Food preference of the sea urchins Echinus acutus and E. esculentus
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1 Mar. Behav. Physiol. 1982, Vol. 8, lx/82/ $06.50/0 c> 1982 Gordon and Breach Science Publishers, Inc. Printed in Great Britain Food preference of the sea urchins Echinus acutus and E. esculentus E. BONSDORFFT and 0. VAHL Institute of Marine Biology, University of Bergen, N-5065 Blornsterdalen, Norway (Received June ) The reactions of the sea urchins Echinus acutus and E. esculentus to Laminaria digitata and L. saccharina with or without the encrusting bryozoan Membranipora membranacea were tested in feeding- and Y-maze experiments. The experiments clearly showed that the two sea urchin species have almost identical responses to the food items offered, and that they prefer to eat L. saccharina encrusted with Membranipora. In their search for food, however, the sea urchins show the strongest attraction to the unencrusted alga. The ecological implications of these seemingly contradictory preferences are discussed. INTRODUCTION Sea urchins are often considered the determining factor with regard to abundance and distribution of marine plants in shallow marine water (Lawrence, 1975). In Western Norway, the two Echinus-species E. acutus Lamarck and E. esculentus L. occur together, often in the same habitat (Dons, 1935). The two species are taxonomically very close and are known to hybridize easily (Hagstrom and Lernning, 1961; Mortensen, 1927). The hybrids are possibly fertile, but there is little doubt that E. acutus and E. esculentus are distinct species (Hagstrom and Lernning, op. cit.). Kain and Jones (1966) showed that E. esculentus was the controlling factor of the lower limit of Laminaria hyperborea. It is not known whether E. acutus has a similar effect on the kelps. There is, however, some uncertainty whether these sea urchins feed mainly on animals or plants, although Laminaria and encrusting animals seem to compose a major food source (Lawrence, 1975; Table I). We therefore decided to test whether E. acutus and E. esculentus showed any discrimination between some possible food types, and whether there is difference between these sea urchin species in this respect. t Present address: Institute of Biology, Abo Akademi, SF Abo, Finland.
2 E. BONSDORFF AND 0. VAHL TABLE I Results from the Y-maze tested with chi-square test. The tested combinations (1-lo), the choice made, and the level of significance (P <) for the choices are given. Laminaria saccharina = L.s., Membranipora-encrusted L. saccharina = LAM., L. digitata = L.d., Membranipora-encrusted L. digitata = L.d.M., H,O = sea water, n.s. = not significant. Alternative given E. esculentus choice made P < E. acutus choice made P < MATERIAL AND METHODS The specimens tested were collected in the vicinity of the Institute of Marine Biology, University of Bergen, Western Norway (60 16'N, 5O13'E) in March 1981 at a surface temperature of 0.5-lS C. Echinus esculentus could easily be reached from the surface, whereas E. acutus was collected by diving at 5-10m depth. The specimens were kept in large tanks with running sea water at 5.s 5.9"C until the experiments were carried out. Only adult animals were used in the experiments. The test height and diameter of E. esculentus were and mm respectively, and those of E. acutus and mm. Twenty-five specimens of each species were used in the experiments, which were carried out at "C. Two different food preference tests were performed. In the first set of experiments, five specimens of each species were kept individually in aquaria, and offered equal amounts of unencrusted Laminaria saccharina Lamour, L. saccharina encrusted with Membranipora membranacea (L.), unencrusted Laminaria digitata (Huds.) Lamour, and L. diyitata encrusted with M. membranacea. The wet weight of the food items was measured before the experiment, and the amount of food eaten by the sea urchins was calculated as the difference in weight of the food at the start of the experiment, and after 24 hours. Using a one way analysis of variance (Parker, 1976) the order of preference was established from the amounts consumed of the different items.
