Abstract
Chemical reactor theory (CRT) suggests that the digestive tract functions as a chemical reactor for processing food. Presumably, gut structure and function should match diet to ensure adequate nutrient and energy uptake to maintain performance. Within CRT, dietary biochemical composition is the most important factor affecting gut structure and function in vertebrates. We fed Danio rerio (zebrafish) diets ranging from high- to moderate- to low-quality (i.e., ranging from high-protein, low-fiber to low-protein, high-fiber), and observed how gut length and surface area, as well as the activity levels of digestive enzymes (amylase, maltase, trypsin, aminopeptidase, and lipase) shifted in response to these dietary changes. Fish on the low-quality diet had the longest guts with the largest intestinal epithelial surface area and enterocyte cellular volumes. Fish on the moderate-quality diet had intermediate values of most of these parameters, and fish on the high-quality diet, the lowest. These data largely support CRT. Digestive enzyme activity levels were generally elevated in fish fed the moderate- and low-quality diets, but were highest in the fish fed the moderate-quality diet, suggesting that a diet with protein levels closest to that of the natural diet of D. rerio (they are omnivorous in nature) may elicit the best gut performance. However, fish fed the carnivore diet reached the largest terminal body size. Our results support CRT in terms of gut structure; however, our enzyme results do not necessarily agree with CRT and largely depend on which enzyme is discussed. In particular, the evidence for lipase activities being elevated in the fish fed the low-protein, high-fiber diet perhaps reflects a lipid-scavenging mechanism in fish consuming high-fiber foods rather than CRT.
Similar content being viewed by others
References
Abrámoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int
Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944
Allison SD, Chacon SS, German DP (2014) Substrate concentration constraints on microbial decomposition. Soil Biol Biochem 79:43–49
Bakke-Mckellep M, Mcl Press C, Baeverfjord G, Krogdahl A, Landsverk T (2000) Changes in immune and enzyme histochemical phenotypes of cell in the intestinal mucosa of Atlantic salmon, Salmo salar L., with soybean meal-induced enteritis. J Fish Dis 23:115–127
Bakke-McKellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, Ringø E, Krogdahl A (2007) Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 97:699–713
Batzli GO, Broussard AD, Oliver RJ (1994) The integrated processing response in herbivorous small mammals. In: Chivers DJ, Langer P (eds) The digestive system in mammal: food, form and function. Cambridge University Press, Cambridge, pp 324–336
Berumen ML, Pratchett MS, Goodman BA (2011) Relative gut lengths of coral reef butterflyfishes (Pisces: Chaetodontidae). Coral Reefs 30:1005–1010
Biswas AK, Kaku H, Ji SC, Seoka M, Takii K (2007) Use of soybean meal and phytase for partial replacement of fish meal in the diet of red sea bream, Pagrus major. Aquaculture 267(1–4):284–491
Boza JJ, Moënnoz D, Vuichoud J, Jarret AR, Gaudard-de-Weck D, Fritsché R, Donnet A, Schiffrin EJ, Perrusseau G, Ballévre O (1999) Food deprivation and refeeding influences growth, nutrient retention and functional recovery of rats. J Nutr 129:1340–1346
Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic Press, New York, pp 279–352
Brugman S (2016) The zebrafish as a model to study intestinal inflammation. Dev Comp Immunol 64:82–92
Calduch-Giner JA, Sitjá-Bobadilla A, Pérez-Sánchez J (2016) Gene expression profiling reveals functional specialization along the intestinal tract of a carnivorous teleostean fish (Dicentrarchus labrax). Front Physiol 7:359. doi:10.3389/fphys.2016.00359
Caviedes-Vidal E, Afik D, Martinez del Rio C, Karasov W (2000) Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptive hypothesis. Comp Biochem Physiol Part A 125:11–24
