Abstract
During the early ontogeny, the transition from endogenous (yolk protein) to exogenous feeding (artificial diets) represents a critical period linked to the undifferentiated digestive system, with low digestibility of food protein. The objectives of this work were to characterize the morphology of the early Nile tilapia (Oreochromis niloticus) developmental stages and determine the activity of alkaline and acid peptidase enzymes during the ontogenesis from hatching to 20 days post-hatching (DPH). Also, the in vitro effect that exogenous enzymes from Argentine red shrimp (Pleoticus muelleri) waste have on the alkaline peptidases of larvae from 6 to 20 DPH (which correspond to the age at which fish eat exogenous food) was studied. Both acid and alkaline peptidase activities varied throughout early ontogeny development (from 0.1 to 1, and from 0.1 to 7.1 UE mg protein−1, respectively). The patterns of both enzyme activity variation would be related with changes in endogenous, mixed and exogenous feeding. Our studies show that the additions of the enzyme extract of shrimp have a synergistic effect (from 3 to 6 times) on endogenous in vitro activity. Moreover, the zymogram analysis demonstrates that the bands corresponding to the activity of each species (tilapia and red shrimp) remain active when they are mixed. The increase in peptidase digestive capacity by addition of exogenous enzymes would maximize the assimilation of nutrients from artificial food during early development.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
Anson ML (1938) The estimation of pepsin, trypsin, papain, and cathepsin with hemoglobin. J Gen Physiol 22:79. https://doi.org/10.1085/jgp.22.1.79
AOAC-Association of Official Analytical Chemists (1995) Official methods of analysis, 16th edn. AOAC International, Gaithersburg, MD
Bradford MM (1976) A rapid and sensitive method for the quantitation 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
Buddington RK, Krogdahl Å (2004) Hormonal regulation of the fish gastrointestinal tract. Comp Biochem Physiol Part A 139(3):261–271. https://doi.org/10.1016/j.cbpb.2004.09.007
Con P, Nitzan T, Slosman T, Harpaz S, Cnaani A (2019) Peptide transporters in the primary gastrointestinal tract of pre-feeding Mozambique tilapia larva. Front Physiol 10:808. https://doi.org/10.3389/fphys.2019.00808
Conceição LEC, Aragão C, Rønnestad I (2011) Proteins. In: Fish L (ed) Holt. Nutrition. John Wiley & Sons Inc, New Jersey, pp 83–116
de Moura Pereira M, Machado Evangelista M, Gisbert E, Romagosa E (2019) Nile tilapia broodfish fed high protein diets: digestive enzymes in eggs and larvae. Aquac Res 50:2181–2190. https://doi.org/10.1111/are.14098
Drossou A, Ueberschär B, Rosenthal H, Herzig KH (2006) Ontogenetic development of the proteolytic digestion activities in larvae of Oreochromis niloticus fed with different diets. Aquaculture 256:479–488. https://doi.org/10.1016/j.aquaculture.2006.01.038
El-Sayed AFM (2019) Tilapia culture. Academic Press, San Diego
FAO (2020) GLOBEFISH Highlights January 2020 ISSUE, with Jan. – Sep. 2019 Statistics – a quarterly update on world seafood markets. Globefish Highlights no. 1–2020. Rome. https://doi.org/10.4060/ca7968en
