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Feeding in Cartilaginous Fishes: An Interdisciplinary Synthesis

  • Daniel HuberEmail author
  • Cheryl Wilga
  • Mason Dean
  • Lara Ferry
  • Jayne Gardiner
  • Laura Habegger
  • Yannis Papastamatiou
  • Jason Ramsay
  • Lisa Whitenack
Chapter
Part of the Fascinating Life Sciences book series (FLS)

Abstract

Fishes, and elasmobranchs in particular, are often described as “opportunistic” predators meaning that they will take advantage of feeding opportunities as they arise. The implication of this term is that elasmobranchs are not selective about what they eat, which is a gross oversimplification of the complex interactions that shape diet, many of which are driven by interactions of an organism’s physiology, ecology, and behavior.

Notes

Acknowledgements

This work is dedicated to the memory of G. Rau, for inspiring a spirit of discovery and nurturing all fascinations, no matter how bizarre. The authors would like to thank the editors of this volume for inviting our contribution to the understanding of feeding in vertebrates. We would also like to recognize the many people and institutions that have contributed to our ability to develop insight into chondrichthyan biology, particularly Drs. Philip Motta and Adam Summers. They have proven a perpetual source of inspiration through their intellect and creativity, and the field of chondrichthyan feeding research is forever indebted to them.

References

  1. Ajemian MJ, Sanford CP (2007) Food capture kinematics in the deep–water chain catshark Scliorhinus retifer. J Mar Biol Ass UK 87:1277–1286Google Scholar
  2. Ajemian MJ, Powers SP, Murdoch TJT (2012) Estimating the potential impacts of large mesopredators on benthic resources: integrative assessment of spotted eagle ray foraging ecology in Bermuda. PLOSone. http://dx.doi.org/10.1371/journal.pone.0040227
  3. Anderson WG, Dasiewicz PJ, Liban S et al (2010) Gastro-intestinal handling of water and solutes in three species of elasmobranch fish, the white-spotted bamboo shark, Chiloscyllium plagiosum, little skate, Leucoraja erinacea and the clear nose skate Raja eglanteria. Comp Biochem Physiol A 155:493–502Google Scholar
  4. Andreev PS (2010) Enameloid microstructure of the serrated cutting edges in certain fossil carcharhiniform and lamniform sharks. Microsc Res Tech 73:704–713PubMedGoogle Scholar
  5. 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. Phil Trans Roy Soc Lond B342:363–380Google Scholar
  6. Armstrong JB, Schindler DE (2011) Excess digestive capacity in predators reflects a life of feast and famine. Nature 476:84–87PubMedGoogle Scholar
  7. Aronson LR, Aronson FR, Clark E (1967) Instrumental conditioning and light-dark discrimination in young nurse sharks. Bull Mar Sci 17:249–256Google Scholar
  8. Atkins AG (2016) Slice-push, formation of grooves and the scale effect in cutting. Interface Focus 6:20160019PubMedPubMedCentralGoogle Scholar
  9. Atema J (1996) Eddy chemotaxis and odor landscapes: exploration of nature with animal sensors. Biol Bull 191:129–138PubMedGoogle Scholar
  10. Atema J (2012) Aquatic odor dispersal fields: opportunities and limits of detection, communication and navigation. In: Bronmark C, Hansson LA (eds) Chemical ecology in aquatic systems. Oxford University Press, Oxford, UK, pp 1–18Google Scholar
  11. Atkinson CJL, Collin SP (2012) Structure and topographic distribution of oral denticles in elasmobranch fishes. Biol Bull 222:26–34PubMedGoogle Scholar
  12. Baker CF, Montgomery JC, Dennis TE (2002) The sensory basis of olfactory search behavior in banded kokopu (Galaxias fasciatus). J Comp Physiol A 188:553–560Google Scholar
  13. Balaban JP, Summers AP, Wilga CA (2015) Mechanical properties of the hyomandibula in four shark species. J Exp Zool A Ecol Genet Physiol. 23(1):1–9Google Scholar
  14. Banner A (1972) Use of sound in predation by young lemon sharks, Negaprion brevirostris (Poey). Bull Mar Sci 22:251–283Google Scholar
  15. Barak MM, Lieberman DE, Hublin J (2011) A Wolff in sheep’s clothing: trabecular bone adaptation in response to changes in joint loading orientation. Bone 49:1141–1151PubMedGoogle Scholar
  16. Bateson W (1890) The sense-organs and perceptions of fishes; with some remarks on the supply of bait. J Mar Biol Assoc UK NS 1:225–256Google Scholar
  17. Bedore CN, Harris LJ, Kajiura SM (2014) Behavioral responses of batoid elasmobranchs to prey-simulating electric fields are correlated to peripheral sensory morphology and ecology. Zoology 117:95–103PubMedGoogle Scholar
  18. Bedore CN, Kajiura SM (2013) Bioelectric fields of marine organisms: voltage and frequency contributions to detectability by electroreceptive predators. Physiol Biochem Zool 86:298–311PubMedGoogle Scholar
  19. Belbenoit P (1986) Fine analysis of predatory and defensive motor events in Torpedo marmorata (Pisces). J Exp Biol 121:197–226Google Scholar
  20. Bethea DM, Hale L, Carlson JK et al (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 152:1009–1020Google Scholar
  21. Bethea DM, Smith KL, Casselberry GA et al (2015) Shark nursery grounds and essential fish habitat studies. GULFSPAN survey—2014. Report to NOAA fisheries, highly migratory species division. National Marine Fisheries Service, Panama City, FL, p 46Google Scholar
  22. Bigelow HB, Schroeder WC (1953) Sharks, sawfishes, guitarfishes, skates and rays. Chimaeroids. In: Tee-Van J, Breder CM, Hildebrand SF et al (eds) Fishes of the Western North Atlantic. Part 2. Sears Foundation for Marine Research, Yale University, New Haven, pp 1–514Google Scholar
  23. Blonder BI, Alevizon WS (1988) Prey discrimination and electroreception in the stingray Dasyatis sabina. Copeia 1988:33–36Google Scholar
  24. Bomgren P, Jonsson AC (1996) Basal H2-receptor stimulated and pH-dependent acid secretion from an isolated stomach mucosa preparation of the cod, Gadus morhua, studied using a modified pH-static titration method. Fish Physiol Biochem 15:275–285PubMedGoogle Scholar
  25. Bush AC, Holland KN (2002) Food limitation in a nursery area: estimates of daily ration in juvenile scalloped hammerheads, Sphyrna lewini, in Kaneohe bay, Oahu. J Exp Mar Bio Ecol 278:157–178Google Scholar
  26. Campbell G (1975) Inhibitory vagal innervation of the stomach in fish. Comp Biochem Physiol C 50:169–170PubMedGoogle Scholar
  27. Cappetta H (1987) Chondrichthyes II. Handbook of paleoichthyology. Gustav Fischer Verlag, New YorkGoogle Scholar
  28. Cappetta H (2012) Chondrichthyes. Mesozoic and cenozoic elasmobranchii: teeth. Gustav Fischer Verlag, New YorkGoogle Scholar
  29. Carter DR, Wong M (2003) Modelling cartilage mechanobiology. Philos Trans R Soc Lond B Biol Sci 358:1461–1471PubMedPubMedCentralGoogle Scholar
  30. Chatchavalvanich K, Marcos R, Poonpriom J et al (2006) Histology of the digestive tract of the freshwater stingray Himantura signifer. Anat Embryol 211:507–518PubMedGoogle Scholar
  31. Chen P, Lin AYM, Lin YS et al (2008) Structure and mechanical properties of selected biological materials. J Mech Beh Biomed Mat 1:208–226Google Scholar
  32. Cicimurri D (2000) Early cretaceous elasmobranchs from the Newcastle Sandstone (Albian) of Crook County, Wyoming. Mount Geol 37:101–107Google Scholar
  33. Cicimurri D (2004) Late cretaceous chondrichthyans from the carlie shale (Middle Turonian to Early Coniacian) of the black hills region, South Dakota and Wyoming. Mount Geol 41:1–16Google Scholar
  34. Clark E (1963) Maintenance of sharks in captivity with a report on their instrumental conditioning. In: Gilbert PW (ed) Sharks and Survival. DC Heath, Boston, pp 115–149Google Scholar
  35. Compagno LJV (1984) FAO species catalogue. Sharks of the world. An annotated and illustrated catalogue of shark species known to date, part 2: carcharhiniformes. Food and agriculture organization of the United Nations, RomeGoogle Scholar
