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Reviews in Fish Biology and Fisheries

, Volume 27, Issue 3, pp 561–585 | Cite as

The nutritional physiology of sharks

  • Samantha C. LeighEmail author
  • Yannis Papastamatiou
  • Donovan P. German
Reviews

Abstract

Sharks compose one of the most diverse and abundant groups of consumers in the ocean. Consumption and digestion are essential processes for obtaining nutrients and energy necessary to meet a broad and variable range of metabolic demands. Despite years of studying prey capture behavior and feeding habits of sharks, there has been little exploration into the nutritional physiology of these animals. To fully understand the physiology of the digestive tract, it is critical to consider multiple facets, including the evolution of the system, feeding mechanisms, digestive morphology, digestive strategies, digestive biochemistry, and gastrointestinal microbiomes. In each of these categories, we make comparisons to what is currently known about teleost nutritional physiology, as well as what methodology is used, and describe how similar techniques can be used in shark research. We also identify knowledge gaps and provide suggestions to continue the progression of the field, ending with a summary of new directions that should be addressed in future studies regarding the nutritional physiology of sharks.

Keywords

Digestive efficiency Digestive biochemistry Gastrointestinal tract Microbiome Spiral intestine Stable isotopes 

Notes

Acknowledgements

We would like to thank the comparative physiology group at UCI for providing guidance and advice, particularly J. Heras, B. Wehrle, and A. Frederick. J. German and A. Dingeldein helped with image creation and analysis. CT scanning facility and assistance provided by A. Summers and the University of Washington at Friday Harbor Laboratories.

References

  1. Aldman G, Jonsson AC, Jensen J, Holmgren S (1989) Gastrin/CCK-like peptides in the spiny dogfish, squalus acanthias-concentrations and actions in the gut. Comp Biochem Physiol C-Pharmacol Toxicol Endocrinol 91(1):103–108CrossRefGoogle Scholar
  2. Anderson WG, McCabe C, Brandt C, Wood CM (2015) Examining urea flux across the intestine of the spiny dogfish, Squalus acanthias. Comp Biochem Physiol 181:71–78CrossRefGoogle Scholar
  3. Andrews PLR, Young JZ (1988) The effect of peptides on the motility of the stomach, intestine and rectum in the skate. Comp Biochem Physiol CB9:343–348Google Scholar
  4. Andrews PLR, Young JZ (1993) Gastric motility patterns for digestion and vomiting evoked by sympathetic nerve stimulation and 5-hydroxytryptamine in the dogfish Scyliorhinus canicula. Philos Trans R Soc Lond 342:363–380CrossRefGoogle Scholar
  5. Armstrong JB, Schindler DE (2011) Excess digestive capacity in predators reflects a life of feast and famine. Nature 476:84–87PubMedCrossRefGoogle Scholar
  6. Baldridge H (1970) Sinking factors and average densities of Florida sharks as a function of liver buoyancy. Copeia 4:744–754CrossRefGoogle Scholar
  7. Ballantyne JS (2016) Metabolism of elasmobranchs (Jaws II). In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: internal processes. Elsevier, LondonGoogle Scholar
  8. Beckmann CL, Mitchell JG, Seuront L, Stone DA, Huveneers C (2013) Experimental evaluation of fatty acid profiles as a technique to determine dietary composition in benthic elasmobranchs. Physiol Biochem Zool 86:266–278PubMedCrossRefGoogle Scholar
  9. Beckmann CL, Mitchell JG, Stone DA, Huveneers C (2014) Inter-tissue differences in fatty acid incorporation as a result of dietary oil manipulation in Port Jackson Sharks (Heterodontus portusjacksoni). Lipids 49(6):577–590PubMedCrossRefGoogle Scholar
  10. Bernal D, Lowe CG (2016) Field studies of elasmobranch physiology. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: structure and interaction with environment. Elsevier, LondonGoogle Scholar
  11. Bertin L (1958) Appareil digestif. In: Grasse PP (ed) Traite de Zoologic, vol 13. Mason, Paris, pp 1248–1302Google Scholar
  12. Bethea DM, Hale L, Carlson JK, Cortés E, Manire CA, Gelsleichter J (2007) Geographic and ontogenetic variation in the diet and daily ration of the bonnethead shark, Sphyrna tiburo, from the eastern Gulf of Mexico. Mar Biol 152:1009–1020CrossRefGoogle Scholar
  13. Bethea DM, Carlson JK, Hollensead LD, Papastamatiou YP, Graham BS (2011) A comparison of the foraging ecology and bioenergetics of the early life-stages of two sympatric hammerhead sharks. Bull Mar Sci 87(4):873–889CrossRefGoogle Scholar
  14. Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic Press, New York, pp 280–352Google Scholar
  15. Bucking C (2016) Feeding and digestion in elasmobranchs: tying diet and physiology together. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: structure and interaction with environment. Elsevier, LondonGoogle Scholar
  16. Bush AC, Holland KH (2002) Food limitation in a nursery area: estimates of daily ration in juvenile scalloped hammerheads, Sphyrna lewini, in Kanéohe Bay, O’ahu. J Exp Mar Biol Ecol 278:157–178CrossRefGoogle Scholar