Cheng D, Shami GJ, Morsch M, Chung RS, Braet F (2016) Ultrastructural mapping of the zebrafish gastrointestinal system as a basis for experimental drug studies. BioMed Res Int. doi:10.1155/2016/8758460
Choat JH, Clements KD (1998) Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol Syst. 375–403
Clements KD, Angert ER, Montgomery WL, Choat JH (2014) intestinal microbiota in fishes: what’s known and what’s not. Mol Ecol 23(8):1891–1898
Clissold FJ, Tedder BJ, Conigrave AD, Simpson SJ (2010) The gastrointestinal tract as a nutrient-balancing organ. Proc R Soc B 277:1751–1759
Dahlqvist A (1968) Assay of intestinal disacharidases. Anal Biochem 22:99–107
Davis AM, Unmack PJ, Pusey BJ, Pearson RG, Morgan DL (2013) Ontogenetic development of intestinal length and relationships to diet in an Australasian fish family (Terapontidae). BMC Evol Biol 13
Day RD, Tibbetts IR, Secor SM (2014) Physiological responses to short-term fasting among herbivorous, omnivorous, and carnivorous fishes. J Comp Physiol B 184:497–512
Dearing MD, Schall JJ (1994) Atypical reproduction and sexual dimorphism of the tropical Bonaire island whiptail lizard, Cnemidorphorus murinus. Copeia (3):760–766
Drewe KE, Horn MH, Dickson KA, Gawlicka A (2004) Insectivore to frugivore: ontogenetic changes in gut morphology and digestive enzyme activity in the characid fish Brycon guatemalensis from Costa Rican rainforest streams. J Fish Biol 64:890–902
Dunel-Erb S, Chevalier C, Laurent P, Bach A, Decrock F, Le Maho Y (2011) Restoration of the jejunal mucosa in rats refed after prolonged fasting. Comp Biochem Physiol 129:933–947
Elliott JP, Bellwood DR (2003) Alimentary tract morphology and diet in three coral reef fish families. J Fish Biol 63:1598–1609
Erlanger BF, Kokowski N, Cohen W (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95:271–278
Frierson E, Foltz J (1992) Comparison and estimation of absorptive intestinal surface area in two species of cichlid fish. Trans Am Fish Soc 121:517–523
Fris MB, Horn MH (1993) Effects of diets of different protein content on food consumption, gut retention, protein conversion, and growth of Cebidichthys violaceus (Girard), an herbivorous fish of temperate zone marine waters. J Exp Mar Biol Ecol 166:185–202
Galluser M, Raul F, Canguilhem B (1988) Adaptation of intestinal enzymes to seasonal and dietary changes in a hibernator: the European hamster (Cricetus cricetus). J Comp Physiol B 158:143–149
Garcia-Carreno FL, Albuquerque-Cavalcanti C, Navarrete del Toro MA, Zaniboni-Filho E (2002) Digestive proteinases of Brycon orbignyanus (Characidae, Teleostei): characteristics and effects of protein quality. Comp Biochem Physiol Part B 132:343–352
Garland T, Rose MR (2009) Experimental evolution: concepts, methods, and applications of selection experiments. University of California Press, Berkley
Gawlicka AK, Horn MH (2006) Trypsin gene expression by quantitative in situ hybridization in carnivorous and herbivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Physiol Biochem Zool 79:120–132
German DP (2009a) Inside the guts of wood-eating catfishes: can they digest wood? J Comp Physiol B 179:1011–1023
German DP (2009b) Do herbivorous minnows have “plug-flow reactor” guts? Evidence from digestive enzyme activities, luminal nutrient concentrations and gastrointestinal fermentation. J Comp Physiol B 179:759–771
German DP (2011) Digestive efficiency. In: Farrell AP, Cech JJ, Richards JG, Stevens ED (eds) Encyclopedia of fish physiology, from genome to environment. Elsevier, San Diego
German DP, Bittong RA (2009) Digestive enzyme activities and gastrointestinal fermentation in wood-eating catfishes. J Comp Physiol B 179:1025–1042
German DP, Horn MH (2006) Gut length and mass in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Mar Biol 148:1123–1134
German JB, Xu R, Walzem R, Kinsella JE, Knuckles B, Nakamura M, Yokoyama WH (1996) Effect of dietary fats and barley fiber on total cholesterol and lipoprotein cholesterol distribution in plasma of hamsters. Nutr Res 16(7):1239–1249
