Tooth length and occlusion in four species of piscivorous fishes: getting a grip on prey

Abstract

Fitness is in part determined by the success of prey capture, often achieved in marine piscivores using teeth to capture and process prey. In ram feeding piscivores, a pattern of monognathic heterodonty has been observed where tooth size either increases posteriorly (Scomberomorus maculatus), or anteriorly (Carcharhinus limbatus), with exceptions such as Trichiurus lepturus and Sphyraena barracuda which have large anterior fangs. Tooth size and placement, as related to prey capture, was examined in Atlantic Spanish Mackerel (S. maculatus), Great Barracuda (S. barracuda), Atlantic Cutlassfish (T. lepturus), and the Blacktip shark (C. limbatus) by quantifying tooth occlusion along the jaw. Percent gape at occlusion in S. maculatus decreased anteriorly in a linear fashion, indicating occlusion from posterior to anterior. Therefore, prey initially contact the posterior teeth with high puncture pressure during high velocity strikes, capitalizing the region of greatest bite force. For S. barracuda and T. lepturus, posterior teeth and premaxillary fangs occlude at similar percent gapes (within 10%). The premaxillary fangs are likely used for initial capture due to the high angular velocity of the anterior section of the jaw and then for cutting, due to their laterally compressed shape. In C. limbatus all teeth occluded within a narrow range of 1.4–8.8% gape, indicating that all teeth meet at almost complete jaw closure. Simultaneous puncture of teeth prevents prey escape while maximizing the cutting area during head shaking. Thus, various tooth size and dentition patterns may yield similar success in prey capture, serving the same function.

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References

  1. Alfaro ME, Bolnick DI, Wainwright PC (2005) Evolutionary consequences of many-to‐one mapping of jaw morphology to mechanics in labrid fishes. Am Nat 165:140–154. https://doi.org/10.1086/429564

    Article  Google Scholar 

  2. Anderson PSL, Rayeld EJ (2012) Virtual experiments, physical validation: Dental morphology at the intersection of experiment and theory. JR Soc Interface 9:1846–1855. https://doi.org/10.1098/rsif.2012.0043

    Article  Google Scholar 

  3. Anderson PSL, LaCosse J, Pankow M (2016) Point of impact: The effect of size and speed on puncture mechanics. Interface Focus 6:20150111. https://doi.org/10.1098/rsfs.2015.0111

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bemis WE (1984) Morphology and growth of lepidosirenid lungfish tooth plates. J Morphol 179:73–93. https://doi.org/10.1002/jmor.1051790108

    Article  PubMed  Google Scholar 

  5. Bemis KE, Burke SM, St John CA, Hilton EJ, Bemis WE (2019) Tooth development and replacement in the Atlantic Cutlassfish, Trichiurus lepturus, with comparisons to other Scombroidei. J Morphol 280:78–94. https://doi.org/10.1002/jmor.20919

    Article  PubMed  Google Scholar 

  6. Bigelow HB, Farfante IP, Schroeder WC (1948) Fishes of the Western North Atlantic: Lancelets, Cyclostomes and Sharks. Sears Foundation for Marine Research. Yale University, New Haven

    Google Scholar 

  7. Cappetta H (1987) Chondrichthyes II, Mesozoic and Cenozoic Elasmobranchii. Vol 3B. In: Shultze HP (ed) Handbook of Paleoichthyology. Verlag, Munich, pp 474–475. https://doi.org/10.1080/02724634.1988.10011678

  8. Castro JI (1996) Biology of the blacktip shark, Carcharhinus limbatus, off the southeastern United States. Bull Mar Sci 59:508–522

    Google Scholar 

  9. Clark E, von Schmidt K (1965) Sharks of the central gulf coast of Florida. Bull Mar Sci 15:13–83

    Google Scholar 

  10. Compagno LJV (1984) Sharks of The World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 1. Hexanchiformes to Lamniformes. United Nations Food and Agriculture Organization, Rome

