Why can't young fish eat plants? Neither digestive enzymes nor gut development preclude herbivory in the young of a stomachless marine herbivorous fish

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 158, Issue 1, 2011, Pages 23-29

  Day, Ryan D ^a   German, Donovan P ^b   Tibbetts, Ian R ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adaptive modulation hypothesis; Halfbeak; Hemiramphidae; Lipase; Pharyngeal mill; Plug flow reactor; RGL; Trypsin; Zihler Index; amylase

Indexed keywords

PROTEINASE; TRIACYLGLYCEROL LIPASE;

ANIMAL TISSUE; ARTICLE; BODY HEIGHT; BODY MASS; BODY SIZE; DIGESTION; ENZYME ACTIVITY; FISH; HERBIVORY; INTESTINE; NONHUMAN; PHARYNX; PRIORITY JOURNAL; TROPHIC LEVEL;

HEMIRAMPHIDAE; HYPORHAMPHUS REGULARIS ARDELIO; PISCES;

EID: 78649634909     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2010.09.010     Document Type: Article

References (72)

1. Al-Hussaini A.H. The feeding habits and the morphology of the alimentary tract of some teleosts living in the neighbourhood of the Marine Biological Station, Ghardaqa, Red Sea. Pub. Mar. Biol. Stat. Al-Ghardaqa 1947, 5:1-61.
2. Anderson T.A. Mechanisms of digestion in the marine herbivore, the luderick, Girella tricuspidata (Quoy and Gaimard). J. Fish Biol. 1991, 39:535-547. 10.1111/j.1095-8649.1991.tb04384.x.
3. Benavides A.G., Cancino J.M., Ojeda F.P. Ontogenetic change in the diet of Aplodactylus punctatus (Pisces: Aplodactylidae): an ecophysiological explanation. Mar. Biol. 1994, 118:1-5. 10.1007/BF00699213.
4. Birch W.R. Some chemical and calorific properties of tropical marine angiosperms compared with those of other plants. J. Appl. Ecol. 1975, 12:201-212. 10.2307/2401729.
5. Bitterlich G. The nutrition of stomachless phytoplanktivorous fish in comparison with Tilapia. Hydrobiologia 1985, 121:173-179. 10.1007/BF00008721.
6. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254. 10.1016/0003-2697(76)90527-3.
7. Bouchard S.S., Bjorndal K.A. Ontogenetic diet shifts and digestive constraints in the omnivorous freshwater turtle Trachemys scripta. Physiol. Biochem. Zool. 2005, 79:150-158. 10.1086/498190.
8. Carr W.E.S., Adams C.A. Food habits of juvenile marine fishes occupying seagrass beds in the estuarine zone near Crystal River, Florida. Trans. Am. Fish. Soc. 1973, 102:511-540. 10.1577/1548-8659(1973) 102<511:FHOJMF>2.0.CO;2.
9. Carseldine L., Tibbetts I.R. Dietary analysis of the herbivorous hemiramphid Hyporhamphus regularis ardelio: an isotopic approach. J. Fish Biol. 2005, 66:1589-1600. 10.1111/j.0022-1112.2005.00701.x.
10. Castillo-Yáñez F.J., Pancheco-Aguilar R., García-Carreño F.L., Navarrete-Del Toro M.A. Isolation and characterization of trypsin from pyloric caeca of Monterey sardine Sardinops sagax caerulea. Comp. Biochem. Physiol. B 2005, 140:91-98. 10.1016/j.cbpc.2004.09.031.
11. Chakrabarti I.A., Gani M.A., Chaki K.K., Sur R., Misra K.K. Digestive enzymes in 11 freshwater teleost fish species in relation to food habit and niche segregation. Comp. Biochem. Phys. A 1995, 112:167-177. 10.1016/0300-9629(95)00072-F.
12. Choat J.H., Clements K.D. Vertebrate herbivores in marine and terrestrial systems: a nutritional ecology perspective. Annu. Rev. Ecol. Syst. 1998, 29:375-403. 10.1146/annurev.ecolsys.29.1.375.
13. Clements K.D., Raubenheimer D., Choat J.H. Nutritional ecology of marine herbivorous fishes: ten years on. Func. Ecol. 2009, 23:79-92. 10.1111/j.1365-2435.2008.01524.x.
14. Cockson A., Bourn D. Protease and amylase in the digestive tract of Barbus paludinosus. Hydrobiologia 1973, 43:357-363. 10.1007/BF00015356.
