Abstract
Understanding the feeding selectivity on phytoplankton by shellfish is currently a big challenge. In order to investigate the feeding behavior of bay scallop (Argopecten irradians) on phytoplankton, we compared its compositions of phytopigments in digestive glands with those in the surrounding seawater, and conducted five consecutive investigations between July and November 2016 in a bay scallop culture area along coast of Qinghuangdao City, northwest of the Bohai Sea, China. Phytopigments in four-size fractionated phytoplankton of seawater (micro- (20–200 µm); nano(L)-[10–20 µm]; nano(S)-[2.7–10 µm], and pico-[<2.7 µm]) and digestive glands of A. irradians were examined to investigate the selective feeding of A. irradians. Results show that fucoxanthin and peridinin constituted the major part of taxonomically diagnostic carotenoids (TDCs) in the micro- and nano(L)-phytoplankton in seawater. Compared with total phytoplankton biomass of seawater (TPB, sum of the four sizes), a substantial decrease of fucoxanthin proportion to total DCs in digestive glands was observed while that of peridinin, 19′-butanoyloxyfucoxanthin, alloxanthin and 19′-hexanoyloxy-fucoxanthin showed an obvious increase when those pigments were mainly confined to micro-sized phytoplankton (20–200 µm). However, zeaxanthin and prasinoxanthin were mainly confined to nano(s)- and pico-phytoplankton, of which the proportions in digestive glands were usually lower in TPB. The contribution of lutein to total DCs in digestive glands (with an average of 7.23%) increased compared with TPB of seawater (with an average of 0.63%) during all five sampling times.
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References
Bianchi T S, Findlay S. 1991. Decomposition of Hudson estuary macrophytes: photosynthetic pigment transformations and decay constants. Estuaries, 14(1): 65–73. https://doi.org/10.2307/1351983.
Bontes B M, Verschoor A M, Pires L M D, van Donk E, Ibelings B W. 2007. Functional response of Anodonta anatina feeding on a green alga and four strains of cyanobacteria, differing in shape, size and toxicity. Hydrobiologia, 584(1): 191–204. https://doi.org/10.1007/s10750-007-0580-2.
Bougrier S, Hawkins A J S, Héral M. 1997. Preingestive selection of different microalgal mixtures in Crassostrea gigas and Mytilus edulis, analysed by flow cytometry. Aquaculture, 150(1–2): 123–134. https://doi.org/10.1016/S0044-8486(96)01457-3.
Cranford P J, Li W, Strand Ø, Strohmeier T. 2008. Phytoplankton depletion by mussel aquaculture: high resolution mapping, ecosystem modeling and potential indicators of ecological carrying capacity. https://doi.org/www.ices.dk/sites/pub/CM%20Doccuments/CM-2008/H/H1208.pdf. Accessed on 2008.
Cranford P J, Ward J E, Shumway S E. 2011. Bivalve filter feeding: variability and limits of the aquaculture biofilter. In: Shumway S E ed. Shellfish Aquaculture and the Environment. Wiley-Blackwell Press, West Sussex, UK, p. 81–124. https://doi.org/10.1002/9780470960967.ch4.
Dupuy C, Vaquer A, Lam-Höai T, Rougier C, Mazouni N, Lautier J, Collos Y, Le Gall S. 2000. Feeding rate of the oyster Crassostrea gigas in a natural planktonic community of the Mediterranean Thau Lagoon. Marine Ecology Progress Series, 205: 171–184. https://doi.org/10.3354/meps205171.
Espinosa E P, Cerrato R M, Wikfors G H, Allam B. 2016. Modeling food choice in the two suspension-feeding bivalves, Crassostrea virginica and Mytilus edulis. Marine Biology, 163(2): 40, https://doi.org/10.1007/s00227-016-2815-0.
Frau D, Molina F R, Mayora G. 2016. Feeding selectivity of the invasive mussel Limnoperna fortunei (Dunker, 1857) on a natural phytoplankton assemblage: what really matters? Limnology, 17(1): 47–57. https://doi.org/10.1007/s10201-015-0459-2.
Jeffrey S W, Vesk M. 1997. Introduction to marine phytoplankton and their pigment signatures. In: Jeffrey S W, Mantoura R F C, Wright S W eds. Phytoplankton Pigments in Oceanography. SCOR-UNESCO, Paris. p. 37–84.
