Beroë cucumis (Fabr.)” . Dokl. Akad. Nauk, 130 (5): 1138-40.

Kamshilov, M. M ., 1960b. “ Biology of Ctenophores off Mur- m an” . ICES, C.M . 1960, Doc. No. 157 (mimeo.).

Kamshilov, M. M., Zelikman, E. A., & Roukhiyainen, M. I., 1958. “ Plankton of M urm an coastal waters” . In “ Collected papers on regularities in concentration and migrations of food fishes” . Izd. Akad. Nauk S.S.S.R .: 59-102.

Kieselev, O . N., 1960. “ Observations on behaviour of fishes in the Barents Sea with the aid of submarine apparatus” . Sov. Fish. Invest. N. Europ. Seas, Moscow, pp. 457-61.

Komarovsky, B., 1959. “ A study of the food of Sardinella aurita V. off the M editerranean coast of Israel during a peak season (M ay-June 1958)” . Proc. Tech. Pap., 5 (42), F.A.O., 1959.

Kühl, W ., 1932. “ Rippenquallen beim Beutefang” . N atur u. Mus., 62: 130-33.

Lebour, M. V., 1916. “ Medusae as hosts for larval trematodes” . J . m ar. biol. Ass. U .K ., 11: 57-59.

Lebour, M. V., 1922. “ T he food of plankton organisms” . J . mar. biol. Ass. U .K ., 12: 644-77.

Lebour, M. V., 1923. “ T he food of plankton organisms, I I ” . J . m ar. biol. Ass. U .K ., 13: 70-92.

M ain, R .J ., 1928. “ Observations on the feeding mechanism of a ctenophore, Mnemiopsis leidyi”. Biol. Bull. Woods Hole, 5 5 (2) : 69-78.

Manteufel, B. P., 1941. “ Plankton and herring in the Barents Sea” . T rudy PIN R O , 7: 125-218.

Mayer, A. G., 1912. “ Ctenophores of the Atlantic coast of North America” . Publ. Carneg. Instn., 162: 1-58.

Mortensen, T . L., 1912. “ C tenophora” . Dan. Ingolf-Exped., 5(2): 1-95.

Nelson, T . C., 1925. “ O n the occurrence and food habits of ctenophores in New Jersey inland coastal waters” . Biol. Bull. Woods Hole, 48 (2) : 92-111.

Rae, K .M ., 1956. “ T he continuous plankton recorder survey: Plankton around the British Isles during 1954” . Ann. biol., Copenhague, 11: 54-58.

Russell, F. S., 1931. “ The study of copepods as a factor in oceanic economy” . 5 th Pacif. Sei. Congr., p. 2023.

Russell, F. S., 1935. “ Seasonal abundance and distribution of the young of teleostean fishes caught in the ring trawl in offshore water in the Plymouth area. Pt. I I . ” J . m ar. biol. Ass. U .K ., 20(2): 147-79.

Scott, A., 1924. “ Food of the Irish Sea herring in 1923” . Proc. Lpool biol. Soc., 38: 115-19.

Steuer, A., 1910. “ Planktonkunde” . Leipzig, 723 pp.van Cleave, H . J . , 1927. “ Ctenophores as the host of a cestode” .

T rans. Amer. Micr. Soc., 46: 214-15.

D iscu ss io n

In presenting his paper Dr. Fraser said tha t a t the previous week’s H erring Symposium there had been discussion on the loss of broods in the early stages : in the northern North Sea a very poor brood year could be produced by each Pleurobrachia eating only one more herring larva.

During the discussion examples of ctenophore and salp swarms were described from various parts of the world, viz. : salps of west Algeria in 1958 (Dr. Bernard) and between the Faroes and south-west Iceland in the summer of 1957 (Mr. Vagn Hansen) and Pleurobrachia in the N orth Sea (Dr. K ram p), in English estuaries from M ay to Ju ly (Professor Raym ont) and in Galway Bay (Dr. Ö Ceidigh). In all these swarms other zooplankton was sparse.

Dr. K ram p said tha t Pleurobrachia in the N orth Sea feed on cod larvae, and Dr. Curl m entioned large

populations of Beroë in N orth American inshore waters when there were no tentaculate ctenophores for them to feed on.

Several speakers referred to observations of fish and birds feeding on salps, viz. : - flying fish feeding on Thalia democratica (Mr. Wickstead), espada off M adeira feeding on Pyrosoma (Mr. Currie) and Antarctic birds feeding on solitary forms of salps (Mr. Currie). Dr. Curl thought that salps and ctenophores are only eaten by fish as a last resort since they supply little nutrient: the test is m ade of mucopolysaccharids and is indigestible. He said that ctenophores respire a t the same rate as copepods bu t eliminate 90 °/0 of the assimilated nitrogen, mainly as ammonia. Dr. Yentsch commented tha t by their excretion ctenophores and salps keep nutrients in the photic zone.

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