Absence of suction feeding ichthyosaurs and its implications for triassic mesopelagic paleoecology

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Motani, Ryosuke ^a   Ji, Cheng ^b   Tomita, Taketeru ^a,c   Kelley, Neil ^a   Maxwell, Erin ^d   Jiang, Da Yong ^b   Sander, Paul Martin ^e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PEKING UNIVERSITY   (China)

^c HOKKAIDO UNIVERSITY   (Japan)

^d PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; CEPHALOPOD; DETRITIVORE; FEEDING BEHAVIOR; ICHTHYOSAURS; JAW; MANDIBLE; MARINE ENVIRONMENT; MARINE MAMMAL; MARINE SPECIES; MOUTH CAVITY; NONHUMAN; PALEOECOLOGY; REPTILE; SHARK; SPERM WHALE; TRIASSIC; WHALE;

ANIMALS; BIOLOGICAL EVOLUTION; FEEDING BEHAVIOR; FOSSILS; PHYLOGENY; REPTILES;

EID: 84892587638     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066075     Document Type: Article

References (90)

1. Motani R (2009) The evolution of marine reptiles. Evolution: Education and Outreach 2: 224-235.
2. Motani R (2010) Warm blooded sea dragons? Science 328: 1361-1362.
3. Massare JA (1987) Tooth morphology and prey preference of Mesozoic marine reptiles. J Vertebr Paleontol 7: 121-137.
4. Kelley NP (2012) Trophic ecomorphology of Triassic marine reptiles. Unpubl Ph.D. dissertation, University of California, Davis.
5. Kelley N, Motani R, Jiang D, Rieppel O, Tintori A (2009) Rapid diversification of dental and jaw morphology among marine reptiles during the Triassic Recovery. J Vertebr Paleontol 29: 125A.
6. McGowan C, Motani R (2003) Ichthyopterygia. Handbuch der Paläoherpetologie Part 8. Verlag Dr. Friedrich Pfeil, München. 175 pp.
7. Motani R (2005) Ichthyosauria: evolution and physical constraints of fish-shaped reptiles. Ann Rev Earth Planet Sci 33: 395-420.
8. Motani R, Rothschild BM, Wahl W Jr (1999) Large eyes in deep diving ichthyosaurs. Nature 402: 747.
9. Ferry-Graham LA, Lauder GV (2001) Aquatic prey capture in Ray-finned fishes: a century of progress and new directions. J Morphol 248: 99-119.
10. Sander PM, Chen X, Cheng L, Wang X (2011) Short-snouted toothless ichthyosaur from China suggests Late Triassic diversification of suction feeding ichthyosaurs. PLoS One 6: e19480.
11. Nicholls EL, Manabe M (2004) Giant ichthyosaurs of the Triassic-a new species of Shonisaurus from the Pardonet Formation (Norian: Late Triassic) of British Columbia. J Vertebr Paleontol 24: 838-849.
12. Rieppel O (2002) Feeding mechanics in Triassic stem-group sauropterygians: the anatomy of a successful invasion of the Mesozoic seas. Zool J Linn Soc 135: 33-63.
13. Li C, Rieppel O, LaBarbera MC (2004) A Triassic aquatic protorosaur with an extremely long neck. Science 305: 1931.
14. Kelley NP, Motani R, Jiang D, Rieppel O, Schmitz L (2012) Selective extinction of Triassic marine reptiles during long-term sea-level changes illuminated by seawater strontium isotopes. Palaeogeogr Palaeoclimatol Palaeoecol. Available: http://dx.doi.org/10.1016/j.palaeo.2012.07.026.
15. Motani R (2008) Combining uniformitarian and historical data to interpret how Earth environment influenced the evolution of Ichthyopterygia. Paleontol Soc Pap 14: 147-164.
16. Ji C, Jiang D, Motani R, Hao W, Sun Z, et al. (2013) A new juvenile specimen of Guanlingsaurus (Ichthyosauria: Shastasauridae) from the Upper Triassic of Southwestern China. J Vertebr Paleontol 33:1-9.
17. Johnston C, Berta A (2011) Comparative anatomy and evolutionary history of suction feeding in cetaceans. Mar Mamm Sci 27: 493-513.
18. Tomita T, Sato K, Suda K, Kawauchi J, Nakaya K (2011) Feeding of the Megamouth Shark (Pisces: Lamniformes: Megachasmidae) predicted by its hyoid arch: a biomechanical approach. J Morphol 272: 513-524.
19. Lemell P, Lemell C, Sneldervaard P, Gumpenberger M, Wochesländer R, et al. (2010) Feeding patterns of Chelus fimbriatus (Pleurodira: Chalidae). J Exp Biol 205: 1495-1506.