15. Coetzee D.J. Analysis of the gut contents of the needlefish Hyporhamphus knysnaensis (Smith) from Rondevlei, South Cape. S. Afr. J. Zool. 1981, 16:14-20.
16. Dall W., Smith D.M., Moore L.E. Biochemical composition of some prey species of Penaeus esculentus Haswell (Penaeidae: Decapoda). Aquaculture 1991, 96:151-166.
17. De Almeida L.C., Lundstedt L.M., Moraes G. Digestive enzyme responses of tambaqui (Colossoma macropomum) fed on different levels of protein and lipid. Aquac. Nutr. 2006, 12:443-450. 10.1111/j.1365-2095.2006.00446.x.
18. Drewe K.E., Horn M.H., Dickson K.A., Gawlicka A. 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. 2004, 64:890-902. 10.1111/j.1095-8649.2004.0357.x.
19. Elliott J.P., Bellwood D.R. Alimentary tract morphology and diet in three coral reef fish families. J. Fish Biol. 2003, 63:1598-1609. 10.1111/j.1095-8649.2003.00272.x.
20. Ferraris R.P., Ahearn G.A. Sugar and amino acid transport in fish intestine. Comp. Biochem. Physiol. A 1984, 77:397-413. 10.1016/0300-9629(84)90204-4.
21. Fish G.R. The comparative activity of some digestive enzymes in the alimentary canal of Tilapia and perch. Hydrobiologia 1960, 15:161-178. 10.1007/BF00048084.
22. Frierson E.W., Foltz J.W. Comparison and estimation of absorptive intestinal surface areas in two species of cichlid fish. Trans. Am. Fish. Soc. 1992, 121:517-523. 10.1577/1548-8659(1992)121<0517:CAEOAI>2.3.CO;2.
23. Fris M.B., Horn M.H. 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. 1993, 166:185-202. 10.1016/0022-0981(93)90218-D.
24. Gerking S.D. Feeding Ecology of Fish 1994, Academic Press, San Diego, CA.
25. German D.P., Horn M.H., Gawlicka A. Digestive enzyme activities in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Physiol. Biochem. Zool. 2004, 77:789-804. 10.1086/422228.
26. German D.P., Horn M.H. Gut length and mass in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Mar. Biol. 2006, 148:1123-1134. 10.1007/s00227-005-0149-4.
27. German D.P. Inside the guts of wood-eating catfishes: can they digest wood?. J. Comp. Physiol. B 2009, 179:1011-1023. 10.1007/s00360-009-0381-1.
28. German D.P. Do herbivorous minnows have "plug-flow reactor" guts? Evidence from digestive enzyme activities, gastrointestinal fermentation, and luminal nutrient concentrations. J. Comp. Physiol. B 2009, 179:759-771. 10.1007/s00360-009-0359-z.
29. German D.P., Bittong R.A. Digestive enzyme activities and gastrointestinal fermentation in wood-eating catfishes. J. Comp. Physiol. B 2009, 179:1025-1042. 10.1007/s00360-009-0383-z.
30. German D.P., Nagle B.C., Villeda J.M., Ruiz A.M., Thompson A.W., Bald S.C., Evans D.H. Evolution of herbivory in a carnivorous clade of minnows (Teleostei: Cyprinidae): effects on gut size and digestive physiology. Physiol. Biochem. Zool. 2010, 83:1-18. 10.1086/648510.
31. Hidalgo M.C., Urea E., Sanz A. Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities. Aquaculture 1999, 170:267-283. 10.1016/S0044-8486(98)00413-X.
32. Hofer R., Schiemer F. Proteolytic activity in the digestive tract of several species of fish with different feeding habits. Oecologia 1981, 48:342-345. 10.1007/BF00346492.
33. Honkanen R.E., Rigler M.W., Patton J.S. Dietary fat assimilation and bile salt absorption in the killifish intestine. Am. J. Physiol.-Gastr. L. 1985, 249:399-407.
34. Horn M.H. Biology of marine herbivorous fishes. Oceanogr. Mar. Biol. 1989, 27:167-272.
35. Horn M.H., Gawlicka A.K., German D.P., Logothetis E.A., Cavanagh J.W., Boyle K.S. 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. 2006, 149:1237-1245. 10.1007/s00227-006-0281-9.