  17. Calduch-Giner JA, Sitja-Bodadilla A, Perez-Sanches J (2016) Gene expression profiling reveals functional specialization along the intestinal tract of a carnivorous teleostean fish (Dicentrarchus labrax). Front Physiol. doi: 10.3389/fphys.2016.00359 PubMedPubMedCentralGoogle Scholar
  18. Camp AL, Brainerd EL (2014) Role of axial muscles in powering mouth expansion during suction feeding in largemouth bass (Micropterus salmoides). J Exp Biol 217(8):1333–1345PubMedCrossRefGoogle Scholar
  19. Camp AL, Roberts TJ, Brainerd EL (2015) Swimming muscles power suction feeding in largemouth bass. Proc Natl Acad Sci USA 112(28):8690–8695PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cant J, McBride B, Croom W Jr (1996) The regulation of intestinal metabolism and its impact on whole animal energetics. J Anim Sci 74:2541–2553PubMedCrossRefGoogle Scholar
  21. Carlisle AB, Litvin SY, Madigan DJ, Lyons K, Bigman JS, Ibarra M, Bizzarro JJ (2017) Interactive effects of urea and lipid content confound stable isotope analysis in elasmobranch fishes. Can J Fish Aquat Sci 74(3):419–428CrossRefGoogle Scholar
  22. Castro L, Goncalves O, Mazan S, Tay B, Venkatesh B, Wilson J (2014) Recurrent gene loss correlates with the evolution of stomach phenotypes in gnathostome history. Proc R Soc B 281:2013–2669Google Scholar
  23. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Delta N-15 and Delta C-13): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46(2):443–453CrossRefGoogle Scholar
  24. Caut S, Jowers MJ, Michel L, Lepoint G, Fisk AT (2013) Diet- and tissue-specific incorporation of isotopes in the shark Scyliorhinus stellaris, a North Sea mesopredator. Mar Ecol Prog Ser 492:185–198CrossRefGoogle Scholar
  25. Chatchavalvanich K, Marcos R, Poonpirom J, Thongpan A, Rocha E (2006) Histology of the digestive tract of the freshwater stingray Himantura signifer Compagno and Roberts, 1982 (Sharkii, Dasyatidae). Anat Embryol 211:507–518PubMedCrossRefGoogle Scholar
  26. Choat JH, Clements KD (1998) Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol Syst 29:375–403CrossRefGoogle Scholar
  27. Churchill DA, Heithaus MR, Vaudo JJ, Grubbs RD, Gastrich K, Castro JI (2015) Trophic interactions of common elasmobranchs in deep-sea communities of the Gulf of Mexico revealed through stable isotope and stomach content analysis. Deep-Sea Res II 115:92–102CrossRefGoogle Scholar
  28. Clements KD, Raubenheimer D, Choat JH (2009) Nutritional ecology of marine herbivorous fishes: ten years on. Funct Ecol 23(1):79–92CrossRefGoogle Scholar
  29. Clements KD, Angert ER, Montgomery WL, Choat JH (2014) Intestinal microbiota in fishes: what’s known and what’s not. Mol Ecol 23:1891–1898PubMedCrossRefGoogle Scholar
  30. Clements KD, German DP, Piche J, Tribollet A, Choat JH (2017) Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol J Linn SocGoogle Scholar
  31. Cnudde C, Moens T, Werbrouck E, Lepoint G, Van Gansbeke D, De Troch M (2015) Trophodynamics of estuarine intertidal harpacticoid copepods based on stable isotope composition and fatty acid profiles. Mar Ecol Prog Ser 524:225–239CrossRefGoogle Scholar
  32. Compagno L (2008) Pelagic shark diversity. In: Camhi MD, Pikitch EK (eds) Sharks of the open ocean: biology, fisheries and conservation. Blackwell, Oxford, pp 14–23CrossRefGoogle Scholar
  33. Corn KA, Farina SC, Brash J, Summers AP (2016) Modeling tooth-prey interactions in sharks: the importance of dynamic testing. R Soc Open Sci 3:160141. doi: 10.1098/rsos.160141 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Cortés E (1996) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to shark fishes. Can J Fish Aquat Sci 54:726–738CrossRefGoogle Scholar
  35. Cortés E, Gruber SH (1996) Gastric evacuation in the young lemon shark, Negaprion brevirostris, under field conditions. Environ Biol Fishes 35:205–212CrossRefGoogle Scholar
  36. Cortés E, Papastamatiou Y, Carlson J, Ferry-Graham L, Wetherbee B (2008) An overview of the feeding ecology and physiology of shark fishes. In: Cyrino J, Bureau D, Kapoor B (eds) Feeding and digestive functions in fishes. Science Publishers, New HampshireGoogle Scholar
  37. Crane R, Boge G, Rigal A (1979) Isolation of brushborder membranes in vesivular form from the intestinal spiral valve of the small dogfish (Scyliorhinus canicula). Biochim Biophys Acta 554:264–267PubMedCrossRefGoogle Scholar
  38. Dalerum F, Angerbjorn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658PubMedCrossRefGoogle Scholar
  39. Day RD, Tibbetts IR, Secor SM (2014) Physiological responses to short-term fasting among herbivorous, omnivorous, and carnivorous fishes. J Comp Physiol B 184:297–512CrossRefGoogle Scholar
  40. Dennis CA, MacNeil MA, Rosati JY, Pitcher TE, Fisk AT (2010) Diet discrimination factors are inversely related to δ15N and δ13C values of food for fish under controlled conditions. Rapid Commun Mass Spectrom 24:3515–3520PubMedCrossRefGoogle Scholar
