Comparison of digestive enzymes activity of trypsin, chymotrypsin and amylase in four species of Cyprinidae (Rutilus frisii kuttum, Rutilus rutilus caspicus, Capoeta capoeta, and Cyprinus carpio)

Document Type : scientific research article

Authors

1 Dept. of Fisheries, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas, Iran.

2 Corresponding Author, Persian Gulf Mollusks Research Station, Persian Gulf and Oman Sea Ecology Research Center, Iranian Fisheries Sciences Research Institute, Agricultural Research Education and Extension Organization (AREEO), Bandar-e-Lengeh, Iran.

3 Persian Gulf and Oman Sea Ecology Research Center, Iranian Fisheries Sciences Research Institute, Agricultural Research Education and Extension Organization (AREEO), Bandar Abbas, Iran.

4 Animal Science Research Institute of Iran (ASRI), Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran.

5 Dept. of Fisheries, Faculty of Fisheries and Environmental Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

Abstract

The aim of this study was to compare digestive enzymes activity (alkaline proteases and amylase) in four species of Cyprinidae including one herbivorous species, the Caucasian scraper (Capoeta capoeta), and three omnivorous species, common carp (Cyprinus carpio), roach (Rutilus rutilus), and Caspian kutum, (Rutilus frisii kutum). All four species were fed with similar diet. The results showed that the enzyme profile was similar in four species and amylase enzyme activity was higher compared to protease enzymes (trypsin and chymotrypsin). However, there was a significant difference in the activity of these enzymes among the studied species. The highest trypsin and chymotrypsin activities were observed in roach, while common carp had the highest amylase enzyme and digestive somatic index. Therefore, the amylase activity was independent of feeding habit, while protease activity was relatively more dependent on feeding habit. The highest amylase / protease ratio was recorded in common carp which indicates the higher capacity of this species to utilize carbohydrates, therefore cost-effective feed can be used for its commercial production.

