More than one way to be an herbivore: Convergent evolution of herbivory using different digestive strategies in prickleback fishes (Stichaeidae)

Zoology

Volumn 118, Issue 3, 2015, Pages 161-170

  German, Donovan P ^a   Sung, Aaron ^a   Jhaveri, Parth ^a   Agnihotri, Ritika ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Digestive physiology; Digestive tract; Fish nutritional ecology; Microbial digestion

Indexed keywords

ANIMALIA; ANOPLARCHUS PURPURESCENS; CEBIDICHTHYS VIOLACEUS; PHYTICHTHYS CHIRUS; PISCES; STICHAEIDAE; XIPHISTER ATROPURPUREUS; XIPHISTER MUCOSUS;

ENZYME;

ANIMAL; CLASSIFICATION; DIET; DIGESTION; ENZYMOLOGY; EVOLUTION; HERBIVORY; INTESTINE; METABOLISM; PERCIFORMES; PHYLOGENY; PHYSIOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; DIET; DIGESTION; ENZYMES; HERBIVORY; INTESTINES; PERCIFORMES; PHYLOGENY;

EID: 84930481902     PISSN: 09442006     EISSN: 18732720     Source Type: Journal    
DOI: 10.1016/j.zool.2014.12.002     Document Type: Article

References (63)