  41. Di Santo V, Bennett WA (2011) Is post-feeding thermotaxis advantageous in shark fishes? J Fish Biol 78:195–207PubMedCrossRefGoogle Scholar
  42. Diamond JM, Karasov WH (1987) Adaptive regulation of intestinal nutrient transporters. Proc Natl Acad Sci USA 84(8):2242–2245PubMedPubMedCentralCrossRefGoogle Scholar
  43. Dove ADM, Leisen J, Zhou M, Byrne JJ, Lim-Hing K, Webb HD, Gelbaum L, Viant MR, Kubanek J, Fernandez FM (2012) Biomarkers of whale shark health: a metabolomic approach. PLoS ONE. doi: 10.1371/journal.pone.0049379 Google Scholar
  44. Dowd WW, Wood CM, Kajimura M, Walsh PJ, Kültz D (2008) Natural feeding influences protein expression in the dogfish shark rectal gland: a proteomic analysis. Comp Biochem Physiol D Genomics Proteomics 3:118–127PubMedCrossRefGoogle Scholar
  45. Fänge R, Grove D (1979) Digestion. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 8. Academic Press, New York, pp 161–260Google Scholar
  46. Fänge R, Lundblad G, Lind J, Slettengren K (1979) Chitinolytic enzymes in the digestive system of marine fishes. Mar Biol 53:317–321CrossRefGoogle Scholar
  47. Ferry-Graham LA, Lauder GV (2001) Aquatic prey capture in ray-finned fishes: a century of progress and new directions. J Morphol 248:99–119PubMedCrossRefGoogle Scholar
  48. Frazetta TH, Prange CD (1987) Movements of cephalic components during feeding in some requiem sharks (Carcharhiniformes: Carcharhinidae). Copeia 1987:979–993CrossRefGoogle Scholar
  49. Fry B (2006) Stable isotope ecology. Springer, New YorkCrossRefGoogle Scholar
  50. Furuse M, Dockray GJ (1995) The regulation of gastrin-secretion in the chicken. Regul Pept 55(3):253–259PubMedCrossRefGoogle Scholar
  51. Gajić A (2013) Comparative odontology of selachians (Chondricthyes: Sharkii): development and morphological characteristics of teeth. Presented at the 17th annual Symposium of Biology Students in Europe. AbstractGoogle Scholar
  52. Gamboa-Delgado J, Canavate JP, Zerolo R, Le Vay L (2008) Natural carbon stable isotope ratios as indicators of the relative contribution of live and inert diets to growth in larval Senegalese sole (Solea senegalensis). Aquaculture 280(1–4):190–197CrossRefGoogle Scholar
  53. German DP (2011) Digestive efficiency. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment, vol 3. Academic Press, San Diego, pp 1596–1607CrossRefGoogle Scholar
  54. German DP, Miles RD (2010) Stable carbon and nitrogen incorporation in blood and fin tissue of the catfish Pterygoplichthys disjunctivus (Siluriformes, Loricariidae). Environ Biol Fishes 89:117–133CrossRefGoogle Scholar
  55. 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):789–804PubMedCrossRefGoogle Scholar
  56. German DP, Nagle BC, Villeda JM, Ruiz AM, Thomson AW, Contreras 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):1–18PubMedCrossRefGoogle Scholar
  57. German DP, Neuberger DT, Callahan MN, Lizardo NR, Evans DH (2010b) Feast to famine: the effects of food quality and quantity on the gut structure and function of a detritivorous catfish (Teleostei: Loricariidae). Comp Biochem Physiol A 155:281–293CrossRefGoogle Scholar
  58. German DP, Sung A, Jhaveri P, 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 118:161–170PubMedCrossRefGoogle Scholar
  59. 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 89:277–293PubMedCrossRefGoogle Scholar
  60. Gidmark NJ, Taylor C, LoPresti E, Brainerd E (2015) Functional morphology of Durophagy in Black Carp, Mylopharyngodon piceus. J Morphol 276(12):1422–1432PubMedCrossRefGoogle Scholar
  61. Givens C, Ransom B, Bano N, Hollibaugh J (2015) Comparison of the gut microbiomes of 12 bony fish and 3 shark species. Mar Ecol Prog Ser 518:209–223CrossRefGoogle Scholar
  62. Goldman KJ, Anderson SD, Latour RJ, Musick JA (2004) Homeothermy in adult salmon sharks, Lamna ditropis. Environ Biol Fishes 71:403–411CrossRefGoogle Scholar
  63. Goran A, Jonsson A, Jensen J, Holmgren S (1988) Gastrin/CCK-like peptides in the spiny dogfish, Squalus acanthias; concentrations and actions in the gut. Comp Biochem Phys 92(1):103–108Google Scholar
  64. Grove DJ, Campbell G (1979) The role of extrinsic and intrinsic nerves in the co-ordination of gut motility in the stomachless flatfish Rhombosolea tapirina and Ammotretis rostrata Guenther. Comp Biochem Physiol C 63(1):143–159CrossRefGoogle Scholar
  65. Guerreiro I, de Vareilles M, Pousao-Ferreira P, Rodrigues V, Dinis MT, Ribeiro L (2010) Effect of age-at-weaning on digestive capacity of white seabream (Diplodus sargus). Aquaculture 300(1–4):194–205CrossRefGoogle Scholar
  66. Halver JE (2002) The vitamins. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 61–141Google Scholar
  67. Hart HR, Evans AN, Gelsleichter J, Ahearn GA (2016) Molecular identification and functional characteristics of peptide transporters in the bonnethead shark (Sphyrna tiburo). J Comp Physiol B 186(7):855–866PubMedCrossRefGoogle Scholar