Keywords

Main Subjects


1.Furne, M., Hidalgo, M. C., Lopez, A., Garcia-Gallego, M., Morales, A. E., Domezain, A., Domezainé, J., & Sanz, A. (2005). Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii
and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture, 250 (1-2), 391-398.
2.Rust, M. B. (2003). Nutritional physiology. In Fish nutrition (pp. 367-452). Academic Press.
3.Pérez-Jiménez, A., Cardenete, G., Morales, A. E., García-Alcázar, A., Abellan, E., & Hidalgo, M. C. (2009). Digestive enzymatic profile of Dentex dentex and response to different dietary formulations. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 154 (1), 157-164.
4.Peretti, D., & Andrian, I. D. F. (2008). Feeding and morphological analysis of the digestive tract of four species of fish (Astyanax altiparanae, Parauchenipterus galeatus, Serrasalmus marginatus and Hoplias aff. malabaricus) from the upper Paraná River floodplain, Brazil. Brazilian Journal of Biology, 68, 671-679.
5.Chakrabarti, I., Gani, M. A., Chaki, K. K., Sur, R., & Misra, K. K. (1995). Digestive enzymes in 11 freshwater teleost fish species in relation to food habit and niche segregation. Comparative Biochemistry and Physiology Part A: Physiology,
112 (1), 167-177.
6.Baker, R., Buckland, A., & Sheaves, M. (2014). Fish gut content analysis: robust measures of diet composition. Fish and Fisheries, 15 (1), 170-177.
7.Manko, P. (2016). Stomach content analysis in freshwater fish feeding ecology. University of Prešov, 116.
8.Buckland, A., Baker, R., Loneragan, N., & Sheaves, M. (2017). Standardising fish stomach content analysis: The importance of prey condition. Fisheries Research, 196, 126-140.
9.Simenstad, C. A., & Cailliet, G. M. (2017). Retrospective on the origin, intent, and impact of the Gutshops and some directions for the future. Environmental Biology of Fishes, 100, 299-308.
10.Tomojiri, D., Musikasinthorn, P., & Iwata, A. (2019). Food habits of three non-native cichlid fishes in the lowermost Chao Phraya River basin, Thailand. Journal of Freshwater Ecology, 34 (1), 419-432.
11.Habib, K. M., & Adugna, A. A. (2021). Stomach content analysis of feed and feeding habit of Oreochromis niloticus fish species in baro-akobo basin, South West Ethiopia in case of Alwero Dam. Journal of Biology, Agriculture and Healthcare, 11 (3), 2212457.
12.Soe, K. K., Hajisamae, S., Sompongchaiyakul, P., Towatana, P., & Pradit, S. (2022). Feeding habits and the occurrence of anthropogenic debris in the stomach content of marine fish from Pattani Bay, Gulf of Thailand. Biology, 11 (2), 331.
13.Wagaw, S., Mengistou, S., & Getahun, A. (2022). Diet composition and feeding habits of Oreochromis niloticus (Linnaeus, 1758) in Lake Shala, Ethiopia. Fisheries and Aquatic Sciences, 25 (1), 20-30.
14.Tesfahun, A., & Alebachew, S. (2023). Food and feeding habits of the Nile tilapia Oreochromis niloticus (Linnaeus, 1758) from Ribb reservoir, Lake Tana sub-basin, Ethiopia. Cogent Food & Agriculture, 9 (1), 2212457.
15.Bolasina, S., Pérez, A., & Yamashita, Y. (2006). Digestive enzymes activity during ontogenetic development and effect of starvation in Japanese flounder, Paralichthys olivaceus. Aquaculture, 252 (2-4), 503-515.
16.German, D. P., Horn, M. H., & Gawlicka, A. (2004). Digestive enzyme activities in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Physiological and Biochemical zoology, 77 (5), 789-804.
17.Hani, Y. M. I., Marchand, A., Turies, C., Kerambrun, E., Palluel, O., Bado-Nilles, A., Beaudouin, R., Porcher, J. M., Geffard, A., & Dedourge-Geffard, O. (2018). Digestive enzymes and gut morphometric parameters of threespine stickleback (Gasterosteus aculeatus): Influence of body size and temperature. PLoS One, 13 (4), e0194932.
18.Huang, Y. S., Wen, X. B., Li, S. K., Xuan, X. Z., & Zhu, D. S. (2017). Effects of protein levels on growth, feed utilization, body composition, amino acid composition and physiology indices of juvenile chu's croaker, Nibea coibor. Aquaculture Nutrition, 23 (3), 594-602.
