Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-13T01:26:13.937Z Has data issue: false hasContentIssue false
  • English
  • Français

Fatty acids from controlled feeding as dietary markers of juvenile Chinese horseshoe crab, Tachypleus tridentatus

Published online by Cambridge University Press:  15 April 2018

Billy K.Y. Kwan ,
Menghong Hu ,
Youji Wang ,
Siu Gin Cheung  and
Paul K.S. Shin
Billy K.Y. Kwan
Affiliation:
Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, Qinzhou University, Qinzhou, China College of Ocean, Qinzhou University, Qinzhou, China Department of Biology and Chemistry, City University of Hong Kong, Hong Kong
Menghong Hu
Affiliation:
Department of Biology and Chemistry, City University of Hong Kong, Hong Kong National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, China Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai, China Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, China
Youji Wang
Affiliation:
Department of Biology and Chemistry, City University of Hong Kong, Hong Kong National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, China Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai, China Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, China
Siu Gin Cheung
Affiliation:
Department of Biology and Chemistry, City University of Hong Kong, Hong Kong State Key Laboratory in Marine Pollution, City University of Hong Kong, Hong Kong
Paul K.S. Shin*
Affiliation:
Department of Biology and Chemistry, City University of Hong Kong, Hong Kong State Key Laboratory in Marine Pollution, City University of Hong Kong, Hong Kong
*
Correspondence should be addressed to: P.K.S. Shin, Department of Biology and Chemistry, City University of Hong Kong, Hong Kong email: paulksshin@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The potential use of fatty acid (FA) profile as a dietary tracer in juvenile Chinese horseshoe crab Tachypleus tridentatus was assessed in a feeding experiment. Selected feed was provided to the juveniles at various growth stages according to their food sources in the wild: larval and adult brine shrimp Artemia salina for the first six months, followed by a mixture of short-neck clam Ruditapes philippinarum and greasyback shrimp Metapenaeus ensis for a further six months. Juvenile horseshoe crab haemolymph and tissues of book gill, opisthosomal spine, chelicera and swimming leg were sampled after the feeding experiment. The FA profiles revealed that the juvenile haemolymph and various tissues had a total of 23–24 FA components. The major FA components consisted of saturated (palmitic and stearic) at 22–34%, monosaturated (oleic) at 7–34% and polyunsaturated (eicosapentaenoic and arachidonic) FAs at 9–27%. According to principal component analysis, the FA signatures of juvenile haemolymph were greatly influenced by the shift of food sources from brine shrimp to clam and shrimp meat, whereas the FA profiles of different tissues were more resistant to the nutrient alteration. The present findings confirmed that the FA profile of both juvenile haemolymph and different tissues reflected the FA composition of recent and previous diets, respectively; and thus may be useful in indicating the foraging information of juvenile horseshoe crabs in the field.

Keywords

Nutritious dietfeeding nichehorseshoe crab instarlaboratory assaygas chromatography analysisfatty acid species
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 2 , March 2019 , pp. 421 - 428
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

B.K.Y. Kwan and M. Hu are co-first authors.