  68. Hesslein RH, Hallard KA, Ramlal P (1993) Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Can J Fish Aquat Sci 50:2071–2076CrossRefGoogle Scholar
  69. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188CrossRefGoogle Scholar
  70. Hogben CAM (1967) Response of the isolated dogfish gastric mucosa to histamine. Proc Soc of Exp Biol Med 124:890–893CrossRefGoogle Scholar
  71. Holmgren S, Nilsson S (1999) Digestive system. In: Hamlett WC (ed) Sharks, skates, and rays: the biology of shark fishes. The Johns Hopkins University Press, Baltimore, pp 144–173Google Scholar
  72. Holmgren S, Grimes D, Brayton P, Colwell R, Gruber S (1985) Vibrios as autochthonous flora of neritic sharks. Syst Appl Microbiol 6:221–226CrossRefGoogle Scholar
  73. Horn MH, Messer KS (1992) Fish guts as chemical reactors: a model of the alimentary canals of marine herbivorous fishes. Mar Biol 113:527–535CrossRefGoogle Scholar
  74. Hume I (2003) Nutrition of carnivorous marsupials. In: Jones M, Dickman C, Archer M (eds) Predators with pouches: the biology of carnivorous marsupial. CSIRO Publishing, Collingwood, Australia, pp 221–227Google Scholar
  75. Hume I (2005) Concepts of digestive efficiency. In: Starck J, Wang T (eds) Physiological ecological adaptations to feeding vertebrates. Science Publishers, Enfield, pp 43–58Google Scholar
  76. Hussey NE, Brush J, McCarthy ID, Fisk AT (2010) δ15N and δ13C diet—tissue discrimination factors for large sharks under semi-controlled conditions. Comp Biochem Physiol A 155:445–453CrossRefGoogle Scholar
  77. Iverson SJ, Frost KJ, Lang SLC (2002) Fat content and fatty acid composition of forage fish and invertebrates in Prince William Sound, Alaska: factors contributing to among and within species variability. Mar Ecol Prog Ser 241:161–181CrossRefGoogle Scholar
  78. Jackson S, Dubby DC, Jenkins JFG (1987) Gastric digestion in marine vertebrate predators: in vitro standards. Funct Ecol 1:287–291CrossRefGoogle Scholar
  79. Jeschke JM (2007) When carnivores are “full and lazy”. Oecologia 152(2):357–364PubMedCrossRefGoogle Scholar
  80. Jhaveri P, Papastamatiou Y, 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 189:76–83CrossRefGoogle Scholar
  81. Johnsen AH, Jonson L, Rourke IJ, Rehfeld JF (1997) Sharks express separate cholecystokinin and gastrin genes. Proc Natl Acad Sci USA 94(19):10221–10226PubMedPubMedCentralCrossRefGoogle Scholar
  82. Jones BC, Green GH (1977) Food and feeding of spiny dogfish (Squalus acanchias) in British Columbia waters. J Fish Res Board Can 43:2067–2078Google Scholar
  83. Kararli T (1995) Comparison of the gastrointestinal anatomy, physiology, and biochemistry of human and commonly used laboratory animals. Biopharm Drug Dispos 16:351–380PubMedCrossRefGoogle Scholar
  84. Karasov WH (1992) Tests of the adaptive modulation hypothesis for dietary control of intestinal nutrient transport. Am J Physiol 263:R496–R502PubMedGoogle Scholar
  85. Karasov WH, Diamond J (1983) Adaptive regulation of sugar and amino acid transport by vertebrate intestine. Am J Physiol 245:G443–G462PubMedGoogle Scholar
  86. Karasov WH, Douglas AE (2013) Comparative and digestive physiology. Compr Physiol 3:741–783PubMedPubMedCentralGoogle Scholar
  87. Karasov WH, Martinez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, PrincetonGoogle Scholar
  88. Karsten AH, Rice CD (2004) c-Reactive protein levels as a biomarker of inflammation and stress in the Atlantic sharpnose shark (Rhizoprionodon terraenovae) from three southeastern USA estuaries. Mar Environ Res 58(2–5):747–751PubMedCrossRefGoogle Scholar
  89. Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22CrossRefGoogle Scholar
  90. Kenaley CP, Lauder GV (2016) A biorobotic model of the suction-feeding system in largemouth bass: the roles of motor program speed and hyoid kinematics. J Exp Biol 219:2048–2059PubMedCrossRefGoogle Scholar
  91. Kim SL, Martinez del Rio C, Casper D, Koch PL (2012) Isotopic incorporation rates for shark tissues from a long-term captive feeding study. J Exp Biol 215(14):2495–2500PubMedCrossRefGoogle Scholar
  92. Kolmann MA, Welch K, Summers AP, Lovejoy NR (2016) Always chew your food: freshwater stingrays use mastication to process tough insect prey. Proc R Soc B Biol Sci 283:20161392. doi: 10.1098/rspb.2016.1392 CrossRefGoogle Scholar
  93. Konturek JW, Thor P, Maczka M, Stoll R, Domschke W, Konturek SJ (1994) Role of cholecystokinin in the control of gastric emptying and secretory response to a fatty meal in normal subjects and duodenal ulcer patients. Scand J Gastroenterol 29(7):583–590PubMedCrossRefGoogle Scholar
  94. Kuz’mina V (1990) Characteristics of enzymes involved in membrane digestion in shark fishes. Zhur Evolyut Biokhim Fiziolog 26:161–166Google Scholar
  95. Laurence-Chasen JD, Jimenez YE, Knorlein BJ, and Brainerd EL (2016) Video Reconstruction of Moving Morphology (VROMM) for studies of suction feeding in ray-finned fishes. Conference: Annual Meeting of the Society-for-Integrative-and-Comparative-Biology (SICB). Integrative and Comparative Biology, 56(1): E321, Meeting Abstract: P2.175, Portland, ORGoogle Scholar
