El Ciclo Diario de la Digestión en Peces Cultivados. Aspectos Funcionales y Metodológicos
Palabras clave:
Peces, digestión, ritmos diarios, protocolo de alimentaciónResumen
La eficiencia de la digestión depende entre otros factores de la adecuada relación entre enzima y sustrato, así
como del tiempo de hidrólisis bajo las condiciones apropiadas. La digestión es un proceso temporal que, en
peces, como en otros vertebrados, empieza con la detección del alimento y finaliza con la expulsión de los
desechos. La disponibilidad del alimento en el medio es variable a lo largo del ciclo diario por lo que también
lo es la ingestión y digestión de los nutrientes. Cabe pues esperar que haya momentos óptimos para
suministrar el alimento y que favorezcan su digestión, y momentos más desfavorables en los que se reduciría
la eficiencia de digestión. Por eso, el diseño de protocolos de alimentación más eficientes requiere del
conocimiento previo de los ciclos digestivos. En esta revisión se describirán los estudios realizados en este
sentido y el estado de conocimiento de la función digestiva en relación a los ciclos diarios. Se muestran tanto
los avances en larvas de peces como en juveniles y adultos que presentan diferentes modos de digestión. Dada
la variabilidad entre especies, y la escasez de estudios, la información disponible es aún muy fragmentaria
para definir patrones de actuación.
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Alarcón., F.J., Díaz, M., Moyano, F.J. y Abellán, E. (1998). Characterization and functional properties of
digestive proteases in two sparids; gilthead seabream (Sparus aurata) and common dentex (Dentex
dentex). Fish Physiology and Biochemistry 19, 257-267.
Andrade, C.A.P., Brazão, I.P.G., Nogueira, N., Ferreira, M.P., Dillinger, T., Dinis, M.T. et al. (2011). Red
porgy (Pagrus pagrus) larval feeding performance and behavior at the onset of exogenous feeding.
Journal of Experimental Marine Biology and Ecology 407, 377-381.
Anson, M. (1938). The estimation of pepsin, trypsin, papain and cathepsin with haemoglobin. Journal of
General Physiology 22, 79-89.
Bayarri, M.J., Muñoz-Cueto, J.A., López-Olmeda, J.F., Vera, L.M., Rol de Lama, M.A. y Madrid, J.A., et al.
(2004). Daily locomotor activity and melatonin rhythms in Senegal sole (Solea senegalensis).
Physiology & Behavior 81, 577-583.
Borey, M., Panserat, S., Surget, A., Cluzeaud, M., Plagnes-Juan, E., Herman, A. et al. (2016). Postprandial
kinetics of gene expression of proteins involved in the digestive process in rainbow trout (O. mykiss)
and impact of diet composition. Fish Physiology and Biochemistry 42, 1187-1202.
Boujard, T. y Leatherland, J.F. (1992) Circadian rhythms and feeding time in fishes. Environmental Biology
of Fishes 35, 109-131.
Bucking, C. y Wood, C.M. (2009). The effect of postprandial changes in pH along the gastrointestinal tract on
the distribution of ions between the solid and fluid phases of chime of rainbow trout. Aquaculture
Nutrition 15, 282-296.
Castro, C., Couto, A., Pérez-Jiménez, A. Serra, C.R., Díaz-Rosales, P., Fernandes, R. et al. (2016). Effects of
fish oil replacement by vegetable oil blend on digestive enzymes and tissue histomorphology of
European sea bass (Dicentrarchus labrax) juveniles. Fish Physiology and Biochemistry 42(1):203-
Chen, W.Q., Cao, M.J., Yoshida, A., Liu, G.M., Weng, W.Y., Sun, L.C. et al. (2009). Study on Pepsinogens
and Pepsins from Snakehead (Channa argus). Journal of Agricultural and Food Chemistry 57,
-10978.
Cowan, M., Azpeleta, C. y López-Olmeda, J.F. (2017). Rhythms in the endocrine system of fish: a review.