German DP, Horn MH, Gawlicka A (2004) Digestive enzyme activities in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Physiol Biochem Zool 77(5):789–804
German DP, Nagle BC, Villeda JM, Ruiz AM, Thomson AW, Contreras-Balderas S, Evans DH (2010a) Evolution of herbivory in a carnivorous clade of minnows (Teleostei: Cyprinidae): effects on gut size and digestive physiology. Physiol Biochem Zool 83:1–18
German DP, Neuberger DT, Callahan MN, Lizardo NR, Evans DH (2010b) Feast to famine: the effects of dietary quality and quantity on the gut structure and function of a detritivorous catfish (Teleostei: Loricariidae). Comp Biochem Physiol Part A 155:281–293
German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397
German DP, Gawlicka AK, Horn MH (2014) Evolution of ontogenetic dietary shifts and associated gut features in prickleback fishes (Teleostei: Stichaeidae). Comp Biochem Physiol B 168:12–18
German DP, Sung A, Jhaveri PK, Agnihotri R (2015) More than one way to be an herbivore: convergent evolution of herbivory using different digestive strategies in prickleback fishes (family Stichaeidae). Zoology 118:161–170
German DP*, Foti DM*, Heras J, Amerkhanian H, Lockwood BL (2016) Elevated gene copy number does not always explain elevated amylase activities in fishes. Physiol Biochem Zool 89:277–293
Ghanbari M, Kneifel W, Domig KJ (2015) A new view of the fish gut microbiome: advances from next-generation sequencing. Aquaculture 448:464–475
Gisbert E, Mozanzadeh MT, Kotzamanis Y, Estevez A (2016) Weaning wild flathead grey mullet (Mugil cephalus) fry with diets with different levels of fish meal substitution. Aquaculture 462:92–100
Gonzalez JM (2012) Preliminary evaluation on the effects of feeds on the growth and early reproductive performance of zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 51(4):412–417
Hakim Y, Uni Z, Hulata G, Harpaz S (2006) Relationship between intestinal brush border enzymatic activity and growth rate in tilapias fed diets containing 30% or 48% protein. Aquaculture 257:420–428
Hakim Y, Rowland SJ, Guy JA, Mifsud C, Uni Z, Harpaz S (2007) Effects of genetic strain and holding facility on the characteristics of alkaline phosphatase and brush border enzymes in silver perch (Bidyanus bidyanus). Aquacult Res 38:361–372
Hall KC, Bellwood DR (1995) Histological effects of cyanide, stress and starvation of the intestinal mucosa of Pomacentrus coelestis, a marine aquarium fish species. J Fish Biol 47(3):438–454
Hedrera MI, Galdames JA, Jimenez-Reyes MF, Reyes AE, Avendano-Herrera R, Romero J, Feijoo CG (2013) Soybean meal induces intestinal inflammation in zebrafish larvae. PloS One 8:e69983
Hernandez MD, Martinez FJ, Jover M, Garcia BG (2007) Effects of partial replacement of fish meal by soybean meal in sharpsnout seabream (Diplodus puntazzo) diet. Aquaculture 263:159–167
Herrel A, Huyghe K, Vanhooydonck B, Backelijau T, Breugelmans K, Grbac I, Van Damme R, Irschick DJ (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proc Natl Acad Sci USA 105(12):4792–4795
Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol Annu Rev 27:167–272
Horn MH, Messer KS (1992) Fish guts as chemical reactors: a model of the alimentary canals of marine herbivorous fishes. Mar Biol 113:527–535
Horn MH, Mailhiot KF, Fris MB, McClanahan LL (1995) Growth, consumption, assimilation and excretion in the marine herbivorous fish Cebidichthys violaceus (Girard) fed natural and high protein diets. J Exp Mar Biol Ecol 190:97–108
Horn MH, Gawlicka A, German DP, Logothetis EA, Cavanagh JW, Boyle KS (2006) Structure and function of the stomachless digestive system in three related species of New World silverside fishes (Atherinopsidae) representing herbivory, omnivory, and carnivory. Mar Biol 149:1237–1245
Jhaveri P, Papastamatiou YP, German DP (2015) Digestive enzyme activities in the guts of bonnethead sharks (Sphyrna tiburo) provide insight into their digestive strategy and evidence for microbial digestion in their hindguts. Comp Biochem Physiol A 189:76–83
Jing L, Zon LI (2011) Zebrafish as a model for normal and malignant hematopoiesis. Dis Model Mech 4:433–438