References

REFERENCES

Alkanani, T, Parrish, C.C., Thompson, R.J. and McKenzie, C.H. (2007) Role of fatty acids in cultured mussels, Mytilus edulis, grown in Notre Dame Bay, Newfoundland. Journal of Experimental Marine Biology and Ecology 348, 33–45.Google Scholar
Bell, M.V., Dick, J.R. and Kelly, M.S. (2001) Biosynthesis of eicosapentaenoic acid in the sea urchin Psammechinus miliaris. Lipids 36, 79–82.Google Scholar
Bell, M.V. and Tocher, D.R. (2009) Biosynthesis of polyunsaturated fatty acids in aquatic ecosystems: general pathways and new directions. In Arts, M.T., Kainz, M.J. and Brett, M.T. (eds) Lipids in aquatic ecosystems. Dordrecht: Springer, pp. 211–236.Google Scholar
Benedito-Palos, L., Navarro, J.C., Kaushik, S. and Pérez-Sánchez, J. (2010) Tissue-specific robustness of fatty acid signatures in cultured gilthead sea bream (L.) fed practical diets with a combined high replacement of fish meal and fish oil. Journal of Animal Science 88, 1759–1770.Google Scholar
Benedito-Palos, M. and Bendiksen, E.A. (2003) Dietary lipids and temperature interact to influence tissue fatty acid compositions of Atlantic salmon, Salmo salar L., parr. Aquaculture Research 34, 1423–1441.Google Scholar
Botton, M.L. and Shuster, C.N. Jr (2003) Horseshoe crabs in a food web: who eats whom. In Shuster, C.N. Jr, Barlow, R.B. and Brockmann, H.J. (eds) The American horseshoe crab. Cambridge, MA: Harvard University Press, pp. 133–153.Google Scholar
Brown, G.G. and Clapper, D.L. (1981) Procedures for maintaining adults, collecting gametes, and culturing embryos and juveniles of the horseshoe crab, Limulus polyphemus L. In Hinegardner, R., Atz, J., Fay, R., Fingerman, M., Josephson, R. and Meinkoth, N. (eds) Laboratory animal management: marine invertebrates. Washington, DC: National Academy Press, pp. 268–290.Google Scholar
Budge, S.M., Iverson, S.J. and Koopman, H.N. (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Marine Mammal Science 22, 759–801.Google Scholar
Calado, R., Rosa, R., Morais, S., Nunes, M.L. and Narciso, L. (2005) Growth, survival, lipid and fatty acid profile of juvenile Monaco shrimp Lysmata seticaudata fed on different diets. Aquaculture Research 36, 493–504.Google Scholar
Carmichael, R.H., Gaines, E., Sheller, Z., Tong, A., Clapp, A. and Valiela, I. (2009) Diet composition of juvenile horseshoe crabs: implications for growth and survival of natural and cultured stocks. In Tanacredi, J.T., Botton, M.L. and Smith, D.R. (eds) Biology and conservation of horseshoe crabs. New York, NY: Springer, pp. 521–534.Google Scholar
Carmichael, R.H., Rutecki, D., Annett, B., Gaines, E. and Valiela, I. (2004) Position of horseshoe crabs in estuarine food webs: N and C stable isotopic study of foraging ranges and diet composition. Journal of Experimental Marine Biology and Ecology 299, 231–253.Google Scholar
Castell, J.D., Kennedy, E.J., Robinson, S.M.C., Parsons, G.J., Blair, T.J. and Gonzalez-Duran, E. (2004) Effect of dietary lipids on fatty acid composition and metabolism in juvenile green sea urchins (Strongylocentrotus droebachiensis). Aquaculture 242, 417–435.Google Scholar
Chan, K.Y., Gao, Q.F., Yip, K.M., Wong, W.H., Shin, P.K.S. and Cheung, S.G. (2003) Lipid content and fatty acid composition in the green-lipped mussel Perna viridis (L.). Journal of Food Lipids 11, 123–130.Google Scholar
Chen, Y., Lau, C.W., Cheung, S.G., Ke, C.H. and Shin, P.K.S. (2010) Enhanced growth of juvenile Tachypleus tridentatus (Chelicerata: Xiphosura) in the laboratory: a step towards population restocking for conservation of the species. Aquatic Biology 11, 37–46.Google Scholar
Cui, Y., Wu, Y., Zhang, J. and Wang, N. (2012) Potential dietary influence on the stable isotopes and fatty acid compositions of jellyfishes in the Yellow Sea. Journal of the Marine Biological Association of the United Kingdom 92, 1325–1333.Google Scholar
Dalsgaard, J., St. John, M., Kattner, G., Müller-Navarra, D and Hagen, W. (2003) Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology 46, 225–340.Google Scholar
Delaporte, M., Soudant, P., Moal, J., Lambert, C., Quéré, C., Miner, P., Choquet, G., Paillard, C. and Samain, J.F. (2003) Effect of a mono-specific algal diet on immune functions in two bivalve species – Crassostrea gigas and Ruditapes philippinarum. Journal of Experimental Biology 206, 3053–3064.Google Scholar