Jiang T, Chen F Y, Yu Z H, Lu L, Wang Z H. 2016. Size-dependent depletion and community disturbance of phytoplankton under intensive oyster mariculture based on HPLC pigment analysis in Daya Bay, South China Sea. Environmental Pollution, 219: 804–814, https://doi.org/10.1016/j.envpol.2016.07.058.
Jiang T, Yu Z H, Qi Z H, Chai C, Qu K M. 2017. Effects of intensive mariculture on the sediment environment as revealed by phytoplankton pigments in a semi-enclosed bay, South China Sea. Aquaculture Research, 48(4): 1 923–1 935, https://doi.org/10.1111/are.13030.
Kamermans P. 1994. Similarity in food source and timing of feeding in deposit-and suspension-feeding bivalves. Marine Ecology Progress Series, 104: 63–75, https://doi.org/10.3354/meps104063.
Lavaud R, Artigaud S, Le Grand F, Donval A, Soudant P, Flye-Sainte-Marie J F, Strohmeier T, Strand Ø, Leynaert A, Beker B, Chatterjee A, Jean F. 2018. New insights into the seasonal feeding ecology of Pecten maximus using pigments, fatty acids and sterols analyses. Marine Ecology Progress Series, 590: 109–129, https://doi.org/10.3354/meps12476.
Leavitt P R, Hodgson D A. 2001. Sedimentary pigments. In: Smol J P, Birks H J B, Last W M eds. Tracking Environmental Change Using Lake Sediments. Volume 3: Terrestrial, Algal, and Siliceous Indicators. Kluwer Academic Publishers, Dordrecht. p. 295–325.
Leavitt P R. 1993. A review of factors that regulate carotenoid and chlorophyll deposition and fossil pigment abundance. Journal of Paleolimnology, 9(2): 109–127, https://doi.org/10.1007/BF00677513.
Loret P, Pastoureaud A, Bacher C, Delesalle B. 2000. Phytoplankton composition and selective feeding of the pearl oyster Pinctada margaritifera in the Takapoto lagoon (Tuamotu Archipelago, French Polynesia): in situ study using optical microscopy and HPLC pigment analysis. Marine Ecology Progress Series, 199: 55–67, https://doi.org/10.3354/meps199055.
Mafra L L Jr., Bricelj V M, Ouellette C, Léger C, Bates S S. 2009. Mechanisms contributing to low domoic acid uptake by oysters feeding on Pseudo-nitzschia cells. I. Filtration and pseudofeces production. Aquatic Biology, 6: 201–212, https://doi.org/10.3354/ab00121.
Makhutova O N, Protasov A A, Gladyshev M I, Sylaieva A A, Sushchik N N, Morozovskaya I A, Kalachova G S. 2013. Feeding spectra of bivalve mollusks Unio and Dreissena from Kanevskoe Reservoir, Ukraine: are they food competitors or not? Zoological Studies, 52(1): 56, https://doi.org/10.1186/1810-522X-52-56.
Ren J S, Ross A H, Hayden B J. 2006. Comparison of assimilation efficiency on diets of nine phytoplankton species of the greenshell mussel Perna canaliculus. Journal of Shellfish Research, 25(3): 887–892, https://doi.org/10.2983/0730-8000(2006)25[887:COAEOD]2.0.CO;2.
Repeta D J, Gagosian R B. 1987. Carotenoid diagenesis in recent marine sediments—I. the Peru continental shelf (15°S, 75°W). Geochimica et Cosmochimica Acta, 51(4): 1 001–1 009, https://doi.org/10.1016/0016-7037(87)90111-6.
Rosa M, Ward J E, Holohan B A, Shumway S E, Wikfors G H. 2017. Physicochemical surface properties of microalgae and their combined effects on particle selection by suspension-feeding bivalve molluscs. Journal of Experimental Marine Biology and Ecology, 486: 59–68, https://doi.org/10.1016/j.jembe.2016.09.007.
Rouillon G, Rivas J G, Ochoa N, Navarro E. 2005. Phytoplankton composition of the stomach contents of the mussel Mytilus edulis L. from two populations: comparison with its food supply. Journal of Shellfish Research, 24(1): 5–14, https://doi.org/10.2983/0730-8000(2005)24[5:PCOTSC]2.0.CO;2.