Karasov W, Douglas A (2013) Comparative digestive physiology. Comprehens Physiol 3:741–783
Karasov W, Hume I (1997) Vertebrate gastrointestinal system. In: Dantzler WH (ed) Handbook of physiology. Volume 1, Sect. 13: comparative physiology. Oxford University Press, New York, pp 409–465
Karasov W, Martinez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, Princeton
Kim KH, Horn MH, Sosa AE, German DP (2014) Sequence and expression of an alpha-amylase gene in four related species of prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and species-level effects. J Comp Physiol B 184(2):221–234
Kohl KD, Brzek P, Caviedes-Vidal E, Karasov WH (2011) Pancreatic and intestinal carbohydrases are matched to dietary starch level in wild passerine birds. Physiol Biochem Zool 84(2):195–203
Kohl KD, Brun A, Magallanes M, Brinkerhoff J, Laspiur A, Acosta JC, Bordenstein SR, Caviedes-Vidal E (2016) Physiological and microbial adjustments to diet quality permit facultative herbivory in an omnivorous lizard. J Exp Biol 219:1903–1912
Kramer DL, Bryant MJ (1995) Intestine length in the fishes of a tropical stream. 2. Relationships to diet—the long and short of a convoluted issue. Environ Biol Fish 42:129–141
Krogdahl Å, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquacult Nutr 9:361–371
Król E, Douglas A, Tocher DR, Crampton VO, Speakman JR, Secombes CJ, Martin CJ (2016) Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon. BMC Genom 17:156
Levey DJ, Place AR, Rey PJ, Martinez del Rio C (1999) An Experimental test of dietary enzyme modulation in pine warblers Dendroica pinus. Physiol Biochem Zool 72(5):576–587
Li Y, Ai Q, Mai K, Xu W, Deng J, Cheng Z (2014) Comparison of high-protein soybean meal and commercial soybean meal partly replacing fish meal on the activities of digestive enzymes and aminotransferases in juvenile Japanese seabass, Lateolabrax japonicus (Cuvier, 1828). Aquaculture 45(6):1051–1060
Lin S, Luo L (2011) Effects of different levels of soybean meal inclusion in replacement for fish meal on growth, digestive enzymes and transaminase activities in practical diets for juvenile tilapia, Oreochromis niloticus × O. aureus. Anim Feed Sci Technol 168:80–87
Linder P, Eshel A, Kolkovski S, Tandler A, Harpaz S (1995) Proteolysis by juvenile sea bass (Dicentrarchus labrax) gastrointestinal enzymes as a method for the evaluation of feed proteins. Fish Physiol Biochem 14(5):399–407
Liu S, Leach SD (2011) Zebrafish models for cancer. Annu Rev Pathol 6:71–93
Magalhaes R, Lopes T, Martins N, Diaz-Rosales P, Couto A, Pousao-Ferreira P, Oliva-Teles A, Peres H (2016) Carbohydrases supplementation increased nutrient utilization in white seabream (Diplodus sargus) juveniles fed high soybean meal diets. Aquaculture 463:43–50
Martin SAM, Dehler CE, Król E (2016) Transcriptomic responses in the fish intestine. Dev Comp Immunol 64:103–117
McDowell EM, Trump BF (1976) Histologic fixatives for diagnostic light and electron microscopy. Arch Pathol Lab Med 100(8):405–414
Moran D, Turner SJ, Clements KD (2005) Ontogenetic development of the gastrointestinal microbiota in the marine herbivorous fish Kyphosus sydneyanus. Microb Ecol 49(4):590–597
Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquacult Res 41:1553–1573
Nayak J, Viswanathan Nair PG, 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 83:1139–1142
Newsome SD, Fogel ML, Kelly L, Martinez del Rio C (2011) Contributions of direct incorporation from diet and microbial amino acids to protein synthesis in Nile tilapia. Funct Ecol 25:1051–1062
Olsson J, Quevedo M, Colson C, Svanback R (2007) Gut length plasticity in perch: into the bowels of resource polymorphisms. Biol J Linn Soc 90:517–523
Parker MO, Millington ME, Combe FJ, Brennan CH (2012) Housing conditions differentially affect physiological and behavioural stress responses of zebrafish, as well as the response to anxiolytics. PLoS One 7:e34992
Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129:69–96