Fernández-Gimenez AV, García-Carreño FL, Del Toro MN, Fenucci JL (2001) Digestive proteinases of red shrimp Pleoticus muelleri (Decapoda, Penaeoidea): partial characterization and relationship with molting. Comp Biochem Physiol Part B 130:331–338. https://doi.org/10.1016/S1096-4959(01)00437-7
Fujimura K, Okada N (2007) Development of the embryo, larva and early juvenile of Nile tilapia Oreochromis niloticus (Pisces: Cichlidae). Dev Staging Syst Dev Growth Differ 49:301–324. https://doi.org/10.1111/j.1440-169X.2007.00926.x
García-Carreño FL (1992) The digestive proteases of langostilla (Pleuroncodes planipes, Decapoda): their partial characterization, and the effect of feed on their composition Comp. Biochem Physiol Part B 103:575–578. https://doi.org/10.1016/0305-0491(92)90373-Y
Gupta G, Kumar M, Rani S, Mohanta B (2020) Vitellogenesis and their endocrine control in fishes. In: Sundaray JK, Rather MA, Kumar S, Agarwal D (eds) Recent updates in molecular Endocrinology and Reproductive Physiology of Fish, 1st edn. Springer, Singapur, pp 23–34
Gwon SH, Kim HK, Baek HJ, Lee YD, Kwon JY (2017) Cathepsin B & D and the survival of early embryos in red spotted grouper Ephinephelus akaara. Dev Reprod 21:457. https://doi.org/10.12717/DR.2017.21.4.457
Heming TA, Buddington RK (1988) Yolk absorption in embryonic and larval fishes. In: Hoar WS, Mason DJ (eds) Fish physiology. Academic Press, pp 407–446
Hiramatsu N, Todo T, Sullivan CV, Schilling J, Reading BJ, Matsubara T, Ryo Y-W, Mizuta H, Luo W, Nishimiya O, Wu M, Mushirobira Y, Yilmaz O, Hara A (2015) Ovarian yolk formation in fishes: molecular mechanisms underlying formation of lipid droplets and vitellogenin-derived yolk proteins. Gen Comp Endocrinol 221:9–15. https://doi.org/10.1016/j.ygcen.2015.01.025
Huang Z, Li Z, Xu A, Zheng D, Ye Y, Wang Z (2020) Effects of exogenous multienzyme complex supplementation in diets on growth performance, digestive enzyme activity and non-specific immunity of the Japanese seabass, Lateolabrax japonicus. Aquac Nutr 26:306–315. https://doi.org/10.1111/anu.12991
Ibrahim AN, Noll MS, Valenti WC (2015) Zooplankton capturing by Nile Tilapia, Oreochromis niloticus (Teleostei: Cichlidae) throughout post-larval development. Zoologia (curitiba) 32:469–475. https://doi.org/10.1590/s1984-46702015000600006
de Jiménez-Badillo ML, Arredondo-Figueroa JL (2000) Effect of oral treatments of synthetic androgens on sex ratio, survival and growth rates, in three strains of tilapia. Hidrobiologica 10:115–120. https://doi.org/10.4236/abb.2011.25047
Khalil NA, Allah HMMK, Mousa MA (2011) The effect of maternal thyroxine injection on growth, survival and development of the digestive system of Nile tilapia, Oreochromis niloticus, larvae. Adv Biosci Biotechnol 2:320–329. https://doi.org/10.4236/abb.2011.25047
Kondakova EA, Efremov VI, Nazarov VA (2016) Structure of the yolk syncytial layer in Teleostei and analogous structures in animals of the meroblastic type of development. Biol Bull 43:208–215. https://doi.org/10.1134/S1062359016030055
Kunz-Ramsay Y (2013) Developmental biology of teleost fishes (Vol. 28). Springer Science & Business Media, Berlin.
