Skip to main content
Log in

Inhibition of growth in juvenile asari clams Ruditapes philippinarum fed Ulva spp. marine silage

  • Original Article
  • Aquaculture
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

The suitability of fermented products of Ulva fronds as diets for juvenile asari clams was tested. Ulva fronds were transformed by fermentation into a single-cell product (Ulva marine silage; UMS) of suitable size for ingestion by the clams. No dietary effect was seen in clams fed UMS alone. Furthermore, combined feeding with UMS and Chaetoceros calcitrans, which is considered a suitable diet for clams, resulted in a reduction in growth. An aqueous suspension of Ulva fronds prepared without fermentation showed inhibitory effects on clam growth, which indicated that the presumed inhibitory component(s) originated from the Ulva fronds. Further feeding tests indicated that the component(s) that inhibited clam growth were water soluble and had a molecular weight of < 1000 Da. An authentic product of glucuronic acid, one of the major components of the water-soluble fraction of UMS, induced inhibitory effects on shell growth. However, further study is necessary to identify the components of Ulva fronds that inhibit growth in the asari clam. The results indicate that the utilization of Ulva fronds as marine silage for the asari clam is problematic because they appear to contain component(s) that inhibit clam growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arasaki S (1984) A new aspect of Ulva vegetation along the Japanese coast. Hydrobiologia 116(117):229–232

    Google Scholar 

  • Brown JR, Hartwick EB (1988) Influences of temperature, salinity and available food upon suspended culture of the Pacific oyster, Crassostrea gigas. II. Condition index and survival. Aquaculture 70:253–267

    Article  Google Scholar 

  • Chiba K, Ohshima Y (1957) Effect of suspending particles on the pumping and feeding of marine bivalves, especially of Japanese neck-clam. Bull Jpn Soc Sci Fish 23:348–353

    Article  Google Scholar 

  • Cuomo V, Perretti A, Palomba I, Verde A, Cuomo A (1995) Utilization of Ulva rigida biomass in the Venice Lagoon (Italy): biotransformation in compost. J Appl Phycol 7:479–485

    Article  Google Scholar 

  • FAO/WHO/UNU (1985) Energy and protein requirements. Report of a joint FAO/WHO/UNU expert consultation. World Health Organization, Geneva

    Google Scholar 

  • Felix S, Pradeepa P (2012) Lactic acid fermentation of seaweed (Ulva reticulata) for preparing marine single cell detritus (MSCD). Tamilnadu J Vet Anim Sci 8:76–81

    Google Scholar 

  • Hamaguchi M (2011) Relationship among primary production, marine environment and fisheries production of bivalves in the Seto Inland Sea. Bull Fish Res Agen 34:33–47

    Google Scholar 

  • Johnson D (1980) Effects of phytoplankton and macroalgae on larval and juvenile winter flounder (Pseudopleuronectes americana albaum) cultures. M.Sc. thesis, University of Rhode Island, Kingston, RI

  • Johnson DA, Welsh BL (1985) Detrimental effects of Ulva lactuca (L.) exudates and low oxygen on estuarine crab larvae. J Exp Mar Biol Ecol 86:73–83

    Article  Google Scholar 

  • Kalla A, Yoshimatsu T, Khan MND, Higano J, Araki T, Sakamoto S (2008) Dietary effect of Porphyra spherpplasts for short-necked bivalve: a preliminary report. Aquacult Sci 56:51–56

    CAS  Google Scholar 

  • Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromol 8:1765–1774

    Article  CAS  Google Scholar 

  • Largo DB, Sembrano J, Hiraoka M, Ohno M (2004) Taxonomic and ecological profile of ‘green tide' species of Ulva (Ulvales, Chlorophyta) in central Philippines. Hydrobiologia 512:247

    Article  Google Scholar 

  • Lemee R, Pesando D, Durand-Clement M, Dubreuil A, Meinesz A, Guerriero A, Pietra F (1993) Preliminary survey of toxicity of green alga Caulerpa taxifolia introduced into the Mediterranean. J Appl Phycol 5:485–493

    Article  CAS  Google Scholar 

  • Magre EJ (1974) Ulva lactuca L. negatively affects Balanus balanoides (L.) (Cirripedia: Thoracica) in tidepools. Crustaceana 27:231–234

    Article  Google Scholar 

  • Merrill J, Fletcher R (1991) Green tides cause major economic burden in Venice Lagoon, Italy. Appl Phycol Forum 8:1–3

    Google Scholar 

  • Ministry of Agriculture, Forestry and Fisheries Japan Statistics Department (2017) The 92nd statistical yearbook of the Ministry of Agriculture, Forestry and Fisheries Japan Statistics Department. Ministry of Agriculture, Forestry and Fisheries Japan, Tokyo (in Japanese, with English index)

  • Nakagawa H, Kasahara S (1986) Effect of Ulva meal supplement to diet on the lipid metabolism of red sea bream. Bull Jpn Soc Sci Fish 52:1887–1893

    Article  CAS  Google Scholar 

  • Nelson TA, Lee DJ, Smith BC (2003) Are “green tides” harmful algal blooms? Toxic properties of water-soluble extracts from two bloom-forming macroalgae, Ulva fenestrata and Ulvaria obscura (Ulvophyceae). J Phycol 39:874–879

