Abstract
Cichlasoma dimerus is a neotropical cichlid that has been used as a biological model for neuroendocrinology studies. However, its culture is problematic in terms of larval feeding to allow having enough fry quantity and quality. Larviculture requires full knowledge about the digestive system and nutrition; therefore, this study was intended to assess the digestive enzymes' changes at different ages during the early ontogeny. Acid protease activity was detectable from the first day after hatching (dah), increasing to its maximum peaks on 9 dah. In contrast, alkaline proteases had low activity in the first days of life but reached their maximum activity on 17 dah. Chymotrypsin, L-aminopeptidase, and carboxypeptidase A activities increased at 6 dah, while trypsin activity was first detected on 13 dah and reached its maximum activity on 17 dah. Lipase and α-amylase activity were detectable at low levels in the first days of life, but the activity fluctuated and reaching its maximum activity at 21 dah. Alkaline phosphatase continued to oscillate and had two maximum activity peaks, the first at 6 dah and the second at 19 dah. Zymograms of alkaline proteases on day 6 dah six revealed four activity bands with molecular weights from 16.1 to 77.7 kDa. On 13 dah, two more activity bands of 24.4 and 121.9 kDa were detected, having a total of six proteases. The enzymatic activity analyzes indicate the digestive system shows the low activity of some enzymes in the first days after hatching, registering significant increases on 6 dah and the maximum peaks of activities around at 17 dah. Therefore, we recommend replacing live food with dry feed and only providing dry feed after day 17 dah.
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References
Alarcón FJ, Martínez MI (1998) Fisiología de la digestión en larvas de peces marinos y sus aplicaciones al cultivo larvario en masa. Aquatic 5:1–12
Albertson RC, Cresko W, Detrich HW, Postlethwait JH (2009) Evolutionary mutant models for human disease. Trends Genet 25(2):74–81. https://doi.org/10.1016/j.tig.2008.11.006
Alonso F, Cánepa M, Guimarães MR, Pandolfi M (2011) Social and reproductive physiology and behavior of the Neotropical cichlid fish Cichlasoma dimerus under laboratory conditions. Neotrop Ichthyol 9(3):559–570. https://doi.org/10.1590/S1679-62252011005000025
Anson ML (1938) The estimation of pepsin, trypsin, papain and cathepsin with hemoglobin. J Gen Physiol 22:79–89. https://doi.org/10.1085/jgp.22.1.79
Applebaum SL (2001) Fish Physiol Biochem 25(4):291–300. https://doi.org/10.1023/a:1023202219919
Asgari R, Rafiee G, Eagderi S, Noori F, Agh N, Poorbagher H, Gisbert E (2013) Ontogeny of the digestive enzyme activities in hatchery produced Beluga (Huso huso). Aquaculture 416–417:33–40. https://doi.org/10.1016/j.aquaculture.2013.08.014
Belitz HD, Grosch W, Schieberle P (2009) Amino acids, peptides, proteins. Food Chemistry. Springer, Berlin, pp 12–15
Bergmeyer HV (1974) Phosphatases methods of enzymatic analysis, vol 2. Academic Press, New York
Blanco A, Planas M, Moyano FJ (2015) Ontogeny of digestive enzymatic capacities in juvenile seahorses Hippocampus guttulatusfed on different live diets. Aquac Res 47(11):3558–3569. https://doi.org/10.1111/are.12806
Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Cai G, Mo C, Huang L, Li J, Wang Y (2015) Characterization of the Two CART Genes (CART1 and CART2) in Chickens (Gallus gallus). PLoS ONE 10(5):e0127107. https://doi.org/10.1371/journal.pone.0127107
Cánepa MM, Pandolfi M, Maggese MC, Vissio PG (2006) Involvement of somatolactin in background adaptation of the cichlid fish Cichlasoma dimerus. J Exp Zool A Comp Exp Biol 305(5):410–419. https://doi.org/10.1002/jez.a.273