20. Sollas WJ (1916). The skull of Ichthyosaurus, studied in serial sections. Philos Trans R Soc Lond B Biol Sci 208: 63-126.
21. Romer AS (1957) Osteology of the Reptiles. Chicago: University of Chicago Press. p. 772.
22. Rieppel O (1981) The hyobranchial skeleton in some little known lizards and snakes. J Herpetol 15: 433-440.
23. Reese AM (1947) The laryngeal region of Alligator mississipiensis. Anat Rec 92:273-277.
24. Natchev N, Heiss E, Singer K, Kummer S, Salaberger D, et al. (2011) Structure and function of the feeding apparatus in the common musk turtle Sternotherus odoratus (Chelonia, Kinosternidae). Contrib Zool 808: 143-156.
25. Langerbartel DA (1968) The hyoid and its associated muscles in snakes. Illinois Biol Monogr 38: 1-156.
26. Kundrát M, Janáček J, Russell AP (2009) Developmental patterns of the crocodilian and avian columella auris: reappraisal of interpretations of the derivation of the dorsal hyoid arch in archosaurian tetrapods. Zool J Linn Soc 156: 384-410.
27. Smith KK (1984) The use of tongue and hyoid apparatus during feeding in lizards (Ctenosaura similis and Tupinambis nigropunctatus). J Zool 202: 115-143.
28. Smith KK (1986) Morphology and function of the tongue and hyoid apparatus in Varanus (Varanidae, Lacertilia). J Morphol 187: 261-287.
29. Meyers JJ, Herrel A, Nishikawa KC (2002) Comparative study of the innervation patterns of the hyobranchial musculature in three iguanian lizards: Sceloporus undulatus, Pseudotrapelus sinaitus, and and Chamaeleo jacksonii. Anat Rec 267: 177-189.
30. Reidenberg JS, Laitman JT (1994) Anatomy of the hyoid apparatus in Odontoceti (Toothed Whales): specializations of their skeleton and musculature compared with those of terrestrial mammals. Anat Rec 240: 598-624.
31. Werth AJ (2007) Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation. Anat Rec 290: 546-568.
32. Motta PJ, Wilga CAD (1995) Anatomy of the feeding apparatus of the Lemon Sharks, Negaprion bervirostris. J Morphol 226: 309-329.
33. Dean MN, Wilga CD, Summers AP (2005) Eating without hands or tongue: specialization, elaboration and the evolution of prey processing mechanisms in cartilaginous fishes. Biol Lett 2005 1: 357-361.
34. Lauder GV, Prendergast T (1992) Kinematics of aquatic prey capture in the snapping turtle Chelydra serpentina. J Exp Biol 164: 55-78.
35. Kane EA, Marshall CD (2009) Comparative feeding kinematics and performance of odontocetes: belugas, Pacific white-sided dolphins and long-finned pilot whales. J Exp Biol 212: 3939-3950.
36. Liem KF (1980) Acquisition of energy by teleosts: adaptive mechanisms and evolutionary patterns. In: Ali MA, editor. Environmental Physiology of Fishes. New York: Plenum Press. pp. 299-334.
37. Lauder GV, Liem KF (1981) Prey capture by Luciocephalus pulcher: implications for models of jaw protrusion in teleost fishes. Evol Biol Fishes 6: 257-268.
38. Alexander RM (1967) Functional Design in Fishes. London: Hutchinson.
39. Wainwright PC, Ferry-Graham LA, Waltzek TB, Carroll AM, Hulsey CD, et al. (2001) Evaluating the use of ram and suction during prey capture by cichlid fishes. J Exp Biol 204: 3039-3051.
40. Higham TE, Day SW, Wainwright PC (2005) Sucking while swimming: evaluating the effects of ram speed on suction generation in bluegill sunfish Lepomis macrochirus using digital particle image velocimetry. J Exp Biol 208:2653-2660.
41. Norton SF, Brainerd EL (1993) Convergence in the feeding mechanics of ecomorphologically similar species in the Centrarchidae and Cichlidae. J Exp Biol 176: 11-29.
42. Lemell P, Beisser CJ, Gumpenberger M, Snelderwaard P, Gemel R, et al. (2002). The feeding apparatus of Chelus fimbriatus (Pleurodira; Chelidae)-adaptation perfected? Amphib-reptl 31: 97-107.
43. Werth AJ (2006) Mandibular and dental variation and the evolution of suction feeding in Odontoceti. J Mammal 87: 579-588.
