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Ontogenetic habitat and dietary shifts in Japanese turban snail Turbo cornutus at Nagai, Sagami Bay, Japan

  • Special Feature: Original Article
  • Coastal Ecosystem Complex (CEC)
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Abstract

A field survey and a laboratory experiment were conducted to examine ontogenetic shifts in habitat and diet of the turban snail Turbo cornutus. The main habitat of turban snail juveniles smaller than 10 mm shell height (SH) was turfs of articulated coralline algae, and that of adults larger than 50 mm SH was kelp beds of Ecklonia bicyclis and Ecklonia cava. However, the ontogenetic habitat shift during the juvenile stage of 20–50 mm SH was unclear. From the results of a long-term feeding experiment and stable isotope analysis, the gelidiacean alga Gelidium elegans was assumed to be more important as a food source for juvenile turban snail than E. cava in the field. However, the frequency of individuals inhabiting gelidiacean algal turfs was low in both juvenile and adult stages. Thus, the ontogenetic shifts in habitat and diet did not coincide and other factors, i.e., daytime refuge, are important. As the growth rate was higher in the juveniles fed on the two algal species than those fed on single algal species, co-occurrence of various algal habitats in rocky shore ecosystems as a coastal ecosystem complex may enhance growth of turban snail juveniles feeding on a combination of different algal species.

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References

  • Akimoto S, Nakanishi T, Koyama T, Kato K (2012) The current status of seaweed beds of Ecklonia cava Kjellman and Eisenia bicyclis (Kjellman) Setchell distributed in Sagami Bay. Bull Kanagawa Pref Fish Tech Cent 5:1–9

    Google Scholar 

  • Chemello R, Milazzo M (2002) Effect of algal architecture on associated fauna: some evidence from phytal molluscs. Mar Biol 140:981–990

    Article  Google Scholar 

  • Dean RL, Connell JH (1987) Marine invertebrates in an algal succession III. Mechanisms linking habitat complexity with diversity. J Exp Mar Biol Ecol 109:249–273

    Article  Google Scholar 

  • Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Foster GG, Hodgson AN (1998) Consumption and apparent dry matter digestibility of six intertidal macroalgae by Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae). Aquaculture 167:211–227

    Article  Google Scholar 

  • Foster GG, Hodgson AN, Balarin M (1999a) Effect of diet on growth and reproductive fitness of Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae). Mar Biol 134:307–315

    Article  Google Scholar 

  • Foster GG, Hodgson AN, Boyd CS (1999b) Polysaccharolytic activity of the digestive enzymes of the macroalgal herbivore, Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae). Comp Biochem Physiol Part B 122:47–52

    Article  Google Scholar 

  • Fujii A (1998) Fisheries biology of the spiny top shell, Batillus cornutus, in the coastal waters of Tsushima Island. Bull Nagasaki Pref Inst Fish 24:71–115 (in Japanese with English abstract)

    Google Scholar 

  • Fujii A, Yotsui T, Ogawa S (1988) Alga preference of young topshell, Batillus cornutus. Bull Nagasaki Pref Inst Fish 14:19–25

    Google Scholar 

  • Fujita D, Okada H, Sakata K (1990) The importance of some marine red algae inhabiting fishing-port waterbreak vertical surface as natural food for juvenile horned turban Turbo (Batillus) cornutus. Bull Toyama Pref Fish Exp Stn 2:41–51

    Google Scholar 

  • Fukuda H (2017) Nomenclature of the horned turbans previously known as Turbo cornutus [Lightfoot], 1786 and Turbo chinensis Ozawa & Tomida, 1995 (Vetigastropoda: Trochoidea: Turbinidae) from China, Japan and Korea. Molluscan Res 45:78–96

    Google Scholar 

  • Hayakawa J, Kawamura T, Horii T, Watanabe Y (2007) Settlement of larval top shell Turbo (Batillus) cornutus in response to several marine algae. Fish Sci 73:371–377

    Article  CAS  Google Scholar 

  • Hayakawa J, Kawamura T, Ohashi S, Horii T, Watanabe Y (2008) Habitat selection of Japanese top shell (Turbo cornutus) on articulated coralline algae; combination of preferences in settlement and post-settlement stage. J Exp Mar Biol Ecol 363:118–123

