The Influence of Phlorotannins and Bromophenols on the Feeding Behavior of Marine Herbivorous Gastropod Turbo cornutus

Toshiyuki Shibata, Taiko Miyasaki, Hideo Miyake, Reiji Tanaka, Shigeo Kawaguchi

Department of Food Science and Technolo- gy, National Fisheries University, Yamaguchi, Japan.
Faculty of Agriculture, Kyushu University, Fukuoka, Japan.
Major of Life Sciences, Graduate School of Bioresources, Mie University, Mie, Japan.

DOI: 10.4236/ajps.2014.53051                

Abstract

The influence of phlorotannins and bromophenols on the feeding behavior of marine herbivores was determined using bioassay of Turbo cornutus. It was found that phloroglucinol and its oligomers isolated from the brown alga Eisenia bicyclis (eckol, fucofuroeckol A, phlorofucofuroeckol A, dieckol, and 8,8’-bieckol) had a deterrent effect against feeding behavior of T. cornutus in the concentration of algal body, respectively. In the case of the examination of 0.1 mM concentration, although fucofuroeckol A and phlorofucofuroeckol A significantly reduced feeding by T. cornutus, phloroglucinol and 8,8’-bieckol did not show any significant influence on feeding behavior, and eckol and dieckol had stimulating activity. 2,4-Dibromophenol and 2,4,6-tribromophenol, which are major components of extracellular secretions from Eisenia and Ecklonia species, caused the death, the torpidity, and the decreased appetite of T. cornutus at the concentration of 0.1 mM. In addition, 2,4-dibromophenol had strong feeding deterrent activity at the concentration of 1 μM. These results indicate that phlorotannins and bromophenols act as chemical defense agents of brown algae against environmental stresses such as the herbivore attack.

Keywords

Bromophenols; Brown Algae; Chemical Defenses; Feeding Deterrent; Eisenia bicyclis; Phlorotannins; Plant-Herbivore Interactions; Turban Shell; Turbo cornutus

