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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)
  • Received : 2021.01.09
  • Accepted : 2021.03.05
  • Published : 2021.03.17

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

References

  1. Agatsuma, Y. 2001. Ecology of Strongylocentrotus nudus. Dev. Aquac. Fish. Sci. 32:347-362. https://doi.org/10.1016/S0167-9309(01)80021-1
  2. 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. https://doi.org/10.1016/j.seares.2012.08.009
  3. 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. https://doi.org/10.1016/0010-406X(64)90109-4
  4. Borines, M. G., de Leon, R. L. & Cuello, J. L. 2013. Bioethanol production from the macroalgae Sargassum spp. Bioresour. Technol. 138:22-29. https://doi.org/10.1016/j.biortech.2013.03.108
  5. Burkepile, D. E. & Hay, M. E. 2006. Herbivore vs. nutrient control of marine primary producers: context‐dependent effects. Ecology 87:3128-3139. https://doi.org/10.1890/0012-9658(2006)87[3128:hvncom]2.0.co;2
  6. 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.
  7. 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. https://doi.org/10.1007/s00449-013-0895-5
  8. 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. https://doi.org/10.3354/meps218249
  9. 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. https://doi.org/10.2307/2937118
  10. 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. https://doi.org/10.1016/j.jembe.2006.08.013
  11. Elner, R. W. & Vadas, R. L. Sr. 1990. Inference in ecology: the sea urchin phenomenon in the northwestern Atlantic. Am. Nat. 136:108-125. https://doi.org/10.1086/285084
  12. Eppley, R. W. & Lasker, R. 1959. Alginase in the sea urchin Strongylocentrotus purpuratus. Science 129:214-215. https://doi.org/10.1126/science.129.3343.214
  13. 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. https://doi.org/10.3354/meps10573
  14. 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. https://doi.org/10.1002/ecy.1638
  15. Freeland, W. J. & Janzen, D. H. 1974. Strategies in herbivory by mammals: the role of plant secondary compounds. Am. Nat. 108:269-289. https://doi.org/10.1086/282907
  16. Fung, A., Hamid, N. & Lu, J. 2013. Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem. 136:1055-1062. https://doi.org/10.1016/j.foodchem.2012.09.024
  17. Garnick, E. 1978. Behavioral ecology of Strongylocentrotus droebachiensis (Muller) (Echinodermata: Echinoidea): aggregating behavior and chemotaxis. Oecologia 37:77-84. https://doi.org/10.1007/BF00349993
  18. Harrold, C. & Reed, D. C. 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160-1169. https://doi.org/10.2307/1939168
  19. 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. https://doi.org/10.3354/meps048185
  20. Hayakawa, Y. & Kittaka, J. 1984. Simulation of feedig behavior of sea urchin Strongylocentrotus nudus. Bull. Jpn. Soc. Sci. Fish. 50:233-240. https://doi.org/10.2331/suisan.50.233
  21. 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. https://doi.org/10.1016/j.jtherbio.2004.03.003
  22. Hillebrand, H. & Cardinale, B. J. 2004. Consumer effects decline with prey diversity. Ecol. Lett. 7:192-201. https://doi.org/10.1111/j.1461-0248.2004.00570.x
  23. 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. https://doi.org/10.1139/f90-116
  24. Huntly, N. 1991. Herbivores and the dynamics of communities and ecosystems. Annu. Rev. Ecol. Syst. 22:477-503. https://doi.org/10.1146/annurev.es.22.110191.002401
  25. 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. https://doi.org/10.1016/j.aquaculture.2012.08.022
  26. 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. https://doi.org/10.1007/s10682-007-9181-9
  27. 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. https://doi.org/10.1016/S0022-0981(97)00236-0
  28. 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. https://doi.org/10.1016/S0022-0981(96)02707-4
  29. 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.
  30. 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. https://doi.org/10.13047/KJEE.2014.28.1.10
  31. 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.
  32. 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.
  33. 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. https://doi.org/10.1073/pnas.1606102113
  34. 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. https://doi.org/10.1007/BF00396982
  35. 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. https://doi.org/10.3354/ab00040
  36. 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. https://doi.org/10.1017/S0025315406012999
  37. Lemire, M. & Himmelman, J. H. 1996. Relation of food preference to fitness for the green sea urchin, Strongylocentrotus droebachiensis. Mar. Biol. 127:73-78. https://doi.org/10.1007/BF00993646
  38. 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. https://doi.org/10.1016/j.jembe.2007.05.012
  39. 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.
  40. 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. https://doi.org/10.1016/0022-0981(84)90197-7
  41. 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. https://doi.org/10.3354/meps07255
  42. 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. https://doi.org/10.1111/j.1365-2745.2005.01058.x
  43. 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. https://doi.org/10.4319/lo.1969.14.5.0710
  44. 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. https://doi.org/10.1016/S1385-1101(97)00061-0
  45. Pearse, J. S. 2006. Ecological role of purple sea urchins. Science 314:940-941. https://doi.org/10.1126/science.1131888
  46. 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. https://doi.org/10.2307/1940813
  47. Pulliam, H. R. 1975. Diet optimization with nutrient constraints. Am. Nat. 109:765-768. https://doi.org/10.1086/283041
  48. Rapport, D. J. 1980. Optimal foraging for complementary resources. Am. Nat. 116:324-346. https://doi.org/10.1086/283631
  49. 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. https://doi.org/10.1111/j.0022-0477.2004.00936.x
  50. 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. https://doi.org/10.1007/s002270100567
  51. 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. https://doi.org/10.1007/s004420000546
  52. 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. https://doi.org/10.1016/j.aquaculture.2013.02.030
  53. 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. https://doi.org/10.4490/ALGAE.2008.23.3.231
  54. 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. https://doi.org/10.2331/suisan.57.1945
  55. 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. https://doi.org/10.4490/ALGAE.2007.22.1.045
  56. 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.
  57. 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.
  58. 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. https://doi.org/10.1111/j.1529-8817.2009.00706.x
  59. Vadas, R. L. 1977. Preferential feeding: an optimization strategy in sea urchins. Ecol. Monogr. 47:337-371. https://doi.org/10.2307/1942173
  60. 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. https://doi.org/10.7717/peerj.1235
  61. Worm, B., Lotze, H. K., Hillebrand, H. & Sommer, U. 2002. Consumer versus resource control of species diversity and ecosystem functioning. Nature 417:848-851. https://doi.org/10.1038/nature00830
  62. Yurchenko, O. V. & Reunov, A. A. 2004. Dimorphism of spermatozoa in the sea urchin Strongylocentrotus nudus. Russ. J. Mar. Biol. 30:354-357. https://doi.org/10.1023/B:RUMB.0000046554.82986.11
  63. 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. https://doi.org/10.1007/s10811-007-9303-3