44. Bloodworth BE, Marshall CD (2005) Feeding kinematics of Kogia and Tursiops (Odontoceti: Cetacea): characterization of suction and ram feeding. J Exp Biol 208: 3721-3730.
45. Van Damme J, Aerts P (1997) Kinematics and functional morphology of aquatic feeding in Australian snake-necked turtles (Pleurodira; Chelodina). J Morphol 233: 113-125.
46. Summers AP, Darouian KF, Richmond AM, Brainerd EL (1998) Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cryptodire turtles. J Exp Zool 281: 280-287.
47. Sokal RR, Rohlf FJ (1995) Biometry, 3rd Ed. New York: W. H. Freeman and Company. 887 p.
48. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81: 259-291.
49. Werth AJ (2006) Odontocete suction feeding: experimental analysis of water flow and head shape. J Morphol 267: 1415-1428.
50. Heyning JE, Mead JG (1996) Suction feeding in beaked whales: morphological and observational evidence. Contrib Sci, Nat Hist Mus Los Angeles County 464: 1-12.
51. Bramble D (1973) Media dependent feeding in turtles. Am Zool 13: 1342.
52. Bloodworth BE, Marshall CD (2007) A functional comparison of the hyolingual complex in pygmy and dwarf sperm whales (Kogia breviceps and K. sima), and bottlenose dolphis (Tursiops truncatus). J Anat 211: 78-91.
53. Motta PJ, Hueter RE, Tricas TC, Summers AP, Huber DR, et al. (2008) Functional morphology of the feeding apparatus, feeding constraints, and suction performance in the Nurse Shark Ginglymostoma cirratum. J Morphol 269: 1041-1055.
54. Wilga CD, Motta PJ, Sanford CP (2007) Evolution and ecology of feeding in elasmobranchs. Integr Comp Biol 47: 55-69.
55. Ray GC, Schevill WE (1974) Feeding of a captive Gray Whale, Eschrichtius robustus. Mar Fisher Pap 36: 31-38.
56. Feyrer LJ, Duffs DA (2011) Predatory disturbance and prey species diversity: the case of gray whale (Eschrichtius robustus) foraging on a multi-species mysid (family Mysidae) community. Hydrobiologia 678: 37-47.
57. Marshall CD, Kovacs KM, Lydersen C (2008) Feeding kinematics, suction and hydraulic jetting capabilities in bearded seals (Erignathus barbatus). J Exp Biol 211:699-708.
58. Hooker SK, Baird RW (1999) Deep-diving behaviour of northern bottlenose whale, Hyperoodon ampullatus (Cetacea: Ziphiidae). Proc R Soc Lond B Biol Sci 266:671-676.
59. Tyack PL, Johnson M, Soto NA, Sturlese A, Madsen PT (2006) Extreme diving of beaked whales. J Exp Biol 209: 4238-4253.
60. Arranz P, de Soto NA, Madsen PT, Brito A, Bordes F, et al. (2011) Following a foraging fish-finder; diel habitat use of Blainville's beaked whales revealed by echolocation. PLoS One 6: e28353.
61. Santos MB, Pierce GJ, Smeenk C, Addink MJ, Kinze CC, et al. (2001) Stomach contents of northern bottlenose whales Hyperoodon ampullatus stranded in the North Sea. J Mar Biol Assoc U. K. 81: 143-150.
62. Santos MB, Pierce GJ, Herman J, López A, Guerra A, et al. (2001) Feeding ecology of Cuvier's beaked whale (Ziphius cavirostris): a review with new information on the diet of this species. J Mar Biol Assoc U. K. 81: 687-694.
63. Santos MB, Martin V, Arbelo M, Fernández A, Pierce GJ (2007) Insights into the diet of beaked whales from the atypical mass stranding in the Canary Islands in September 2002. J Mar Biol Assoc U. K. 87: 243-251.
64. Childress JJ (1995) Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol Evol 10: 30-36.
65. Seibel BA, Thuesen EV, Childress JJ (2000) Light-limitation of predator-prey interactions: consequences for metabolism and locomotion of deep-sea cephalopods. Biol Bull 198: 284-298.
66. Kubodera T, Koyama Y, Mori K (2007). Observations of wild hunting behaviour and bioluminescence of a large deep-sea, eight-armed squid, Taningia danae. Proc Biol Sci 274:1029-1034.
67. Kubodera T, Mori K (2005) First-ever observations of a live giant squid in the wild. Proc Biol Sci 272: 2583-2586.