1. Alliot E. Absorption intestinale de l' N-acetyl-glucosamine chez la petite rousette (Scylliorhinus canicula). Compt. Rend. Seances Soc. Biol. Fil. 1967, 161:2544-5546.
2. Allison S.D., Chacon S.S., German D.P. Substrate concentration constraints on microbial decomposition. Soil Biol. Biochem. 2014, 79:43-49.
3. Axelsson E., Ratnakumar A., Arendt M.L., Maqbool K., Webster M.T., Perloski M., Liberg O., Arnemo J.M., Hedhammar A., Lindblad-Toh K. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 2013, 495:360-364.
4. Boyle K.S., Horn M.H. Comparison of feeding guild structure and ecomorphology of intertidal fish assemblages from central California and central Chile. Mar. Ecol. Progr. Ser. 2006, 319:65-84.
5. Chan A.S., Horn M.H., Dickson K.A., Gawlicka A. Digestive enzyme activity in carnivores and herbivores: comparisons among four closely related prickleback fishes (Teleostei: Stichaeidae) from a California rocky intertidal habitat. J. Fish Biol. 2004, 65:848-858.
6. Chereshnev I.A., Radchenko O.A., Petrovskaya A.V. Relationships and position of the taxa of the subfamily Xiphisterinae in the system of the suborder Zoarcoidei (Perciformes). Russ. J. Mar. Biol. 2013, 39:276-286.
7. Choat J.H., Clements K.D. Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annu. Rev. Ecol. Syst. 1998, 29:375-403.
8. Choat J.H., Robbins W.D., Clements K.D. The trophic status of herbivorous fishes on coral reefs. 2. Food processing modes and trophodynamics. Mar. Biol. 2004, 145:445-454.
9. Clements K.D., Choat J.H. Comparison of herbivory in the closely-related marine fish genera Girella and Kyphosus. Mar. Biol. 1997, 127:579-586.
10. Clements K.D., Raubenheimer D. Feeding and nutrition. The Physiology of Fishes 2006, 47-82. CRC Press, Boca Raton, FL. D.H. Evans (Ed.).
11. Clements K.D., Rees D. Preservation of inherent contractility in isolated gut segments of herbivorous and carnivorous marine fish. J. Comp. Physiol. B 1998, 168:61-72.
12. Clements K.D., Gleeson V., Slaytor M. Short-chain fatty acid metabolism in temperate marine herbivorous fish. J. Comp. Physiol. B 1994, 164:372-377.
13. Clements K.D., Raubenheimer D., Choat J.H. Nutritional ecology of marine herbivorous fishes: ten years on. Funct. Ecol. 2009, 23:79-92.
14. Clements K.D., Angert E.R., Montgomery W.L., Choat J.H. Intestinal microbiota in fishes: what's known and what's not. Mol. Ecol. 2014, 23:1891-1898.
15. Crossman D.J., Choat J.H., Clements K.D. Nutritional ecology of nominally herbivorous fishes on coral reefs. Mar. Ecol. Prog. Ser. 2005, 296:129-142.
16. Dahlqvist A. Assay of intestinal disacharidases. Anal. Biochem. 1968, 22:99-107.
17. Danulat E. The effects of various diets on chitinase and β-glucosidase activities and the condition of cod, Gadus morhua. J. Fish Biol. 1986, 28:191-197.
18. Day R.D., German D.P., Manjakasy J.M., Farr I., Hansen J., Tibbetts I.R. Enzymatic digestion in stomachless fishes: how a simple gut accommodates both herbivory and carnivory. J. Comp. Physiol. B 2011, 181:603-613.
19. Erlanger B.F., Kokowsky N., Cohen W. The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 1961, 95:271-278.
20. Felicetti L., Shipley L., Witmer G., Robbins C.T. Digestibility, nitrogen excretion, and mean retention time by North American porcupines (Erethizon dorsatum) consuming natural forages. Physiol. Biochem. Zool. 2000, 73:772-780.
21. Ferry-Graham L.A., Hernandez L.P., Gibb A.C., Pace C. Unusual kinematics and jaw morphology associated with piscivory in the poeciliid, Belonesox belizanus. Zoology 2010, 113:140-147.
22. 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.
23. 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.
24. German D.P. Inside the guts of wood-eating catfishes: can they digest wood?. J. Comp. Physiol. B 2009, 179:1011-1023.
25. German D.P. Digestive efficiency. Encyclopedia of Fish Physiology: From Genome to Environment 2011, 1596-1607. Academic Press, San Diego. A.P. Farrel (Ed.).
26. German D.P., Bittong R.A. Digestive enzyme activities and gastrointestinal fermentation in wood-eating catfishes. J. Comp. Physiol. B 2009, 179:1025-1042.
27. 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.
28. 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.
29. German D.P., Nagle B.C., Villeda J.M., Ruiz A.M., Thomson A.W., Contreras-Balderas S., 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.
30. German D.P., Neuberger D.T., Callahan M.N., Lizardo N.R., Evans D.H. 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. A 2010, 155:281-293.
31. German D.P., Weintraub M.N., Grandy A.S., Lauber C.L., Rinkes Z.L., Allison S.D. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol. Biochem. 2011, 43:1387-1397.
32. German D.P., Gawlicka A.K., Horn M.H. Evolution of ontogenetic dietary shifts and associated gut features in prickleback fishes (Teleostei: Stichaeidae). Comp. Biochem. Physiol. B 2014, 168:12-18.
33. Goodrich T.D., Morita R.Y. Incidence and estimation of chitinase activity associated with marine fish and other estuarine samples. Mar. Biol. 1977, 41:349-353.
34. Gutowska M., Drazen J., Robison B. Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comp. Biochem. Physiol. A 2004, 139:351-358.