    Google Scholar 

  11. Curio E (1976) The Ethology of Predation. Springer-Verlag, Berlin

    Google Scholar 

  12. de Schepper N, Van Wassenbergh S, Adriaens D (2008) Morphology of the jaw system in trichiurids: trade-offs between mouth closing and biting performance. Zool J Linn Soc 152:717–736. https://doi.org/10.1111/j.1096-3642.2008.00348.x

    Article  Google Scholar 

  13. de Sylva DP (1963) Systematics and life history of the great barracuda, Sphyraena barracuda. University of Miami Press, Coral Gables

    Google Scholar 

  14. 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. Zool 111:123–134. https://doi.org/10.1016/j.zool.2007.05.004

    Article  Google Scholar 

  15. Deang JF, Persons AK, Oppedal AL, Rhee H, Moser RD, Horstemeyer MF (2018) Structure, property, and function of sheepshead (Archosargus probatocephalus) teeth. Arch Oral Biol 89:1–8. https://doi.org/10.1016/j.archoralbio.2018.01.013

    Article  PubMed  Google Scholar 

  16. Dickson GC (1979) Concepts of occlusion. Ann R Coll Surg Engl 61:177–182

    PubMed  PubMed Central  Google Scholar 

  17. Enax J, Prymak O, Raabe D, Epple M (2012) Structure, composition, and mechanical properties of shark teeth. J Struct Biol 178:290–299. https://doi.org/10.1016/j.jsb.2012.03.012

    Article  PubMed  Google Scholar 

  18. Ferguson AR, Huber DR, Marc JL, Motta PJ (2015) Feeding performance of king mackerel, Scomberomorus cavalla. J Exp Zool 323A:339–413. https://doi.org/10.1002/jez.1933

    Article  Google Scholar 

  19. Fink WL (1981) Ontogeny and phylogeny of tooth attachment modes in actinopterygian fishes. J Morphol 167:167–184. https://doi.org/10.1002/jmor.1051670203

    Article  PubMed  Google Scholar 

  20. Frazetta TH (1988) The mechanics of cutting and the form of shark teeth (Chondrichthyes, Elasmobranchii). Zoomorphology 108:93–107. https://doi.org/10.1007/BF00539785

    Article  Google Scholar 

  21. Freeman PW (1998) Form, function, and evolution in skulls and teeth of bats. Papers in Nat Res 9:140–156

  22. Freeman PW, Lemen CA (2007) The trade-off between tooth strength and tooth penetration: Predicting optimal shape of canine teeth. J Zool 273:273–280. https://doi.org/10.1111/j.1469-7998.2007.00325.x

    Article  Google Scholar 

  23. 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. Springer-Verlag, Berlin, pp 127–146. https://doi.org/10.1007/978-3-642-41446-6_5

  24. Grubich JR (2005) Disparity between feeding performance and predicted muscle strength in the pharyngeal musculature of black drum, Pogonias cromis (Sciaenidae). Environ Biol Fish 74:261–272. https://doi.org/10.1111/j.1439-0426.2010.01459.x

    Article  Google Scholar 

  25. Grubich JR, Rice AN, Westneat MK (2008) Functional morphology of bite mechanics in the great barracuda (Sphyraena barracuda). Zool 111:16–29. https://doi.org/10.1016/j.zool.2007.05.003

  26. Habegger ML, Motta PJ, Huber DR, Deban SM (2011) Feeding biomechanics in the Great Barracuda during ontogeny. J Zool 283:63–72. https://doi.org/10.1111/j.1469-7998.2010.00745.x

    Article  Google Scholar 

  27. Helfman GS, Collette BB, Facey DE, Bowen BW (2009) The Diversity of Fishes. Biology, Evolution, and Ecology. Wiley-Blackwell, West Sussex, 720 pp

    Google Scholar 

  28. Hernandez LP, Motta PJ (1997) Trophic consequences of differential performance: Ontogeny of oral jaw-crushing performance in the sheepshead, Archosargus probatocephalus (Teleostei, Sparidae). J Zool 243:737–756. https://doi.org/10.1111/j.1469-7998.1997.tb01973.x