Journal of Comparative Physiology B (en prensa) DOI 10.1007/s00360-017-1094-5
Davie, A., Sanchez, J.A., Vera, L.M., Sanchez-Vazquez, J. y Migaud, H. (2011). Ontogeny of the circadian
system during embryogenesis in rainbow trout (Oncorhynchus Mykyss) and the effect of prolonged
exposure to continuous illumination on daily rhythms of per1, clock, and aanat2 expression.
Chronobiology International 28, 177-86.
Deguara, S., Jauncey, K. y Agiuss, C. (2003). Enzyme activities and pH variations in the digestive tract of
gilthead sea bream. Journal of Fish Biology 62, 1033–1043.
Del Pozo, A., Montoya, A., Vera, L.M. y Sánchez-Vázquez, F.J. (2012). Daily rhythms of clock gene
expression, glycaemia and digestive physiology in diurnal/nocturnal European seabass. Physiology
& Behavior 106, 446-50.
Dou, S., Seikai, T. y Tsukamoto, K. (2000). Feeding behavior of Japanese flounder larvae under laboratory
conditions. Journal of Fish Biology 56, 654-666.
Espinosa-Chaurand, D., Vega-Villasante, F., Carrillo-Farnés, O. y Nolasco-Soria, H. (2017). Effect of
circadian rhythm, photoperiod, and molt cycle on digestive enzymatic activity of Macrobrachium
tenellum juveniles. Aquaculture 479, 225-232.
Feliciano, A., Vivas, Y., de Pedro, N., Delgado, M.J., Velarde, E. y Isorna, E. (2011). Feeding time
synchronizes clock gene rhythmic expression in brain and liver of goldfish (Carassius auratus).
Journal of Biological Rhythms 26, 24-33.
Fujii, A., Kurokawa, Y., Kawai, S., Yoseda, K., Dan, S., Kai, A. et al. (2007). Diurnal variation of tryptic
activity in larval stage and development of proteolytic enzyme activities of malabar grouper
(Epinephelus malabaricus) after hatching. Aquaculture 270, 68-76.
Hlophe, S.N., Moyo, N.A.G. y Ncube, I. (2014). Postprandial changes in pH and enzyme activity from the
stomach and intestines of Tilapia rendalli (Boulenger, 1897), Oreochromis mossambicus (Peters,
and Clarias gariepinus (Burchell, 1822). Journal of Applied Ichthyology 30, 35-41.
Jacob, S., Pouil, S., Lecchini, D., Oberhänsli, F., Swarzenski, P. y Metian, M. (2017). Trophic transfer of
essential elements in the clownfish Amphiprion ocellaris in the context of ocean acidification. PLoS
ONE 12(4), e0174344.
Jonhston, J.D. (2014). Physiological responses to food intake throughout the day. Nutrition Research Reviews
, 107-118.
Kotani, T.Y. y Fushimi, H. (2011). Determination of appropriate feeding schedules from diel feeding rhythms
in finfish larviculture. Aquaculture 315, 104-113.
Lazo, J.P., Darias, M.J. y Gisbert, E. (2011). Ontogeny of the digestive tract. In: Larval fish nutrition (ed. by
G.J. Holt). Wiley, West Sussex, pp 1-47.
López-Olmeda, J.F., López-García, I., Sánchez-Muros, M.J., Blanco-Vives, B, Aparicio, R. y Sánchez-
Vázquez, F.J. (2012). Daily rhythms of digestive physiology, metabolism and behaviour in the
European eel (Anguilla anguilla). Aquaculture International 20, 1085–1096.
López-Olmeda, J.F. (2017). Nonphotic entrainment in fish. Comparative Biochemistry and Physiology Part A
, 133-143.
Ma, A.J., Liu, X.Z., Xu, Y.J., Liang, Y. y Zhuang, Z.M. (2006). Feeding rhythm and growth in the tongue
sole, Cynoglossus semilaevis Günther, during its early life stages. Aquaculture Research 37, 586-
Mackenzie, B.R., Ueberschär, B., Basford, B., Heath, M. y Gallego, A. (1999). Diel variability of feeding
activity in haddock (Melanogrammus aeglefinus) larvae in the East Shetland area, North Sea. Marine
Biology 138, 361-368.