19.Tu, Y., Xie, S., Han, D., Yang, Y., Jin, J., Liu, H., & Zhu, X. (2015). Growth performance, digestive enzyme, transaminase and GH-IGF-I axis gene responsiveness to different dietary protein levels in broodstock allogenogynetic gibel carp (Carassius auratus gibelio) CAS III. Aquaculture, 446, 290-297.
20.Furné, M., García-Gallego, M., Hidalgo, M. C., Morales, A. E., Domezain, A., Domezain, J., & Sanz, A. (2008). Effect of starvation and refeeding on digestive enzyme activities in sturgeon (Acipenser naccarii) and trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 149 (4), 420-425.
21.Fernandez, I., Moyano, F. J., Dıaz, M., & Martınez, T. (2001). Characterization of α-amylase activity in five species of Mediterranean sparid fishes (Sparidae, Teleostei). Journal of Experimental Marine Biology and Ecology, 262 (1), 1-12.
22.Drewe, K. E., Horn, M. H., Dickson, K. A., & Gawlicka, A. (2004). Insectivore to frugivore: ontogenetic changes in gut morphology and digestive enzyme activity in the characid fish Brycon guatemalensis from Costa Rican rain forest streams. Journal of Fish Biology, 64 (4), 890-902.
23.German, D. P., Neuberger, D. T., Callahan, M. N., Lizardo, N. R., & Evans, D. H. (2010). Feast to famine: the effects of food quality and quantity on the gut structure and function of a detritivorous catfish (Teleostei: Loricariidae). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 155 (3), 281-293.
24.López‐Vásquez, K. A. T. H. E. R. I. N. E., Castro‐Pérez, C. A., & Val, A. L. (2009). Digestive enzymes of eight Amazonian teleosts with different feeding habits. Journal of Fish Biology, 74 (7), 1620-1628.
25.Hidalgo, M. C., Urea, E., & Sanz, A. (1999). Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities. Aquaculture, 170 (3-4), 267-283.
26.Debnath, D., Pal, A. K., Sahu, N. P., Yengkokpam, S., Baruah, K., Choudhury, D., & Venkateshwarlu, G. (2007). Digestive enzymes and metabolic profile of Labeo rohita fingerlings fed diets with different crude protein levels. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 146 (1), 107-114.
27.García-Meilán, I., Ordóñez-Grande, B., Machahua, C., Buenestado, S., Fontanillas, R., & Gallardo, M. A. (2016). Effects of dietary protein-to-lipid ratio on digestive and absorptive processes in sea bass fingerlings. Aquaculture, 463, 163-173.
28.Salehi, H. (2004). An economic analysis of carp culture production cost in Iran. Iranian Journal of Fisheries Sciences,
4, 1-24.
29.Mazumder, S. K., Das, S. K., Rahim, S. M., & Abd Ghaffar, M. (2018). Temperature and diet effect on the pepsin enzyme activities, digestive somatic index and relative gut length of Malabar blood snapper (Lutjanus malabaricus Bloch & Schneider, 1801). Aquaculture Reports, 9, 1-9.
30.Abolfathi, M., Hajimoradloo, A., Ghorbani, R., & Zamani, A. (2012). Effect of starvation and refeeding on digestive enzyme activities in juvenile roach, Rutilus rutilus caspicus. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 161 (2), 166-173.
31.Lowry, O., Rosebrough, N., Farr, A., & Randall, R. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1), 265-75.
32.Erlanger, B. F., Kokowsky, N., & Cohen, W. (1961). The preparation and properties of two new chromogenic substrates of trypsin. Archives of biochemistry and biophysics, 95 (2), 271-278.
33.Hummel, B. C. (1959). A modified spectrophotometric determination of chymotrypsin, trypsin, and thrombin. Canadian journal of biochemistry and physiology, 37 (12), 1393-1399.
34.Bernfeld, P. (1951). Amylases α and β: In method in enzymology. in: Colowick, P. and Kaplan, N.O. (Eds). Vol. 1 Academic Press Newyork. pp. 149-157.
35.Chan, A. S., Horn, M. H., Dickson, K. A., & Gawlicka, A. (2004). Digestive enzyme activities in carnivores and herbivores: comparisons among four closely related prickleback fishes (Teleostei: Stichaeidae) from a California rocky intertidal habitat. Journal of Fish Biology, 65 (3), 848-858.