  36. Compagno LJV (1988) Sharks of the order Carcharhiniformes. Princeton University Press, PrincetonGoogle Scholar
  37. Cook MH, Neal HV (1921) Are taste buds of elasmobranchs endodermal in origin? J Comp Neurol 33:45–63Google Scholar
  38. Coombs S, Anderson E, Braun CB et al (2007) The hydrodynamic footprint of a benthic, sedentary fish in unidirectional flow. J Acoust Soc Am 122:1227–1237PubMedGoogle Scholar
  39. Corn KA, Farina SC, Brash, J et al (2016) Modelling tooth-prey interactions in sharks: the importance of dynamic testing. R Soc Open Sci.  https://doi.org/10.1098/rsos.160141PubMedPubMedCentralGoogle Scholar
  40. Cornett AD (2006) Ecomorphology of shark electroreceptors. MS Thesis. Florida Atlantic UniversityGoogle Scholar
  41. Cortés E, Manire CA, Hueter RE (1996) Diet, feeding habits, and diel feeding chronology of the bonnethead shark, Sphyrna tiburo, in southwest Florida. Bull Mar Sci 58:353–367Google Scholar
  42. Crofts SB, Summers AP (2014) How to best smash a snail: the effect of tooth shape on crushing load. J R Soc Inter 11:20131053Google Scholar
  43. Currey JD (1998) Mechanical properties of vertebrate hard tissues. J Eng Med 212(6):399–411Google Scholar
  44. Currey J (2008) Collagen and the mechanical properties of bone and calcified cartilage. In: Fratzl P (ed) Collagen: structure and mechanics. Springer Science + Business Media, New York, pp 397–420Google Scholar
  45. de Sousa Rangel B, Ciena AP, Wosnick N et al (2016) Ecomorphology of oral papillae and denticles of Zapteryx brevirostris (Chondrichthyes, Rhinobatidae). Zoomorphol 135:189–195Google Scholar
  46. Dean M, Motta PJ (2004) Feeding behavior and kinematics of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea). Zoology 107:171–189PubMedGoogle Scholar
  47. Dean M, Huber D, Nance H (2006) Functional morphology of jaw trabeculation in the lesser electric ray Narcine brasiliensis, with comments on the evolution of structural support in the Batoidea. J Morphol 267:1137–1146PubMedGoogle Scholar
  48. Dean MN, Summers AP (2006) Mineralized cartilage in the skeleton of chondrichthyan fishes. Zoology 109:164–168PubMedGoogle Scholar
  49. Dean MN, Bizzarro JJ, Summers AP (2007) The evolution of cranial design, diet, and feeding mechanisms in batoids fishes. Integ Comp Biol 47:70–81Google Scholar
  50. Dean MN, Ramsay JB, Schaefer JT (2008) Tooth reorientation affects tooth function during prey processing and tooth ontogeny in the lesser electric ray, Narcine brasiliensis. Zoology 111:123–134PubMedGoogle Scholar
  51. Dean MN, Mull CG, Gorb SN et al (2009) Ontogeny of the tesselated skeleton: Insight from the skeletal growth of the round stingray Urobatis halleri. J Anat 215:227–239PubMedPubMedCentralGoogle Scholar
  52. Dehnhardt G, Mauck B, Hanke W et al (2001) Hydrodynamic trail-following in harbor seals (Phoca vitulina). Science 293:102–104PubMedGoogle Scholar
  53. Derby CD, Zimmer RK (2012) Neuroecology of predator-prey interactions. In: Bronmark C, Hansson LA (eds) Chemical ecology in aquatic systems. Oxford University Press, Oxford, pp 158–171Google Scholar
  54. Didier DA (1995) Phylogenetic systematics of extant chimaeroid fishes (Holocephali, Chimeroidei). Amer Mus Novit 3119:1–86Google Scholar
  55. Didier DA, Kempter JM, Ebert DA (2012) Phylogeny, biology, and classification of extant holocephalans. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of Sharks and their relatives, 2nd edn. CRC Press, New York, pp 97–122Google Scholar
  56. Dingerkus G, Seret B, Guilbert E (1991) Multiple prismatic calcium phosphate layers in the jaws of present–day sharks (Chondrichthyes; Selachii). Experientia 47:38–40PubMedGoogle Scholar
  57. Di Santo V, Bennett WA (2011) Is post-feeding thermotaxis advantageous in elasmobranch fishes? J Fish Biol 78:195–207PubMedGoogle Scholar
  58. Domenici P, Blake RW (2000) Biomechanics in behaviour. In: Domenici P, Blake RW (eds) Biomechanics in animal behaviour. BIOS Scientific Publishers Ltd, Oxford, pp 1–17Google Scholar
  59. Dove ADM (2015) Foraging and investigative behaviors of whale sharks, Rhincodon typus, in response to chemical stimulus cues. Biol Bull 228:65–74PubMedGoogle Scholar
  60. Duffin CJ, Cuny G (2008) Carcharopsis prototypus and the adaptations of single crystallite enameloid in cutting dentitions. Acta Geol Polon 58:181–184Google Scholar
  61. Dumont ER, Dávalos LM, Goldberg A et al (2012) Morphological innovation, diversification and invasion of a new adaptive zone. Proc R Soc B 79:1797–1805Google Scholar
  62. Duntley SQ (1963) Light in the sea. J Opt Soc Am 53:214–233Google Scholar
  63. Dwyer SL, Visser IN (2011) Cookie cutter shark (Isistius sp.) bites on cetaceans, with particular reference to killer whales (Orca) (Orcinus orca). Aquat Mamm 37(2):111–138Google Scholar
  64. Eames BF, Allen N, Young J et al (2007) Skeletogenesis in the swell shark Cephaloscyllium ventriosum. J Anat 210:542–554PubMedPubMedCentralGoogle Scholar
  65. Ellis JR, ShackleySE (1995) Ontogenetic changes and sexual dimoprhism in the head, mouth and teeth of the lesser spotted dogfish. J Fish Biol 47:155–164Google Scholar
  66. Enault S, Muñoz DN, Silva WTAF et al (2015) Molecular footprinting of skeletal tissues in the catshark Scyliorhinus canicula and the clawed frog Xenopus tropicalis identifies conserved and derived features of vertebrate calcification. Front Genet 6:1–14Google Scholar
  67. Fahle SR, Thomason JC (2008) Measurement of jaw viscoelasticity in newborn and adult lesser spotted dogfish Scyliorhinus canicula (L., 1758). J Fish Biol 72:1553–1557Google Scholar
  68. Fairfax D (1998) The Basking Shark in Scotland: natural history, fishery and conservation. Tuckwell Press LtdGoogle Scholar
  69. Fallows C, Fallows M, Hammerschlag N (2016) Effects of lunar phase on predator-prey interactions between white shark (Carcharodon carcharias) and Cape fur seals (Arctocephalus pusillus pusillus). Env Biol Fish 99(11):805–812Google Scholar
  70. Fange R, Lundbland G, Lind J et al (1979) Chitinolytic enzymes in the digestive system of marine fishes. Mar Biol 53:317–321Google Scholar
  71. Fedducia A, Slaughter BH (1974) Sexual dimorphism in skates (Rajidae) and its possible role in differential niche utilization. Evolution 28:164–168Google Scholar
  72. Ferguson A, Huber D, Motta P (2015) Feeding performance of king mackerel Scomberomorus cavalla. J Exp Zool A 323(7):399–413Google Scholar
  73. Ferrando S, Gallus L, Gambardella C et al (2012) First detection of taste buds in a chimaeroid fish (Chondrichthyes: Holocephali) and their Gαi-like immunoreactivity. Neurosci Lett 517:98–101PubMedGoogle Scholar
  74. Ferrara TL, Clausen P, Huber DR et al (2011) Mechanics of biting in great white and sandtiger sharks. J Biomech 44(3):430–435PubMedGoogle Scholar
  75. Ferrara TL, Boughton P, Slavich E et al (2013) A novel method for single sample multi-axial nanoindentation of hydrated heterogeneous tissues based on testing great white shark jaws. PLoS ONE 8(11):e81196PubMedPubMedCentralGoogle Scholar
  76. Ferry-Graham LA (1998) Effects of prey size and mobility on prey-capture kinematics in leopard sharks Triakis semifasciata. J Exp Biol 201:2433–2444Google Scholar
  77. Ferry-Graham LA, Gibb AC (2001) Comparison of fasting and postfeeding metabolic rates in a sedentary shark, Cephaloscyllium ventriosum. Copeia 4:1108–1113Google Scholar
  78. Ferry-Graham LA, Bolnick DI, Wainwright PC (2002) Using functional morphology to examine the ecology and evolution of specialization. Int Comp Biol 42(2):265–277Google Scholar
  79. Fields RD, Bullock TH, Lange GD (1993) Ampullary sense organs, peripheral, central, and behavioral electroreception in chimaeras (Hydrolagus, Holocephali, Chondrichthyes). Brain Behav Evol 41:269–289PubMedGoogle Scholar
  80. Fields RD, Lange GD (1980) Electroreception in the ratfish (Hydrolagus colliei). Science 207:547–548PubMedGoogle Scholar