Madrid, J.A., Boujard, T. y Sánchez-Vázquez, F.J. (2001) Feeding rhythms. In: Food Intake in Fish. (ed. by
D. Houlihan, T. Boujard and M. Jobling) Blackwell Science, London, pp. 189-215.
Márquez, L., Robles, R., Morales, G. y Moyano, F.J. (2012). Gut pH as a limiting factor for digestive
proteolysis in cultured juveniles of the gilthead sea bream (Sparus aurata).Fish Physiology and
Biochemistry 38, 859-869.
Martín-Robles, A.J., Whitmore, D., Pendón, C. y Muñoz-Cueto, J.A. (2013). Differential effects of transient
constant light-dark conditions on daily rhythms of Period and Clock transcripts during Senegalese
sole metamorphosis. Chronobiology International 30, 699-710.
Mata, J.A., Moyano, F.J., Martínez-Rodríguez, G. y Yúfera, M. (2014). Effect of feeding frequency on
digestive function of gilthead seabream (Sparus aurata) larvae fed microdiets. Aquaculture Europe
, San Sebastián, España, 14-17 October 2014.
Mata-Sotres, J.A., Martínez-Rodríguez, G., Pérez-Sánchez, J. y Sánchez-Vázquez, F.J., Yúfera, M. (2015).
Daily rhythms of clock gene expression and feeding behaviour during the development in gilthead
seabream, Sparus aurata. Chronobiology International 32, 1061-1074.
Mata-Sotres, J.A., Moyano, F.J., Martínez-Rodríguez, G. y Yúfera, M. (2016). Daily rhythms of digestive
enzyme activity and gene expression in gilthead seabream (Sparus aurata) during ontogeny.
Comparative Biochemistry and Physiology Part A, 197, 3-51.
Molina, C., Cadena, E. y Orellana, F. (2000). Alimentación de camarones en relación a la actividad
enzimática como una respuesta natural al ritmo circadiano y ciclo de muda. In: Avances en Nutrición
Acuícola V. (ed. por L.E. Cruz-Suárez, D. Ricque-Marie, M. Tapia-Salazar, M.A. Olvera-Novoa, R.
Civera-Cerecedo), Memorias del V Simposium Internacional de Nutrición Acuícola. 19–22 Nov.
Merida, Yucatán, México, pp. 358-379.
Montoya, A., López-Olmeda, J.F., Yúfera, M., Sánchez-Muros, M.J. y Sánchez-Vázquez, F.J. (2010).
Feeding time synchronizes daily rhythms of behavior and digestive physiology in gilthead seabream
(Sparus aurata). Aquaculture 306, 315-21.
Morais, S., Lacuisse, M., Conceição, L.E.C., Dinis, M.T. y Rønnestad I. (2004) Ontogeny of the digestive
capacity of Senegalese sole (Solea senegalensis), with respect to digestion, absorption and
metabolism of amino acids from Artemia. Marine Biology 145, 243-250
Morales, G.A., Márquez, L., Saenz de Rodrigañez, M.A., Bermúdez, L., Robles, R. y Moyano, F.J. (2014).
Effect of phytase supplementation of a plant-based diet on phosphorus and nitrogen bioavailability in
sea bream Sparus aurata. Aquaculture Nutrition 20, 172-182.
Nalinanon, S., Benjakul, S., Visessanguan, W. y Kishimira, H. (2008). Tuna pepsin: characteristics and its use
for collagen extraction from the skin of threadfin bream (Nemipterus spp.). Journal of Food Science
(5), C413-C419.
Navarro-Guillén, C., Moyano, F.J. y Yúfera, M. (2015). Diel food intake and digestive enzyme production
patterns in Solea senegalensis larvae. Aquaculture 435, 33-42.
Nikolopulou, D., Moutou, K.A., Fountoulaki, E., Venou, B., Adamidou, S. y Alexis, M.N. (2011). Patterns of
gastric evacuation, digesta characteristics and pH changes along the gastrointestinal tract of gilthead
sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). Comparative
Biochemistry and Physiology A 158, 406-414.