    Article  Google Scholar 

  • Hayakawa J, Kawamura T, Ohashi S, Horii T, Watanabe Y (2010) Importance of epiphytic diatoms and fronds of two red algae species as diets for juvenile Japanese turban snail Turbo cornutus. J Shellfish Res 29:233–240

    Article  Google Scholar 

  • Hayakawa J, Kawamura T, Kurogi H, Watanabe Y (2013) Shelter effects of coralline algal turfs: protection for Turbo cornutus juveniles from predation by a predatory gastropod and wrasse. Fish Sci 79:15–20

    Article  CAS  Google Scholar 

  • Howell LN, Reich KJ, Shaver DJ, Landry AM Jr, Gorga CC (2016) Ontogenetic shifts in diet and habitat of juvenile green sea turtles in the northwestern Gulf of Mexico. Mar Ecol Prog Ser 559:217–229

    Article  CAS  Google Scholar 

  • Ito Y, Hayashi I (2001) Diel behavior of three herbivorous gastropods dominantly dwelling in shallow rocky areas of the Japan Sea. Nippon Suisan Gakkaishi 67:1089–1095 (in Japanese with English abstrtact)

    Article  Google Scholar 

  • Kono N, Yamakawa H (2002) Comparison of larval shell morphology of two coastal turbinid snails, Turbo (Batillus) cornutus and Turbo (Marmarostoma) stenogyrus (Vetigastropoda; Turbinidae). Bull Fish Res Agen 4:19–24

    Google Scholar 

  • McDonald PS, Bingham BL (2010) Comparing macroalgal food and habitat choice in sympatric, tube-building amphipods, Ampithoe lacertosa and Peramphithoe humeralis. Mar Biol 157:1513–1524

    Article  Google Scholar 

  • Parker JD, Duffy JE, Orth RJ (2001) Plant species diversity and composition: experimental effects on marine epifaunal assemblages. Mar Ecol Prog Ser 224:55–67

    Article  Google Scholar 

  • Poore AGB, Steinberg PD (1999) Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecol Monogr 69:443–464

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Roberts RD, Kasper HF, Barker RJ (2004) Settlement of abalone (Haliotis iris) larvae in response to five species of coralline algae. J Shellfish Res 23:975–987

    Google Scholar 

  • Sanchez-Hernandez J (2016) Do age-related changes in feeding habits of brown trout alter structural properties of food webs? Aquat Ecol 50:685–695

    Article  CAS  Google Scholar 

  • Sasaki T (2003) Early growth and change of population density of 0–1 age top shell, Turbo (Batillus) cornutus, at the eastern coastal waters, Shimane prefecture. Bull Shimane Pref Fish Exp Stn 11:23–29 (in Japanese with English abstract)

    Google Scholar 

  • Schoepf V, Herler J, Zuschin M (2010) Microhabitat use and prey selection of the coral-feeding snail Drupella cornus in the northern Red Sea. Hydrobiologia 641:45–57

    Article  Google Scholar 

  • Smoothey AF (2013) Habitat-associations of turban snails on intertidal and subtidal rocky reefs. PLoS ONE 8:e61257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takami H, Kawamura T (2018) Ontogenetic habitat shift in abalone Haliotis discus hannai: a review. Fish Sci. https://doi.org/10.1007/s12562-017-1169-y

  • Takami H, Kawamura T, Won N-I, Muraoka D, Hayakawa J, Onitsuka T (2017) Effects of macroalgal expansion triggered by the 2011 earthquake and tsunami on recruitment density of juvenile abalone Haliotis discus hannai at Oshika Peninsula, northeastern Japan. Fish Oceanogr 26:141–154

    Article  Google Scholar 

  • Turner AM, Bernot RJ, Boes CM (2000) Chemical cues modify species interactions: the ecological consequences of predator avoidance by freshwater snails. Oikos 88:148–158