  81. Fishbeck DW, Sebastiani AS (2008) Manual of Vertebrate dissection: comparative anatomy, 2nd edn. Morton Publishing, Englewood, COGoogle Scholar
  82. Fouts WR, Nelson DR (1999) Prey capture by the Pacific angle shark, Squatina californica: visually mediated strikes and ambush-site characteristics. Copeia 1999:304–312Google Scholar
  83. Frazzetta TH (1988) The mechanics of cutting and the form of shark teeth (Chondrichthyes: Elasmobranchii). Zoomorphol 108:93–107Google Scholar
  84. Frazzetta TH (1994) Feeding mechanisms in sharks and other elasmobranchs. In: Bels VL, Chardon M, Vanderwalle P (eds) Biomechanics of feeding in vertebrates: advances in comparative and environmental physiology. Springer, New York, pp 31–57Google Scholar
  85. Frazzetta TH, Prange CD (1987) Movements of cephalic components during feeding in some requiem sharks (Carcharhiniformes: Carcharhinidae). Copeia 1987:979–993Google Scholar
  86. Fuss T, Bleckmann H, Schluessel V (2014) Visual discrimination abilities in the gray bamboo shark (Chiloscyllium griseum). Zoology 117:104–111PubMedGoogle Scholar
  87. Gardiner JM, Atema J (2007) Sharks need the lateral line to locate odor sources: rheotaxis and eddy chemotaxis. J Exp Biol 210:1925–1934PubMedGoogle Scholar
  88. Gardiner JM, Atema J (2010) The function of bilateral timing differences in olfactory orientation of sharks. Curr Biol 20:1187–1191PubMedGoogle Scholar
  89. Gardiner JM, Atema J (2014) Flow sensing in sharks: lateral line contributions to navigation and prey capture. In: Bleckmann H, Mogdans J, Coombs SL (eds) Flow sensing in air and water: behavioural, neural, and engineering principles of operation. Springer, pp 127–146Google Scholar
  90. Gardiner JM, Atema J, Hueter RE et al (2014) Multisensory integration and behavioral plasticity in sharks from different ecological niches. PLoS ONE 9:e93036PubMedPubMedCentralGoogle Scholar
  91. Gardiner JM, Atema J, Hueter RE et al (2016) Modulation of shark prey capture kinematics in response to sensory deprivation. Zoology In PressGoogle Scholar
  92. Geniz JLC, Nishizaki OS, Jimenéz JCP (2007) Morphological variation and sexual dimporphism in the California skate, Raja inornata Jordan and Gilbert, 1881 from the Gulf of California, Mexico. Zootaxa 1545:1–16Google Scholar
  93. German DP (2011) Digestive efficiency. In: Farrell AP, Cech JJ, Richards JG et al (eds) Encyclopedia of fish physiology, from genome to environment. Elsevier, San Diego, CA, pp 1596–1607Google Scholar
  94. Gerry SP, Ramsay JB, Dean MN et al (2008) Evolution of asynchronous motor activity in paired muscles: effects of ecology, morphology, and phylogeny. Integ Comp Biol 48:272–282Google Scholar
  95. Gerry SP, Summers AP, Wilga CD et al (2010) Pairwise modulation of jaw muscle activity in two species of elasmobranchs. J Zool 281(4):282–292Google Scholar
  96. Gilbert PW (1963) The visual apparatus of sharks. In: Gilbert PW (ed) Sharks and survival. DC Heath and Co, Boston, MA, pp 283–326Google Scholar
  97. Gilbert PW, Hodgson ES, Mathewson RF (1964) Electroencephalograms of sharks. Science 145:949–951PubMedGoogle Scholar
  98. Gillis JA, Donoghue CJ (2007) The homology and phylogeny of chondrichthyan tooth enameloid. J Morphol 268:33–49PubMedGoogle Scholar
  99. Ginter M, Maisey JG (2007) The braincase and jaws of Cladodus from the lower Carboniferous of Scotland. Paleontology. 50(2):305–322Google Scholar
  100. Graeber RC (1978) Behavioral studies correlated with central nervous system integration of vision in sharks. In: Hodgson ES, Mathewson RF (eds) Sensory Biology of Sharks, Skates, and Rays. US Government Printing Office, Washington, pp 195–225Google Scholar
  101. Gregory WK (1904) The relations of the visceral arches to the chondrocranium. Biol Bull 7:55–69Google Scholar
  102. Grogan ED, Lund R (2000) Debeerius ellefseni (Fam. Nov, General Nov, Spec. Nov), an autodiastylic chondrichthyan from the Mississippian bear gulch limestone of Montana (USA), the relationships of the Chondrichthyes, and comments on gnathostome evolution. J Morphol 243:219–245PubMedGoogle Scholar
  103. Guerard F, Le Gal Y (1987) Characterization of a chymosin-like pepsin from the dogfish Scyliorhinus canicula. Comp Biochem Physiol B 88:823–827PubMedGoogle Scholar
  104. Gutteridge AN, Bennett MB (2014) Functional implications of ontogenetically and sexual dimoprhic dentition in the eastern shovelnose ray, Aptychotrema rostrata. J Exp Biol 217:192–200PubMedGoogle Scholar
  105. Gutowska MA, Drazen JC, Robinson BH (2004) Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comp Biochem Physiol A 139:351–358Google Scholar
  106. Habegger ML, Motta PJ, Huber DR et al (2011) Feeding biomechanics in the great barracuda (Sphyraena barracuda) during ontogeny. J Zool 283(1):63–72Google Scholar
  107. Habegger ML, Motta PJ, Huber DR et al (2012) Feeding biomechanics and theoretical calculations of bite force in bull sharks (Carcharhinus leucas) during ontogeny. Zoology. 115(6):354–364PubMedGoogle Scholar
  108. Haddock SHD, Moline MA, Case JF (2010) Bioluminescence in the sea. Ann Rev Mar Sci 2:443–493PubMedGoogle Scholar
  109. Haine OS, Ridd PV, Rowe RJ (2001) Range of electrosensory detection of prey by Carcharhinus melanopterus and Himantura granulata. Mar Freshw Res 52:291–296Google Scholar
  110. Hanke W, Bleckmann H (2004) The hydrodynamic trails of Lepomis gibbosus (Centrarchidae), Colomesus psittacus (Tetraodontidae) and Thysochromis ansorgii (Cichlidae) investigated with scanning particle image velocimetry. J Exp Biol 207:1585–1596PubMedGoogle Scholar
  111. Hanke W, Brücker C, Bleckmann H (2000) The ageing of the low frequency water disturbances caused by swimming goldfish and its possible relevance to prey detection. J Exp Biol 203:1193–2000PubMedGoogle Scholar
  112. Harris LJ, Bedore CN, Kajiura SM (2015) Electroreception in the obligate freshwater stingray, Potamotrygon motoro. Mar Freshw Res 66:1027–1036Google Scholar
  113. Hart HR, Evans AN, Gelsleichter J et al (2016) Molecular identification and functional characteristics of peptide transporters in the bonnethead shark (Sphyrna tiburo). J Comp Physiol B 186(7):855–866PubMedGoogle Scholar
  114. Heithaus MR (2004) Fish communities of seagrass meadows and associated habitats in Shark Bay, Western Australia. Bull Mar Sci 75:79–99Google Scholar
  115. Herrel A, Podos J, Huber SK et al (2005) Evolution of bite force in Darwin’s finches: a key role for head width. J Evol Biol 18:669–675PubMedGoogle Scholar
  116. Hobson ES (1963) Feeding behavior in three species of sharks. Pac Sci 17:171–194Google Scholar
  117. Hodgson ES, Mathewson RF (1971) Chemosensory orientation in sharks. Ann NY Acad Sci 188:175–182PubMedGoogle Scholar
  118. Hodgson ES, Mathewson RF (1978) Electrophysiological studies of chemoreception in elasmobranchs. In: Hodgson ES, Mathewson RF (eds) Sensory biology of Sharks, Skates, and Rays. US Government Printing Office, Washington, pp 195–225Google Scholar
  119. Hogben CAM (1967) Response of the isolated dogfish gastric mucosa to histamine. Proc Soc Exp Biol Med 124:890–893PubMedGoogle Scholar
  120. Holmgren S, Holmberg A (2005) Control of gut motility and secretion in fasting and fed nonmammalian vertebrates. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, New JerseyGoogle Scholar
  121. Holmgren S, Nilsson S (1999) Digestive system. In: Hamlett WC (ed) Sharks, Skates and Rays. The biology of elasmobranch fishes. John Hopkins University Press, Baltimore, pp 144–173Google Scholar
  122. Holmgren S, Olsson C (2009) The neuronal and endocrine regulation of gut function. Fish Physiol 28:467–512Google Scholar
  123. Huber DR, Motta PJ (2004) Comparative analysis of methods for determining bite force in the spiny dogfish Squalus acanthias. J Exp Zool A 301(1):26–37Google Scholar