Nolasco-Soria, H. y Vega-Villasante, F. (2000). Actividad enzimática digestiva, ritmos circadianos y su
relación con la alimentación del camarón. In: Avances en Nutrición Acuícola IV (ed. Por R. Civera-
Cevedo, C.J. Pérez-Estrada, D. Ricque-Marie, L.E. Cruz-Suárez). Memorias del IV Simposio
Internacional de Nutrición Acuícola. Nov 15-18, La Paz, B.C.S., México, pp. 149-165.
Okauchi, M., Oshiro, T., Kitamura, S., Tsujigado, A. y Fukusho, K. (1980). Number of rotifer, Brachionus
plicatilis, consumed daily by a larva and juvenile of porgy, Acanthopagrus schlegeli. Bulletin of
National Research Institute of Aquaculture 1, 39-45.
Ortiz-Monís, M.A., Mancera, J.M. y Yúfera M. (2017). Determining gut transit rates in gilthead seabream
larvae fed microdiets. Larvi 2017, 7th fish & shellfish larviculture symposium, Ghent, Belgium, 4-7
September 2017.
Østergaard, P., Munk, P. y Janekarn, V. (2005). Contrasting feeding patterns among species of fish larvae
from the tropical Andaman Sea. Marine Biology 146, 595-606.
Papastamatiou, Y.P. y Lowe, C.G. (2005). Variations in gastric acid secretion during fasting between two
species of shark. Comparative Biochemistry and Physiology A 141, 210–214
Pittendrigh, C.S. (1993) Temporal organization: reflections of a Darwinian clock-watcher. Annual Reviews of
Physiology 55, 16-54.
Reebs, S.G. (2002) Plasticity of diel and circadian activity rhythms in fishes. Reviews in Fish Biology and
Fisheries 12, 349-371.
Rodiles, A., Santigosa, E., Herrera, M., Hachero-Cruzado, I., Cordero, M.L., Martínez-Llorens, S. et al.
(2012). Effect of dietary protein level and source on digestive proteolytic enzyme activity in juvenile
Senegalese sole, Solea senegalensis Kaup 1850. Aquaculture International 20, 1053-1070.
Rønnestad, I., Yúfera, M., Ueberschär, B., Ribeiro, L., Sæle, Ø. y Boglione, C. (2013) Feeding behaviour and
digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Reviews
in Aquaculture 5, S59-S98.
Rosero, A.P. (2013). Comparación de la fisiología digestiva entre un pez carnívoro (Corvina, Argyrosomus
regius) y un pez omnívoro (Liseta, Chelon labrosus), e influencia de la inclusión de un acidificante
en el pienso sobre el proceso digestivo. Tesis de Master, Universidad de Cádiz, 52 p.
Santigosa, E., Sánchez, J., Médale, F., Kaushik, S., Pérez-Sánchez, J. y Gallardo, M.A. (2008). Modifications
of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to
dietary fish meal replacement by plant protein sources. Aquaculture 282, 68-74.
Secor, S. (2003). Gastric function and its contribution to the postprandial metabolic reponses in the Burmese
python, Python molurus. Journal of Experimental Biology 206, 1621–1630.
Shoji, J., Maehara, T. y Tanaka, M. (1999.) Diel vertical movement and feeding rhythm of Japanese mackerel
larvae in the central Seto inland sea. Fisheries Science 65, 726-730.
Solovyev, M.M., Kashinskaya, E.N., Rusinek, O.T. y Izvekova, G.I. (2016). Physiological pH values in the
digestive tract of perch Perca fluviatilis from different habitats. Journal of Ichthyology 56(2), 312-
Spieler, R.E. (1992) Feeding-entrained circadian rhythms in fishes. In: Rhythms in Fishes (ed. by M.A. Ali,),
Plenum, New York, pp. 137-147.
Sugiura, S.H., Roy P.K. y Ferraris, R.P. (2006). Dietary acidification enhances phosphorus digestibility but
decreases H+/K+-ATPase expression in rainbow trout. Journal of Experimental Biology 209, 3719-
Ueberschär, B. (1993). Measurement of proteolytic enzyme activity: significance and application in larval fish
research. In: Physiological and Biochemical Aspects of Fish Development. (ed. by B.T. Walther, and
H.J. Fyhn), University of Bergen, Norway, pp. 233-239.