36. Horn M.H., Mailhiot K.F., Fris M.B., McClanahan L.L. Growth, consumption, assimilation and excretion in the marine herbivorous fish Cebidichthys violaceus (Girard) fed natural and high protein diets. J. Exp. Mar. Biol. Ecol. 1995, 190:97-108. 10.1016/0022-0981(95)00034-O.
37. Horn M.H., Messer K.S. Fish guts as chemical reactors - a model of the alimentary canals of marine herbivorous fishes. Mar. Biol. 1992, 113:527-535. 10.1007/BF00349695.
38. Iijima N., Tanaka S., Ota Y. Purification and characterization of bile salt-activated lipase from the hepatopancreas of red sea bream, Pagrus major. Fish Physiol. Biochem. 1998, 18:59-69. 10.1023/A:1007725513389.
39. Kapoor B.G., Smit H., Verighina I.A. The alimentary canal and digestion in teleosts. Adv. Mar. Biol. 1975, 13:109-239. 10.1016/S0065-2881(08)60281-3.
40. Karasov W.H., Hume I.D. Vertebrate gastrointestinal system. Handbook of Comparative Physiology 1997, 409-480. American Physiological Society, Bethesda, MD. W. Danzler (Ed.).
41. Karasov W.H., Martinez del Rio C. Physiological ecology: how animals process energy, nutrients, and toxins 2007, Princeton University Press, Princeton, NJ.
42. Klumpp D.W., Nichols P.D. Nutrition of the southern sea garfish Hyporhamphus melanochir: gut passage rate and daily consumption of two food types and assimilation of seagrass components. Mar. Ecol. Prog. Ser. 1983, 12:207-216. 10.3354/meps012207.
43. Kramer D., Bryant M. Intestine length in the fishes of a tropical stream: 1. Ontogenetic allometry. Environ. Biol. Fish. 1995, 42:115-127. 10.1007/BF00001990.
44. Kramer D., Bryant M. Intestine length in the fishes of a tropical stream: 2. Relationships to diet - the long and short of a convoluted issue. Environ. Biol. Fish. 1995, 42:129-141. 10.1007/BF00001991.
45. Kuz'mina V.V., Golovanova I.L., Izvekova G.I. Influence of temperature and season on some characteristics of intestinal mucosa carbohydrases in six freshwater fishes. Comp. Biochem. Physiol. B 1996, 113:255-260. 10.1016/0305-0491(95)02019-5.
46. 2+, gel filtrations. Comp. Biochem. Physiol. B 1977, 57:359-363. 10.1016/0305-0491(77)90067-0.
47. Logothetis E.A., Horn M.H., Dickson K.A. Gut morphology and function in Atherinops affinis (Teleostei: Atherinopsidae), a stomachless omnivore feeding on macroalgae. J. Fish Biol. 2001, 59:1298-1312. 10.1111/j.1095-8649.2001.tb00193.x.
48. Manjakasy J.M., Day R.D., Kemp A., Tibbetts I.R. Functional morphology of digestion in the stomachless, piscivorous needlefish Strongylura leiura ferox (Teleostei: Beloniformes). J. Morphol. 2009, 270:1155-1165. 10.1002/jmor.10745.
49. Montgomery W.L. Diet and gut morphology in fishes, with special reference to the monkeyface prickleback, Cebidichthys violaceus (Stichaeidae: Blennioidei). Copeia 1977, 1977:178-182. 10.2307/1443527.
50. Montgomery J.L.M., Targett T.E. The nutritional role of seagrass in the diet of the omnivorous pinfish Lagodon rhomboides (L.). J. Exp. Mar. Biol. Ecol. 1992, 158:37-57. 10.1016/0022-0981(92)90307-V.
51. Moran D., Clements K.D. Diet and endogenous carbohydrases in the temperate marine herbivorous fish Kyphosus sydneyanus. J. Fish Biol. 2002, 60:1190-1203. 10.1111/j.1095- 8649.2002.tb01714.x.
52. Neighbors M.A., Horn M.H. Nutritional quality of macrophytes eaten and not eaten by two temperatezone herbivorous fishes: a multivariate comparison. Mar. Biol. 1991, 108:471-476. 10.1007/BF01313657.
53. Nichols P.D., Klumpp D.W., Johns R.B. Lipid components of the seagrasses Posidonia australis and Heterozostera tasmanica as indicators of carbon source. Phytochemical 1982, 21:1613-1621. 10.1016/S0031-9422(82)85027-9.