Fluckiger, M., Jackson, G.D., Nichols, P., Virtue, P., Daw, A. and Wotherspoon, S. (2008) An experimental study of the effect of diet on the fatty acid profiles of the European cuttlefish (Sepia officinalis). Marine Biology 154, 363–372.Google Scholar
Gaines, E.F., Carmichael, R.H., Grady, S.P. and Valiela, I. (2002) Stable isotopic evidence for changing nutritional sources of juvenile horseshoe crabs. Biological Bulletin 203, 228–230.Google Scholar
Hall, D., Lee, S.Y. and Meziane, T. (2006) Fatty acids as trophic tracers in an experimental estuarine food chain: tracer transfer. Journal of Experimental Marine Biology and Ecology 336, 42–53.Google Scholar
Hall, J.M., Parrish, C.C. and Thompson, R.J. (2002) Eicosapentaenoic acid regulates scallop (Placopecten magellanicus) membrane fluidity in response to cold. Biological Bulletin 202, 201–203.Google Scholar
Hong, S. (2011) Feeding habits. In Hong, S. (eds) Biology of horseshoe crabs, Tachypleus tridentatus. Xiamen: Xiamen University Press, pp. 79–81.Google Scholar
Hsieh, H.L. and Chen, C.P. (2015) Current status of Tachypleus tridentatus in Taiwan for Red List assessment. In Tanacredi, J.T., Botton, M.L. and Smith, D.R. (eds) Changing global perspectives on horseshoe crab biology, conservation and management. Cham: Springer International Publishing, pp. 383–396.Google Scholar
Hu, M., Wang, Y., Cheung, S.G. and Shin, P.K.S. (2013) Comparison of different frozen natural foods on survival and growth of juvenile Chinese horseshoe crab Tachypleus tridentatus (Leach, 1819): implications on laboratory culture. Aquaculture Research 44, 567–573.Google Scholar
Iverson, S.J., Field, C., Don Bowen, W. and Blanchard, W. (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecological Monographs 74, 211–235.Google Scholar
Iverson, S.J., Frost, K.J. and Lang, S.L. (2002) Fat content and fatty acid composition of forage fish and invertebrates in Prince William Sound, Alaska: factors contributing to among and within species variability. Marine Ecology Progress Series 241, 161–181.Google Scholar
Kelly, J.R., Krumhansl, K.A. and Scheibling, R.E. (2012) Drift algal subsidies to sea urchins in low-productivity habitats. Marine Ecology Progress Series 452, 145–157.Google Scholar
Kelly, J.R. and Scheibling, R.E. (2011) Fatty acids as dietary tracers in benthic food webs. Marine Ecology Progress Series 446, 1–22.Google Scholar
Kelly, J.R., Scheibling, R.E. and Iverson, S.J. (2009) Fatty acids tracers for native and invasive macroalgae in an experimental food web. Marine Ecology Progress Series 391, 53–63.Google Scholar
Ko, A.R., Ju, S.J., Choi, S.G. and Shin, K.H. (2016) The feasibility of assessing the diets of minke whale (Balaenoptera acutorostrata) in the East Sea through fatty acid composition in blubber and stable isotopic ratio of skin. Ocean Science Journal 51, 397–410.Google Scholar
Kwan, B.K.Y., Chan, A.K.Y., Cheung, S.G. and Shin, P.K.S. (2014) Hemolymph quality as indicator of health status in juvenile Chinese horseshoe crab Tachypleus tridentatus (Xiphosura) under laboratory culture. Journal of Experimental Marine Biology and Ecology 457, 135–142.Google Scholar
Kwan, B.K.Y., Chan, A.K.Y., Cheung, S.G. and Shin, P.K.S. (2015 a) Responses of growth and hemolymph quality in juvenile Chinese horseshoe crab Tachypleus tridentatus (Xiphosura) to sublethal tributyltin and cadmium. Ecotoxicology 24, 1880–1895.Google Scholar
Kwan, B.K.Y., Chan, A.K.Y., Cheung, S.G. and Shin, P.K.S. (2017) Marine microalgae as dietary supplements in the culture of juvenile Chinese horseshoe crabs, Tachypleus tridentatus (Xiphosura). Aquaculture Research 48, 3910–3924.Google Scholar
Kwan, B.K.Y., Cheung, S.G. and Shin, P.K.S. (2015 b) A dual stable isotope study for diet composition of juvenile Chinese horseshoe crab (Xiphosura) on a seagrass-covered intertidal mudflat. Marine Biology 162, 1137–1143.Google Scholar
Kwan, B.K.Y., Hsieh, H.Y., Cheung, S.G. and Shin, P.K.S. (2016) Present population and habitat status of potentially threatened Asian horseshoe crabs Tachypleus tridentatus and Carcinoscorpius rotundicauda in Hong Kong: a proposal for marine protected area. Biodiversity and Conservation 25, 673–692.Google Scholar
Levine, D.M. and Sulkin, S.D. (1984) Nutritional significance of long-chain polyunsaturated fatty acids to the zoeal development of the brachyuran crab, Eurypanopeus depressus (Smith). Journal of Experimental Marine Biology and Ecology 81, 211–223.Google Scholar
