Abstract
Two common live feeds, the Brachionus plicatilis species complex SS-type and L-type were used to assess whether there were any differences in protein hydrolysis and digestive trypsin activity in first feeding Japanese flounder. There were no significant differences in hydrolysis activity at 2, 3 and 7 days after hatching (DAH). At 5 DAH, hydrolysis activity was significantly higher in larvae fed SS-type (p < 0.05) at 50 kDa in 1.5- and 3-h incubation whereas L-type treatment had not completely hydrolyzed the proteins after 3 h at the same molecular weight. Larvae fed SS-type had significantly higher (p < 0.05) trypsin activity at 3, 5, 6, 7 DAH. Contribution of live prey to trypsin fraction in larvae showed significantly higher (p < 0.05) fraction for SS-type at 5 DAH (2.18 ± 0.44%) and 6 DAH (2.04 ± 0.29%) and the effect of exogenous trypsin from live prey was relatively low when compared to the total trypsin activity in larvae. This study discusses the differences in ability to digest proteins in Japanese flounder when fed different rotifer morphotypes and highlights the adaptability of this species to alternative rotifer morphotypes during its early developmental stages.
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References
Akazawa A, Sakakura Y, Hagiwara A (2008) Feeding selectivity of marine fish larvae, Verasper variegatus, Seriola quinqueradiata, Platycephalus sp. on different sizes and shape of three rotifer strains. Nippin Suisan Gakkaishi 74:380–388 (in Japanese with English abstract)
Bolasina S, Pérez A, Yamashita Y (2006) Digestive enzymes activity during ontogenetic development and effect of starvation in Japanese flounder, Paralichthys olivaceus. Aquaculture 252:503–515
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Busch A (1996) Transition from endogenous to exogenous nutrition: larval size parameters determining the start of external feeding and size of prey ingested by Ruegen spring herring Clupea harengus. Mar Ecol Prog Ser 130:39–46
Cahu CL, Zambonino Infante JL (1994) Early weaning of sea bass (Dicentrarchus labrax) larvae with a compound diet; effect on digestive enzymes. Comp Biochem Physiol A 109:213–222
Cahu C, Rønnestad I, Grangler V, Zambonino I (2004) Expression and activities of pancreatic enzymes in developing sea bass larvae (Dicentrarchys labrax) in relation to intact and hydrolyzed dietary protein; involvement of cholecystokinin. Aquaculture 238:295–308
Cara JB, Moyano FJ, Cardenas S, Fernandez-Diaz C, Yufera M (2003) Assessment of digestive enzyme activities during larval development of white bream. J Fish Biol 63:48–58
Dabrowski K (1979) The role of proteolytic enzymes in fish digestion. In: Styczunska-Jurewivcsk E et al (eds) Cultivation of fish fry and its live food. European Mariculture Society, Bredene, pp 107–126
Dabrowski K (1984) The feeding of fish larvae: present (state of the art) and perspective. Reprod Nutr Dev 24:807–833
Danesi EDG, Rangel CO, Carvalho JCM, Sato S (2002) An investigation of effect of replacing nitrate by urea in the growth and production of chlorophyll by Spirulina platensis. Biomass Bioenerg 23:261–269
Dhert P, Rombaut G, Suantika G, Sorgeloos P (2001) Advancement of rotifer culture and manipulation techniques in Europe. Aquaculture 200:129–146
Diaz M, Moyano FJ, Garcia-Carreno FL, Alarcon FJ, Sarasquete MC (1997) Substrate-SDS-PAGE determination of protease activity through larval development in sea bream. Aquact Int 5:461–471
Engrola S, Conceição LEC, Dias L, Pereira R, Ribeiro L, Dinis MT (2007) Improving weaning strategies for Senegalese sole: effects of body weight and digestive capacity. Aquac Res 38:696–707
Fu Y, Hirayama K, Natsukari Y (1991) Morphological differences between two types of the rotifer Brachionus plicatilis O.F Müllér. J Exp Mar Biol Ecol 151:29–41
Fukuhara O (1986) Morphological and functional development of Japanese flounder in early life stage. Nippon Suisan Gakkaishi 52:81–91