  96. Lauzon HL, Perez-Sanchez T, Merrifield DL, Ringo E, Balcazar JL (2014) Probiotic applications in cold water fish species. Aquac Nutr Gut Health Probiotics Prebiotics 9:223–252Google Scholar
  97. LeBlanc J, Milani C, Savoy de Giori G, Sesma F, van Sinderen D, Ventura M (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 24:160–168PubMedCrossRefGoogle Scholar
  98. Li Y, Zhang Y, Hussey NE, Dai X (2015) Urea and lipid extraction treatment effects on δ15N and δ13C values in pelagic sharks. Rapid Commun Mass Spectrom 30:1–8CrossRefGoogle Scholar
  99. Lloyd KCK, Debas HT (1994) Peripheral regulation of gastric acid secretion. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Plenum Publishing Corporation, New York, pp 229–334Google Scholar
  100. Logan JM, Lutcavage ME (2010) Stable isotope dynamics in elasmobranch fishes. Hydrobiologia 644:231–244CrossRefGoogle Scholar
  101. Longo SJ, McGee MD, Oufiero CE, Waltzek TB, Wainwright PC (2016) Body ram, not suction, is the primary axis of suction-feeding diversity in spiny-rayed fishes. J Exp Biol 219(1):119–128PubMedCrossRefGoogle Scholar
  102. Lujan NK, German DP, Winemiller KL (2011) Do wood grazing fishes partition their niche? Morphological and isotopic evidence for trophic segregation in Neotropical Loricariidae. Funct Ecol 25:1327–1338CrossRefGoogle Scholar
  103. Mara KR, Motta PJ, Martin AP, Hueter RE (2015) Constructional morphology within the head of hammerhead sharks (Sphyrnidae). J Morphol 276(5):526–539PubMedCrossRefGoogle Scholar
  104. Martin RA (2003) Biology of sharks and rays. Illustrations. World Wide Web Publication, www.elasmo-research.org/copyright.htm
  105. Martine A, Fuhrman F (1995) The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol Biochem Zool 28:18–34Google Scholar
  106. Martínez del Rio C, Carleton SA (2012) How fast and how faithful—the dynamics of isotopic incorporation into animal tissues. J Mamm 93:353–359CrossRefGoogle Scholar
  107. Martinez del Rio C, Wolf N (2005) Mass-balance models for animal isotopic ecology. In: Starck MA, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, New Hampshire, pp 141–174Google Scholar
  108. Martinez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111CrossRefGoogle Scholar
  109. McCosker JE (1987) The white shark, Carcharodon carcharias, has a warm stomach. Copeia 1987:195–197CrossRefGoogle Scholar
  110. Meyer CG, Holland KN (2012) Autonomous measurement of ingestion and digestion processes in free-swimming sharks. J Exp Biol 215:3681–3684PubMedCrossRefGoogle Scholar
  111. Michelangeli F, Ruiz MC, Dominquez MG, Parthe V (1988) Mammalian like differentiation of gastric cells in the shark Hecanchus griseus. Cell Tissue Res 251:225–227PubMedCrossRefGoogle Scholar
  112. Moro GV, Silva TSC, Zanon RB, Cyrino JEP (2016) Starch and lipid in diets for dourado Salminus brasiliensis (Cuvier 1816): growth, nutrient utilization and digestive enzymes. Aquac Nutr 22(4):890–898CrossRefGoogle Scholar
  113. Motta PJ, Wilga CAD (1995) Anatomy of the feeding apparatus of the lemon shark, Negaprion brevirostris. J Morphol 226:309–329CrossRefGoogle Scholar
  114. Motta PJ, Wilga CAD (2001) Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environ Biol Fish 60:131–156CrossRefGoogle Scholar
  115. Motta PJ, Hueter RE, Tricas TC, Summers AP, Huber DR, Lowry D, Mara KR, Matott MP, Whitenack LB, Wintzer AP (2008) Functional morphology of the feeding apparatus, feeding constraints, and suction performance in the nurse shark. J Morphol 269:1041–1055PubMedCrossRefGoogle Scholar
  116. Motta PJ, Maslanka M, Hueter RE, Davis RL, de la Parra R, Mulvany SL, Habegger ML, Strother JA, Mara KR, Gardiner JM, Tyminski JP, Zeigler LD (2010) Feeding anatomy, filter-feeding rate, and diet of whale sharks, Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology 113:199–212PubMedCrossRefGoogle Scholar
  117. Muller M, Osse JWM (1984) Hydrodynamics of suction feeding in fish. Trans Zool Soc Lond 37:51–135CrossRefGoogle Scholar
  118. Mulley JF, Hargreaves AD, Hegarty MJ, Heller RS, Swain MT (2014) Transcriptomic analysis of the lesser spotted catshark (Scyliorhinus canicula) pancreas, liver and brain reveals molecular level conservation of vertebrate pancreas function. BioMed Cent. doi: 10.1186/1471-2164-15-1074 Google Scholar
  119. Murphy KP, Crush L, Twomey M, McLaughlin PD, Mildenberger IC, Moore N, Bye J, O’Connor OJ, McSweeney SE, Shanahan F, Maher MM (2015) Model-based iterative reconstruction in CT enterography. AJR Am J Roentgenol 205(6):1173–1181PubMedCrossRefGoogle Scholar
  120. Nakaya K (2001) White band on upper jaw of megamouth shark, Megachasma pelagios, and its presumed function (Lamniformes: Megachasmidae). Bull Fac Sci Hokkaido Univ Sapporo 52:125–129Google Scholar
  121. Nakaya K, Matsumoto R, Suda K (2008) Feeding strategy of the megamouth shark Megachasma pelagios (Lamniformes: Megachasmidae). J Fish Biol 73(1):17–34CrossRefGoogle Scholar