Cánepa M, Pozzi A, Astola A, Maggese MC, Vissio P (2008) Effect of salmon melanin-concentrating hormone and mammalian gonadotrophin-releasing hormone on somatolactin release in pituitary culture of Cichlasoma dimerus. Cell Tissue Res 333(1):49–59. https://doi.org/10.1007/s00441-008-0622-8
Cánepa MM, Zhu Y, Fossati M, Stiller JW, Vissio PG (2012) Cloning, phylogenetic analysis and expression of somatolactin and its receptor in Cichlasoma dimerus: their role in long-term background color acclimation. Gen Comp Endocrinol 176(1):52–61. https://doi.org/10.1016/j.ygcen.2011.12.023
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. https://doi.org/10.1046/j.1095-8649.2003.00120.x
Cara JB, Moyano FJ, Zambonino-Infante JL, Fauvel C (2007a) Trypsin and chymotrypsin as indicators of nutritional status of post-weaned sea bass larvae. J Fish Biol 70:1798–1808. https://doi.org/10.1111/j.1095-8649.2007.01457.x
Cara JB, Moyano FJ, Zambonino JL, Alarcón FJ (2007b) The whole amino acid profile as indicator of the nutritional condition in cultured marine fish larvae. Aquac Nutr 13:94–103. https://doi.org/10.1111/j.1365-2095.2007.00459.x
Casciotta JR, Almirón AE, Bechara J (2005) Peces del Iberá Hábitat y Diversidad. UNDP, Fundación Ecos, UNLP, UNNE, Glafikar, La Plata
Castro-Ruiz D, Mozanzadeh MT, Fernández-Méndez C, Andree KB, García-Dávila C, Cahu C, Gisbert E, Darias MJ (2019) Ontogeny of the digestive enzyme activity of the Amazonian pimelodid catfish Pseudoplatystoma punctifer (Castelnau, 1855). Aquaculture 504:210–218. https://doi.org/10.1016/j.aquaculture.2019.01.059
Chakrabarti R, Mansingh Rathore R, Mittal P, Kumar S (2006) Functional changes in digestive enzymes and characterization of proteases of silver carp (♂) and bighead carp (♀) hybrid, during early ontogeny. Aquaculture 253(1–4):694–702. https://doi.org/10.1016/j.aquaculture.2005.08.018
Chong AS, Hashim R, Chow-Yang L, Ali AB (2002) Partial characterization and activities of proteases from the digestive tract of discus fish (Symphysodon aequifasciata). Aquaculture 203(3–4):321–333. https://doi.org/10.1016/s0044-8486(01)00630-5
Córdova-Montejo M, Álvarez-González CA, López LM, True CD, Frías-Quintana CA, Galaviz MA (2019) Changes of digestive enzymes in totoaba (Totoaba macdonaldi Gilbert, 1890) during early ontogeny. Lat Am J Aquat Res 47(1):102–113. https://doi.org/10.3856/vol47-issue1-fulltext-11
Cuvier-Péres A, Kestemont P (2002) Development of some digestive enzymes in Eurasian perch larvae Perca fluviatilis. Fish Physiol Biochem 24(4):279–285. https://doi.org/10.1023/a:1015033300526
Da Cuña RH, Rey Vázquez G, Dorelle L, Rodríguez EM, Guimarães Moreira R, Lo Nostro FL (2016) Mechanism of action of endosulfan as disruptor of gonadal steroidogenesis in the cichlid fish Cichlasoma dimerus. Comp Biochem Physiol C Toxicol Pharmacol 187:74–80. https://doi.org/10.1016/j.cbpc.2016.05.008
David-Ruales CA, Machado-Fracalossi D, Vásquez-Torres W (2018) Desenvolvimento inicial em larvas de peixes, chave para iniciar a alimentação exógena. Revista Lasallista de Investigación 15:180–194. https://doi.org/10.22507/rli.v15n1a10
De Almeida LC, Lundstedt LM, Moraes G (2006) Digestive enzyme responses of tambaqui (Colossoma macropomum) fed on different levels of protein and lipid. Aquac Nut 12:443–450. https://doi.org/10.1111/j.1365-2095.2006.00446.x
Delgadín T, Pérez Sirkin D, Karp P, Fossati M, Vissio PG (2014) Evaluation of somatic growth and spawning/body size relationship between males and females of the cichlid fish Cichlasoma dimerus. Belg J Zool 144(2):102–111
Delgadin TH, Simó I, Pérez Sirkin DI, Di Yorio MP, Arranz SE, Vissio PG (2018) Cichlasoma dimerus responds to refeeding with a partial compensatory growth associated with an increment of the feed conversion efficiency and a rapid recovery of GH/IGFs axis. Aquac Nut 24(4):1234–1243. https://doi.org/10.1111/anu.12661