Kurokawa T, Shiraishi M, Suzuki T (1998) Quantification of exogenous protease derived from zooplankton in the intestine of Japanese sardine (Sardinops melanotictus) larvae. Aquaculture 161:491–499. https://doi.org/10.1016/S0044-8486(97)00296-2
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
Lo MJ, Weng CF (2006) Developmental regulation of gastric pepsin and pancreatic serine protease in larvae of the euryhaline teleost, Oreochromis mossambicus. Aquaculture 261:1403–1412. https://doi.org/10.1016/j.aquaculture.2006.09.016
Maas RM, Verdegem MC, Stevens TL, Schrama JW (2020) Effect of exogenous enzymes (phytase and xylanase) supplementation on nutrient digestibility and growth performance of Nile tilapia (Oreochromis niloticus) fed different quality diets. Aquaculture 529:735–723. https://doi.org/10.1016/j.aquaculture.2020.735723
Marjani M, Jamili S, Mostafavi PG, Ramin M, Mashinchian A (2009) Influence of 17-alpha methyl testosterone on masculinization and growth in tilapia (Oreochromis mossambicus). J Fish Aquat Sci 4:71–74. https://doi.org/10.3923/jfas.2009.71.74
Monier MN (2020) Efficacy of dietary exogenous enzyme supplementation on growth performance, antioxidant activity, and digestive enzymes of common carp (Cyprinus carpio) fry. Fish Physiol Biochem 46:713–723. https://doi.org/10.1111/are.12828
Morrison CM, Miyake T, Wright JR Jr (2001) Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces: Cichlidae). J Morphol 247:172–195. https://doi.org/10.1002/1097-4687(200102)247:2%3c172::AID-JMOR1011%3e3.0.CO;2-H
Morrison CM, Pohajdak B, Tam J, Wright JR Jr (2004) Development of the islets, exocrine pancreas, and related ducts in the Nile tilapia, Oreochromis niloticus (Pisces: Cichlidae). J Morphol 261:377–389. https://doi.org/10.1002/jmor.10256
Oh HJ, Kim JH, Mun SH, Kim JH, Kim DJ, Kwon JY (2018) Expression of yolk processing enzyme genes in fertilized eggs from artificially matured female eel, Anguilla japonica. Dev Reprod 22:289. https://doi.org/10.12717/DR.2018.22.3.289
Otieno ON, Kitaka N, Njiru JM (2014) Some aspects of the feeding ecology of Nile tilapia, Oreochromis niloticus in Lake Naivasha. Kenya Int J Fish Aquat Stud 2:1–8
Palomino J, Herrera G, Torres-Fuentes J, Dettleff P, Patel A, Martínez V (2017) Assessment of cathepsin mRNA expression and enzymatic activity during early embryonic development in the yellowtail kingfish Seriola lalandi. Anim Reprod Sci 180:23–29. https://doi.org/10.1016/j.anireprosci.2017.02.009
Prabu E, Rajagopalsamy CBT, Ahilan B, Jeevagan IJMA, Renuhadevi M (2019) Tilapia–an excellent candidate species for world aquaculture: a review. Ann Res Rev Biol 31(3):1–14. https://doi.org/10.9734/arrb/2019/v31i330052
Raldúa D, Fabra M, Bozzo MG, Weber E, Cerdà J (2006) Cathepsin B-mediated yolk protein degradation during killifish oocyte maturation is blocked by an H+-ATPase inhibitor: effects on the hydration mechanism. Am J Physiol Regul Integr Comp Physiol 290:R456–R466. https://doi.org/10.1152/ajpregu.00528.2005
Riddle MR, Hu CK (2021) Fish models for investigating nutritional regulation of embryonic development. Dev Biol. https://doi.org/10.1016/j.ydbio.2021.03.012
Robert D, Murphy HM, Jenkins GP, Fortier L (2014) Poor taxonomical knowledge of larval fish prey preference is impeding our ability to assess the existence of a “critical period” driving year-class strength. ICES J Mar Sci 71:2042–2052. https://doi.org/10.1093/icesjms/fst198
Rodriguez YE, Pereira NA, Haran NS, Mallo JC, Fernández-Gimenez AV (2017) A new approach to fishery waste revalorization to enhance Nile tilapia (Oreochromis niloticus) digestion process. Aquac Nutr 23:1351–1361. https://doi.org/10.1111/anu.12510
Silva WS, Costa LS, López-Olmeda JF, Costa NCS, Santos WM, Ribeiro PAP, Luz RK (2019) Gene expression, enzyme activity and performance of Nile tilapia larvae fed with diets of different CP levels. Animal 13(7):1376–1384. https://doi.org/10.1017/S175173111800318X
Sullivan CV, Yilmaz O (2018) Vitellogenesis and yolk proteins, fish. Encyclopedia of reproduction, 2nd ed. Elsevier, Amsterdam.