    Article  CAS  Google Scholar 

  • Varisco M, Martin L, Zaixso H, Velasquez C, Vinusea J (2015) Food and habitat choice in the spider crab Leucippa pentagona (Majoidea: Epialtidae) in Bahia Bustamante, Patagonia, Argentina. Scientia Marina 79:107–116

    Article  Google Scholar 

  • Wakefield RL, Murray SN (1998) Factors influencing food choice by the seaweed-eating marine snail Norrisia norrisi (Trochidae). Mar Biol 130:631–642

    Article  Google Scholar 

  • Watanabe JM (1984) Food preference, food quality and diets of three herbivorous gastropods (Trochidae: Tegula) in a temperate kelp forest habitat. Oecologia 62:47–52

    Article  CAS  PubMed  Google Scholar 

  • Watanabe Y, Kawamura T, Yamashita Y (2018) Introduction: the coastal ecosystem complex as a unit of structure and function of biological productivity in coastal areas. Fish Sci. https://doi.org/10.1007/s12562-017-1176-7

  • Wernberg T, White M, Vanderklift MA (2008) Population structure of turbinid gastropods on wave-exposed subtidal reefs: effect of density, body size and algae on grazing behavior. Mar Ecol Prog Ser 362:169–179

    Article  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Annu Rev Ecol Syst 15:393–425

    Article  Google Scholar 

  • Worthington DG, Fairweather PG (1989) Shelter and food: interactions between Turbo undulatum (Archaeogastropoda: Turbinidae) and coralline algae on rocky seashores in New South Wales. J Exp Mar Biol Ecol 129:61–79

    Article  Google Scholar 

  • Yamakawa H, Hayashi I (2004) Relation between food habits of the turban shell, Turbo (Batillus) cornutus and algal distribution on Awa-shima Island, Niigata, Japan. Suisanzoshoku 52:57–63

    Google Scholar 

  • Yamazaki A, Ishiwata N (1987) Population ecology of the spiny turban shell Batillus cornutus II. Habitats of juvenile shell. La mer 25:184–189

    Google Scholar 

  • Yokohama Y, Tanaka J, Chihara M (1987) Productivity of the Ecklonia cava community in a bay of Izu Peninsula on the Pacific coast of Japan. Bot Mag Tokyo 100:129–141

    Article  Google Scholar 

  • Yoshiya M, Kuwahara A, Hamanaka Y (1987a) Study on the growth and survival of the young topshell Batillus cornutus in connection with algal vegetation and hydrographic conditions. Nippon Suisan Gakkaishi 53:239–247

    Article  Google Scholar 

  • Yoshiya M, Kuwahara A, Hamanaka Y, Wada Y (1987b) Food and feeding habits of a topshell Batillus cornutus, in the coastal area of Aoshima, Kyoto Japan. Nippon Suisan Gakkaishi 53:1359–1366

    Article  Google Scholar 

  • Zamzow JP, Amsler CD, McClintock JB, Baker BJ (2010) Habitat choice and predator avoidance by Antarctic amphipods: the roles of algal chemistry and morphology. Mar Ecol Prog Ser 400:155–163

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful to staff of the National Research Institute of Fisheries Science Yokosuka Station for their kind help in carrying out the experiments and collection of experimental animals and algae. We also thank the staff of the Kanagawa Sea Farming Association for their cooperation in offering the juveniles of the turban snail. This research was financially supported by the Coastal Ecosystem Complex Project of the Ocean Resources Use Promotion Technology Development Program, of the Ministry of Education, Culture, Sports, Science and Technology Japan.

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Correspondence to Jun Hayakawa.

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This article is sponsored by the coastal ecosystem complex project of the ocean resource use promotion technology development program, the Ministry of Education, Culture, Sports, Science and Technology, Japan.

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Hayakawa, J., Ohtsuchi, N., Kawamura, T. et al. Ontogenetic habitat and dietary shifts in Japanese turban snail Turbo cornutus at Nagai, Sagami Bay, Japan. Fish Sci 84, 201–209 (2018). https://doi.org/10.1007/s12562-017-1170-5

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  • DOI: https://doi.org/10.1007/s12562-017-1170-5

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