Browse > Article
http://dx.doi.org/10.4490/algae.2021.36.3.5

Feeding behaviors of a sea urchin, Mesocentrotus nudus, on six common seaweeds from the east coast of Korea  

Yang, Kwon Mo (Department of Biological Sciences, Sungkyunkwan University)
Jeon, Byung Hee (Ecological Restoration Division, Korea Fisheries Resources Agency)
Kim, Hyung Geun (Department of Marine Bioscience, Gangneung-Wonju National University)
Kim, Jeong Ha (Department of Biological Sciences, Sungkyunkwan University)
Publication Information
ALGAE / v.36, no.1, 2021 , pp. 51-60 More about this Journal
Abstract
The sea urchin, Mesocentrotus nudus, is widely distributed in North West Pacific regions. It has a substantial impact on macroalgal communities as a generalist herbivore. This study examined various aspects of its feeding ecology, including algal preference, foraging behaviors, and possible effects of past feeding history on its algal preference. We used six common algal species (Ulva australis, Undaria pinnatifida, Sargassum confusum, Dictyopteris divaricata, Grateloupia elliptica, and Grateloupia angusta) from the east coast of Korea as food choice in a series of indoor aquarium experiments. The first choice of starved M. nudus was exclusively U. pinnatifida, followed by G. elliptica and S. confusum. Unlike large urchins, small urchins equally preferred U. pinnatifida and G. elliptica. On the other hand, Undaria-fed urchins preferred to feed only G. elliptica, although its preference slightly differed over time. We then grouped sea urchins into three categories (starved, Undaria-fed, mixed species-fed) to observe 12-days feeding preference as well as early foraging movements. Foraging behaviors of the three groups were distinctively different, although they could not completely reflect the actual consumption. For example, U. australis was highly attractive, but rarely eaten. Undaria-fed urchins seemed to stay with only S. confusum and U. australis. This study demonstrates that M. nudus shows high flexibility in food preference depending on past feeding history and body size. Its foraging behaviors are also affected by past feeding conditions, exhibiting active chemoreceptive movements.
Keywords
feeding preference; foraging behavior; Mesocentrotus nudus; past feeding history; sea urchin; Undaria pinnatifida;
Citations & Related Records
Times Cited By KSCI : 3  (Citation Analysis)
연도 인용수 순위
1 Lemire, M. & Himmelman, J. H. 1996. Relation of food preference to fitness for the green sea urchin, Strongylocentrotus droebachiensis. Mar. Biol. 127:73-78.   DOI
2 Lyons, D. A. & Scheibling, R. E. 2007. Effect of dietary history and algal traits on feeding rate and food preference in the green sea urchin Strongylocentrotus droebachiensis. J. Exp. Mar. Biol. Ecol. 349:194-204.   DOI
3 Machiguchi, Y., Mizutori, S. & Sanbonsuga, Y. 1994. Food preference of sea urchin Strogylocentrotus nudus in laboratory. Bull. Hokkaido Natl. Fish. Res. Inst. 58:35-43.
4 Mann, K. H., Wright, J. L. C., Welsford, B. E. & Hatfield, E. 1984. Responses of the sea urchin Strongylocentrotus droebachiensis (O.F. Müller) to water-borne stimuli from potential predators and potential food algae. J. Exp. Mar. Biol. Ecol. 79:233-244.   DOI
5 Molis, M., Korner, J., Ko, Y. W. & Kim, J. H. 2008. Specificity of inducible seaweed anti-herbivory defences depends on identity of macroalgae and herbivores. Mar. Ecol. Prog. Ser. 354:97-105.   DOI
6 Molis, M., Korner, J., Ko, Y. W., Kim, J. H. & Wahl, M. 2006. Inducible responses in the brown seaweed Ecklonia cava: the role of grazer identity and season. J. Ecol. 94:243-249.   DOI