Perera E, Yúfera M (2016) Soybean meal and soy protein concentrate in early diet elicit different nutritional programming effects on juvenile zebrafish. Fish Haus 13(1):61–69
Perez-Jimenez A, Cardenete G, Morales AE, Garcia-Alcazar A, Abellan E, Hidalgo MC (2009) Digestive enzymatic profile of Dentex dentex and response to different dietary formulations. Comp Biochem Physiol Part A 154:157–164
Presnell JK, Schreibman MP (1997) Humason’s animal tissue techniques, 5th edn. Johns Hopkins University Press, Baltimore
Rahmatnejad E, Saki A (2016) Effect of dietary fibres on small intestine histomorphology and lipid metabolism in young broiler chickens. J Anim Physiol Anim Nutr (Berl) 100:665–672
Rawls JF (2012) Special issue: gut microbial communities in health and disease. Gut Microb (4):277–278
Refstie S, Korsøen ØJ, Strorebakken T, Baeverfjord G, Lein I, Roem AJ (2000) Differing nutritional responses to dietary soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Aquaculture 190:49–63
Reimer G (1982) The influence of diet on the digestive enzymes of the Amazon fish Matrinchã, Brycon cf. melanopterus. J Fish Biol 21(6):637–642
Ribeiro L, Moura J, Santos M, Colen R, Rodrigues V, Bandarra N, Soares F, Ramalho P, Barata M, Moura P et al (2015) Effect of vegetable based diets on growth, intestinal morphology, activity of intestinal enzymes and haematological stress indicators in meagre (Argyrosomus regius). Aquaculture 447:116–128
Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5:1595–1608
Russell JR, Young AW, Jorgensen NA (1981) Effect of dietary corn starch intake on pancreatic amylase and intestinal maltase and pH in cattle. J Anim Sci 52:1177–1182
Sabat P, Novoa F, Bozinovic F (1998) Dietary flexibility and intestinal plasticity in birds: a field and laboratory study. Physiol Biochem Zool 71(2):226–236
Sabat P, Lagos J, Bozinovic F (1999) Test of the adaptive modulation hypothesis in rodents: dietary flexibility and enzyme plasticity. Comp Biochem Physiol Part A 123:83–87
Sadler KC, Rawls JF, Farber SA (2013) Getting the inside tract: new frontiers in zebrafish digestive system biology. Zebrafish 10:129–131. doi:10.1089/zeb.2013.1500
Samuelsson LM, Young W, Fraser K, Tannock GW, Lee J, Roy NC (2016) Digestive-resistant carbohydrates affect lipid metabolism in rats. Metabolomics 12:79
Santigosa E, Sanchez J, Medale F, Kaushik S, Perez-Sanchez J, Gallardo MA (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
Schondube JE, Herrera L, Martinez del Rio CM (2001) Diet and the evolution of digestion and renal function in phyllostomid bats. Zool Anal Compl Syst 104(1):59–73
Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56. doi:10.1007/s00360-008-0283-7
Semova I, Carten JD, Stombaugh J, Mackey LC, Knight R, Farber SA, Rawls JF (2012) Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microb 12:277–288
Sibly RM (1981) Strategies of digestion and defecation. In: CR Townsend, Callow P (eds) Physiological ecology: an evolutionary approach to resource use. Sinauer, Sunderland, pp 109–139
Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68:1299–1311
Starck J (1996) Phenotypic plasticity, cellular dynamics, and epithelial turnover of the intestine of Japanese quail (Coturnix coturnix japnica). J Zool Lond 238:53–79
Starck J (2005) Structural flexibility of the digestive system of tetrapods: patterns and processes at the cellular and tissue level. In: Starck J, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers Inc., Enfield, pp 175–200
Starck JM, Kloss E (1995) Structural responses of Japanese quail intestine to different diets. Dtsch Tierärztl Wochenschr 102:146–149
Stephens WZ, Burns AR, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJM (2015) The composition of the zebrafish intestinal microbial community varies across development. ISME J 10(3): 644–654
Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system, 2nd edn. Cambridge University Press, Cambridge
Sullam KE, Dalton CM, Russel JA, Kilham SS, El-Sabaawi R, German DP, Flecker AS (2015) Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies. Oecologia 177:245–257