DelMar EG, Largman C, Broderick JW, Geokas MC (1979) A sensitive new substrate for chymotrypsin. Anal Biochem 99:316–320. https://doi.org/10.1016/S0003-2697(79)80013-5
Di Yorio MP, Pérez Sirkin DI, Delgadin TH, Shimizu A, Tsutsui K, Somoza GM, Vissio PG (2017) Gonadotrophin-inhibitory hormone in the cichlid fish Cichlasoma dimerus: structure, brain distribution and differential effects on the secretion of gonadotrophins and growth hormone. J Neuroendocrinol 28(5). https://doi.org/10.1111/jne.12377
Di Yorio MP, Sallemi JE, Toledo Solís FJ, Pérez Sirkin DI, Delgadin TH, Tsutsui K, Vissio PG (2018) Ontogeny of gonadotropin-inhibitory hormone (GnIH) in the cichlid fish Cichlasoma dimerus. J Neuroendocrinol 30:e12608. https://doi.org/10.1111/jne.12608
Dimes LE, Haard NF (1994) Estimation of protein digestibility-I. Development of an in vitro method for estimating protein digestibility in salmonids (Salmo gairdneri). Camp Eiochem Physiol 108(2–3):349–362. https://doi.org/10.1016/0300-9629(94)90106-6
Dorelle LS, Da Cuña RH, Rey Vázquez G, Höcht C, Shimizu A, Genovese G, Lo Nostro FL (2017) The SSRI fluoxetine exhibits mild effects on the reproductive axis in the cichlid fish Cichlasoma dimerus (Teleostei, Cichliformes). Chemosphere 171:370–378. https://doi.org/10.1016/j.chemosphere.2016.11.141
Erlanger B, Kokowsky N, Cohen W (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95:271–278. https://doi.org/10.1016/0003-9861(61)90145-X
Espoìsito TS, Marcuschi M, Amaral IPG, Carvalho LB, Bezerra RS (2010) Trypsin from the Processing Waste of the Lane Snapper (Lutjanus synagris) and Its Compatibility with Oxidants, Surfactants and Commercial Detergents. J Agric Food Chem 58(10):6433–6439. https://doi.org/10.1021/jf100111e
Folk JE, Schirmer EW (1963) The porcine pancreatic carboxypeptidase a system. J Biol Chem 238:3884–3894
Frías-Quintana CA, Márquez-Couturier G, Alvarez-González CA, Tovar-Ramírez D, Nolasco-Soria H, Galaviz-Espinosa MA, Martínez-García R, Camarillo-Coop S, Martínez-Yañez R, Gisbert E (2015) Development of digestive tract and enzyme activities during the early ontogeny of the tropical gar Atractosteus tropicus. Fish Physiol Biochem 41:1075–1091. https://doi.org/10.1007/s10695-015-0070-9
Frías-Quintana CA, Álvarez-González CA, Guerrero-Zárate R, Valverde-Chavarría S, Ulloa-Rojas JB (2019) Changes in digestive enzymes activities during the initial ontogeny of wolf cichlid, Parachromis dovii (Perciformes: Cichlidae). Neotrop Ichthyol 17(1):e180161. https://doi.org/10.1590/1982-0224-20180161
García-Carreño FL, Dimes LE, Haard NF (1993) Substrate-gel electrophoresis for composition and molecular weight of proteinases or proteinaceous proteinase inhibitors. Anal Biochem 214:65–69. https://doi.org/10.1006/abio.1993.1457
García-Gasca A, Galaviz MA, Gutiérrez JN, García-Ortega A (2006) Development of the digestive tract, trypsin activity and gene expression in eggs and larvae of the bullseye puffer fish Sphoeroides annulatus. Aquaculture 251(2–4):366–376. https://doi.org/10.1016/j.aquaculture.2005.05.029
Ghosh SK, Chakrabarti P (2016) Comparative studies on histology and histochemistry of pancreas between Labeo calbasu (Hamilton, 1822) and Mystus gulio (Hamilton, 1822). Iran J Ichthyol 3(4):251–265. https://doi.org/10.7508/iji.2016.02.015
Gioda CR, Pretto A, Freitas CS, Leitemperger J, Loro VL, Lazzari R, Lissner LA, Baldisserotto B, Salbego J (2017) Different feeding habits influence the activity of digestive enzymes in freshwater fish. Ciência Rural 47(3). https://doi.org/10.1590/0103-8478cr20160113
Gisbert E, Morais S, Moyano FJ (2013) Feeding and digestion. In: Qin JG (ed) Larval fish aquaculture. Nova Publishers, New York, pp 73–124
Gisbert E, Giménez G, Fernández I, Kotzamanis Y, Estévez A (2009) Development of digestive enzymes in common dentex Dentex dentex during early ontogeny. Aquaculture 287(3–4):381–387. https://doi.org/10.1016/j.aquaculture.2008.10.039