7 Paine, R. T. & Vadas, R. L. 1969. The effects of grazing by sea urchins Strongylocentrotus spp., on benthic algal populations. Limnol. Oceanogr. 14:710-719.   DOI
8 Palacin, C., Giribet, G., Carner, S., Dantart, L. & Turon, X. 1998. Low densities of sea urchins influence the structure of algal assemblages in the western Mediterranean. J. Sea Res. 39:281-290.   DOI
9 Pearse, J. S. 2006. Ecological role of purple sea urchins. Science 314:940-941.   DOI
10 Pennings, S. C., Nadeau, M. T. & Paul, V. J. 1993. Selectivity and growth of the generalist herbivore Dolabella auricularia feeding upon complementary resources. Ecology 74:879-890.   DOI
11 Pulliam, H. R. 1975. Diet optimization with nutrient constraints. Am. Nat. 109:765-768.   DOI
12 Rapport, D. J. 1980. Optimal foraging for complementary resources. Am. Nat. 116:324-346.   DOI
13 Rohde, S., Molis, M. & Wahl, M. 2004. Regulation of anti‐herbivore defence by Fucus vesiculosus in response to various cues. J. Ecol. 92:1011-1018.   DOI
14 Scheibling, R. & Anthony, S. 2001. Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides. Mar. Biol. 139:139-146.   DOI
15 Schnitzler, I., Pohnert, G., Hay, M. & Boland, W. 2001. Chemical defense of brown algae (Dictyopteris spp.) against the herbivorous amphipod Ampithoe longimana. Oecologia 126:515-521.   DOI
16 Seymour, S., Paul, N. A., Dworjanyn, S. A. & de Nys, R. 2013. Feeding preference and performance in the tropical sea urchin Tripneustes gratilla. Aquaculture 400-401:6-13.   DOI
17 Shin, J. D., Ahn, J. K., Kim, Y. H., Lee, S. B., Kim, J. H. & Chung, I. K. 2008. Community structure of benthic marine algae at Daejin and Jukbyeon on the mid-east coast of Korea. Algae 23:231-240.   DOI
18 Shiraishi, K., Taniguchi, K., Kurata, K. & Suzuki, M. 1991. Effects of the methanol extracts from the brown alga Dictyopteris divaricata on feeding by the sea urchin Strongylocentrotus nudus and the abalone Haliotis discus hannai. Nippon Suisan Gakkaishi 57:1945-1948.   DOI
19 Steneck, R. S. 2013. Sea urchins as drivers of shallow benthic marine community structure. In Lawrence, J. M. (Ed.) Sea Urchins: Biology and Ecology, 3rd ed. Academic Press Inc., London, pp. 195-212.
20 Sohn, C. H., Choi, C. G. & Kim, H. G. 2007. Algal communities and useful seaweed distribution at Gangnung and it's vicinity in east coast of Korea. Algae 22:45-52.   DOI
21 Teixeira, V. L., Barbosa, J. P., Rocha, F. D., Kaplan, M. A. C., Houghton, P. J. & Pereira, R. C. 2006. Hydroperoxysterols from the Brazilian brown seaweeds Dictyopteris justii and Spatoglossum schroederi (Dictyotales): a defensive strategy against herbivory. Nat. Prod. Commun. 1:293-297.
22 Terasaki, M., Hirose, A., Narayan, B., Baba, Y., Kawagoe, C., Yasui, H., Saga, N., Hosokawa, M. & Miyashita, K. 2009. Evaluation of recoverable finctional lipid components of several brown seaweeds (Phaeophyta) from Japan with special reference to fucoxanthin and fucosterol contents. J. Phycol. 45:974-980.   DOI
23 Vadas, R. L. 1977. Preferential feeding: an optimization strategy in sea urchins. Ecol. Monogr. 47:337-371.   DOI
24 Westbrook, C. E., Ringang, R. R., Cantero, S. M. A. & Toonen, R. J. 2015. Survivorship and feeding preferences among size classes of outplanted sea urchins,Tripneustes gratilla, and possible use as biocontrol for invasive alien algae. PeerJ 3:e1235.   DOI
25 Worm, B., Lotze, H. K., Hillebrand, H. & Sommer, U. 2002. Consumer versus resource control of species diversity and ecosystem functioning. Nature 417:848-851.   DOI