Safi K A, Gibbs M M. 2003. Importance of different size classes of phytoplankton in Beatrix Bay, Marlborough Sounds, New Zealand, and the potential implications for the aquaculture of the mussel, Perna canaliculus. New Zealand Journal of Marine and Freshwater Research, 37(2): 267–272, https://doi.org/10.1080/00288330.2003.9517164.
Safi K A, Hayden B. 2010. Differential grazing on natural planktonic populations by the mussel Perna canaliculus. Aquatic Biology, 11(2): 113–125, https://doi.org/10.3354/ab00297.
Safi K A, Hewitt J E, Talman S G. 2007. The effect of high inorganic seston loads on prey selection by the suspension feeding bivalve, Atrinazelandica. Journal of Experimental Marine Biology and Ecology, 344(2): 136–148, https://doi.org/10.1016/j.jembe.2006.12.023.
Seoane S, Laza A, Orive E. 2006. Monitoring phytoplankton assemblages in estuarine waters: the application of pigment analysis and microscopy to size-fractionated samples. Estuarine, Coastal and Shelf Science, 67(3): 343–354, https://doi.org/10.1016/j.ecss.2005.10.020.
Shumway S E, Cucci T L, Newell R C, Yentsch C M. 1985. Particle selection, ingestion, and absorption in filter-feeding bivalves. Journal of Experimental Marine Biology andEcology, 91(1–2): 77–92, https://doi.org/10.1016/0022-0981(85)90222-9.
Shumway S E, Selvin R, Shick D F. 1987. Food resources related to habitat in the scallop Placopecten magellanicus (Gmelin, 1791): a qualitative study. Journal of Shellfish Research, 6(2): 89–95.
Sidari L, Nichetto P, Cok S, Sosa S, Tubaro A, Honsell G, Della Loggia R. 1998. Phytoplankton selection by mussels, and diarrhetic shellfish poisoning. Marine Biology, 131(1): 103–111, https://doi.org/10.1007/s002270050301.
Ward J E, Shumway S E. 2004. Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. Journal of Experimental Marine Biology and Ecology, 300(1–2): 83–130, https://doi.org/10.1016/j.jembe.2004.03.002.
Wetz M S, Lewitus A J, Koepfler E T, Hayes K C. 2002. Impact of the eastern oyster Crassostrea virginica on microbial community structure in a salt marsh estuary. Aquatic Microbial Ecology, 28(1): 87–97, https://doi.org/10.3354/ame028087.
Zapata M, Rodriguez F, Garrido J L. 2000. Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Marine Ecology Progress Series, 195: 29–45, https://doi.org/10.3354/meps195029.
Zhang F S, He Y C, Liu X S, Ma J H, Li S Y, Qi L G. 1991. Introduction, spat-rearing and experimental culture of bay scallop, Argopecten irradians Lamarck. Chinese Journal of Oceanology and Limnology, 9(2): 123–131, https://doi.org/10.1007/BF02850671.
Zhang J H, Hansen P K, Fang J G, Wang W, Jiang Z J. 2009. Assessment of the local environmental impact of intensive marine shellfish and seaweed farming — application of the MOM system in the Sungo Bay, China. Aquaculture, 287(3–4): 304–310, https://doi.org/10.1016/j.aquaculture.2008.10.008.
Zhang Q C, Qiu L M, Yu R C, Kong F Z, Wang Y F, Yan T, Gobler C J, Zhou M J. 2012. Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China. Harmful Algae, 19: 117–124, https://doi.org/10.1016/j.hal.2012.06.007.
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The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supported by the Qingdao National Laboratory for Marine Science and Technology Program (No. 2016ASKJ02), the Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (No. 20603022018002), and the National Natural Science Foundation of China (Nos. 41676103, 41476098)
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Jiang, T., Wang, L., Zhang, F. et al. Selective feeding of bay scallop Argopecten irradians on phytoplankton community revealed by HPLC analysis of phytopigments in Bohai Sea, China. J. Ocean. Limnol. 37, 1746–1755 (2019). https://doi.org/10.1007/s00343-019-8280-0
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DOI: https://doi.org/10.1007/s00343-019-8280-0