Guerrera MC, De Pasquale F, Muglia U, Caruso G (2015) Digestive enzymatic activity during ontogenetic development in zebrafish (Danio rerio). J Exp Zool Part B 324(8):699–706. https://doi.org/10.1002/jez.b.22658
Hamid SNIN, Abdullah MF, Zakaria Z, Yusof SJHM, Abdullah R (2016) Formulation of Fish Feed with Optimum Protein-bound Lysine for African Catfish (Clarias Gariepinus) Fingerlings. Procedia Eng 148:361–369. https://doi.org/10.1016/j.proeng.2016.06.468
Hamre K, Yúfera M, Rønnestad I, Boglione C, Conceição LEC, Izquierdo M (2013) Fish larval nutrition and feed formulation: knowledge gaps and bottlenecks for advances in larval rearing. Rev Aquac 5:S26–S58. https://doi.org/10.1111/j.1753-5131.2012.01086.x
He T, Xiao Z, Liu Q, Ma D, Xu S, Xiao Y, Li J (2012) Ontogeny of the digestive tract and enzymes in rock bream Oplegnathus fasciatus (Temminck et Schlegel 1844) larvae. Fish Physiol Biochem 38:297–308. https://doi.org/10.1007/s10695-011-9507-y
Heckel J (1840) Johann Natterer’s neue Flussfische Brasilien’s nach den Beobachtungen und Mittheilungen des Entdeckers beschrieben. (Erste Abtheilung, die Labroiden.) Annalen des Wiener Museums der Naturgeschichte 2:327–470. https://doi.org/10.5962/bhl.title.101457
Hekimoğlu MA, Suzer C, Saka S, Firat K (2014) Enzymatic characteristics and growth parameters of ornamental koi carp (Cyprinus carpio var. koi) larvae fed by Artemia nauplii and cysts. Turkish J Fish Aquat Sci 14:125–133. https://doi.org/10.4194/1303-2712-v14_1_14
Hernandez DR, Santinon JJ, Sanchez S, Domitrovic HA (2014) Estudio histologico e histoquimico de la organogenesis del tubo digestivo de Rhamdia quelen en condiciones de larvicultura intensiva. Lat Am J Aquat Res 42(5):1136–1147. https://doi.org/10.3856/vol42-issue5-fulltext-17
Hoehne-Reitan K, Kjorsvik E, Gjellesvik DR (2001) Development of bile salt-dependent lipase in larval turbot. J Fish Biol 58(3):737–745. https://doi.org/10.1111/j.1095-8649.2001.tb00526.x
Horzmann KA, Freeman JL (2018) Making Waves: New Developments in Toxicology with the Zebrafish. Toxicol Sci 163(1):5–12. https://doi.org/10.1093/toxsci/kfy044
Igbokwe EC, Downe AER (1978) Electrophoretic and histochemical comparison of three strains of Aedes aegypti. Comp Biochem Physiol 60B:131–136
Jiménez-Martínez LD, Álvarez-González CA, Tovar-Ramírez D, Gaxiola G, Sánchez-Zamora A, Moyano FJ, Alarcón FJ, Márquez-Couturier G, Gisbert E, Contreras-Sánchez WM, Perales-García N, Arias-Rodríguez L, Indy JR, Páramo-Delgadillo S, Palomino-Albarrán IG (2012) Digestive enzyme activities during early ontogeny in common snook (Centropomus undecimalis). Fish Physiol Biochem 38:441–454. https://doi.org/10.1007/s10695-011-9525-9
Jonas E, Ragyanssszki M, Olah J, Boross L (1983) Proteolytic digestive enzymes of carnivorous (Silurus glanis L.), herbivorous (Hypophtlamichthys molitrix Val.) and omnivorous (Cyprinus carpio) fishes. Aquaculture 30:145–154
Kämpfer P, Rute I, Hans-Jürgen B, Poblete-Morales M, Kleinhagauer T, Glaeser SP, Avendaño-Herrera R (2016) Pseudoduganella danionis sp. nov., isolated from zebrafish (Danio rerio). Int J Syst Evol Microbiol 66(11). https://doi.org/10.1099/ijsem.0.001408
Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EHK (2008) Reconstruction of Zebrafish Early Embryonic Development by Scanned Light Sheet Microscopy. Science 14:1065–1069. https://doi.org/10.1126/science.1162493
Khoa TND, Waqalevu V, Honda A, Shiozaki K, Kotani T (2019) Early ontogenetic development, digestive enzymatic activity and gene expression in red sea bream (Pagrus major). Aquaculture 512:734283. https://doi.org/10.1016/j.aquaculture.2019.734283
Kim BG, Divakaran S, Brown CL, Ostrowski AC (2001) Comparative digestive enzyme ontogeny in two larval fishes: Pacific threadfin (Polydactylus sexfilis) and bluefin trevally (Caranx melampygus). Fish Physiol Biochem 24:225–241. https://doi.org/10.1023/A:1014054431627