  124. Huber DR, Eason TG, Hueter RE et al (2005) Analysis of the bite force and mechanical design of the feeding mechanism of the durophagous horn shark Heterodontus francisci. J Exp Biol 208:3553–3571Google Scholar
  125. Huber DR, Weggelaar CL, Motta PJ (2006) Scaling of bite force in the blacktip shark Carcharhinus limbatus. Zoology. 109:109–119PubMedGoogle Scholar
  126. Huber DR (2006) Cranial biomechanics and feeding performance in sharks. Dissertation, University of South FloridaGoogle Scholar
  127. Huber DR, Dean MN, Summers AP (2008) Hard prey, soft jaws, and the ontogeny of feeding biomechanics in the spotted ratfish Hydrolagus colliei. J R Soc Inter 5:941–952Google Scholar
  128. Huber DR, Claes JM, Mallefet J et al (2009) Is extreme biting performance associated with extreme morphologies in sharks? Physiol Biochem Zool 82(1):20–28Google Scholar
  129. Huber DR, Neveu DE, Stinson CM et al (2013) Mechanical properties of sand tiger shark Carcharias taurus vertebrae in relation to spinal deformity. J Exp Biol 216:4256–4263PubMedGoogle Scholar
  130. Hume ID (1989) Optimal digestive strategies in mammalian herbivores. Physiol Zool 62:1145–1163Google Scholar
  131. Hume ID (2005) Concepts of digestive efficiency. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, New JerseyGoogle Scholar
  132. Huxley TH (1876) On Ceratodus fosteri, observation on the classification of fishes. Proc Zool Soc Lond 1876:24–59Google Scholar
  133. Jagnandan K, Huber D (2010) Structural and material properties of the jaws of the lemon shark Negaprion brevirostris and horn shark Heterodontus francisci. Florida Sci 73:38Google Scholar
  134. Jeschke JM (2007) When carnivores are ‘full and lazy’. Oecologia 152:357–364PubMedGoogle Scholar
  135. 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 189:76–83Google Scholar
  136. Johnson SE (1917) Structure and development of the sense organs of the lateral canal system of selachians (Mustelus canis and Squalus acanthius). J Comp Neurol 28:1–74Google Scholar
  137. Johnsen PB, Teeter JH (1985) Behavioral responses of bonnethead sharks (Sphyrna tiburo) to controlled olfactory stimulation. Mar Behav Physiol 11:283–291Google Scholar
  138. Johnsen S (2005) Visual ecology on the high seas. Mar Ecol Prog Ser 287:281–285Google Scholar
  139. Johnsen S, Sosik HM (2004) Shedding light on light in the sea. Oceanus 43:24–28Google Scholar
  140. Johnson AG, Horton HF (1972) Length-weight relationship, food habits, parasites, and sex and age determination of the ratfish, Hydrolagus colliei. Fish Bull 70:421–429Google Scholar
  141. Jordan LK, Kajiura SM, Gordon MS (2009a) Functional consequences of structural differences in stingray sensory systems. Part I: mechanosensory lateral line canals. J Exp Biol 212:3037–3043PubMedGoogle Scholar
  142. Jordan LK, Kajiura SM, Gordon MS (2009b) Functional consequences of structural differences in stingray sensory systems. Part II: electrosensory system. J Exp Biol 212:3044–3050PubMedGoogle Scholar
  143. Jordan LK, Mandelman JW, Kajiura SM (2011) Behavioral responses to weak electric fields and a lanthanide metal in two shark species. J Exp Mar Biol Ecol 409:345–350Google Scholar
  144. Kajiura SM, Tricas TC (1996) Seasonal dynamics of dental sexual dimorphism in the Atlantic Stingray, Dasyatis sabina. J Exp Biol 199:2297–2306PubMedGoogle Scholar
  145. Kajiura SM (2003) Electroreception in neonatal bonnethead sharks, Sphyrna tiburo. Mar Biol 143:603–611Google Scholar
  146. Kajiura SM, Fitzgerald TP (2009) Response of juvenile scalloped hammerhead sharks to electric stimuli. Zoology 112:241–250PubMedGoogle Scholar
  147. Kajiura SM, Holland KN (2002) Electroreception in juvenile scalloped hammerhead and sandbar sharks. J Exp Biol 205:3609–3621PubMedGoogle Scholar
  148. Kalmijn AJ (1971) The electric sense of sharks and rays. J Exp Biol 55:371–383PubMedGoogle Scholar
  149. Kalmijn AJ (1972) Bioelectric fields in seawater and the function of the ampullae of Lorenzini in elasmobranch fishes. Scripps Inst Oceanogr Ref Ser Oct:1–21Google Scholar
  150. Kalmijn AJ (1982) Electric and magnetic field detection in elasmobranch fishes. Science 218:916–918PubMedGoogle Scholar
  151. Kasumyan AO (2008) Sounds and sound production in fishes. J Ichthyol 48:981–1030Google Scholar
  152. Kawakoshi A, Kaiya H, Riley LG et al (2007) Identification of a ghrelin-like peptide in two species of shark, Sphryna lewini and Carcharhinus melanopterus. Gen Comp Endocrinol 151:259–268PubMedGoogle Scholar
  153. Kemp NS, Westrin SK (1979) Ultrastructure of calcified cartilage in the endoskeletal tesserae of sharks. J Morphol 160:75–102PubMedGoogle Scholar
  154. Kempster RM, McCarthy ID, Collin SP (2012) Phylogenetic and ecological factors influencing the number and distribution of electroreceptors in elasmobranchs. J Fish Biol 80:2055–2088PubMedGoogle Scholar
  155. Kempster RM, Egeberg CA, Hart NS et al (2016) Electrosensory-driven feeding behaviours of the Port Jackson shark (Heterodontus portusjacksoni) and western shovelnose ray (Aptychotrema vincentiana). Mar Freshw Res 67:187–194Google Scholar
  156. Kirwet J, Witzmann F, Kulg S et al (2008) First direct evidence of a vertebrate three-level trophic chain in the fossil record. Proc R Soc B 275:181–186Google Scholar
  157. Koehl MAR (1996) When does morphology matter? Ann Rev Ecol Syst 27:501–542Google Scholar
  158. Kolmann MA, Huber DR (2009) Scaling of feeding biomechanics in the horn shark Heterodontus francisci: ontogenetic constraints on durophagy. Zoology. 112:351–361PubMedGoogle Scholar
  159. Kolmann MA, Huber DR, Dean MN et al (2014) Myological variability in a decoupled skeletal system: batoid cranial anatomy. J Morphol 275(8):862–881PubMedGoogle Scholar
  160. Kolmann MA, Huber DR, Motta PJ et al (2015a) Feeding biomechanics of the Cownose ray, Rhinoptera bonasus, over ontogeny. J Anat 227(3):341–351PubMedPubMedCentralGoogle Scholar
  161. Kolmann MA, Crofts SB, Dean MN et al (2015b) Morphology does not predict performance: jaw curvature and prey crushing in durophagous Stingrays. J Exp Biol 218:3941–3949PubMedGoogle Scholar
  162. Kolmann MA, Welch KC, Summers AP et al (2016) Always chew your food: freshwater stingrays use mastication to process tough insect prey. Proc Roy Soc B 283(1838).  https://doi.org/10.1098/rspb.2016.1392PubMedGoogle Scholar
  163. Laasanen MS, Saarakkala S, Toyras J (2003) Ultrasound indentation of bovine knee articular cartilage in situ. J Biomech 36:1259–1267PubMedGoogle Scholar
  164. Lane JA, Maisey JG (2012) The visceral skeleton and jaw suspension in the durophagous hybodontid shark Tribodus limae from the Lower Cretaceous of Brazil. J Paleontol 86(5):886–905Google Scholar
  165. Lauder GV (1995) On the inference of function from structure. In: Thomason JJ (ed) Functional Morphology in Vertebrate Paleontology. Cambridge University Press, Cambridge, pp 1–18Google Scholar
  166. Liem KF (1980) Adaptive significance of intra-and interspecific differences in the feeding repertoires of Cichlid fishes. Am Zool 20:295–314Google Scholar
  167. Liem KF, Bemis WE, Walker WF Jr et al (2001) Functional anatomy of the vertebrates: an evolutionary perspective. Harcourt College Publishers, New YorkGoogle Scholar
  168. Lisney TJ, Theiss SM, Collin SP et al (2012) Vision in elasmobranchs and their relatives: 21st century advances. J Fish Biol 80:2024–2054PubMedGoogle Scholar
  169. Liu X, Dean MN, Summers AP et al (2010) Composite model of the shark’s skeleton in bending: a novel architecture for biomimetic design of functional compression bias. Mat Sci Eng C 30:1077–1084Google Scholar
  170. Liu X, Dean MN, Youssefpour H et al (2014) Stress relaxation behavior of tessellated cartilage from the jaws of blue sharks. J Mech Beh Biomed Mat 29:68–80.  https://doi.org/10.1016/j.jmbbm.2013.08.014CrossRefGoogle Scholar