36.De Almeida, L. C., Lundstedt, L. M., & Moraes, G. (2006). Digestive enzyme responses of tambaqui (Colossoma macropomum) fed on different levels of protein and lipid. Aquaculture Nutrition, 12 (6), 443-450.
37.Langeland, M., Lindberg, J. E., & Lundh, T. (2013). Digestive enzyme activity in Eurasian perch (Perca fluviatilis) and Arctic charr (Salvelinus alpinus). J. Aquac. Res. Develop. 5 (208), 2.
38.Solovyev, M. M., Kashinskaya, E. N., Izvekova, G. I., Gisbert, E., & Glupov, V. V. (2014). Feeding habits and ontogenic changes in digestive enzyme patterns in five freshwater teleosts. Journal of Fish Biology, 85 (5), 1395-1412.
39.Sabat, P., Lagos, J. A., & Bozinovic, F. (1999). Test of the adaptive modulation hypothesis in rodents: dietary flexibility and enzyme plasticity. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 123 (1), 83-87.
40.Martínez del Rio, C. (1990). Dietary, phylogenetic, and ecological correlates of intestinal sucrase and maltase activity in birds. Physiological Zoology, 63 (5), 987-1011.
41.Caviedes-Vidal, E., Afik, D., del Rio, C. M., & Karasov, W. H. (2000). Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptive hypothesis. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 125 (1), 11-24.
42.Chaudhuri, A., Mukherjee, S., & Homechaudhuri, S. (2012). Diet composition and digestive enzymes activity in carnivorous fishes inhabiting mudflats of Indian Sundarban estuaries. Turkish Journal of Fisheries and Aquatic Sciences, 12 (2).
43.Kumar, S., & Tembre, M. (1998). Digestive system. In: Kumar, S. & Tembre, M. (Eds). Anatomy and Physiology of Fishes. Chapter 6. UBS press. 56-76.
44.Moran, D., & Clements, K. D. (2002). Diet and endogenous carbohydrases in the temperate marine herbivorous fish Kyphosus sydneyanus. Journal of Fish Biology, 60 (5), 1190-1203.
45.Odedeyi, D. O., & Fagbenro, O. A. (2010). Feeding habits and digestive enzymes in the gut of Mormyrus rume (Valenciennes 1846) (Osteichthyes Mormyridae). Tropical zoology, 23 (1), 75.
46.Rosa Gioda, C., Pretto, A., Freitas, C. D. S., Leitemperger, J., Loro, V. L., Lazzari, R., Lissner, L. A., Baldisserotto, B., & Salbego, J. (2017). Different feeding habits influence the activity of digestive enzymes in freshwater fish. Ciência Rural, 47.
47.Rungruangsak-Torrissen, K., Moss, R., Andresen, L. H., Berg, A., & Waagbø, R. (2006). Different expressions of trypsin and chymotrypsin in relation to growth in Atlantic salmon (Salmo salar L.). Fish physiology and Biochemistry, 32, 7-23.
48.Bitterlich, G. (1985). Digestive enzyme pattern of two stomachless filter feeders, silver carp, Hypophthalmichthys molitrix Val., and bighead carp, Aristichthys nobilis Rich. Journal of Fish Biology, 27 (2), 103-112.
49.Horn, M. H., Gawlicka, A. K., German, D. P., Logothetis, E. A., Cavanagh, J. W., & Boyle, K. S. (2006). Structure and function of the stomachless digestive system in three related species of New World silverside fishes (Atherinopsidae) representing herbivory, omnivory, and carnivory. Marine Biology, 149, 1237-1245.
50.Lemieux, H., Blier, P., & Dutil, J. D. (1999). Do digestive enzymes set a physiological limit on growth rate and food conversion efficiency in the Atlantic cod (Gadus morhua)?. Fish Physiology and Biochemistry, 20, 293-303.
51.Santos, W. M., Costa, L. S., López-Olmeda, J. F., Costa, N. C. S., Santos, F. A. C., Oliveira, C. G., Guilherme, H. O., Bahiense, R. N., Luz, R. K., & Ribeiro, P. A. P. (2020). Dietary protein modulates digestive enzyme activities and gene expression in red tilapia juveniles. animal, 14 (9), 1802-1810.
52.Kumar, V., Makkar, H. P. S., & Becker, K. (2011). Detoxified Jatropha curcas kernel meal as a dietary protein source: growth performance, nutrient utilization and digestive enzymes in common carp (Cyprinus carpio L.) fingerlings. Aquaculture Nutrition, 17 (3), 313-326.
53.Manorama, M. A. I. S. N. A. M., & Ramanujam, S. N. (2017). Diet of threatened fish Pethia shalynius (Yazdani and Talukdar 1975) in the Umiam River, Northeast India. Asian Fisheries Science, 30 (1).