Kim KH, Horn MH, Sosa AE, German DP (2014) Sequence and expression of an α-amylase gene in four related species of prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and species-level effects. J Comp Physiol Biochem Syst Environ Physiol 184B:221–234. https://doi.org/10.1007/s00360-013-0780-1
Kjørsvik E, Hoehne-Reitan K, Reitan KI (2003) Egg and larval quality criteria as predictive measures for juvenile production in turbot (Scophthalmus maximus L.). Aquaculture 227(1–4):9–20. https://doi.org/10.1016/s0044-8486(03)00492-7
Kunitz M (1947) Crystalline soybean trypsin inhibitor II General Properties. J Gen Physiol 30:291–310
Kurtovic I, Marshall SN, Zhao X, Simpson BK (2009) Lipases from Mammals and Fishes. Rev Fish Sci 17(1):18–40. https://doi.org/10.1080/10641260802031322
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
Lazo JP, Mendoza R, Holt GJ, Aguilera C, Arnold CR (2007) Characterization of digestive enzymes during larval development of red drum (Sciaenops ocellatus). Aquaculture 265(1–4):194–205. https://doi.org/10.1016/j.aquaculture.2007.01.043
Li P, Mai K, Trushenski J, Wu G (2008) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37(1):43–53. https://doi.org/10.1007/s00726-008-0171-1
Lilleeng E, Froystad MK, Ostby GC, Valen EC, Krogdahl A (2007) Effects of diets containing soybean meal on trypsin mRNA expression and activity in Atlantic salmon (Salmo salar L). Comp Biochem Physiol Part A 147(1):25–36. https://doi.org/10.1016/j.cbpa.2006.10.043
Liu BX, Du XL, Zhou LG, Hara K, Su WJ, Cao MJ (2008) Purification and characterization of a leucine aminopeptidase from the skeletal muscle of common carp (Cyprinus carpio). Food Chem 108(1):140–147. https://doi.org/10.1016/j.foodchem.2007.10.055
Liu W, Zhang X, Wang L (2010) Digestive enzyme and alkaline phosphatase activities during the early stages of Silurus soldatovi development. Zool Res 31(6):627–632. https://doi.org/10.3724/SP.J.1141.2010.06627
López-Ramírez G, Cuenca-Soria CA, Alvarez-González CA, Tovar-Ramírez D, Ortiz-Galindo JL, Perales-García N, Moyano FJ (2010) Development of digestive enzymes in larvae of Mayan cichlid Cichlasoma urophthalmus. Fish Physiol Biochem 37(1):197–208. https://doi.org/10.1007/s10695-010-9431-6
López-Vásquez K, Castro-Pérez CA, Val AL (2009) Digestive enzymes of eight Amazonian teleosts with different feeding habits. J Fish Biol 74(7):1620–1628. https://doi.org/10.1111/j.1095-8649.2009.02196.x
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(1–4):239–248. https://doi.org/10.1016/j.aquaculture.2004.11.032
Ma Z, Guo H, Zheng P, Wang L, Jiang S, Qin JG, Zhang D (2014) Ontogenetic development of digestive functionality in golden pompano Trachinotus ovatus (Linnaeus 1758). Fish Physiol Biochem 40(4):1157–1167. https://doi.org/10.1007/s10695-014-9912-0
Maraux S, Louvard D, Baratti J (1973) The aminopeptidase from hog-intestinal brush border. Biochem Biophys Acta 321:282–295. https://doi.org/10.1016/0005-2744(73)90083-1
Martínez-Cárdenas L, Álvarez-González C, Hernández-Almeida O, Frías-Quintana C, Ponce-Palafox J, Castillo-Vargasmachuca S (2017) Partial characterization of digestive proteases in the Green Cichlid Cichlasoma Beani. Fishes 2(1):4. https://doi.org/10.3390/fishes2010004
Maruska KP (2014) Social regulation of reproduction in male cichlid fishes. Gen Comp Endocrinol 207:2–12. https://doi.org/10.1016/j.ygcen.2014.04.038
Meijide FJ, Guerrero GA (2000) Embryonic and larval development of a substrate-brooding cichlid Cichlasoma dimerus (Heckel, 1840) under laboratory conditions. J Zool 252:481–493. https://doi.org/10.1111/j.1469-7998.2000.tb01231.x
Mente E, Solovyev MM, Vlahos N, Rotllant G, Gisbert E (2016) Digestive enzyme activity during initial ontogeny and after feeding diets with different protein sources in Zebra Cichlid Archocentrus Nigrofasciatus. J World Aquac Soc 48(5):831–848. https://doi.org/10.1111/jwas.12381