  171. Lowe CG, Wetherbee BM, Crow GL et al (1996) Ontogenetic dietary shifts and feeding behavior of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Env Biol Fish 47:203–211Google Scholar
  172. Luer CA, Blum PC, Gilbert PW (1990) Rate of tooth replacement in the nurse shark, Ginglymostoma cirratum. Copeia 1990:182–191Google Scholar
  173. Luger A, Schotte M, Baum D et al (2015) On the jaws of lamniforms sharks. Paper presented at the tomography for scientific advancement symposium, Manchester, UK, 3–4 Sep 2015Google Scholar
  174. Lund R, Grogan ED (1997) Relationships of the Chimaeriformes and the basal radiation of the Chondrichthyes. Rev Fish Biol Fish 7:65–123Google Scholar
  175. Maisey JG (1980) An evaluation of jaw suspension in sharks. Am Mus Novit 2706:1–17Google Scholar
  176. Maisey JG (2013) The diversity of tessellated calcification in modern and extinct chondrichthyans. Rev de Paleobiol Geneve 32(2):355–371Google Scholar
  177. Mara KR, Motta PJ, Huber DR (2010) Bite force and performance in the durophagous bonnethead shark Sphyrna tiburo. J Exp Zool A 313(2):95–105Google Scholar
  178. Martin RA, Hammerschlag N, Collier RS et al (2005) Predatory behaviour of white sharks (Carcharodon carcharias) at Seal Island, South Africa. J Mar Biol Assoc UK 85:1121–1135Google Scholar
  179. Maruska KP (2001) Morphology of the mechanosensory lateral line system in elasmobranch fishes: ecological and behavioral considerations. Env Biol Fish 60:47–75Google Scholar
  180. Maruska KP, Tricas TC (1998) Morphology of the mechanosensory lateral line system in the Atlantic stingray, Dasyatis sabina: the mechanotactile hypothesis. J Morphol 238:1–22PubMedGoogle Scholar
  181. Maruska KP, Tricas TC (2004) Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray. J Exp Biol 207:3463–3476PubMedGoogle Scholar
  182. Mathewson RF, Hodgson ES (1972) Klinotaxis and rheotaxis in orientation of sharks toward chemical stimuli. Comp Biochem Physiol A 42:79–84PubMedGoogle Scholar
  183. Matott MP, Motta PJ, Hueter RE (2005) Modulation in feeding kinematics and motor pattern of the nurse shark Ginglymostoma cirratum. Env Biol Fish 74:163–174Google Scholar
  184. Mazur MM, Beauchamp DA (2003) A comparison of visual prey detection among species of piscivorous salmonids: effects of light and low turbidities. Env Biol Fish 67:397–405Google Scholar
  185. McComb DM, Tricas TC, Kajiura SM (2009) Enhanced visual fields in hammerhead sharks. J Exp Biol 212:4010–4018PubMedGoogle Scholar
  186. McCosker JE (1987) The white shark, Carcharodon carcharias has a warm stomach. Copeia 1987:195–197Google Scholar
  187. Medved RJ (1985) Gastric evacuation in the sandbar shark, Carcharhinus plumbeus. J Fish Biol 26:239–253Google Scholar
  188. McCourt RM, Kerstitch AN (1980) Mating behavior and sexual dimorphism in dentition in the stingray Urolophus concentricus from the Gulf of California. Copeia 1980:900–901Google Scholar
  189. McEachern JD (1977) Reply to ‘Sexual dimorphism in skates (Rajidae)’. Evolution 31:218–220Google Scholar
  190. McGowan DW, Kajiura SM (2009) Electroreception in the euryhaline stingray, Dasyatis sabina. J Exp Biol 212:1544–1552PubMedGoogle Scholar
  191. Meredith TM, Kajiura SM (2010) Olfactory morphology and physiology of elasmobranchs. J Exp Biol 213:3449–3456PubMedGoogle Scholar
  192. Mertinene RA (1982) The histology of the teeth of elasmobranchs. Paleontol J 16:74–82Google Scholar
  193. Meyer CG, Holland KN (2012) Autonomous measurement of ingestion and digestion processes in free-swimming sharks. J Exp Biol 215:3681–3684PubMedGoogle Scholar
  194. Michelangeli F, Ruiz MC, Dominguez MG et al (1988) Mammalian like differentiation of gastric cells in the shark Hexanchus griseus. Cell Tissue Res 251:225–227PubMedGoogle Scholar
  195. Miyake T (1988) The systematics of the stingray genus Urotrygon with comments on the interrelationships within Urolophidae (Chondricthyes, Myliobatiformes). Dissertation, Texas AandM UniversityGoogle Scholar
  196. Miyake T, McEachran JD, Hall BK (1992) Edgeworth’s legacy of cranial muscle development with an analysis of muscles in the ventral gill arch region of batoid fishes (Chondrichthyes: Batoidea). J Morphol 212:213–256PubMedGoogle Scholar
  197. Montgomery JC (1989) Lateral line detection of planktonic prey. In: Coombs S, Gorner P, Munz H (eds) The Mechanosensory lateral line: neurobiology and evolution. Springer, New York, pp 561–574Google Scholar
  198. Montgomery JC, Skipworth E (1997) Detection of weak water jets by the short-tailed stingray Dasyatis brevicaudata (Pisces: Dasyatidae). Copeia 1997:881–883Google Scholar
  199. Moore PA, Atema J (1991) Spatial information in the three-dimensional fine structure of an aquatic odor plume. Biol Bull 181:408–418PubMedGoogle Scholar
  200. Moore PA, Scholz N, Atema J (1991) Chemical orientation of lobsters, Homarus americanus, in turbulent odor plumes. J Chem Ecol 17:1293–1307PubMedGoogle Scholar
  201. Moss ML (1967) Tooth replacement in the lemon shark, Negaprion brevirostris. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, Skates, and Rays. John Hopkins University Press, Baltimore, pp 319–329Google Scholar
  202. Moss SA (1977) Feeding mechanisms in sharks. Amer Zool 17:355–364Google Scholar
  203. Motta PJ (2004) Prey capture behavior and feeding mechanics of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of Sharks and their relatives. CRC Press, Boca Raton, pp 165–202Google Scholar
  204. Motta PJ, Hueter RE, Tricas TC et al (1997) Feeding mechanism and functional morphology of the jaws of the lemon shark, Negaprion brevirostris (Chondrichthyes, Carcharhinidae). J Exp Biol 200:2765–2780PubMedGoogle Scholar
  205. Motta PJ, Wilga CD (1999) Anatomy of the feeding apparatus of the nurse shark, Ginglymostoma cirratum. J Morphol 241:33–60PubMedGoogle Scholar
  206. Motta PJ, Wilga CD (2001) Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Env Biol Fish 20:131–156Google Scholar
  207. Motta PJ, Hueter RE, Tricas TC et al (2002) Kinematic analysis of suction feeding in the nurse shark, Ginglymostoma cirratum (Orectolobiformes, Ginglymostomatidae). Copeia 2002:24–38Google Scholar
  208. Motta PJ, Huber DR (2012) Prey capture behavior and feeding mechanics of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of Sharks and their relatives, 2nd edn. CRC Press, New York, pp 153–209Google Scholar
  209. Motta PJ, Hueter RE, Tricas TC et al (2008) Functional morphology of the feeding apparatus, feeding constraint and suction performance in the nurse shark Ginglymostoma cirratum. J Morphol 269:1041–1055PubMedGoogle Scholar
  210. Motta PJ, Maslanka M, Hueter RE et al (2010) Feeding anatomy, filter–feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology 113:199–212Google Scholar
  211. Moy-Thomas JA, Miles RS (1971) Paleozoic fishes. Chapman and Hall Ltd, LondonGoogle Scholar
  212. Moyer JK, Riccio ML, Bemis WE (2015) Development and microstructure of tooth histotypes in the blue shark, Prionace glauca (Carcharhiniformes: Carcharhinidae) and the great white shark, Carcharodon carcharias (Lamniformes: Lamnidae). J Morphol 276:797–817PubMedGoogle Scholar
  213. Mulvany S, Motta PJ (2013) The morphology of the cephalic lobes and anterior pectoral fins in six species of batoids. J Morphol 274(9):1070–1083PubMedGoogle Scholar
  214. Mulvany S, Motta PJ (2014) Prey capture kinematics in batoids using different prey types: Investigating the role of the cephalic lobes. J Exp Zool A 321(9):515–530Google Scholar
  215. Munroe SEM, Simpfendorfer CA, Heupel MR (2014) Defining shark ecological specialisation: concepts, context, and examples. Rev Fish Biol Fish 24(1):317–331Google Scholar
  216. Myrberg J, Banner A, Richard JD (1969) Shark attraction using a video-acoustic system. Mar Biol 2:264–276Google Scholar
  217. Myrberg J, Ha SJ, Walewski S et al (1972) Effectiveness of acoustic signals in attracting epipelagic sharks to an underwater sound source. Bull Mar Sci 22:926–949Google Scholar