  29. Herrel A, Adriaens D, Verraes W, Aerts P (2002) Bite performance in clariid fishes with hypertrophied jaw adductors as deduced by bite modeling. J Morphol 253:196–205. https://doi.org/10.1002/jmor.1121

    Article  PubMed  Google Scholar 

  30. Huber DR, Eason TG, Hueter RE, Motta PJ (2005) Analysis of the bite force and mechanical design of the feeding mechanism of the durophagous horn shark Heterodontus francisci. J Exp Biol 208:3553–3571. https://doi.org/10.1242/jeb.01816

    Article  PubMed  Google Scholar 

  31. Huber DR, Weggelaar CL, Motta PJ (2006) Scaling of bite force in the blacktip shark Carcharhinus limbatus. Zoology 109:109–119. https://doi.org/10.1016/j.zool.2005.12.002

    Article  PubMed  Google Scholar 

  32. Jernvall J, Thesleff I (2012) Tooth shape formation and tooth renewal: evolving with the same signals. Development 139:3487–3497. https://doi.org/10.1242/dev.085084

    Article  PubMed  Google Scholar 

  33. Kadison E, D’Alessandro EK, Davis GO, Hood PB (2010) Age, growth, and reproductive patterns of the great barracuda, Sphyraena barracuda, from the Florida Keys. Bull Mar Sci 86:773–784. https://doi.org/10.5343/bms.2009.1070

    Article  Google Scholar 

  34. Knapp FT (1950) Menhaden utilization in relation to the conservation of food and game fishes of the Texas gulf coast. Trans Am Fish Soc 79:137–144. https://doi.org/10.1577/1548-8659(1949)79[137:MUIRTT]2.0.CO;2

    Article  Google Scholar 

  35. Liem KF (1980) Acquisition of energy by teleosts: adaptive mechanisms and evolutionary patterns. In: Ali MA (ed) Environmental Physiology of Fishes. Springer, Boston, pp 299–344

    Google Scholar 

  36. Liem KF, Bemis WE, Walker WF, Grande L (2001) Functional Anatomy of Vertebrates. An Evolutionary Perspective. Thomson Brooks/Cole, Belmont

    Google Scholar 

  37. Mara KR, Motta PJ, Huber DR (2010) Bite force and performance in the durophagous bonnethead shark, Sphyrna tiburo. J Exp Zool Part A 313:95–105. https://doi.org/10.1002/jez.576

    Article  Google Scholar 

  38. Martins AS, Haimovici M (1997) Distribution, abundance and biological interactions of the cutlassfish Trichiurus lepturus in the southern Brazil subtropical convergence ecosystem. Fish Res 30:217–227. https://doi.org/10.1016/S0165-7836(96)00566-8

    Article  Google Scholar 

  39. Martins AS, Haimovici M, Palacios R (2005) Diet and feeding of the cutlassfish Trichiurus lepturus in the subtropical convergence ecosystem of southern Brazil. J Mar Biol Assoc UK 85:1223–1229. https://doi.org/10.1017/S002531540501235X

    Article  Google Scholar 

  40. Mihalitsis M, Bellwood D (2019) Functional implications of dentition-based morphotypes in piscivorous fishes. R Soc Open Sci 6. https://doi.org/10.1098/rsos.190040

  41. Moss SA (1972) The feeding mechanism of sharks of the family Carcharhinidae. J Zool Lond 167:423–436. https://doi.org/10.1111/j.1469-7998.1972.tb01734.x

    Article  Google Scholar 

  42. 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 165–202

    Google Scholar 

  43. Motta PJ, Huber DR (2012) Prey capture behavior and feeding mechanics of elasmobranchs. In: Carrier CJ, Musick JA, Heithaus MR (eds) Biology of Sharks and Their Relatives, 2nd edn. CRC Press, Boca Raton, pp 139–164