Ueberschär, B. (1995). The use of tryptic enzyme activity measurement as a nutritional condition index:
laboratory calibration data and field application. ICES Marine Science Symposiums 201, 119-129.
Vatine, G., Vallone, Y. Gothilf, Y. y Foulkes, N.S. (2011). It's time to swim! Zebrafish and the circadian
clock. FEBS Letters 585, 1485-1494.
Vera, L.M., De Pedro, N., Gomez-Milán, E., Delgado, M.J., Sánchez-Muros, M.J., Madrid, J.A. et al. 2007
Feeding entrainment of locomotor activity rhythms, digestive enzymes and neuroendocrine factors in
goldfish. Physiology & Behavior 90, 518-24.
Wang, H.Y, Wang, Y.J., Wang, Q.Y., Xue, C.H. y Sun, M. (2006). Purification and characterization of
stomach protease from the turbot (Scophthalmus maximus L.). Fish Physiology and Biochemistry 32,
-188.
Wang Y, Hu M, Wang W, Cao L, Yang Y, Lü B. et al. (2008). Transpositional feeding rhythm of loach
Misgurnus anguillicaudatus from larvae to juveniles and its ontogeny under artificial rearing
conditions. Aquaculture International 16, 539-549
Whitmore, D., Foulkes, N.S. y Sassone-Corsi, P. (2000). Light acts directly on organs and cells in culture to
set the vertebrate circadian clock. Nature 404, 87-91.
Yoseda, K., Yamamoto, K., Asami, K., Chimura, M., Hashimoto, K. y Kosaka S. (2008). Influence of light
intensity on feeding, growth and early survival of leopard coral grouper (Plectropomus leopardus)
larvae under mass-scale rearing conditions. Aquaculture 279, 55-62.
Yúfera M., Fernández-Díaz, C. y Pascual, E. (1995). Feeding rates of gilthead seabream, Sparus aurata,
larvae on microcapsules. Aquaculture 34, 257-268.
Yúfera, M., Fernández-Dıáz, C., Vidaurreta, A., Cara, J.B. y Moyano, F.J. (2004). Gastrointestinal pH and
development of the acid digestion in larvae and early juveniles of Sparus aurata L. (Pisces:
Teleostei). Marine Biology 144, 863-9.
Yúfera, M., Moyano, F.J., Astola, A., Pousão-Ferreira, P. y Martínez-Rodríguez, G. (2012). Acidic digestion
in a teleost: Postprandial and circadian pattern of gastric pH, pepsin activity, and pepsinogen and
proton pump mRNAs expression. PLoS ONE 7(3) e33687.
Yúfera, M., Romero, M.J., Pujante, I.M., Astola, A., Mancera, J.M., Sánchez-Vázquez, F.J. et al. (2014).
Effect of feeding frequency on the daily rhythms of acidic digestion in a teleost fish (gilthead
seabream). Chronobiology International 31, 1024-1033.
Yúfera, M., Nguyen, M.V., Engrola, S., Conceição, L., Jordal, A-EO., Le, M.H. et al. (2016). Cobia exhibits a
permanent gastric acidity as digestion strategy. Aquaculture Europe 2016, Edinburgh, Scotland, UK,
-23 September 2016.
Yúfera, M., Nguyễn, M.V. y Trần, H.V. (2017). Preliminary outcomes on the gastrointestinal luminal ionic
conditions in orange-spotted grouper juveniles. Aquaculture Europe 2017, Dubrovnik, Croacia, 17-
October 2017.
Zambonino-Infante, J.L. y Cahu, C.L. (2001). Ontogeny of the gastrointestinal tract of marine fish larvae.
Comparative Biochemistry and Physiology Part C 130 (4), 477-487.
Zeng, L.Q., Fu, S.J., Li, X.M., Li, F.J., Li, B., Cao, Z.D. et al. (2014). Physiological and morphological
responses to the first bout of refeeding in southern catfish (Silurus meridionalis). Journal of
Comparative Physiology B 184, 329-346.