  122. Navarro-Garcia G, Aguilar-Pacheco R, Cordova-Vallejo B, Suarez-Ramirez J, Bolanos A (2000) Lipid composition of the liver oil of shark species from the Caribbean and gulf of California waters. J Food Compos Anal 13(5):791–798CrossRefGoogle Scholar
  123. Navia A, Mejia-Falla P, Giraldo A (2007) Feeding ecology of shark fishes in coastal waters of the Columbian Eastern Tropical Pacific. BMC Ecol 7:8PubMedPubMedCentralCrossRefGoogle Scholar
  124. Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41(11):1553–1573CrossRefGoogle Scholar
  125. Nelson JD (2004) Distribution and foraging ecology by Whale Sharks (Rhincodon typus) within Bahia de los Angeles, Baja California Norte, Mexico. M.Sc. Thesis. San Diego State University, CA, USAGoogle Scholar
  126. 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(5):1051–1062CrossRefGoogle Scholar
  127. Newsome SD, Wolf N, Peters J, Fogel ML (2014) Amino acid δ13C analysis shows flexibility in the routing of dietary protein and lipids to the tissue of an omnivore. Integr Comp Biol 54(5):890–902PubMedCrossRefGoogle Scholar
  128. Newsome SD, Sabat P, Wolf N, Rader JA, Martinez del Rio C (2015) Multi-tissue δ2H analysis reveals altitudinal migration and tissue-specific discrimination patterns in Cinclodes. Ecosphere 6(11):1–18CrossRefGoogle Scholar
  129. Newton K, Wraith J, Dickson K (2015) Digestive enzyme activities are higher in the shortfin mako shark, Isurus oxyrinchus, than in ectothermic sharks as a result of visceral endothermy. Fish Physiol Biochem 41:887–898PubMedCrossRefGoogle Scholar
  130. Nielsen JM, Popp BN, Winder M (2015) Meta-analysis of amino acid stable nitrogen isotope ratios for estimating trophic position in marine organisms. Oecologia 178:631–642PubMedCrossRefGoogle Scholar
  131. Oliver AS, Vigna SR (1996) CCK-X receptors in the endothermic mako shark (Isurus oxyrinchus). Gen Comp Endocrinol 102(1):61–73PubMedCrossRefGoogle Scholar
  132. Olsson C, Holmgren S (2001) The control of gut motility. Comp Biochem Physiol A-Mol Integr Physiol 128(3):481–503PubMedCrossRefGoogle Scholar
  133. Olsson C, Aldman G, Larsson A, Holmgren S (1999) Cholecystokinin affects gastric emptying and stomach motility in the rainbow trout Oncorhynchus mykiss. J Exp Biol 202(2):161–170PubMedGoogle Scholar
  134. Paig-Tran EWM, Lowe C (2010) Elemental and energy assimilation in the round stingray, Urobatis halleri. Annu Meet Soc Integr Comp Biol 50(1):E227Google Scholar
  135. Paig-Tran EWM, Summers AP (2013) Comparison of the structure and composition of the branchial filters of suspension feeding sharks. Anat Rec 297(4):701–715CrossRefGoogle Scholar
  136. Paig-Tran EWM, Bizzarro JJ, Strother JA, Summers AP (2011) Bottles as models: predicting the effects of varying swimming speed and morphology on size selectivity and filtering efficiency in fishes. J Exp Biol 214:1643–1654PubMedCrossRefGoogle Scholar
  137. Papastamatiou Y (2007) The potential influence of gastric acid secretion during fasting on digestion time in leopard sharks (Triakis semifasciata). Comp Biochem Physiol A 147:37–42CrossRefGoogle Scholar
  138. Papastamatiou YP, Lowe CG (2004) Postprandial response of gastric pH in leopard sharks (Triakis semifasciata) and its use to study foraging ecology. J Exp Biol 207(Pt2):225–232PubMedCrossRefGoogle Scholar
  139. Papastamatiou Y, Lowe C (2005) Variations in gastric acid secretion during periods of fasting between two species of shark. Comp Biochem Physiol A 141:210–214CrossRefGoogle Scholar
  140. Papastamatiou Y, Purkis S, Holland K (2007) The response of gastric pH and motility to fasting and feeding in free-swimming blacktip reef sharks, Carcharhinus melanopterus. J Exp Mar Biol Ecol 345:129–140CrossRefGoogle Scholar
  141. Papastamatiou YP, Watanabe YY, Bradley D, Dee LE, Weng K, Lowe CG, Caselle JE (2015) Drivers of daily routines in an ectothermic marine predator: Hunt warm, rest warmer? PLoS ONE 10:e0127807PubMedPubMedCentralCrossRefGoogle Scholar
  142. Parker TJ (1885) On the intestinal spiral valve in the genus Raja. Zool Soc Lond Trans 11:49–61CrossRefGoogle Scholar
  143. Pei-You G, Jun-Xia L, Feng-Li L, Liang-Ming Z, Hai-Zhu X, Yan-Bin S (2015) Retrospective comparison of computed tomography enterography and magnetic resonance enterography in diagnosing small intestine disease. J Pak Med Assoc 65(7):710–714PubMedGoogle Scholar
  144. Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129(1):69–96CrossRefGoogle Scholar
  145. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  146. Pethybridge H, Daley R, Virtue P, Nichols P (2010) Lipid composition and partitioning of deepwater chondrichthyans: inferences of feeding ecology and distribution. Mar Biol 157(6):1367–1384CrossRefGoogle Scholar
  147. Pinhal D, Shivji MS, Nachtigall PG, Chapman DD, Martins C (2012) A streamlined DNA tool for global identification of heavily exploited coastal shark species (genus Rhizoprionodon). PLoS ONE 7(4):e34797PubMedPubMedCentralCrossRefGoogle Scholar