    Google Scholar 

  44. Motta PJ, Wilga CD (2001) Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environ Biol Fish 60:131–156

    Article  Google Scholar 

  45. Nakamura I, Parin NV (1993) Snake mackerels and cutlassfishes of the world. FAO, Rome

    Google Scholar 

  46. 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

    Google Scholar 

  47. Osse JWM (1990) Form changes in fish larvae in relation to changing demands of function. Netherlands J Zool 40:362–385. https://doi.org/10.1163/156854289X00354

  48. Plikus MV, Zeichner-David M, Mayer JA, Reyna J, Bringas P, Thewissen JGM, Snead ML, Chai Y, Chuong CM (2005) Morphoregulation of teeth: modulating the number, size, shape and differentiation by tuning Bmp activity. Evol Dev 7:440–457. https://doi.org/10.1111/j.1525-142X.2005.05048.x

    Article  PubMed  PubMed Central  Google Scholar 

  49. Porter HT, Motta PJ (2004) A comparison of strike and prey capture kinematics of three species of piscivorous fishes: Florida gar (Lepisosteus platyrhincus), redfin needlefish (Strongylura notata), and great barracuda (Sphyraena barracuda). Mar Biol 145:989–1000. https://doi.org/10.1007/s00227-004-1380-0

    Article  Google Scholar 

  50. Powlik JJ (1995) On the geometry and mechanics of tooth position in the white shark, Carcharodon carcharias. J Morphol 226:277–288. https://doi.org/10.1002/jmor.1052260304

    Article  PubMed  Google Scholar 

  51. Ramsay JB, Wilga CD (2007) Morphology and mechanics of the teeth and jaws of white-spotted bamboo sharks (Chiloscyllium plagiosum). J Morphol 268:664–682

    Article  Google Scholar 

  52. Schmidt TW (1989) Food habits, length-weight relationship and condition factor of young great barracuda, Syphraena barracuda (Walbaum), from Florida Bay, Everglades National Park, Florida. Bull Mar Sci 44:163–170

    Google Scholar 

  53. Schofield RMS, Choi S, Coon JJ, Goggans MS, Kreisman TF, Silver DM, Nesson MH (2016) Is fracture a bigger problem for smaller animals? Force and fracture scaling for a simple model of cutting, puncture and crushing. Interface Focus 6:20160002. https://doi.org/10.1098/rsfs.2016.0002

    Article  PubMed  PubMed Central  Google Scholar 

  54. Song J, Ortiz C, Boyce MC (2011) Threat-protection mechanics of an armored fish. J Mech Behav Biomed Mater 4:699–712. https://doi.org/10.1016/j.jmbbm.2010.11.011

    Article  PubMed  Google Scholar 

  55. Sonnefeld MJ, Turingan RG, Sloan TJ (2014) Functional morphological drivers of feeding mode in marine teleost fishes. Adv Zool Bot 2:6–14. https://doi.org/10.13189/azb.2014.020102

    Article  Google Scholar 

  56. Streelman JT, Webb JF, Albertson RC, Kocher TD (2003) The cusp of evolution and development: a model of cichlid tooth shape diversity. Evol Dev 5:600–608. https://doi.org/10.1046/j.1525-142X.2003.03065.x

    Article  PubMed  Google Scholar 

  57. Tabor RA, Shively RS, Poe TP (1993) Predation of juvenile salmonids by smallmouth bass and northern squawfish in the Columbia River near Richland, Washington. N Am J Fish Manag 13:831–838

    Article  Google Scholar 

  58. Trapani J (2001) Position of developing replacement teeth in teleosts. Copeia 2001:35–51. https://doi.org/10.1643/0045-8511

  59. van Casteren A, Crofts SB (2019) The Materials of Mastication: Material Science of the Humble Tooth. Integr Comp Biol 59:1681–1689. https://doi.org/10.1093/icb/icz129

    Article  PubMed  Google Scholar 

  60. Videler JJ, Hess F (1984) Fast Continuous Swimming of Two Pelagic Predators, Saithe (Pollachius Virens) and Mackerel (Scomber Scombrus): a Kinematic Analysis. J Exp Biol 109:209–228