    Article  CAS  Google Scholar 

  • Pérez Camacho A, Salina JM, Fuertes C, Delgado M (2004) Preparation of single cell detritus from Laminaria saccharina as a hatchery diet for bivalve mollusks. Mar Biotechnol 6:642–649

    Article  Google Scholar 

  • Robic A, Bertrand D, Sassi JF, Lerat Y, Lahaye M (2009a) Determination of the chemical composition of ulvan, a cell wall polysaccharide from Ulva spp. (Ulvales, Chlorophyta) by FT-IR and chemometrics. J Appl Phycol 21:451–456

    Article  CAS  Google Scholar 

  • Robic A, Gaillard C, Sassi JF, Lerat Y, Lahaye M (2009b) Ultrastructure of ulvan: a polysaccharide from green seaweeds. Biopolymer 91:652–664

    Article  CAS  Google Scholar 

  • Tabata A, Morinaga T, Arakawa H (2000) Influences of concentration, particle-size and kind of inorganic suspended matter on feed caught by Manila clam, Ruditapes philippinarum. La mer 37:163–171

    CAS  Google Scholar 

  • The Council for Science and Technology, Ministry of Education, Culture, Sports, Science, and Technology, Japan (2004) Analytical manual for standard tables of food composition in Japan—reference materials for the subdivision on resources. Kenpakusha, Tokyo

  • Tsubaki S, Oono K, Hiraoka M, Ueda T, Onda A, Yanagisawa K, Azuma J (2014) Hydrolysis of green-tide forming Ulva spp. by microwave irradiation with polyoxometalate clusters. Green Chem 16:2227–2233

    Article  CAS  Google Scholar 

  • Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, Kanazawa M, Vandergheynst J, Fiehn O, Arita M (2015) MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Methods 12:523–526

    Article  CAS  Google Scholar 

  • Uchida M, Miyoshi T (2013) Algal fermentation-the seed for a new fermentation industry of foods and related products. JARQ 47:53–63

    Article  CAS  Google Scholar 

  • Uchida M, Murata M (2002) Fermentative preparation of single cell detritus from seaweed, Undaria pinnatifida, suitable as a replacement hatchery diet for unicellular algae. Aquaculture 207:345–357

    Article  CAS  Google Scholar 

  • Uchida M, Nakata K, Maeda M (1997a) Introduction of detrital food webs into an aquaculture system by supplying single cell algal detritus produced from Laminaria japonica as a hatchery diet for Artemia nauplii. Aquaculture 154:125–137

    Article  Google Scholar 

  • Uchida M, Nakata K, Maeda M (1997b) Conversion of Ulva fronds to a hatchery diet for Artemia nauplii utilizing the degrading and attaching abilities of Pseudoalteromonas espejiana. J Appl Phycol 9:541–549

    Google Scholar 

  • Uchida M, Numaguchi K, Murata M (2004) Mass preparation of marine silage from Undaria pinnatifida and its dietary effect for young pearl oysters. Fish Sci 70:456–462

    Article  CAS  Google Scholar 

  • Uchida M, Kanematsu M, Miyoshi T (2010) Growth promotion of the juvenile clam, Ruditapes philippinarum, on sugars supplemented to the rearing water. Aquaculture 302:243–247

    Article  CAS  Google Scholar 

  • Uchimura M, Yoshida G, Hiraoka M, Komatsu T, Arai S, Terawaki T (2004) Ecological studies of green tide, Ulva spp. (Chlorophyta) in Hiroshima Bay, the Seto Inland Sea. Jpn J Phycol 52:17–22

    Google Scholar 

  • Yamamoto T (2003) The Seto Inland Sea—eutrophic or oligotrophic? Mar Poll Bull 47:37–42

    Article  CAS  Google Scholar 

  • Yamasaki Y, Ishii K, Taga S, Kishioka M (2015) Preliminary observation of growth-promoting effects of alginate hydrolysates on juvenile Manila clams, Ruditapes philippinarum. Aquacult Res 46:1013–1017

    Article  CAS  Google Scholar 

  • Yamasaki Y, Ishii K, Taga S, Kishioka M (2018) Enhancement of dietary effect of Nannochloropsis sp. on juvenile Ruditapes philippinarum clams by alginate hydrolysates. Aquacult Rep 9:31–36

    Article  Google Scholar 

  • Yokohama-shi Rinkai-kankyo Hozen Jigyodan (2010) Gyogyo tengyo taisaku to rinkaibu kankyo hozen no ayumi. Yokohama-shi Rinkai-kankyo Hozen Jigyodan (presently, Yokohama Greenery Foundation), Yokohama

Download references

Acknowledgments

This work was supported by the Fisheries Agency of Japan. We thank Drs. Toshinobu Terawaki, Goro Yoshida, and Masayuki Uchimura for helpful suggestions regards the study of Ulva spp.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Motoharu Uchida.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Uchida, M., Miyoshi, T., Kanematsu, M. et al. Inhibition of growth in juvenile asari clams Ruditapes philippinarum fed Ulva spp. marine silage. Fish Sci 86, 519–530 (2020). https://doi.org/10.1007/s12562-020-01424-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-020-01424-2

Keywords

Navigation