  148. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecol. 83:703–718CrossRefGoogle Scholar
  149. Post DM, Layman CA, Arrinton DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analysis. Oecologia 152:179–189PubMedCrossRefGoogle Scholar
  150. Qian X, Ba Y, Zhuang Q, Zhong G (2014) RNA-seq technology and its application in fish transcriptomics. OMICS 18(2):98–110PubMedPubMedCentralCrossRefGoogle Scholar
  151. Reich KJ, Bjorndal KA, Bolten AB (2007) The ‘lost years’ of green turtles: using stable isotopes to study cryptic lifestages. Biol Let 3:712–714CrossRefGoogle Scholar
  152. Reich KJ, Bjorndal KA, Martinez del Rio C (2008) Effects of growth and tissue type on the kinetics of (13)C and (15)N incorporation in a rapidly growing ectotherm. Oecologia 155(4):651–663PubMedCrossRefGoogle Scholar
  153. Ringo E, Zhou Z, Vecino JLG, Wadsworth S, Romero J, Krojdahl A, Olsen RE, Dimitroglou A, Foey A, Davies S, Owen M, Lauzon HL, Martinsen LL, De Schryver P, Bossier P, Perstad S, Merrifield DL (2016) Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquac Nutr 22(2):219–282CrossRefGoogle Scholar
  154. Ruan GL, Li Y, Gao ZX, Wang HL, Wang WM (2010) Molecular characterization of trypsinogens and development of trypsinogen gene expression and tryptic activities in grass carp (Ctenopharyngodon idellus) and topmouth culter (Culter alburnus). Comp Biochem Physiol B Biochem Mol Biol 155(1):77–85PubMedCrossRefGoogle Scholar
  155. Sachs G, Prinz C, Loo D, Bamberg K, Besancon M, Shin JM (1994) Gastric acid secretion: activation and inhibition. Yale J Biol Med 67:81–95PubMedPubMedCentralGoogle Scholar
  156. Schubert ML (2015) Functional anatomy and physiology of gastric secretion. Curr Opin Gastroenterol 31(6):479–485PubMedCrossRefGoogle Scholar
  157. Secor S, Taylor J, Grosell M (2012) Selected regulation of gastrointestinal acid-base secretion and tissue metabolism for the diamondback water snake and Burmese python. J Exp Biol 215:185–196PubMedCrossRefGoogle Scholar
  158. Sepulveda CA, Kohin S, Chan C, Vetter R, Graham JB (2004) Movement patterns, depthpreferences, and stomach temperatures of free-swimming juvenile mako sharks, Isurus oxyrinchus, in the Southern California Bight. Mar Biol 145:191–199CrossRefGoogle Scholar
  159. Shamur E, Zilka M, Hassner T, China V, Liberzon A, Holzmen R (2016) Automated detection of feeding strikes by larval fish using continuous high-speed digital video: a novel method to extract quantitative data from fast, sparse kinematic events. J Exp Biol 219(11):1608–1617PubMedCrossRefGoogle Scholar
  160. Sibly RM (1981) Strategies of digestion and defecation. In: Townsend CR, Callow P (eds) Physiological ecology: an evolutionary approach to resource use. Sinauer, Sunderland, pp 109–139Google Scholar
  161. Silverthorn D (ed) (2013) Human physiology: an integrated approach, vol 6. Pearson, Boston, p 699Google Scholar
  162. Sims D, Davies S, Bone Q (1996) Gastric emptying rate and return of appetite in lesser spotted dogfish, Scyliorhinus canicula. J Mar Biol. Assn UK 76:479–491CrossRefGoogle Scholar
  163. Sims D, Wearmouth VJ, Southall EJ, Hill JM, Moore P, Rawlinson K, Hutchinson N, Budd GC, Righton D, Metcalfe JD, Nash JP, Morritt D (2006) Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration in a benthic shark. J Anim Ecol 75:176–190PubMedCrossRefGoogle Scholar
  164. Smith MM, Johanson Z, Underwood C, Diekwisch TGH (2013) Pattern formation in development of chondrichthyan dentitions: a review of an evolutionary model. Hist Biol Int J Paleobiol 25(2):127–142Google Scholar
  165. Sole M, Lobera G, Aljinovic B, Rios J, de la Parra LMG, Maynou F, Cartes JE (2008) Cholinesterases activities and lipid peroxidation levels in muscle from shelf and slope dwelling fish from the NW Mediterranean: its potential use in pollution monitoring. Sci Total Environ 402:306–317PubMedCrossRefGoogle Scholar
  166. Sole M, Anto M, Baena M, Carrasson M, Cartes JE, Maynou F (2010) Hepatic biomarkers of xenobiotic metabolism in eighteen marine fish from NW Mediterranean shelf and slope waters in relation to some of their biological and ecological variables. Mar Environ Res 70(2):181–188PubMedCrossRefGoogle Scholar
  167. Song Z, Wang J, Qiao H, Li P, Zhang L, Xia B (2016) Ontogenetic changes in digestive enzyme activities and the amino acid profile of starry flounder Platichthys stellatus. Chin J Oceanol Limnol 34(5):1013–1024CrossRefGoogle Scholar
  168. Sullam KE, Dalton CM, Russell JA, Kilham SS, El-Sabaawi R, German DP, Flecker AS (2014) Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies. Oecologia 177(1):245–257PubMedCrossRefGoogle Scholar
  169. Summers AP, Hayes M (2016) CT scans. Retrieved from www.osf.io/ecmz4
  170. Suzuki KW, Kasai A, Nakayama K, Tanaka M (2005) Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Can J Fish Aquat Sci 62(3):671–678CrossRefGoogle Scholar
  171. Suzuki T, Kakizaki H, Ikeda M, Matsumiya M (2014) Molecular cloning of the novel chitinase gene from blue shark (Prionace glauca; Chondrichthyes) stomach. J Chitin Chitosan Sci 2(2):143–148CrossRefGoogle Scholar