68. Aoki K, Amano M, Mori K, Kourogi A, Kubodera T, et al. (2012) Active hunting by deep-diving sperm whales: 3D dive profiles and maneuvers during bursts of speed. Mar Ecol Progr Ser 444: 289-301.
69. Lindberg DR, Pyenson ND (2007) Things that go bump in the night: evolutionary interactions between cephalopods and cetaceans in the tertiary. Lethaia 40: 335-343.
70. Kröger B, Vinther J, Fuchs D (2011) Cephalopod origin and evolution: a congruent picture emerging from fossils, development and molecules. Bioessays 33: 602-613.
71. Zhu K, Bian Z (1984) Sinobelemnitidae, a new Family of belemnitida from the Upper Triassic of Longmenshan, Sichuan. Gu Sheng Wu Xue Bao 23: 300-317. [in Chinese with English Summary]
72. Iba Y, Sano S, Mutterlose J, Kondo Y (2012) Belemnites originated in the Triassic - A new look at an old group. Geology 40: 911-914.
73. Doyle P, Donovan DT, Nixon M (1994) Phylogeny and systematic of the Coleoidea. Univ Kansas Paleontol Contrib 5: 1-15.
74. Doyle P, Kelly SRA, Pirrie D, Riccardi AC (1997) Jurassic belemnite distribution patterns: implications of new data from Antarctica and Argentina. Alcheringa 21: 219-228.
75. Westermann GEG (1973) Strength of concave septa and depth limits of fossil cephalopods. Lethaia 6: 383-403.
76. Dutton A, Huber BT, Lohmann KC, Zinsmeister WJ (2007) High-resolution stable isotope profiles of a dimitobelid belemnite: implications for paleodepth habitat and Late Maastrichtian climate seasonality. Palaios 22: 642-650.
77. Price GD, Page KN (2008) A carbon and oxygen isotopic analysis of molluscan faunas from the Callovian-Oxfordian boundary at Redcliff Point, Weymouth, Dorset: implications for belemnite behaviour. Proc Geol Assoc 119:153-160.
78. Jeletzky JA (1966) Mollusca 7. Comparative morphology, phylogeny, and classification of fossil Coleoidea. Univ Kansas Paleontol Contrib 42: 1-162.
79. Donovan DT (2006) Phragmoteuthida (Cephalopoda: Coleoidea) from the Lower Jurassic of Dorset, England. Palaeontology 49: 673-684.
80. Bandel K (1985) Composition and ontogeny of Dictyoconites (Aulacocerida, Cephalopoda). Paläontol Z 59: 223-244.
81. Nilsson D-E, Warrant EJ, Johnsen S, Hanlon R, Shashar N (2012) A unique advantage for giant eyes in Giant Squid. Curr Biol 22: 1-6.
82. Schmitz L, Motani R, Oufiero CE, Martin CH, McGee MD, et al. (2013) Allometry indicates giant eyes of giant squid are not exceptional. BMC Evolutionary Biology 13:45.
83. Smith AS, Dyke GJ (2008) The skull of the giant predatory pliosaur Rhomaleosaurus cramptoni: implications for plesiosaur phylogenetics. Naturwissenschaften 95:975-980.
84. Rothschild BM, Xiaoting Z, Martin LD (2012) Adaptations for marine habitat and the effect of Triassic and Jurassic predator pressure on development of decompression syndrome in ichthyosaurs. Naturwissenschaften 99:443-448.
85. Westermann GEG, Ward P (1980). Septum morphology and bathymetry in cephalopods. Paleobiology 6:48-50.
86. Hewitt RA, Westermann GEG (1988) Nautiloid septal strength: revisited and revised concepts. Alcheringa 12: 123-128.
87. Hassan MA, Westermann GEG, Hewitt RA, Dokainish MA (2002) Finiteelement analysis of simulated ammonoid septa (extinct Cephalopoda): septal and sutural complexities do not reduce strength. Paleobiology 28: 113-126.
88. Ritterbush KA, Bottjer DJ (2012) Westermann morphospace displays ammonoid shell shape and hypothetical paleoecology. Paleobiology 28:424-446.
89. Fuchs D, Larson N (2011) Diversity, Morphology, and Phylogeny of coleoid cephalopods from the Upper Cretaceous Plattenkalks of Lebanon-Part II: Teudopseina. J Paleontol 85: 815-834.
90. Zakharov YD, Pletnev SP, Mel'nikov ME, Smyshlyaeva OP, Khudik VD, et al. (2007) The first find of Cretaceous belemnites from the Magellan Rise, Pacific Ocean. Russ J Pac Geol 1: 29-41.