35. Hofmann R. Evolutionary steps of ecophysiological adaptation and diversification of ruminants - a comparative view of their digestive system. Oecologia 1989, 78:443-457.
36. Horn M.H., Messer K.S. Fish guts as chemical reactors: a model for the alimentary canals of marine herbivorous fishes. Mar. Biol. 1992, 113:527-535.
37. Horn M.H., Neighbors M.A., Murray S.N. Herbivore responses to a seasonally fluctuating food supply: growth potential of two temperate intertidal fishes based on the protein and energy assimilated from their macroalgal diets. J. Exp. Mar. Biol. Ecol. 1986, 103:217-234.
38. Horn M.H., Gawlicka A., 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.
39. Karasov W.H. Digestive physiology: a view from molecules to ecosystem. Am. J. Physiol. - Regul. Integr. Comp. Physiol. 2011, 301:R276-R284.
40. Karasov W.H., Martínez del Rio C. Physiological Ecology: How Animals Process Energy, Nutrients, and Toxins 2007, Princeton University Press, Princeton, NJ.
41. Kim K.H., Horn M.H., Sosa A.E., German D.P. Sequence and expression of an α-amylase gene in four related species of prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and species-level effects. J. Comp. Physiol. B 2014, 184:221-234.
42. Kohl K.D., Brzek P., Caviedes-Vidal E., Karasov W.H. Pancreatic and intestinal carbohydrases are matched to dietary starch level in wild passerine birds. Physiol. Biochem. Zool. 2011, 84:195-203.
43. Lujan N.K., German D.P., Winemiller K.O. Do wood grazing fishes partition their niche? Morphological and isotopic evidence for trophic segregation in Neotropical Loricariidae. Funct. Ecol. 2011, 25:1327-1338.
44. Lujan N.K., Armbruster J.W., Lovejoy N.R., López-Fernández H. Multilocus molecular phylogeny of the suckermouth armored catfishes (Siluriformes: Loricariidae) with a focus on subfamily Hypostominae. Mol. Phylogenet. Evol. 2015, 82:269-288.
45. Mountfort D., Campbell J., Clements K.D. Hindgut fermentation in three species of marine herbivorous fish. Appl. Environ. Microbiol. 2002, 68:1374-1380.
46. Painter T.J. Algal polysaccharides. The Polysaccharides 1983, vol. 2:196-285. Academic Press, New York, NY.
47. Peres G., Boge B., Colin D., Rigal A. Effects of temperature on the fish digestive process. Enzymic activities and intestinal absorption. Rev. Trav. Inst. Pêches Marit. 1973, 37:223-232.
48. Perry G.H., Dominy N.J., Claw K.G., Lee A.S., Fiegler H., Redon R., Werner J., Villanea F.A., Mountain J.L., Misra R., Carter N.P., Lee C., Stone A.C. Diet and the evolution of human amylase gene copy number variation. Nat. Genet. 2007, 39:1256-1260.
49. Pryor G.S., Bjorndal K. Symbiotic fermentation, digesta passage, and gastrointestinal morphology in bullfrog tadpoles (Rana catesbeiana). Physiol. Biochem. Zool. 2005, 78:201-215.
50. Ralston S.L., Horn M.H. High tide movements of the temperate-zone herbivorous fish Cebidichthys violaceus (Girard) as determined by ultrasonic telemetry. J. Exp. Mar. Biol. Ecol. 1986, 98:35-50.
51. Saba M. Trophic Ontogeny in Four Closely Related Species of Herbivorous and Carnivorous Prickleback Fishes (Stichaeidae) 2004, (Master's thesis), California State University, Fullerton.
52. Sibly R.M. Strategies of digestion and defecation. Physiological Ecology: An Evolutionary Approach to Resource Use 1981, 109-139. Sinauer Associates, Sunderland. C.R. Townsend, P. Calow (Eds.).
53. Skea G., Mountfort D., 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.
54. Skea G., Mountfort D., Clements K.D. Contrasting digestive strategies in four New Zealand herbivorous fishes as reflected by carbohydrase activity profiles. Comp. Biochem. Physiol. B 2007, 146:63-70.
55. Smith P., Krohn R., Hermanson G., Mallia A., Gartner F., Provenzano M., Fujimoto E., Goeke N., Olson B., Klenk D. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150:76-85.
56. Stevens C.E., Hume I.D. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol. Rev. 1998, 78:393-427.
57. Sorenson L., Santini F., Carnevale G., Alfaro M.E. A multi-locus timetree of surgeonfishes (Acanthuridae, Percomorpha), with revised family taxonomy. Mol. Phylogenet. Evol. 2013, 68:150-160.
58. Taylor B.W., Flecker A.S., Hall R.O. Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 2006, 313:833-836.
59. Urquhart K.A.F. Macroalgal digestion by Cebidichthys violaceus, a temperate marine fish with highly acidic stomach fluids 1984, (Master's thesis), California State University, Fullerton.
60. Vispo C., Hume I.D. The digestive tract and digestive function in the North American porcupine and beaver. Can. J. Zool. 1995, 73:967-974.
61. Wainwright P.C., Smith W.L., Price S.A., Tang K.L., Sparks J.S., Ferry L.A., Kuhn K.L., Eytan R.I., Near T.J. The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond. Syst. Biol. 2012, 61:1001-1027.
62. White W.L., Coveny A.H., Robertson J., Clements K.D. Utilisation of mannitol by temperate marine herbivorous fishes. J. Exp. Mar. Biol. Ecol. 2010, 391:50-56.
63. Willmott M.E., Clements K.D., Wells R.M.G. The influence of diet and gastrointestinal fermentation on key enzymes of substrate utilization in marine teleost fishes. J. Exp. Mar. Biol. Ecol. 2005, 317:97-108.