3 FOOD PREFERENCE OF THE SEA URCHINS 245 The significance of the choice was further tested by calculating the least significant difference (LSD) at the 95% probability level (Parker, 1976). In the second series of experiments a large Y-maze was used. The total length of the maze was 180 cm, the arms of the Y were 80 cm long and 25 wide, and the stem was 100 cm long and 50cm wide. The water level was kept at 11 cm. The food items offered were kept in enclosed sections of 250cm2, - separated from the arms of the Y-maze by a grid with mesh size l.omm. During the experiments sea water kept running through the compartments, creating a flow in the Y-maze of approximately 5 cm sec l. To avoid reactions due to other causes than food type, the contents of the food-compartments were interchanged between each run. The sea urchins were allowed to chose between 10 combinations (Table I) of Laminaria saccharina and L. digitata with or without encrusting Membranipora membranacea and pure sea water. In the Y-maze the order of preference was thus tested in a situation where the specimens had to chose between pairs of all the food items offered in the feeding experiments, including those not eaten. For each species a total of 250 separate tests were carried out in the Y-maze, using five individuals at a time. The specimens were placed in the middle of the stem to allow a choice of (a) moving into one of the arms of the maze (i.e. upstream and towards a possible food item), or (b) moving downstream, and thus chosing none of the arms of the Y-maze. No specimen remained in the starting position. Each run lasted from three to five hours. The choice was considered completed when an individual was either at least half-way up one of the arms of the Y-maze, or had reached the downstream end of the maze. The results were tested with the chi-square test for goodness-of-fit (Parker, 1976). The three different choices possible were thus given an equal expected frequency. In the present study, no evident hybrids (Hagstrom and Larnning, 1966; Mortensen, 1927) were used, although a few were noted in the field. RESULTS Feeding experiments It appeared that Echinus esculentus showed a highly significant (P < 0.01) food preference. At the 5% significance level the LSD test showed that Laminaria saccharina encrusted with Membranipora membranacea was preferred to encrusted L. digitata, which in turn was preferred to unencrusted L. digitata and unencrusted L. saccharina. No significant preference could be demonstrated between clean L. saccharina and clean L. digitata. Echinus acutus also showed a highly significant (P < 0.001) food preference.
4 246 E. BONSDORFF AND O. VAHL The LSD test showed that encrusted L. saccharina was preferred to any other available food item, but among the other three possibilities no order of preference could be demonstrated at the 5% significance level. Accordingly, it seems clear that both sea urchin species studied prefer eating encrusted algae to unencrusted, and encrusted L. saccharina to encrusted L. digitata. The only difference in this respect is that E. esculentus has a marked order of preference (encrusted L. saccharina > encrusted L. digitata > clean L. saccharina and clean L. digitata), whereas E. acutus only shows a preference for encrusted L. saccharina over the other alternatives offered in the present experiments. Y-maze experiments With reference to Table I it is clearly seen that both E. esculentus and E. acutus show the strongest attraction to unencrusted L. saccharina (combinations 1 and 7 in Table I). This response may, however, be modified by the presence of M. membranacea (combinations 4 and 8). Thus it is not only the "smell" of the alga that determines the choice. DISCUSSION McClintock et al. (1981) found that the echinoids Echinometra lucunter, Lytechinus variegatus, and Eucidaris tribuloides preferred animal food to plants. It was suggested by Miller and Mann (1973) that Laminaria had too low protein content to support growth in the sea urchin Strongylocentros droebachiensis unless the animal had special adaptation. Propp (1977) showed that it excreted excess carbon, and Fong and Mann (1980) showed that it had symbiontic bacteria in the gut which enabled the sea urchin to utilize cellulose and supplied it with essential amino acids. An amino acid supplement in the diet is probably also the reason for enhanced growth in Psammechinus miliaris when fed Membranipora-encrusted L. saccharina (Jensen, 1969). No details of excretion and gut flora are available for E. acutus and E. esculentus. The preference for eating encrusted Laminaria may, however, add essential nutrients to their diet, by supplementing the Laminaria-food with animal tissue. The modification by Membranipora of the sea urchins' preference (Table I, combinations 4 and 8) may thus be of significance for the urchins in obtaining a diet of the right composition. Nevertheless, the sea urchins primarily follow the stimuli emitted by the algae. Since the algae is the habitat of the bryozooan, the urchins, by following the stimuli from the algae instead of those from the animal, will under all circumstances find acceptable food, and possibly also encrusted plants. Accordingly, the combination of the