Moguel-Hernández I, Peña R, Nolasco-Soria H, Dumas S, Zavala-Leal I (2014) Development of digestive enzyme activity in spotted rose snapper, Lutjanus guttatus (Steindachner, 1869) larvae. Fish Physiol Biochem 40(3):839–848. https://doi.org/10.1007/s10695-013-9890-7
Mortensen AH, Camper SA (2016) Cocaine-and amphetamine regulated transcript (CART) peptide is expressed in precursor cells and somatotropes of the mouse pituitary gland. PLoS ONE 11(9):e0160068. https://doi.org/10.1371/journal.pone.0160068
Moyano FJ, Diaz M, Alarcon FJ, Sarasquete MC (1996) Characterization of digestive enzyme activity during larval development of gilthead sea bream (Sparus aurata). Fish Physiol Biochem 15:121–130. https://doi.org/10.1007/BF01875591
Moyano FJ, Barros AM, Ana P, Cañavate JP, Cárdenas S (2005) Evaluación de la ontogenia de enzimas digestivas en larvas de hurta, Pagrus auriga (Pisces: Sparidae). AquaTIC 22:39–47
Nabzdyk LP, Kuchibhotla S, Guthrie PH, Chun M, Auster ME, Nabzdyk CS, Deso S, Andersen ND, Gnardellis C, Logerfo FW, Veves A (2013) Expression of neuropeptides and cytokines in a rabbit model of diabetic neuroischemic wound healing. J Vas Surg 58(3):766–775. https://doi.org/10.1016/j.jvs.2012.11.095
Nayak J, Viswanathan NP, Ammu K, Mathew S (2003) Lipase activity in different tissues of four species of fish: rohu (Labeo rohita Hamilton), oil sardine (Sardinella longiceps Linnaeus), mullet (Liza subviridis Valenciennes) and Indian mackerel (Rastrelliger kanagurta Cuvier). J Sci Food Agric 83(11):1139–1142. https://doi.org/10.1002/jsfa.1515
O’Brien-Macdonald K, Brown J, Parrish C (2006) Growth, behavior, and digestive enzyme activity in larval Atlantic cod (Gadus morhua) in relation to rotifer lipid. J Mar Sci 63(2):275–284. https://doi.org/10.1016/j.icesjms.2005.11.017
Onumah EE, Wessels S, Wildenhayn N, Brummer B, Schwark GH (2010) Stocking density and photoperiod manipulation in relation to Estradiol profile to enhance spawning activity in female Nile Tilapia. Turk J Fish Aquat Sci 10:463–470. https://doi.org/10.4194/trjfas.2010.0404
Pandolfi M, Cánepa MM, Meijide FJ, Alonso F, Vázquez GR, Maggese MC (2009) Vissio PG (2009) Studies on the reproductive and developmental biology of Cichlasoma dimerus (Percifomes, Cichlidae). Biocell 33(1):1–18
Pereira MM, Machado EM, Gisbert E, Romagosa E (2019) Nile tilapia broodfish fed high-protein diets: digestive enzymes in eggs and larvae. Aquac Res 50(8):2181–2190. https://doi.org/10.1111/are.14098
Pérez-Sirkin DI, Cánepa MM, Fossati M, Fernandino JI, Delgadin T, Canosa LF, Somoza GM, Vissio PG (2012) Melanin concentrating hormone (MCH) is involved in the regulation of growth hormone in Cichlasoma dimerus (Cichlidae, Teleostei). Gen Comp Endocrinol 176(1):102–111. https://doi.org/10.1016/j.ygcen.2012.01.002
Pérez-Sirkin DI, Suzuki H, Cánepa MM, Vissio PG (2013) Orexin and neuropeptide Y: tissue specific expression and immunoreactivity in the hypothalamus and preoptic area of the cichlid fish Cichlasoma dimerus. Tissue Cell 45(6):452–459. https://doi.org/10.1016/j.tice.2013.09.001
Perlman RL (2016) Mouse models of human disease: an evolutionary perspective. Evol Med Public Health 1:170–176. https://doi.org/10.1093/emph/eow014
Pradhan PK, Jena J, Mitra G, Sood N, Gisbert E (2013) Ontogeny of the digestive enzymes in butter catfish Ompok bimaculatus (Bloch) larvae. Aquaculture 372–375:62–69. https://doi.org/10.1016/j.aquaculture.2012.10.024
Ramallo MR, Birba A, Honji RM, Morandini L, Moreira RG, Somoza GM, Pandolfi M (2015) A multidisciplinary study on social status and the relationship between inter-individual variation in hormone levels and agonistic behavior in a Neotropical cichlid fish. Horm Behav 69:139–151. https://doi.org/10.1016/j.yhbeh.2015.01.008