Gawlicka A, Parent B, Horn MH, Ross N, Opstad I, Torrissen OJ (2000) Activity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquaculture 184:303–314
Gisbert E, Conklin DB, Piedrahita RH (2004) Effects of delayed first feeding on the nutritional condition and mortality of California halibut larvae. J Fish Biol 64:116–132
Hagiwara A, Gallardo WG, Assavaaree M, Kotani T, De Araujo AB (2001) Live food production in Japan; recent progress and future aspects. Aquaculture 200:11–127
Hagiwara A, Suga K, Akazawa A, Kotani T, Sakakura Y (2007) Development of rotifer strains with useful traits for rearing fish larvae. Aquaculture 268:44–52
Hagiwara A, Wullur S, Marcial HS, Narisato H, Yoshitaka S (2014) Euryhaline rotifer Proalis similis as initial food for rearing fish with small mouth. Aquaculture 432:470–474
Hara K, Arano H, Ishihara T (1984a) Purification of alkaline protease of the rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 50:1605–1609
Hara K, Arano H, Ishihara T (1984b) Some enzymatic properties of alkaline proteases of the rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 50:1611–1616
Heming TA, McInerney JE, Alderdice DF (1982) Effect of temperature on initial feeding in alevins of shinook salmon (Oncorhyncus tshawytscha). Can J Fish Aquat Sci 39:1154–1562
Howell BR, Yamashita R (2005) Aquaculture and stock enhancement. In: Gibson R (ed) Flatfishes. Biology and Exploitation. Blackwell Publishing, Oxford, pp 347–371
Ikewaki Y, Tanaka M (1993) Feeding habits of Japanese flounder (Paralichthys olivaceus) larvae in the western part of Wakasa Bay, the Japan Sea. Nippon Suisan Gakkaishi 59:951–956
Kolkovski S, Tandler A, Kissil GW, Gertler A (1993) The effect of dietary exogenous digestive enzymes on ingestion, assimilation, growth and survival of gilthead seabream (Sparus aurata, Sparidae, Linnaeus) larvae. Fish Physiol Biochem 12:203–209
Kotani T, Hagiwara A, Snell TW (1997) Genetic variations among marine rotifer strains and function of mate recognition pheromone (MRP). Hydrobiologia 358:105–112
Kotani T, Hagiwara A, Snell TW, Serra M (2005) Euryhaline Brachionus strains (Rotifera) from tropical habitats: morphology and allozyme patterns. Hydrobiologia 546:161–167
Kotani T, Genka T, Fushimi H, Hayashi M, Dierckens K, Sorgeloos P (2009) Effect of cultivation methods on nutritional enrichment of euryhaline rotifer Brachionus plicatilis. Fish Sci 75:975–984
Kotani T, Haraguchi T, Yamazaki Y, Doi T, Matsui H, Yokoyama S, Ishikawa M, Koshio S (2017) Effect of the duration of nutritional enrichment on the fatty acid composition of commonly used rotifers Brachionus plicatilis sp. complex and larviculture performance of red sea bream Pagrus major. Aquacult Sci 65:133–144
Kühle K, Kleinow W (1990) Glycosidases in Brachionus plicatilis (Rotifera). Comp Biochem Physiol B 95:393–402
Kurokawa T, Suzuki T (1996) Formation of the diffuse pancreas and the development of digestive enzyme synthesis in larvae of the Japanese flounder Paralichthys olivaceus. Aquaculture 141:267–276
Kurokawa T, Suzuki T (1998) Development of intestinal brush border aminopeptidase in the larval Japanese flounder Paralichthys olivaceus. Aquaculture 162:113–124
Kurokawa T, Suzuki T, Andoh T (2000) Development of cholecystokinin and pancreatic polypeptide endocrine systems during larval stage of Japanese flounder, Paralichthys olivaceus. Gen Comp Endocrinol 120:8–16
Lauff M, Hoffer R (1984) Proteolytic enzymes in fish development and the importance of dietary enzymes. Aquaculture 37:335–346
Lazo JP, Holt GJ, Arnold CR (2000) Ontogeny of pancreatic enzymes in larval red drum Scianops ocellatus. Aquac Nutr 6:183–192
Ma H, Cahu C, Zambonino J, Yu H, Duan Q, Le Gall MM, Mai K (2005) Activities of selected digestive enzymes during larval development of large yellow croaker (Pseudosciaena crocea). Aquaculture 245:239–248