5 FOOD PREFERENCE OF THE SEA URCHINS 247 feeding- and Y-maze experiments clearly shows that relying on one type of experiment to establish echinoid food-preference may give rise to misleading conclusions. The preference of the two Echinus-species for the food types offered is almost identical, as may perhaps be expected in species as closely related as E. acutus and E. esculentus. The similarity of the preferences found here suggests, however, that no interspecific competition for Laminaria and/or Membranipora has been involved in the evolution of these sea urchin species. Accordingly, these resources are probably not limiting to E. acutus and E. esculentus. This means that either the sea urchins always have enough Laminaria/Membranipora available, or if this resource is overgrazed, they have alternative food in sufficient abundance. A control of competition between algae by grazing of sea urchins has been demonstrated (for references ; see Duggins, 1981 ; Sousa et al., 1981). Laminaria saccharina and L. digitata often occur together (Kain, 1979), and L. saccharina is the most opportunistic of the two species (see Kain, 1975, 1976; Liining, 1979). Since E. acutus and E. esculentus clearly show a preference for L. saccharina, they may regulate the competition between these algae by reducing the density of L. saccharina thereby enabling L. digitata to extend its range towards deeper water. It would be of interest to test this hypothesis by field experiments. Acknowledgements We wish to thank Professor J. M. Lawrence for commenting on the manuscript. This work was in part supported by a grant to E.B. from The Nordic Council for Marine Biology. References Dons, C. (1935). Norges strandfuna X. Echinider. K. norske Vidensk. Selsk. Forth. 20, Duggins, D. 0. (1981). Interspecific facilitation in a guild of benthic marine herbivores. Oecologia (Berl) 48, Fong, W. and Mann, K. H. (1980). Role of the gut flora in the transfer of amino acids through a marine food chain. Can. J. Fish. Aquat. Sci. 37, Hagstrom, B. E. and Lonning, S. (1961). Morphological and experimental studies on the genus Ecinus. Sarsia 4, 21-31, Jensen, M. (1969). Breeding and growth of Psammechinus miliaris (Gmelin). Ophelia 7, Kain, J. M. (Mrs N. S. Jones) (1975). Algal recolonization of some cleared subtidal areas. J. Ecol. 63, Kain, J. M. (1976). The biology of Laminaria hyperborea. VIII. Growth on cleared areas. J. mar. biol. Ass. U.K. 56, Kain, J. M. (1979). A view of the genus Laminaria. Oceanogr. Mar. Biol. Ann. Rev. 17, Kain, J. M. and Jones, N. S. (1966). Algal colonization after removal of Echinus. In Proceedings of thefifth internation sea-weed symposium, Halifax, Canada (E. G. Young and J. L. McLachlan, eds). Pergamon Press, Oxford, pp Lawrence, J. M. (1975). On the relationships between marine plants and sea urchins. Oceanogr. Mar. Biol. Ann. Rev. 13,
6 248 E. BONSDORFF AND O. VAHL Liining, K. (1979). Growth strategies of three Laminaria species (Phaeophycea) inhabiting different depth zones in thesublittoral region ofhelgoland (North Sea). Mar. Ecol. Progr. Ser. 1, McClintock, J. B., Klinger, T. S. and Lawrence, J. M. (1981). Feeding preferences of echinoids for plant and animal foods. Bull. Mar. Sci. (in press). Miller, R. J. and Mann, K. H. (1973). Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of Canada Energy transformations by sea urchins. Mar. Biol. 18, Mortensen, T. (1927). Echinoderms of the British Isles. Oxford University Press. Edinburgh. 471 pp. Parker, R. E. (1976). Introductory statistics for biology. Studies in Biology no. 43 Camelot Press. Southampton. 122 pp. Propp, M. V. (1977). Ecology of the sea urchin Stronqylocentrotus droebachiensis in the Barents Sea: Metabolism and abundance regulation. Biol. Morya (Vladivostok) 1, (In Russian.) Sousa, W. P., Schweter, S. C. and Gaines, S. D. (1981). Latitudinal variation in intertidal algal community structure : the influence of grazing and vegetation propagation. Oecologia (Berl) 48,
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