26 Yurchenko, O. V. & Reunov, A. A. 2004. Dimorphism of spermatozoa in the sea urchin Strongylocentrotus nudus. Russ. J. Mar. Biol. 30:354-357.   DOI
27 Boolootian, R. A. & Lasker, R. 1964. Digestion of brown algae and the distribution of nutrients in the purple sea urchin Strongylocentrotus purpuratus. Comp. Biochem. Physiol. 11:273-289.   DOI
28 Zubia, M., Payri, C. & Deslandes, E. 2008. Alginate, mannitol, phenolic compounds and biological activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria ornata (Phaeophyta: Fucales), from Tahiti (French Polynesia). J. Appl. Phycol. 20:1033-1043.   DOI
29 Agatsuma, Y. 2001. Ecology of Strongylocentrotus nudus. Dev. Aquac. Fish. Sci. 32:347-362.   DOI
30 Agnetta, D., Bonaviri, C., Badalamenti, F., Scianna, C., Vizzini, S. & Gianguzza, P. 2013. Functional traits of two co-occurring sea urchins across a barren/forest patch system. J. Sea Res. 76:170-177.   DOI
31 Borines, M. G., de Leon, R. L. & Cuello, J. L. 2013. Bioethanol production from the macroalgae Sargassum spp. Bioresour. Technol. 138:22-29.   DOI
32 Cruz-Rivera, E. & Hay, M. E. 2001. Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Mar. Ecol. Prog. Ser. 218:249-266.   DOI
33 Burkepile, D. E. & Hay, M. E. 2006. Herbivore vs. nutrient control of marine primary producers: context‐dependent effects. Ecology 87:3128-3139.   DOI
34 Chang, Y., Wang, Z. & Wang, G. 1999. Effect of temperature and algae on feeding and growth in sea urchin Strongylocentrotus intermedius. J. Fish. China 23:69-76.
35 Cho, Y., Kim, H. & Kim, S. -K. 2013. Bioethanol production from brown seaweed, Undaria pinnatifida, using NaCl acclimated yeast. Bioprocess Biosyst. Eng. 36:713-719.   DOI
36 Dayton, P. K., Tegner, M. J., Parnell, P. E. & Edwards, P. B. 1992. Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecol. Monogr. 62:421-445.   DOI
37 Dumont, C. P., Himmelman, J. H. & Robinson, S. M. C. 2007. Random movement pattern of the sea urchin Strongylocentrotus droebachiensis. J. Exp. Mar. Biol. Ecol. 340:80-89.   DOI
38 Elner, R. W. & Vadas, R. L. Sr. 1990. Inference in ecology: the sea urchin phenomenon in the northwestern Atlantic. Am. Nat. 136:108-125.   DOI
39 Filbee-Dexter, K. & Scheibling, R. E. 2014. Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar. Ecol. Prog. Ser. 495:1-25.   DOI
40 Eppley, R. W. & Lasker, R. 1959. Alginase in the sea urchin Strongylocentrotus purpuratus. Science 129:214-215.   DOI
41 Garnick, E. 1978. Behavioral ecology of Strongylocentrotus droebachiensis (Muller) (Echinodermata: Echinoidea): aggregating behavior and chemotaxis. Oecologia 37:77-84.   DOI
42 Filbee‐Dexter, K. & Scheibling, R. E. 2017. The present is the key to the past: linking regime shifts in kelp beds to the distribution of deep‐living sea urchins. Ecology 98:253-264.   DOI
43 Freeland, W. J. & Janzen, D. H. 1974. Strategies in herbivory by mammals: the role of plant secondary compounds. Am. Nat. 108:269-289.   DOI
44 Fung, A., Hamid, N. & Lu, J. 2013. Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem. 136:1055-1062.   DOI
45 Harrold, C. & Reed, D. C. 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160-1169.   DOI
46 Hay, M. E., Duffy, J. E., Fenical, W. & Gustafson, K. 1988. Chemical defense in the seaweed Dictyopteris delicatula: differential effects against reef fishes and amphipods. Mar. Ecol. Prog. Ser. 48:185-192.   DOI
47 Hayakawa, Y. & Kittaka, J. 1984. Simulation of feedig behavior of sea urchin Strongylocentrotus nudus. Bull. Jpn. Soc. Sci. Fish. 50:233-240.   DOI