Ramallo MR, Honji RM, Birba A, Morandini L, Varela ML, Genovese G, Moreira RG, Somoza GM, Pandolfi M (2017) A game of two? Gene expression analysis of brain (cyp19a1b) and gonadal (cyp19a1a) aromatase in females of a Neotropical cichlid fish through the parental care period and removal of the offspring. Gen Comp Endocrinol 252:119–129. https://doi.org/10.1016/j.ygcen.2017.08.009
Rathore RM, Kumar S, Chakrabati R (2005) Digestive enzyme patterns and evaluation of protease classes in Catla catla (Family: Cyprinidae) during early developmental stages. Comp Biochem Physiol 142B:98–106. https://doi.org/10.1016/j.cbpc.2005.06.007
Robyt JF, Whelan WJ (1968) The amylase. In: Radley JA (ed) Starch and its derivates. Chapman and Hall, London, pp 430–497
Rønnestad I, Yúfera M, Ueberschär 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:S59–S98. https://doi.org/10.1111/raq.12010
Sáenz RM, Alarcón FJ, Martínez MI, Ruiz F, Díaz M, Moyano FJ (2005) Caracterización de las proteasas digestivas del lenguado senegalés Solea senegalensis Kaup (1858). Bol Inst Esp Oceanogr 21(1–4):95–104
Santos JF, Soares KLS, Assis CRD, Guerra CAM, Lemos D, Carvalho LB, Bezerra RS (2016) Digestive enzyme activity in the intestine of Nile tilapia (Oreochromis niloticus L.) under pond and cage farming systems. Fish Physiol Biochem 42(5):1259–1274. https://doi.org/10.1007/s10695-016-0215-5
Schartl M (2014) Beyond the zebrafish: diverse fish species for modeling human disease. Dis Mod Mech 7(2):181–192. https://doi.org/10.1242/dmm.012245
Shan XJ, Huang W, Cao L, Xiao ZZ, Dou SZ (2008) Ontogenetic development of digestive enzymes and effect of starvation in miiuy croaker Miichthys miiuy larvae. Fish Physiol Biochem 35(3):385–398. https://doi.org/10.1007/s10695-008-9263-9
Song SH, Jang WJ, Hwang J, Park B, Jang JH, Seo YH, Yang CH, Lee S, Jeong CH (2018) Transcriptome profiling of whisker follicles in methamphetamine self-administered rats. Sci Rep 8(1). https://doi.org/10.1038/s41598-018-29772-1
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 Physiol Part A 132(3):629–635. https://doi.org/10.1016/s1095-6433(02)00107-1
Staeck W, Linke H (1995) American Cichlids II. Large Cichlids. A Handbook for their Identification, Care and Breeding. Tetra-Verlag, Germany
Stewart AM, Braubach O, Spitsbergen J, Gerlai R, Kalueff AV (2014) Zebrafish models for translational neuroscience research: from tank to bedside. Trends Neurosci 37(5):264–278. https://doi.org/10.1016/j.tins.2014.02.011
Sveinsdóttir H, Thorarensen H, Gudmundsdóttir Á (2006) Involvement of trypsin and chymotrypsin activities in Atlantic cod (Gadus morhua) embryogenesis. Aquaculture 260(1–4):307–314. https://doi.org/10.1016/j.aquaculture.2006.06.009
Teles A, Salas-Leiva J, Alvarez-González CA, Tovar-Ramírez D (2018) Changes in digestive enzyme activities during early ontogeny of Seriola rivoliana. Fish Physiol Biochem 45:733–742. https://doi.org/10.1007/s10695-018-0598-6
Teles A, Salas-Leiva J, Alvarez-González CA, Gisbert E, Ibarra-Castro L, Urbiola JCP, Tovar-Ramírez D (2019) Histological study of the gastrointestinal tract in longfin yellowtail (Seriola rivoliana) larvae. Fish Physiol Biochem 43(6):1613–1628. https://doi.org/10.1007/s10695-017-0397-5
Tengjaroenkul B, Smith BJ, Smith SA, Chatreewongsin U (2002) Ontogenic development of the intestinal enzymes of cultured Nile tilapia Oreochromis niloticus L. Aquaculture 211(1–4):241–251. https://doi.org/10.1016/s0044-8486(01)00888-2
Tocher DR (2003) Metabolism and Functions of Lipids and Fatty Acids in Teleost Fish. Rev Fish Sci 11(2):107–184. https://doi.org/10.1080/713610925
Toledo-Solís FJ, Uscanga-Martínez A, Guerrero-Zárate R, Márquez-Couturier G, Martínez-García R, Camarillo-Coop S, Perales-García N, Rodríguez-Valencia W, Gómez-Gómez MA, Álvarez-González CA (2015) Changes on digestive enzymes during initial ontogeny in the three-spot cichlid Cichlasoma trimaculatum. Fish Physiol Biochem 41:267–279. https://doi.org/10.1007/s10695-014-0023-8