Martinez I, Moyano FJ, Fernandez-Diaz C, Yufera M (1999) Digestive enzyme activity during larval development of the Senegal sole (Solea senegalensis). Fish Physiol Biochem 21:317–323
Melianawati R, Pratiwi R, Puniawati N, Astuti P (2015) The effect of various kinds of live feeds to digestive enzymes activity of coral trout Plectropomus leopardus (Lacepede, 1802) larvae. Int J Fish Aquat Stud 3:83–88
Mills S, Alcántara-Rodríguez AJ, Ciros-Pérez J, Gómez A, Hagiwara A, Galindo KH, Jersabek CD, Malekzadeh-Viayeh R, Leasi F, Lee JS, Mark Welch DB, Papakostas S, Riss S, Segers H, Serra M, Shiel R, Smolak R, Snell TW, Stelzer CP, Tang CQ, Wallace RL, Fontaneto D, Walsh EJ (2016) Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia 796:39–58
Moteki M, Ishikawa T, Fushimi H (2002) Changes in feeding function inferred from osteological development in the early stage larvae of the Japanese flounder, Paralichthys olivaceus, reared in the laboratory. Aquac Sci 50:285–294
Moyano FJ, Diaz M, Alarcon FJ, Sarasquete MC (1996) Characterization of digestive enzyme activity during larval development of gilthead seabream (Sparus aurata). Fish Physiol Biochem 15:121–130
Oozeki Y, Bailey KM (1995) Ontogenetic development of digestive enzyme activities in larval walleye pollock, Theragra chalcogramma. Mar Biol 122:177–186
Park HG, Puvanendran V, Kellet A, Parrich CC, Brown JA (2006) Effect of enriched rotifers on growth, survival, and composition of larval Atlantic cod (Gadus morhua). J Mar Sci 63:285–295
Pedersen BH, Nilssen EM, Hjelmeland K (1987) Variations in the content of trypsin and trysinogen in larval herring (Clupea harengus) digesting copepod nauplii. Mar Biol 94:171–181
Perez-Casanova JC, Murray HM, Gallant JW, Ross NW, Douglas SE, Johnson SC (2006) Development of the digestive capacity in larvae of haddock (Melanogrammus aeglefinus) and Atlantic cod (Gadus morhua). Aquaculture 251:337–401
Rice JA, Crowder LB, Binkowski FB (1987) Evaluating potential sources of mortality for larval bloater (Corengonus hoyi): starvation and vulnerability to predation. Can J Fish Aquat Sci 44:467–472
Rønnestad I, Yüfera M, Ueberschar B, Ribeiro L, Sæle Ø, Boglione C (2013) Feeding behavior and digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Rev Aquac 5:59–98
Rungruanksak-Torrisen K, Moss R, Andresen LH, Berg A, Waagbø R (2006) Different expressions of trypsin and chymotrypsin in relation to growth in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 32:7–23
Russo T, Boglione C, De Marzi P, Cataudella S (2009) Feeding preferences of the dusky grouper (Epinephelus marginatus, Lowe 1834) larvae reared in semi-intensive conditions: a contribution addressing the domestication of this species. Aquaculture 289:289–296
Segers H (1995) Nomenclature consequences of some recent studies on Brachionus plicatilis (Rotifera, Brachionidae). Hydrobiologia 313(314):121–122
Soletto D, Binaghi L, Lodi A, Carvalho JCM, Converti A (2005) Batch and fed-batch cultivations of Spirulina platensis using ammonium sulphate and urea as nitrogen sources. Aquaculture 243:217–224
Srivastava AS, Kurokawa T, Suzuki T (2002) mRNA expression of pancreatic enzyme precursors and estimation of protein digestibility in first feeding larvae of the Japanese flounder, Paralichthys olivaceus. Comp Biochem Phys A 132:629–635
Sunde J, Taranger GL, Rungruangsak-Torrissen K (2001) Digestive protease activities and free amino acids in white muscle as indicators for feed conversion efficiency and growth rate in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 25:335–345
Takahashi Y (1985) Morphological and behavioural changes with growth in reared larvae and juveniles of a flounder, Paralichthys olivaceus. Aquac Sci 33:43–52 (in Japanese with English abstract)