  61. Wainwright PC, Ferry-Graham LA, Waltzek TB et al (2001) Evaluating the use of ram and suction during prey capture by cichlid fishes. J Exp Biol 204:3039–3051

    PubMed  Google Scholar 

  62. Wainwright PC, Alfaro ME, Bolnick DI, Hulsey CD (2005) Many-to-one mapping of form to function: a general principle in organismal design? Integr Comp Biol 45:256–262. https://doi.org/10.1093/icb/45.2.256

    Article  PubMed  Google Scholar 

  63. Walters V (1962) Body form and swimming performance in the scombroid fishes. Am Zool 2:143–149

    Article  Google Scholar 

  64. Wautier K, Van der heyden C, Huysseune A (2001) A quantitative analysis of pharyngeal tooth shape in the zebrafish (Danio rerio, Teleostei, Cyprinidae). Arch Oral Biol 46:67–75. https://doi.org/10.1016/S0003-9969(00)00091-1

    Article  PubMed  Google Scholar 

  65. Westneat MW (1994) Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes). Zoomorphology 114:103–118. https://doi.org/10.1007/BF00396643

    Article  Google Scholar 

  66. Westneat MW (2003) A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. J Theor Biol 223:269–281. https://doi.org/10.1016/S0022-5193(03)00058-4

    Article  PubMed  Google Scholar 

  67. Whitenack LB, Motta PJ (2010) Performance of shark teeth during puncture and draw: implications for the mechanics of cutting. Biol J Linn Soc 100:271–286. https://doi.org/10.1111/j.1095-8312.2010.01421.x

    Article  Google Scholar 

  68. Wilga CD, Motta PJ, Sanford CP (2007) Evolution and ecology of feeding in elasmobranchs. Integr Comp Biol 47:55–69. https://doi.org/10.1093/icb/icm029

    Article  PubMed  Google Scholar 

  69. Wroe S, Huber DR, Lowry M et al (2008) Three-dimensional computer analysis of white shark jaw mechanics: how hard can a great white bite? J Zool 276:336–342. https://doi.org/10.1111/j.1469-7998.2008.00494.x

    Article  Google Scholar 

  70. Yamaoka K (1983) Feeding behavior and dental morphology of algal scraping cichlids (Pisces:Teleostei) in Lake Tanganyika. African Study Monographs 4:77–89. https://doi.org/10.14989/68000

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Acknowledgements

This work was in-part supported by the Porter Family Foundation grant to EC. We thank Capt. Dave Zalewski and the crew of the Lucky Too charters, Rob Robins from the Florida Museum of Natural History, and Jayne Gardiner from New College of Florida for their generous support of specimens. This work is dedicated to David and Rebecca Carr. Animal welfare was approved under IACUC protocol number IS00005719 to PJM.

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Online Resource 1
figure6

One Way ANOVA results for normality tests (Shapiro-Wilk) and equal variance tests. Multiple comparison procedures (Holm-Sidak method) were performed for d1, d2, d3, and d7 in T. lepturus and d4 in C. limbatus. When equal variance tests failed, such as in d1 and d2 of S. malculatus and d3 of T. lepturus, data was added to one and log transformed. Equal variance tests for d2 of S. malculatus still failed after transformation so a Kruskal-Wallis test was conducted. (PNG 360 kb)

Online Resource 2
figure7

Equations and r2 values for regressions of inter-tooth distance as a percent of maximum gape against percent gape as shown in Fig. 1 and Online Resource 1. (PNG 700 kb)

Online Resource 3
figure8

Length of all teeth in the upper and lower jaws as a percent of total length. The missing values indicate that the number of teeth varied in upper and lower jaws. aS. maculatusbS. barracudacT. lepturusdC. limbatus. (PNG 1216 kb)

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Carr, E.M., Motta, P.J. Tooth length and occlusion in four species of piscivorous fishes: getting a grip on prey. Environ Biol Fish (2020). https://doi.org/10.1007/s10641-020-00991-8

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Keywords

  • Prey capture
  • Ram feeding
  • Dentition
  • Heterodonty
  • Piscivorous fishes