48 Hernandez, M., Bückle, F., Guisado, C., Baron, B. & Estavillo, N. 2004. Critical thermal maximum and osmotic pressure of the red sea urchin Strongylocentrotus franciscanus acclimated at different temperatures. J. Therm. Biol. 29:231-236.   DOI
49 Hillebrand, H. & Cardinale, B. J. 2004. Consumer effects decline with prey diversity. Ecol. Lett. 7:192-201.   DOI
50 Himmelman, J. H. & Nedelec, H. 1990. Urchin foraging and algal survival strategies in intensely grazed communities in eastern Canada. Can. J. Fish. Aquat. Sci. 47:1011-1026.   DOI
51 Huntly, N. 1991. Herbivores and the dynamics of communities and ecosystems. Annu. Rev. Ecol. Syst. 22:477-503.   DOI
52 James, P. & Siikavuopio, S. I. 2012. The effect of continuous and intermittent feeding regimes on survival and somatic and gonadal growths of the sea urchin, Strongylocentrotus droebachiensis. Aquaculture 364-365:173-179.   DOI
53 Jormalainen, V., Honkanen, T. & Vesakoski, O. 2008. Geographical divergence in host use ability of a marine herbivore in alga-grazer interaction. Evol. Ecol. 22:545-559.   DOI
54 Kawakami, T., Tsushima, M., Katabami, Y., Mine, M., Ishida, A. & Matsuno, T. 1998. Effect of β,β-carotene, β-echinenone, astaxanthin, fucoxanthin, vitamin A and vitamin E on the biological defense of the sea urchin Pseudocentrotus depressus. J. Exp. Mar. Biol. Ecol. 226:165-174.   DOI
55 Kawamata, S. 1997. Modelling the feeding rate of the sea urchin Strongylocentrotus nudus (A. Agassiz) on kelp. J. Exp. Mar. Biol. Ecol. 210:107-127.   DOI
56 Kelly, M. S. & Symonds, R. C. 2013. Carotenoids in sea urchins. In Lawrence, J. M. (Ed.) Sea Urchins: Biology and Ecology. 3rd ed. Academic Press Inc., London, pp. 171-178.
57 Kim, C., Kim, Y. S., Choi, H. G. & Nam, K. W. 2014. Variations of seaweed community structure and distribution of crustose coralline algae at Gallam, Samchuk, eastern coast of Korea. Korean J. Environ. Ecol. 28:10-23.   DOI
58 Krumhansl, K. A., Okamoto, D. K., Rassweiler, A., Novak, M., Bolton, J. J., Cavanaugh, K. C., Connell, S. D., Johnson, C. R., Konar, B., Ling, S. D., Micheli, F., Norderhaug, K. M., Perez-Matus, A., Sousa-Pinto, I., Reed, D. C., Salomon, A. K., Shears, N. T., Wernberg, T., Anderson, R. J., Barrett, N. S., Buschmann, A. H., Carr, M. H., Caselle, J. E., Derrien-Courtel, S., Edgar, G. J., Edwards, M., Estes, J. A., Goodwin, C., Kenner, M. C., Kushner, D. J., Moy, F. E., Nunn, J., Steneck, R. S., Vasquez, J., Watson, J., Witman, J. D. & Byrnes, J. E. K. 2016. Global patterns of kelp forest change over the past half-century. Proc. Natl. Acad. Sci. U. S. A. 113:13785-13790.   DOI
59 Kim, S. -K., Kim, Y. -D., Jeon, C. -Y., Gong, Y. -G., Kim, D. -S., Kim, J. -H., Kim, M. -L. & Han, H. -K. 2007. Algal consumption and preference of sea urchins, Strongylocentrotus nudus, S. intermedius and abalone, Haliotis discus hannai. J. Korean Fish. Soc. 40:133-140.
60 Kolb, N., Vallorani, L., Milanovic, N. & Stocchi, V. 2004. Evaluation of marine algae wakame (Undaria pinnatifida) and kombu (Laminaria digitata japonica) as food supplements. Food Technol. Biotechnol. 42:57-61.
61 Larson, B. R., Vadas, R. L. & Keser, M. 1980. Feeding and nutritional ecology of the sea urchin Strongylocentrotus drobachiensis in Maine, USA. Mar. Biol. 59:49-62.   DOI
62 Lauzon-Guay, J. -S. & Scheibling, R. E. 2008. Evaluation of passive integrated transponder (PIT) tags in studies of sea urchins: caution advised. Aquat. Biol. 2:105-112.   DOI
63 Lauzon-Guay, J. -S., Scheibling, R. E. & Barbeau, M. A. 2006. Movement patterns in the green sea urchin, Strongylocentrotus droebachiensis. J. Mar. Biol. Assoc. U. K. 86:167-174.   DOI