Tengjaroenkul B, Smith BJ, Smith SA, Chatreewongsin U (2002) Ontogenic development of the intestinal enzymes of cultured Nile tilapia, Oreochromis niloticus L. Aquaculture 211:241–251. https://doi.org/10.1016/S0044-8486(01)00888-2
Underwood W, Anthony R (2020) AVMA Guidelines for the Euthanasia of Animals: 2020, in: American Veterinary Medical Association (Ed.). Retrieved on March, 2013, vol. 30, no 2020, p. 2020–01.N. Meacham Road Schaumburg, IL 60173--ISBN 978–1–882691–54–8
Volkoff H (2016) The neuroendocrine regulation of food intake in fish: a review of current knowledge. Front Neurosci 10:540. https://doi.org/10.3389/fnins.2016.00540
Yúfera M, Darias MJ (2007) The onset of exogenous feeding in marine fish larvae. Aquaculture 268:53–63. https://doi.org/10.1016/j.aquaculture.2007.04.050
Wallace CK, Bright LA, Marx JO, Andersen RP, Mullins MC, Carty AJ (2018) Effectiveness of rapid cooling as a method of euthanasia for young zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 57(1):58–63
Zavala I (2011) Caracterización bioquímica del consumo de reservas vitelinas en peces teleósteos de ontogenia indirecta. REDVET. Rev. Electron. Vet. 12: 1–32. https://www.redalyc.org/articulo.oa?id=63616934008.
Zheng CC, Wu JW, Jin ZH, Ye ZF, Yang S, Sun YQ, Fei H (2019) Exogenous enzymes as functional additives in finfish aquaculture. Aquac Nutr 26:213–224. https://doi.org/10.1111/anu.12995
Acknowledgements
We are grateful to Paula Waldman, Federico Cecchi, Arturo Assain, and Brian Tomaselli from the Laboratory of Aquaculture (UTN-FRMdP, Mar del Plata) for assisting during fish reproduction, rearing and sampling. We want to thank to Graciela Alvarez from the Laboratory of Histology (IIMyC, Mar del Plata) for helping during fish measures and photo. Also, we are grateful to the Universidad Nacional de Mar del Plata for funding this research (EXA 865-18; 874-18 and 875-18 projects). We thank Professor Julieta Santos for the revision of English grammar and syntax.
Funding
This work was supported by Universidad Nacional de Mar del Plata (EXA 865–18; 874–18 and 875–18 projects).
Author information
Authors and Affiliations
Contributions
del Valle, J.C.: conceptualization, supervision, methodology, investigation, validation, formal analysis, writing — original draft preparation, and visualization. Zanazzi, A.N.: resources, methodology, reviewing, and editing. Rodriguez, Y.E.: methodology, investigation, formal analysis, and writing — reviewing and editing. Haran, N.S.: methodology, investigation, formal analysis, and original draft preparation. Laitano, M.V.: investigation, formal analysis, reviewing, and editing. Mallo, J.C.: resources, methodology, reviewing, and editing. Fernández-Gimenez, A.V.: conceptualization, supervision, methodology, investigation, validation, formal analysis, writing — original draft preparation, and visualization.
Corresponding author
Ethics declarations
Ethics approval
The care and use of experimental animals complied with “Institutional Committee for the Care and Use of Experimental Animals” animal welfare laws, guidelines, and policies as approved by FCEyN-UNMdP (RD 395–19).
Conflict of interest
The authors declare no competing interests.
Additional information
Handling Editor: Gavin Burnell
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
del Valle, J.C., Zanazzi, A.N., Rodriguez, Y.E. et al. Morphological changes, peptidase activity, and effects of exogenous enzymes in the early ontogeny of Nile tilapia, Oreochromis niloticus. Aquacult Int 30, 1645–1658 (2022). https://doi.org/10.1007/s10499-022-00932-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-022-00932-5