  218. Nakaya K, Matsumoto R, Suda K (2008) Feeding strategy of the megamouth shark Megachasma pelagios (Lamniformes: Megachasmidae). J Fish Biol 73:17–34Google Scholar
  219. Nauwelaerts S, Wilga C, Sanford C et al (2007) Hydrodynamics of prey capture in sharks: effects of substrate. J R Soc Interface 4:341–345PubMedGoogle Scholar
  220. Nelson DR (1967) Hearing thresholds, frequency discrimination, and acoustic orientation in the lemon shark, Negaprion brevirostris (Poey). Bull Mar Sci 17:741–767Google Scholar
  221. Nelson DR, Gruber SH (1963) Sharks: attraction by low-frequency sounds. Science 142:975–977PubMedGoogle Scholar
  222. Nelson DR, Johnson RH, Waldrop LG (1969) Responses of Bahamanian sharks and groupers to low-frequency, pulsed sounds. Bull So Cal Acad Sci 68:131–137Google Scholar
  223. Nelson GA, Ross MR (1995) Gastric evacuation in little skate. J Fish Biol 46:977–986Google Scholar
  224. Nelson JD, Eckert SA (2007) Foraging ecology of whale sharks (Rhincodon typus) within Bahia de Los Angeles, Baja California Norte, Mexico. Fish Res 84:47–64Google Scholar
  225. Newton KC, Wraith J, Dickson KA (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 41:887–898PubMedGoogle Scholar
  226. Niesterok B, Hanke W (2013) Hydrodynamic patterns from the fast-starts in teleost fish and their possible relevance to predator-prey interactions. J Comp Physiol A 199:139–149Google Scholar
  227. Nikonov AA, Illyin YN, Zherelove OM et al (1990) Odour thresholds of the black sea skate (Raja clavata). Electrophysiological study. Comp Biochem Physiol A 95:325–328Google Scholar
  228. Norton SF, Brainerd EL (1993) Convergence in the feeding mechanics of ecomorphologically similar species in the Centrarchidae and Cichlidae. J Exp Biol 176:11–29Google Scholar
  229. Notarbartolo–Di–Sciara G, Hillyer EV (1989) Mobulid rays off Eastern Venezuela. Copeia 1989:607–614Google Scholar
  230. Omelon S, Georgiou J, Variola F et al (2014) Colocation and role of polyphosphates and alkaline phosphatase in apatite biomineralization of elasmobranch tesserae. Acta Biomater 10:3899–3910PubMedGoogle Scholar
  231. Orvig T (1951) Histologic studies of placoderm and fossil elasmobranchs. I. The endoskeleton, with remarks on the hard tissues of lower vertebrates in general. Arkiv Zool 2:321–454Google Scholar
  232. Owen SF (2001) Meeting energy budgets by modulation of behavior and physiology in the eel (Anguillar anguillar). Comp Biochem Physiol A 128:631–644Google Scholar
  233. Paig-Tran EW, Summers AP (2014) Comparison of the structure and composition of the branchial filters in suspension feeding elasmobranchs. Anat Rec 297:701–715Google Scholar
  234. Paig-Tran EWM, Bizzarro JJ, Strother JA et al (2011) Bottles as models: predicting the effects of varying swimming speed and morphology on size selectivity and filtering efficiency in fishes. J Exp Biol 214:1643–1654Google Scholar
  235. Paig-Tran EWM, Kleinteich T, Summers AP (2013) The filter pads and filtration mechanisms of the devil rays: Variation at macro and microscopic scales. J Morphol 274(9):1026–1043Google Scholar
  236. Palmer LM, Deffenbaugh M, Mensinger AF (2005) Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus). J Exp Biol 208:3441–3450PubMedGoogle Scholar
  237. Papastamatiou YP (2007) The potential influence of gastric acid secretion during fasting on digestion time in leopard sharks (Triakis semifasciata). Comp Biochem Physiol A 147:37–42Google Scholar
  238. 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 207:225–232PubMedGoogle Scholar
  239. Papastamatiou YP, Lowe CG (2005) Variations in gastric acid secretion during periods of fasting between two species of shark. Comp Biochem Physiol A 141:210–214Google Scholar
  240. Papastamatiou YP, Wetherbee BM, Lowe CG et al (2006) Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 320:239–251Google Scholar
  241. Papastamatiou YP, Purkis SJ, Holland KN (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 345:129–140Google Scholar
  242. Papastamatiou YP, Wetherbee BM, O’Sullivan J et al (2010) Foraging ecology of cookiecutter sharks (Isistius brasiliensis) on pelagic fishes in Hawaii, inferred from prey bite wounds. Env Biol Fish 88(4):361–368Google Scholar
  243. Papastamatiou YP, Watanabe YY, Bradley D et al (2015) Drivers of daily routines in an ectothermic marine predator: hunt warm, rest warmer? PLoS ONE 10:e0127807PubMedPubMedCentralGoogle Scholar
  244. Peach MB (2001) The dorso-lateral pit organs of the Port Jackson shark contribute sensory information for rheotaxis. J Fish Biol 59:696–704Google Scholar
  245. Peach MB (2003) The behavioral role of pit organs in the epaulette shark. J Fish Biol 62:793–802Google Scholar
  246. Penry DL, Jumars PA (1987) Modelling animal guts as chemical reactors. Am Naturalist 129:69–96Google Scholar
  247. Peyer B (1968) Comparative odontology. University of Chicago Press, ChicagoGoogle Scholar
  248. Pohlmann K, Atema J, Breithaupt T (2004) The importance of the lateral line in nocturnal predation of piscivorous catfish. J Exp Biol 207:2971–2978PubMedGoogle Scholar
  249. Pohlmann K, Grasso FW, Breithaupt T (2001) Tracking wakes: the nocturnal predatory strategy of piscivorous catfish. Proc Natl Acad Sci USA 98:7371–7374PubMedGoogle Scholar
  250. Porter ME, Beltran JL, Koob TJ et al (2006) Material properties and biochemical composition of mineralized vertebral cartilage in seven elasmobranch species (Chondrichthyes). J Exp Biol 209:2920–2928PubMedGoogle Scholar
  251. Porter ME, Koob TJ, Summers AP (2007) The contribution of mineral to the material properties of vertebral cartilage from the smooth-hound shark Mustelus californicus. J Exp Biol 210:3319–3327PubMedGoogle Scholar
  252. Powlik JJ (1995) On the geometry and mechanics of tooth position in the white shark Carcharodon carcharias. J Morphol 226:277–288PubMedGoogle Scholar
  253. Powter DM, Gladstone W, Platell M (2010) The influence of sex and maturity on the diet, mouth morphology and dentition of the Port Jackson shark, Heterodontus portusjacksoni. Mar Freshw Res 61:74–85Google Scholar
  254. Pratt HKL, Carrier JC (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark Ginglymostoma cirratum. Env Biol Fish 60:157–158Google Scholar
  255. Preuschoft H, Reif WE, Muller WH (1974) Funktionsanpassungen in form und struktur an haifischzahnen. Z Anat Entwickl-Gesch 143:315–344Google Scholar
  256. Quinn TP, Miller BS, Wingert RC (1980) Depth distribution and seasonal and diel movements of ratfish, Hydrolagus colliei, in Puget Sound, Washington. Fish Bull 78:816–821Google Scholar
  257. Ramsay JB, Wilga CD (2007) Morphology and mechanics of the teeth and jaws of white-spotted bamboo sharks (Chiloscyllium plagiosum). J Morphol 268:664–682PubMedGoogle Scholar
  258. Ramsay JB, Wilga CD, Tapanila L et al (2015) Eating with a saw for a jaw: Functional morphology of the jaws and tooth-whorl in Helicoprion davisii. J Morphol 276(1):47–64PubMedGoogle Scholar
  259. Raschi W (1978) Notes on the gross functional morphology of the ampullary system in two similar species of skates, Raja erinacea and R. ocellata. Copeia 1978:48–53Google Scholar
  260. Rebolledo IM, Vial JD (1979) Fine structure of the oxynticopeptic cell in the gastric glands of an elasmobranch species (Halaelurus chilensis). Anat Rec 193:805–822PubMedGoogle Scholar
  261. Reidenberg JS, Laitman JT (2010) Generation of sound in marine mammals. In: Brudzynski SM (ed) Handbook of Mammalian Vocalization: an integrative neuroscience approach. Academic Press, Amsterdam, pp 451–465Google Scholar
  262. Reif WE (1983) Functional morphology and evolutionary ecology. Paläontologie Zeitschrift 57:255–266Google Scholar
  263. Reif WE, McGill D, Motta PJ (1978) Tooth replacement rates of the sharks Triakis semifasciata and Ginglymostoma cirratum. Zool Jahrb Anat Ontog 99:151–156Google Scholar