Ulloa PE, Medrano JF, Feijóo CG (2014) Zebrafish as animal model for aquaculture nutrition research. Front Genet 5:313. https://doi.org/10.3389/fgene.2014.00313
Uscanga-Martínez A, Perales-García N, Álvarez-González CA, Moyano FJ, Tovar-Ramírez D, Gisbert GE, Márquez-Couturier G, Contreras-Sánchez WM, Arias-Rodríguez L, Indy JR (2011) Changes in digestive enzyme activity during initial ontogeny of bay snook Petenia splendida. Fish Physiol Biochem 37:667–680. https://doi.org/10.1007/s10695-011-9467-2
Vaz RL, Outeiro TF, Ferreira JJ (2018) Zebrafish as an animal model for drug discovery in parkinson’s disease and other movement disorders: a systematic review. Front Neuro (9). https://doi.org/10.3389/fneur.2018.00347
Vendrell J, Querol E, Avilés FX (2000) Metallocarboxypeptidases and their protein inhibitors. Structure, function and biomedical properties. Biochim Biophys Acta 1477:284–298. https://doi.org/10.1016/s0167-4838(99)00280-0
Versaw W, Cuppett SL, Winters DD, Williams LE (1989) An improved colorimetric assay for bacterial lipase in nonfat dry milk. J Food Sci 54:232–254. https://doi.org/10.1111/j.1365-2621.1989.tb05159.x
Walter HE (1984) Proteinases: Methods with hemoglobin, casein and azocoll as substrates. In: Bergmeyern HJ (ed) Methods of enzymatic analysis, vol V. Verlag Chemie, Weinham, pp 270–277
Williams DE, Reisfeld RA (1964) Disc electrophoresis in polyacrylamide gels: extension to new conditions of pH and buffers. Ann N Y Acad Sci 121:373–381. https://doi.org/10.1111/j.1749-6632.1964.tb14210.x
Yúfera M, Moyano FJ, Martínez-Rodríguez G (2018) The digestive function in developing fish larvae and fry. From molecular gene expression to enzymatic activity. Emer Issues Fish Larvae Res 51–86. https://doi.org/10.1007/978-3-319-73244-2_3
Zambonino-Infante J, Cahu C (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol Part C 130(4):477–487. https://doi.org/10.1016/s1532-0456(01)00274-5
Zambonino Infante JL, Gisbert E, Sarasquete C, Navarro I, Gutierrez J, Cahu CL (2008) Ontogeny and physiology of the digestive system of marine fish larvae. In: Cyrino JEO, Bureau D, Kapoor BG (eds) Feeding and digestive functions of fish. Science Publishers, Inc., Enfield, pp 281–384
Acknowledgements
F.J T-S. acknowledges the National Council for Science and Technology (CONACYT, Mexico) for the post-doctoral fellowship No. 2019-000012-01EXTV-00292. This work was carried out with the collaboration of Red CYTED LARVAplus (117RT0521). Authors thanks Dr. Warren Burggren from University of North Texas for the professional native English-speaking review.
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This research was supported by Universidad de Buenos Aires (grant number: 20020160100110BA to PV), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) (PIP 2014–2016:11220130100501CO to PV).
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Francisco Javier Toledo-Solís, Andrea Guadalupe Hilerio-Ruiz, Tomás Delgadin and Daniela Pérez Sirkin. The first draft of the manuscript was written by Francisco Javier Toledo-Solís, Emyr Saul Peña-Marín, Rafael Martínez-García, Claudia Ivette Maytorena-Verdugo, María Paula Di Yorio, Paula Gabriela Vissio, Carlos Alfonso Álvarez-González and Miguel Angel Sáenz de Rodrigáñez and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Toledo-Solís, F.J., Hilerio-Ruiz, A.G., Delgadin, T. et al. Changes in digestive enzyme activities during the early ontogeny of the South American cichlid (Cichlasoma dimerus). Fish Physiol Biochem 47, 1211–1227 (2021). https://doi.org/10.1007/s10695-021-00976-z
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DOI: https://doi.org/10.1007/s10695-021-00976-z