Liyana-Pathirana, C., Shahidi, F. and Whittick, A. (2002) The effect of an artificial diet on the biochemical composition of the gonads of the sea urchin (Strongylocentrotus droebachiensis). Food Chemistry 79, 461–472.Google Scholar
MacPherson, J.C., Pavlovich, J.G. and Jacobs, R.S. (1998) Phospholipid composition of the granular amebocyte from the horseshoe crab, Limulus polyphemus. Lipids 33, 931–940.Google Scholar
Nelson, B.R., Satyanarayana, B., Zhong, J.M.H., Shaharom, F., Sukumaran, M. and Chatterji, A. (2015) Episodic human activities and seasonal impacts on the Tachypleus gigas (Müller, 1785) population at Tanjung Selangor in Peninsular Malaysia. Estuarine, Coastal and Shelf Science 164, 313–323.Google Scholar
Passi, S., Cataudella, S., Di Marco, P., De Simone, F. and Rastrelli, L. (2002) Fatty acid composition and antioxidant levels in muscle tissue of different Mediterranean marine species of fish and shellfish. Journal of Agricultural and Food Chemistry 50, 7314–7322.Google Scholar
Pernet, F. and Tremblay, R. (2004) Effect of varying levels of dietary essential fatty acid during early ontogeny of the sea scallop Placopecten magellanicus. Journal of Experimental Marine Biology and Ecology 310, 73–86.Google Scholar
Pielou, E.C. (1984) The interpretation of ecological data: a primer on classification and ordination. New York, NY: John Wiley & Sons.Google Scholar
Redmond, K.J., Magnesen, T., Hansen, P.K., Strand, Ø. and Meier, S. (2010) Stable isotopes and fatty acids as tracers of the assimilation of salmon fish feed in blue mussels (Mytilus edulis). Aquaculture 298, 202–210.Google Scholar
Regost, C., Arzel, J., Robin, J., Rosenlund, G. and Kaushik, S.J. (2003) Total replacement of fish oil by soybean or linseed oil with a return to fish oil in turbot (Psetta maxima): growth performance, flesh fatty acid profile, and lipid metabolism. Aquaculture 217, 465–482.Google Scholar
Schreibman, M.P. and Zarnoch, C.B. (2009) Aquaculture methods and early growth of juvenile horseshoe crabs (Limulus polyphemus). In Tanacredi, J.T., Botton, M.L. and Smith, D.R. (eds) Biology and conservation of horseshoe crabs. New York, NY: Springer, pp. 501–512.Google Scholar
Schulz, C., Knaus, U., Wirth, M. and Rennert, B. (2005) Effects of varying dietary fatty acid profile on growth performance, fatty acid, body and tissue composition of juvenile pike perch (Sander lucioperca). Aquaculture Nutrition 11, 403–413.Google Scholar
Shin, P.K.S., Yip, K.M., Xu, W.Z., Wong, W.H. and Cheung, S.G. (2008) Fatty acid as markers to demonstrating trophic relationships among diatoms, rotifers and green-lipped mussels. Journal of Experimental Marine Biology and Ecology 357, 75–84.Google Scholar
Skalli, A., Robin, J. H., Le Bayon, N., Le Delliou, H. and Person-Le Ruyet, J. (2006) Impact of essential fatty acid deficiency and temperature on tissues’ fatty acid composition of European sea bass (Dicentrarchus labrax). Aquaculture 255, 223–232.Google Scholar
Skonberg, D.I., Rasco, B.A. and Dong, F.M. (1994) Fatty acid composition of salmonid muscle changes in response to a high oleic acid diet. Journal of Nutrition 124, 1628–1638.Google Scholar
Stowasser, G., Pierce, G.J., Moffat, C.F., Collins, M.A. and Forsythe, J.W. (2006) Experimental study on the effect of diet on fatty acid and stable isotope profiles of the squid Lolliguncula brevis. Journal of Experimental Marine Biology and Ecology 333, 97–114.Google Scholar
Suprayudi, M.A., Takeuchi, T. and Hamasaki, K. (2004) Effects of Artemia enriched with eicosapentaenoic and docosahexaenoic acid on survival and occurrence of molting failure in megalop larvae of the mud crab Scylla serrata. Fisheries Science 70, 650–658.Google Scholar
Van der Horst, D.J., Oudejans, R.C.H.M., Plug, A.G. and Van der Sluis, I. (1973) Fatty acids of the female horseshoe crab Xiphosura (Limulus) polyphemus. Marine Biology 20, 291–296.Google Scholar
Zainudin, B., Takaomi, A. and Razikin, A. (2016) Influence of growth on fatty acid composition of the moon wrasse Thalassoma lunare collected in coral reef habitats of the Malaysian South China Sea. Tropical Ecology 57, 779–785.Google Scholar
Zhou, H. and Morton, B. (2004) The diets of juvenile horseshoe crabs, Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura), from nursery beaches proposed for conservation in Hong Kong. Journal of Natural History 38, 1915–1925.Google Scholar
Supplementary material: File

Kwan et al. supplementary material

Figure S1

Download Kwan et al. supplementary material(File)
File 354 KB