  264. Ribéreau-Gayon A, Rando C, Schuliar Y et al (2016) Extensive unusual lesions on a large number of immersed human victims found to be from cookiecutter sharks (Isistius spp.): an examination of the Yemenia plane crash. Int J Legal Med.  https://doi.org/10.1007/s00414-016-1449-6PubMedPubMedCentralGoogle Scholar
  265. Richard JD (1968) Fish attracted with low-frequency pulsed sound. J Fisheries Res Board Can 25:1441–1452Google Scholar
  266. Roberts BL (1978) Mechanoreceptors and the behavior of elasmobranch fishes with special reference to the acoustico-lateralis system. In: Hodgson ES, Mathewson RF (eds) Sensory biology of Sharks, Skates and Rays. Office of Naval Research, Department of the Navy, Arlington, pp 331–390Google Scholar
  267. Rosenberg LR (1998) A comparison of the mineralized endoskeletal tissues of several recent and fossil chondrichthyans from the Bear Gulch limestone of Montana. MS thesis. Adelphi UniversityGoogle Scholar
  268. Rosenthal GG (2007) Spatiotemporal dimensions of visual signals in animal communication. Ann Rev Ecol Evol Syst 28:155–178Google Scholar
  269. Rubenstein DI, Koehl MAR (1977) The mechanisms of filter feeding: some theoretical considerations. Am Naturalist 111:981–994Google Scholar
  270. Schaeffer B (1967) Comments on elasmobranch evolution. In: Gilbert PW, Mathewson RF, Rall DB (eds) Sharks, Skates, and Rays. John Hopkins Press, Baltimore, pp 3–35Google Scholar
  271. Schluessel V, Bennett MB, Collin SP (2010) Diet and reproduction in the white-spotted eagle ray Aetobatus narinari from Queensland, Australia and the Penghu Islands, Taiwan. Mar Freshw Res 61:1278–1289Google Scholar
  272. Schmitz B (2002) Sound production in crustacea with special reference to Alpheidae. In: Wiese DK (ed) The Crustacean Nervous System. Springer-Verlag, Berlin, pp 536–547Google Scholar
  273. Schnetz L, Pfaff C, Kriwet J (2016) Tooth development and histology patterns in lamniform sharks (Elasmobranchii, Lamniformes) revisited. J Morphol 277:1584–1598PubMedGoogle Scholar
  274. Schofield RMS, Choi S, Coon JJ et al (2016) Is fracture a bigger problem for smaller animals? Force and fracture scaling for a simple model of cutting, puncture, and crushing. Interface Focus 6:20160002PubMedPubMedCentralGoogle Scholar
  275. Schwimmer DR, Stewart JD, Williams GD (1997) Scavenging by sharks of the genus Squalicorax in the Late Cretaceous of North America. Palaios 12:71–83Google Scholar
  276. Schulte-Pelkum N, Wieskotten S, Hanke W et al (2007) Tracking of biogenic hydrodynamic trails in harbour seals (Phoca vitulina). J Exp Biol 201:781–787Google Scholar
  277. Secor SM, Carey HV (2016) Integrative physiology of fasting. Compr. Phys. 6:773–825Google Scholar
  278. Segura-Zarzosa JC, Abitia-Cardenas LA, Galvan-Magana F (1997) Observations on the feeding habits of the shark Heterodontus francisci Girard 1854 (Chondrichthyes: Heterodontidae), in San Ignacio Lagoon, Baja California Sur, Mexico. Cienc Mar 23:111–128Google Scholar
  279. Seidel R, Lyons K, Blumer M et al (2016) Ultrastructural and developmental features of the tessellated endoskeleton of elasmobranchs (sharks and rays). J Anat 229(5):681–702PubMedPubMedCentralGoogle Scholar
  280. Seilacher A (1979) Constructional morphology of sand dollars. Paleobiology 5:191–221Google Scholar
  281. Sheldon RE (1911) The sense of smell in selachians. J Exp Zool 10:51–62Google Scholar
  282. Shirai S, Nakaya K (1992) Functional morphology of the feeding apparatus of the cookie-cutter shark, Isistius brasiliensis (Elasmobranchii, Dalatiinae). Zool Sci 9:811–821Google Scholar
  283. Silver WL (1979) Olfactory responses from a marine elasmobranch, the Atlantic stingray, Dasyatis sabina. Mar Behav Physiol 6:297–305Google Scholar
  284. Silver WL, Caprio J, Blackwell JF et al (1976) The underwater electro-olfactogram: a tool for the study of the sense of smell of marine fishes. Experientia 32:1216–1217PubMedGoogle Scholar
  285. Sims DW, Davies SJ (1994) Does specific dynamic action (SDA) regulate return of appetite in the lesser spotted dogfish, Scyliorhinus canicula? J Fish Biol 45:341–348Google Scholar
  286. Sims DW, Davies SJ, Bone Q (1996) Gastric emptying rate and return of appetite in lesser-spotted dogfish, Scyliorhinus canicula. J Mar Biol Assoc UK 76:479–491Google Scholar
  287. Sims DW (2000) Filter–feeding and cruising swimming speeds of basking sharks compared with optimal models: they filter–feed slower than predicted for their size. J Exp Mar Biol Ecol 249:65–76Google Scholar
  288. Sims DW, Wearmouth VJ, Southall EJ et al (2006) Hunt warm, rest cold: bioenergetic strategy underlying diel vertical migration of a benthic shark. J Anim Ecol 75:176–190PubMedGoogle Scholar
  289. Sisnero JA, Rogers PH (2016) Directional hearing and sound source localization in fishes. In: Sisneros JA (ed) Fish hearing and bioacoustics. Springer International Publishing, Switzerland, pp 121–155Google Scholar
  290. Springer S (1967) Social organization of shark populations. In: Gilbert PW, Mattewson RF, Rall DP (eds) Sharks, Skates and Rays. Johns Hopkins Press, Baltimore, pp 149–174Google Scholar
  291. Stahl BJ, Parris DC (2004) The complete dentition of Edaphodon mirificus (Chondrichthyes: Holocephali) from a single individual. J Paleontol 78:388–392Google Scholar
  292. Strong WR Jr (1989) Behavioral ecology of horn sharks, Heterodontus francisci, at Santa Catalina Island, California, with emphasis on patterns of space utilization. MS thesis, California State University, Long Beach, CAGoogle Scholar
  293. Sullivan MX (1905) The physiology of the digestive tract of elasmobranchs. Amer J Physiol 15:42–45Google Scholar
  294. Summers AP (2000) Stiffening the stingray skeleton—an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). J Morphol 243:113–126PubMedGoogle Scholar
  295. Summers AP, Ketcham R, Rowe T (2004) Structure and function of the horn shark (Heterodontus francisci) cranium through ontogeny: the development of a hard prey specialist. J Morphol 260:1–12PubMedGoogle Scholar
  296. Tagliofierro G, Faraldi G, Pestarino M (1985) Interrelationships between somatostatin-like cells and other endocrine cells in the pancreas of some cartilaginous fish. Cell Molec Biol 31:201–207Google Scholar
  297. Taniuchi T, Shimizu M (1993) Dental sexual dimorphism and food habits in the stingray Dasyatis akajei from Tokyo Bay, Japan. Nippon Suisan Gekkaishi 59:53–60Google Scholar
  298. Taylor JG (2007) Ram filter–feeding and nocturnal feeding of whale sharks (Rhincodon typus) at Ningaloo Reef, Western Australia. Fish Res 84:65–70Google Scholar
  299. Tester AL (1963a) Olfaction, gustation, and the common chemical sense in sharks. In: Gilbert PW (ed) Sharks and survival. DC Heath and Company, Lexington, pp 255–282Google Scholar
  300. Tester AL (1963b) The role of olfaction in shark predation. Pac Sci 17:145–170Google Scholar
  301. Tester AL, Kato S (1966) Visual target discrimination in blacktip sharks (Carcharhinus melanopterus) and grey sharks (C. menisorrah). Pac Sci 20:461–471Google Scholar
  302. Tricas TC (1977) Food habits, movement and seasonal abundance of the blue shark (Prionace glauca) in southern California waters. MS Thesis. California State University Long Beach, CA, USAGoogle Scholar
  303. Tricas TC (1982) Bioelectric mediated predation by the swell shark, Cephaloscyllium ventriosum. Copeia 1982:948–952Google Scholar
  304. Tricas TC, McCosker JE (1984) Predatory behavior of the white shark (Carcharodon carcharias) with notes on its biology. Proc Calif Acad Sci 43:221–238Google Scholar
  305. Tricas TC, Kajiura SM, Summers AP (2009) Response of the hammerhead shark olfactory epithelium to amino acid stimuli. J Comp Physiol A 195:947–954Google Scholar
  306. Underwood CJ, Johanson Z, Welten M et al (2015) Development and evolution of dentition pattern and tooth order in the skates and rays (Batoidea: Chondrichthyes). PLOSone 10:e1022553Google Scholar