Timofeeva NM, Egorova VV, Nikitina AA, Dmitrieva YV (2009) Activities of digestive enzymes in rats kept on standard or excessive breast feeding and on low-protein diet at once after weaning. J Evol Biochem Physiol 45(3):356–364
Ulloa P, Iturra P, Neira R, Araneda C (2011) Zebrafish as a model organism for nutrition and growth: towards comparative studies of nutritional genomics applied to aquacultured fishes. Rev Fish Biol Fish 21:649–666
Urán PA, Gonçalves AA, Taverne-Thiele JJ, Schrama JW, Verreth JA, Rombout JHWM (2008) Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 25:751–760
Wagner CE, McIntyre PB, Buels KS, Gilbert DM, Michel E (2009) Diet predicts intestine length in Lake Tanganyika’s cichlid fishes. Funct Ecol 23:1122–1131
Waheed AA, Gupta PD (1997) Changes in structural and functional properties of rat intestinal brush-border membrane during starvation. Life Sci 61:2425–2433
Watanabe T (1982) Lipid nutrition in fish. Comp Biochem Physiol B 73:3–15
Watts SA, Powell M, D’Abramo LR (2012) Fundamental approaches to the study of zebrafish nutrition. ILAR J 53(2):144–160. doi:10.1093/ilar.53.2.144
Wiwgeer MI, Zhao Z, van Merkesteyn RJP, Roehl HH, Hogendoorn PCW (2012) HSPG-deficient zebrafish uncovers dental aspect of multiple Osteochondromas. PLoS One 7(1):e29734
Wong S, Rawls JF (2012) Intestinal microbiota composition in fishes is influenced by host ecology and environment. Mol Ecol 21(13):3100–3102
Wong S*, Waldrop T*, Summerfelt S, Davidson J, Barrows F, Kenney PB, Welch T, Wiens GD, Snekvik K, Rawls JF et al (2013) Aquacultured rainbow trout (Oncorhynchus mykiss) possess a large core intestinal microbiota that is resistant to variation in diet and rearing density. Appl Environ Microbiol 79(16):4974–4984
Wong S, Burns AR, Stephens WZ, Stagaman K, David LA, Guillemin K, Bohannan BJM, Rawls JF (2015) Ontogenetic differences in dietary fat differentially influence microbiota assembly in the zebrafish gut and environment. mBio 6(5):e00687–e00715
Yaghoubi M, Mozanzadeh MT, Marammazi JG, Safari O, Gisbert E (2016) Dietary replacement of fish meal by soy products (soybean meal and isolated soy protein) in silvery-black porgy juveniles (Sparidentex hasta). Aquaculture 464:50–59
Zandoná E, Auer SK, Kilham SS, Reznick DN (2015) Contrasting population and diet influences on gut length of an omnivorous tropical fish, the Tinidadian guppy (Poecilia reticulata). PLoS One. doi:10.1371/journal.pone.0136079
Acknowledgements
We thank Zachary Chan, Abraham Sosa, Faisal Chaabani, Parth Jhaveri, Ritika Agnihotri, Hooree Amerkhanian, Aaron Sung, Diana Gevorgyan, Tanjot Saini, Shirley Kuan, Amy Liang, Nasim Faryabi, Robert Dang, Steven Huynh, Aalia Hardeman, Lauren Strope, Sarwat Siddiqi, Jessie Kaur, Priscilla San Juan, Kunheng Cai, Brandy McCurdy, David Perez, Michelle Herrera, Caitlyn Catabay, Tien Tran, Cam Vandenakker, and Leyna Vo for help in tank maintenance, feedings, and general fish husbandry. We thank the comparative physiology group at UCI for providing guidance and advice, particularly J. Heras, B. Wehrle, and A. Frederick. We are indebted to Andres Carrillo for aid in multiple levels of the husbandry process. We also thank C. Nell for assistance with the running of statistical analyses using Rstudio. This work was funded by University of California, Irvine laboratory start-up funds and National Science Foundation grant IOS-1355224 (both to DPG). Funds were also provided by the National Science Foundation Graduate Research Fellowship Program and the University of California, Irvine Graduate Division Competitive Edge Program (both to SCL).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by I. D. Hume.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Leigh, S.C., Nguyen-Phuc, BQ. & German, D.P. The effects of protein and fiber content on gut structure and function in zebrafish (Danio rerio). J Comp Physiol B 188, 237–253 (2018). https://doi.org/10.1007/s00360-017-1122-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-017-1122-5