Tanaka Y, Sakakura Y, Chuda H, Hagiwara A, Yasumoto S (2005) Food selectivity of seven-band grouper Epinephelus septemfasciatus larvae fed different sizes of rotifers. Nippon Suisan Gakkaishi 71:911–916 (in Japanese with English abstract)
Taylor WW, Freeberg MH (1984) Effects of food abundance on larval lake whitefish, Coregonus lupeaformis Mitchell, growth and survival. J Fish Biol 25:733–741
Tomoda T, Koiso M, Kuwada H, Chern JN, Takeuchi T (2004) Dietary value of marine rotifer Brachionus plicatilis in different population growth stages for larval red sea bream Pagrus major. Nippon Suisan Gakkaishi 70:573–582 (in Japanese with English abstract)
Torre P, Sassano CEN, Sato S, Converti A, Gioielli LA, Carvalho JCM (2003) Fed-batch addition of urea for Spirulina platensis cultivation thermodynamics and material and energy balances. Enzyme Microb Technol 33:698–707
Ueberschär B (1988) Determination of the nutritional condition of individual marine fish larvae by analyzing their proteolytic enzyme activities with a highly sensitive fluorescence technique. Meeresforschung 32:144–154
Ueberschär B (1995) The use of tryptic enzyme activity measurement as a nutritional condition index. Laboratory calibration data and field application. ICES Mar Sci Symp 201:119–129
Watanabe T, Kitajima C, Arakawa T, Fukusho K, Fujita S (1978) Nutritional quality of rotifer Brachionus plicatilis as a living feed from the viewpoint of essential fatty acids for fish. Nippon Suisan Gakkaishi 44:1109–1114 (in Japanese with English abstract)
Wethmar C, Kleinow W (1993) Characterization of proteolytic activities stimulated by SDS or urea and two-dimensional gel electrophoresis of proteins from Brachionus plicatilis (Rotifera). Comp Biochem Phys B 106:349–358
Wullur S, Sakakura Y, Hagiwara A (2009) The minute monogonont rotifer Proalis similis de Beauchamp: culture and feeding to small mouth marine fish larvae. Aquaculture 293:62–67
Yamashita Y, Yamada H (1999) Release strategy for Japanese flounder fry in stock enhancement programmes. In: Howell BH et al (eds) Marine Enhancement and Sea Ranching. Fishing News Books, Blackwell Science, pp 191–204
Yoseda K, Asami K, Fukumoto M, Takaira S, Kurokawa Y, Kawa S (2003) Effects of two types of rotifer on first-feeding success and early survival in coral trout Plectropomus leopardus larvae. Aquac Sci 51:101–108
Yoshimura K, Usuki K, Yoshimatsu T, Kitajima C, Hagiwara A (1997) Recent development of a high density mass culture system for the rotifer Brachionus rotundiformis Tschugunoff. Hydrobiologia 358:139–144
Zambonino Infante JL, Cahu C (1994) Development and response to a diet change of some digestive enzymes in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem 12:399–408
Zambonino Infante JL, Cahu C (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Phys C 130:477–487
Acknowledgements
We would like to acknowledge the assistance from the members of the Laboratory of Larval Rearing Management and the Laboratory of Marine Glycobiology at the Faculty of Fisheries, Kagoshima University. We would also like to thank Professor Atsushi Hagiwara of Nagasaki University for providing the rotifer stock population to conduct this study and also Professor Manabu Ishikawa, Mr. Oishi, and Mr. Serge Dossou of Kagoshima University in assisting with the technical aspects of this study. We would also like to acknowledge the Government of Japan and the Ministry of Education, Culture, Sports, Science and Technology (MEXT) under the Monbukakusho Scholarship for sponsoring the first author to conduct his research at Kagoshima University.
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Waqalevu, V., Honda, A., Matsui, H. et al. Proteolytic digestive enzyme response in Japanese flounder larvae Paralichthys olivaceus fed two types of rotifers Brachionus plicatilis species complex. Fish Sci 84, 1037–1049 (2018). https://doi.org/10.1007/s12562-018-1241-2
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DOI: https://doi.org/10.1007/s12562-018-1241-2