  307. Van-Eyk SM, Siebeck UE, Champ CM et al (2011) Behavioural evidence for colour vision in an elasmobranch. J Exp Biol 214:4186–4192PubMedGoogle Scholar
  308. Verwaijen D, Van Damme R, Herrel A (2002) Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Funct Ecol 16:842–850Google Scholar
  309. Vigna S (1983) Evolution of endocrine regulation of gastrointestinal function in lower vertebrates. Amer Zool 23:729–738Google Scholar
  310. Vincent JFV, Owers P (1986) Mechanical design of hedgehog spines and porcupine quills. J Zool Lond 210:55–75Google Scholar
  311. Vogel S (2003) Comparative biomechanics: life’s physical world. Princeton University PressGoogle Scholar
  312. Vullo R (2011) Direct evidence of hybodont shark predation on Late Jurassic ammonites. Naturwissenschaften 98:545–549PubMedGoogle Scholar
  313. Wainwright PC (1999) Ecomorphology of prey capture in fishes. In: Saksena E (ed) Advances in Ichthyological research. Jiwaji University Press, Gwalior, India, pp 375–387Google Scholar
  314. Wainwright SA, Biggs WD, Currey JD et al (1976) Mechanical design in organisms. Princeton University Press, PrincetonGoogle Scholar
  315. Wass RC (1973) Size, growth, reproduction of the sandbar shark, Carcharhinus milberti, in Hawaii. Pac Sci 27:305–318Google Scholar
  316. Webster DR (2007) Structure of turbulent chemical plumes. In: Woodfin RL (ed) Trace chemical sensing of explosives. Wiley, New York, pp 109–129Google Scholar
  317. Webster DR, Weissburg MJ (2001) Chemosensory guidance cues in a turbulent chemical odor plume. Limnol Oceanogr 46:1034–1047Google Scholar
  318. Weissburg MJ, Dusenbery DB, Ishida H et al (2002) A multidisciplinary study of spatial and temporal scales containing information in turbulent chemical plume tracking. Env Fluid Mech 2:65–94Google Scholar
  319. Wetherbee BM, Gruber SH, Ramsey AL (1987) X-radiographic observation of food passage through digestive tracts of lemon sharks. Trans Am Fisher Soc 116:763–767Google Scholar
  320. Wetherbee BM, Gruber SH (1990) The effects of ration level on food retention time in juvenile lemon sharks, Negaprion brevirostris. Env Biol Fish 29:59–65Google Scholar
  321. Wetherbee BM, Gruber SH (1993) Absorption efficiency of the lemon shark, Negaprion brevirostris, at varying rates of energy intake. Copeia 1993:416–424Google Scholar
  322. Whitear M, Moate RM (1994a) Chemosensory cells in the oral epithelium of Raja clavata (Chondrichtyes). J Zool 232:295–312Google Scholar
  323. Whitear M, Moate RM (1994b) Microanatomy of the taste buds in the dogfish, Scyliorhinus canicula. J Submicroscop Cytol Pathol 26:357–367Google Scholar
  324. Whitenack LB, Motta PJ (2010) Performance of shark teeth during puncture and draw: implications for the mechanics of cutting. Biol J Linn Soc 100:271–286Google Scholar
  325. Whitenack LB, Simkins DC Jr, Motta PJ et al (2010) Young’s modulus and hardness of shark tooth materials. Arch Oral Biol 55:203–209PubMedGoogle Scholar
  326. Whitenack LB, Simkins DC Jr, Motta PJ (2011) Biology meets engineering: the structural mechanics of fossil and extant shark teeth. J Morphol 272:169–179PubMedGoogle Scholar
  327. Wilga, CAD (1997) Evolution of feeding mechanisms in elasmobranchs: A functional morphological approach. Dissertation. University of South FloridaGoogle Scholar
  328. Wilga CD, Motta PJ (1998a) Conservation and variation in the feeding mechanism of the spiny dogfish Squalus acanthias. J Exp Biol 201:1345–1358PubMedGoogle Scholar
  329. Wilga CD, Motta PJ (1998b) Feeding mechanism of the Atlantic guitarfish Rhinobatos lentiginosus: modulation of kinematic and motor activity. J Exp Biol 201:3167–3183PubMedGoogle Scholar
  330. Wilga CD, Motta PJ (2000) Durophagy in sharks: feeding mechanics of hammerhead sharks, Sphyrna tiburo. J Exp Biol 203:2781–2796Google Scholar
  331. Wilga CD, Hueter RE, Wainwright PC et al (2001) Evolution of upper jaw protrusion mechanisms in elasmobranchs. Amer Zool 41:1248–1257Google Scholar
  332. Wilga CD (2002) A functional analysis of jaw suspension in elasmobranchs. Biol J Linn Soc 75(4):483–502Google Scholar
  333. Wilga CD (2005) Morphology and evolution of the jaw suspension in lamniform sharks. J Morphol 265(1):102–119PubMedGoogle Scholar
  334. Wilga CD, Motta PJ, Sanford CP (2007) Evolution and ecology of feeding in elasmobranchs. Integr Comp Biol 47(1):55–69PubMedGoogle Scholar
  335. Wilga CD, Sanford CP (2008) Suction generation in white–spotted bamboo sharks Chiloscyllium plagiosum. J Exp Biol 211:3128–3138PubMedGoogle Scholar
  336. Wilga CA, Diniz SE, Steele PR et al (2016) Ontogeny of feeding mechanics in smoothhound sharks: morphology and cartilage stiffness. Integr Comp Biol 56(3):442–448PubMedGoogle Scholar
  337. Williams JG, Patel Y (2016) Fundamentals of cutting. interface. Focus 6:20150108Google Scholar
  338. Williams ME (1990) Feeding behavior in Cleveland Shale fishes. In: Boucot AJ (ed) Evolutionary paleobiology of behavior and coevolution. Elsevier, Amsterdam, pp 273–287Google Scholar
  339. Williams ME (2001) Tooth retention in cladodont sharks: with a comparison between primitive grasping and swallowing, and modern cutting and gouging feeding mechanisms. J Vert Paleontol 21:214–226Google Scholar
  340. Wingert RC, Terry CB, Miller BS (1979) Food and feeding habits of ecologically important nearshore and demersal fishes in central puget sound: final report. Fisheries Research Institute, College of Fisheries, University of WashingtonGoogle Scholar
  341. Wood CM, Kajimura M, Bucking C et al (2006) Osmoregulation, ionoregulation and acid-base regulation by the gastrointestinal tract after feeding in the elasmobranch (Squalus acanthias). J Exp Biol 210:1335–1349Google Scholar
  342. Wroe S, Huber DR, Lowry et al (2008) Three–dimensional computer analysis of white shark jaw mechanics: How hard can a great white bite? J Zool 276:336–342Google Scholar
  343. Wueringer BE, Squire L, Kajiura SM et al (2012) Electric field detection in sawfish and shovelnose rays. PLoS ONE 7:e41605PubMedPubMedCentralGoogle Scholar
  344. Yen J, Weissburg MJ, Doall MH (1998) The fluid physics of signal perception by mate-tracking copepods. Philos Trans R Soc Lond B Biol Sci 353:787–804PubMedPubMedCentralGoogle Scholar
  345. Zeiske E, Caprio J, Gruber SH (1986) Morphological and electrophysiological studies on the olfactory organ of the lemon shark Negaprio brevirostris (Poey). In: Uyeno T, Arai R, Taniuchi T et al (eds) Indo-Pacific fish biology: proceedings of the second international conference on Indo-Pacific Fishes. Ichthyological Society of Japan, Tokyo, pp 381–391Google Scholar
  346. Zimmer-Faust RK, Finelli CM, Pentcheff ND et al (1995) Odor plumes and animal navigation in turbulent water flow: a field study. Biol Bull 188:111–116PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Daniel Huber
    • 1
    Email author
  • Cheryl Wilga
    • 2
  • Mason Dean
    • 3
  • Lara Ferry
    • 4
  • Jayne Gardiner
    • 5
  • Laura Habegger
    • 6
  • Yannis Papastamatiou
    • 7
  • Jason Ramsay
    • 8
  • Lisa Whitenack
    • 9
  1. 1.Department of BiologyThe University of TampaTampaUSA
  2. 2.Department of Biological SciencesUniversity of Alaska AnchorageAnchorageUSA
  3. 3.Department of BiomaterialsMax Planck Institute of Colloids and InterfacesPotsdamGermany
  4. 4.Math and Natural Sciences DivisionArizona State UniversityGlendaleUSA
  5. 5.Division of Natural SciencesNew College of FloridaSarasotaUSA
  6. 6.Biology DepartmentFlorida Southern CollegeLakelandUSA
  7. 7.Marine Sciences ProgramFlorida International UniversityNorth MiamiUSA
  8. 8.Biological Sciences DepartmentWestfield State UniversityWestfieldUSA
  9. 9.Department of BiologyAllegheny CollegeMeadvilleUSA

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