54. Papoutsoglou E.S., Lyndon A.R. Digestive enzymes along the alimentary tract of the parrotfish Sparisoma cretense. J. Fish Biol. 2006, 69:130-140. 10.1111/j.1095-8649.2006.01082.x.
55. Penry D.L., Jumars P.A. Modeling animal guts as chemical reactors. Am. Nat. 1987, 129:69-96. 10.1086/284623.
56. Pillans R.D., Franklin C.E., Tibbetts I.R. Food choice in Siganus fuscescens: influence of macrophyte nutrient content and availability. J. Fish Biol. 2004, 64:297-309. 10.1111/j.0022-1112.2004.00261.x.
57. Preiser H., Schmitz J., Maestracci D., Crane R.K. Modification of an assay for trypsin and its application for the estimation of enteropeptidase. Clin. Chim. Acta 1975, 59:169-175. 10.1016/0009-8981(75)90025-X.
58. Randall J.E. Food habits of reef fishes of the West Indies. Stud. Trop. Oceanogr. 1967, 5:665-847.
59. Robertson A.I., Klumpp D.W. Feeding habits of the southern Australian garfish Hyporhamphus melanochir: a diurnal herbivore and nocturnal carnivore. Mar. Ecol. Prog. Ser. 1983, 10:197-201. 10.3354/meps010197.
60. Rosenthal H., Paffenhöfer G.A. On the digestion rate and calorific content of food and feces in young gar fish. Naturwissenschaften 1972, 59:274-275. 10.1007/BF00610211.
61. Skea G.L., Mountfort D.O., Clements K.D. Gut carbohydrases from the New Zealand marine herbivorous fishes Kyphosus sydneyanus (Kyphosidae), Aplodactylus arctidens (Aplodactylidae) and Odax pullus (Labridae). Comp. Biochem. Physiol. B 2005, 140:259-269. 10.1016/j.cbpc.2004.10.008.
62. Smoot J.C., Findlay R.H. Digestive enzyme and gut surfactant activity of detritivorous gizzard shad (Dorosoma cepedianum). Can. J. Fish. Aquat. Sci. 2000, 57:1113-1119. 10.1139/cjfas-57-6-1113.
63. Stoner A.W., Livingston R.J. Ontogenetic patterns in diet and feeding morphology in sympatric sparid fishes from seagrass meadows. Copeia 1984, 1984:174-187. 10.2307/1445050.
64. Stroband H.W.J., Van Der Veen F.H. Localization of protein absorption during transport. J. Exp. Zool. 1981, 218:149-156. 10.1002/jez.1402180207.
65. Tengjaroenkul B., Smith B.J., Caceci T., Smith S.A. Distribution of intestinal enzyme activities along the intestinal tract of cultured Nile tilapia, Oreochromis niloticus L. Aquaculture 2000, 182:317-327. 10.1016/S0044-8486(99)00270-7.
66. Tibbetts, I.R., 1991. The trophic ecology, functional morphology and phylogeny of the Hemiramphidae (Beloniformes). PhD thesis, University of Queensland, St. Lucia.
67. Tibbetts I.R., Carseldine L. Anatomy of a hemiramphid pharyngeal mill with reference to Arrhamphus sclerolepis krefftii (Steindachner) (Teleostei: Hemiramphidae). J. Morphol. 2003, 255:228-243. 10.1002/jmor.10057.
68. Tibbetts I.R., Carseldine L. Trophic shifts in three subtropical Australian halfbeaks (Teleostei: Hemiramphidae). Mar. Freshwater Res. 2005, 56:925-932. 10.1071/MF04305.
69. Tibbetts I.R., Day R.D., Carseldine L. Development of the pharyngeal dentition of two herbivorous hemiramphids (Teleostei: Hemiramphidae) and implications for the hemiramphid ontogenetic trophic shift. Mar. Freshwater Res. 2007, 59:117-124. 10.1071/MF07026.
70. Waltham N.J., Connolly R.M. Trophic strategies of garfish, Arrhamphus sclerolepis, in natural coastal wetlands and artificial urban waterways. Mar. Biol. 2006, 148:1135-1141. 10.1007/s00227-005-0154-7.
71. White T.C.R. When is a herbivore not a herbivore?. Oecologia 1985, 67:596-597. 10.1007/BF00790034.
72. Zihler F. Gross morphology and configuration of digestive tracts of Cichlidae (Teleostei, Perciformes): phylogenetic and functional significance. Neth. J. Zool. 1982, 32:544-571. 10.1163/002829682X00210.