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	M. A. Ragan and K.-W. Glombitza, “Phlorotannins, Brown Algal Polyphenols,” In: F. E. Round and D. J. Chapman, Eds., Progress in Phycological Research, Biopress, Bristol, Vol. 4, 1986, pp. 129-241.
[2]	C. D. Amsler and V. A. Fairhead, “Defensive and Sensory Chemical Ecology of Brown Algae,” In: J. A. Callow, Ed., Advances in Botanical Research, Elsevier, Amsterdam, Vol. 43, 2006, pp. 1-91. http://dx.doi.org/10.1016/S0065-2296(05)43001-3
[3]	J. A. Geiselman and O. J. McConell, “Polyphenols in Brown Algae Fucus vesiculosus and Ascophyllum nodosum: Chemical Defenses against the Marine Herbivorous Snail, Littorina littorea,” Journal of Chemical Ecology, Vol. 7, No. 6, 1981, pp. 1115-1133. http://dx.doi.org/10.1007/BF00987632
[4]	P. D. Steinberg, “Algal Chemical Defense against Herbivores: Allocation of Phenolic Compounds in the Kelp Alaria marginata,” Science, Vol. 223, No. 4634, 1984, pp. 405-407. http://dx.doi.org/10.1126/science.223.4634.405
[5]	K. Taniguchi, Y. Akimoto, K. Kurata and M. Suzuki, “Chemical Defense Mechanism of the Brown Alga Eisenia bicyclis against Marine Herbivores,” Nippon Suisan Gakkaishi, Vol. 58, No. 3, 1992, pp. 571-575. http://dx.doi.org/10.2331/suisan.58.571
[6]	K. Taniguchi, K. Kurata and M. Suzuki, “Feeding-Deterrent Activity of Some Laminariaceous Brown Algae against the Ezo-abalone,” Nippon Suisan Gakkaishi, Vol. 58, No. 3, 1992, pp. 577-581. http://dx.doi.org/10.2331/suisan.58.577
[7]	N. M. Targett and T. M. Arnold, “Predicting the Effects of Brown Algal Phlorotannins on Marine Herbivores in Tropical and Temperate Oceans,” Journal of Phycolgy, Vol. 34, No. 2, 1998, pp. 195-205. http://dx.doi.org/10.1046/j.1529-8817.1998.340195.x
[8]	T. Shibata, S. Kawaguchi, Y. Hama, M. Inagaki, K. Yamaguchi and T. Nakamura, “Local and Chemical Distribution of Phlorotannins in Brown Algae,” Journal of Applied Phycology, Vol. 16, No. 4, 2004, pp. 291-296. http://dx.doi.org/10.1023/B:JAPH.0000047781.24993.0a
[9]	T. Yoshida, “Marine Algae of Japan,” Uchida Rokakuho Publishing, Tokyo, 1988.
[10]	T. Shibata, K. Yamaguchi, K. Nagayama, S. Kawaguchi and T. Nakamura, “Inhibitory Activity of Brown Algal Phlorotannins against Glycosidases from the Viscera of the Turban Shell Turbo cornutus,” European Journal of Phycology, Vol. 37, No. 4, 2002, pp. 493-500. http://dx.doi.org/10.1017/S0967026202003918
[11]	T. Shibata, Y. Hama, T. Miyasaki, M. Ito and T. Nakamura, “Extracellular Secretion of Phenolic Substances from Living Brown Algae,” Journal of Applied Phycology, Vol. 18, No. 6, 2006, pp. 787-794. http://dx.doi.org/10.1007/s10811-006-9094-y
[12]	T. Shibata, Y. Tashiro and Y. Hama, “Extracellular Secretion of Phenolic Substances from Living Brown Algae: Phlorotannins Are Not Secreted from the Algae into the Seawater Medium,” Annual Report Venture Business Laboratory Saga University, Vol. 5, 2004, pp. 89-94.
[13]	J. McN. Sieburth and J. T. Conover, “Sargassum Tannin, an Antibiotic Which Retards Fouling,” Nature, Vol. 208, No. 5005, 1965, pp. 52-53. http://dx.doi.org/10.1038/208052a0
[14]	T. Sakami, “Effects of Algal Excreted Substances on the Respiration Activities of Epiphytic Bacteria on the Brown Alga, Eisenia bicyclis Kjellman,” Fisheries Science, Vol. 62, No. 3, 1996, pp. 394-396.
[15]	A. K. Swanson and L. D. Druehl, “Induction, Exudation and the UV Protective Role of Kelp Phlorotannins,” Aquatic Botany, Vol. 73, No. 3, 2002, pp. 241-253. http://dx.doi.org/10.1016/S0304-3770(02)00035-9
[16]	T. Shibata, K. Ishimaru, S. Kawaguchi, H. Yoshikawa and Y. Hama, “Antioxidant Activities of Phlorotannins Isolated from Japanese Laminariaceae,” Journal of Applied Phycology, Vol. 20, No. 5, 2008, pp. 705-711. http://dx.doi.org/10.1007/s10811-007-9254-8
[17]	Y. Fujii, R. Tanaka, H. Miyake, Y. Tamaru, M. Ueda and T. Shibata, “Evaluation for Antioxidative Properties of Phlorotannins Isolated from the Brown Alga Eisenia bicyclis, by the H-ORAC Method,” Food and Nutrition Sciences, Vol. 4, No. 8A, 2013, pp. 78-82. http://dx.doi.org/10.4236/fns.2013.48A010
[18]	T. Miyasaki and K. Harada, “Feeding Attractants and Stimulants for Aquatic Animals,” Fisheries Science, Vol. 68, Suppl. 2, 2002, pp. 1406-1409.
[19]	F. B. Whitfield, F. Helidoniotis, K. J. Shaw and D. Svoronos, “Distribution of Bromophenols in Species of Marine Algae from Eastern Australia,” Journal of Agricultural and Food Chemistry, Vol. 47, No. 6, 1999, pp. 2367-2373. http://dx.doi.org/10.1021/jf981080h
[20]	H. Y. Chung, W. C. Joyce Ma, P. O. Ang Jr., J.-S. Kim and F. Chen, “Seasonal Variations of Bromophenols in Brown Algae (Padina arborescens, Sargassum siliquastrum, and Lobophora variegata) Collected in Hong Kong,” Journal of Agricultural and Food Chemistry, Vol. 51, No. 9, 2003, pp. 2619-2624. http://dx.doi.org/10.1021/jf026082n
[21]	Y. Agatsuma, H. Endo and K. Taniguchi, “Inhibitory Effect of 2,4-Dibromophenol and 2,4,6-Tribromophenol on Larval Survival and Metamorphosis of the Sea Urchin Strongylocentrotus nudus,” Fisheries Science, Vol. 74, No. 4, 2008, pp. 837-841. http://dx.doi.org/10.1111/j.1444-2906.2008.01596.x
[22]	J.-Y. Li, H. Endo, Y. Agatsuma and K. Taniguchi, “Inhibition of Larval Survival and Metamorphosis of the Sea Urchin Strongylocentrotus intermedius by 2,4-Dibromophenol and 2,4,6-Tribromophenol,” Aquaculture Science, Vol. 59, No. 2, 2011, pp. 247-253.