  172. Teles OA (2012) Nutrition and health of aquaculture fish. J Fish Dis 35:83–108CrossRefGoogle Scholar
  173. Trueman CN, McGill RAR, Guyard PH (2005) The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Spectrom 19(22):3239–3247PubMedCrossRefGoogle Scholar
  174. Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM, Swann JB, Ohta Y, Flajnik MF, Sutoh Y, Kasahara M, Hoon S, Gangu V, Roy SW, Irimia M, Korzh V, Kondrychyn I, Lim ZW, Tay BH, Tohari S, Kong KW, Ho S, Lorente-Galdos B, Quilez J, Marques-Bonet T, Raney BJ, Ingham PW, Tay A, Hillier LW, Minx P, Boehm T, Wilson RK, Brenner S, Warren WC (2014) Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–179PubMedPubMedCentralCrossRefGoogle Scholar
  175. Viana TP, Inacio AF, de Albuquerque C, Linde-Arias AR (2008) Biomarkers in a shark species to monitor marine pollution: Effects of biological parameters on the reliability of the assessment. Mar Environ Res 66:171Google Scholar
  176. Vigna S (1983) Evolution of endocrine regulation of gastrointestinal function in lower vertebrates. Am Zool 23:729–738CrossRefGoogle Scholar
  177. Vollaire Y, Banas D, Marielle T, Roche H (2007) Stable isotope variability in tissues of the Eurasian perch Perca fluviatilis. Comp Biochem Physiol A-Mol Integr Physiol 148(3):504–509PubMedCrossRefGoogle Scholar
  178. Wainwright D, Lauder GV (2016) Three-dimensional analysis of scale morphology in bluegill sunfish, Lepomis macrochirus. Zoology 119(3):182–195PubMedCrossRefGoogle Scholar
  179. Weidel BC, Carpenter SR, Kitchell JF, Vander Zanden MJ (2011) Rates and components of carbon turnover in fish muscle: insights from bioenergetics models and a whole-lake 13C addition. Can J Fish Aquat Sci 68:387–399CrossRefGoogle Scholar
  180. Wetherbee B, Gruber S (1993) Absorption efficiency of the lemon shark negaprion brevirostris at varying rates of energy intake. Copeia 2:416–425CrossRefGoogle Scholar
  181. Wetherbee B, Gruber S, Ramsey A (1987) X-radiographic observations of food passage through digestive tracts of lemon sharks. Trans Am Fish Soc 116:763–767CrossRefGoogle Scholar
  182. Wetherbee BM, Gruber SH, Cortés E (1990) Diet, feeding habits, digestion, and consumption in sharks, with special reference to the lemon shark, Negaprion brevirostris. NOAA Tech Rep NMFS 90:29–47Google Scholar
  183. Whitehead A, Galvez F, Zhang S, Williams LM, Oleksiak MF (2011) Functional genomics of physiological plasticity and local adaptation in killfish. J Hered 102(5):499–511PubMedCrossRefGoogle Scholar
  184. Wilga CD, Ferry LA (2016) Functional anatomy and biomechanics of feeding in elasmobranchs. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: internal processes. Elsevier, LondonGoogle Scholar
  185. Wilga CD, Motta PJ (2000) Durophagy in sharks: Feeding mechanics of the hammerhead Sphyrna tiburo. J Exp Biol 201:1345–1358Google Scholar
  186. Wilson J, Castro L (2011) Morphological diversity of the gastrointestinal tract in fishes. Fish Physiol 30:1–55Google Scholar
  187. Wolesensky W, Logan JD (2006) Chemical reactor models of digestion modulation. In: Burk AR (ed) Focus on ecology research, pp 197–247Google Scholar
  188. Wolf N, Newsome SD, Fogel ML, Martinez del Rio C (2012) An experimental exploration of the incorporation of hydrogen isotopes from dietary tissues into avian tissues. J Exp Biol 215:1915–1922PubMedCrossRefGoogle Scholar
  189. Wood CM, Kajimura M, Bucking C, Walsh PJ (2007) Osmoregulation, ionoregulation and acid-base regulation by the gastrointestinal tract after feeding in the shark (Squalus acanthias). J Exp Biol 210:1335–1349PubMedCrossRefGoogle Scholar
  190. Wu JL, Zhang JL, Du XX, Shen YJ, Lao X, Zhang ML, Chen LQ, Du ZY (2015) Evaluation of the distribution of adipose tissues in fish using magnetic resonance imaging (MRI). Aquaculture 448:112–122CrossRefGoogle Scholar
  191. Wyffels J, King BL, Vincent J, Chen C, Wu CH, Polson SW (2014) SkateBase, an shark genome project and collection of molecular resources for chondrichthyan fishes. F1000 Research, v1; ref status: indexed, http://f1000r.es/445
  192. Zarkasi KZ, Taylor RS, Abell GC, Tamplin ML, Glencross BD, Bowman JP (2016) Atlantic salmon (Salmo salar L.) gastrointestinal microbial community dynamics in relation to digesta properties and diet. Microb Ecol 71(3):589–603PubMedCrossRefGoogle Scholar
  193. Zuanon JAS, Pezzato AC, Ducatti C, Barros MM, Pezzato LE, Passos JRS (2007) Muscle delta C-13 change in nile tilapia (Oreochromis niloticus) fingerlings fed lants grain-based diets. Comp Biochem Physiol A-Mol Integr Physiol 147(3):761–765PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Samantha C. Leigh
    • 1
    Email author
  • Yannis Papastamatiou
    • 2
  • Donovan P. German
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA
  2. 2.Marine Sciences Program, Department of Biological ScienceFlorida International UniversityMiamiUSA

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