Advertisement

Environmental Biology of Fishes

, Volume 102, Issue 9, pp 1193–1200 | Cite as

Jaw muscle activation patterns of several Batoids

  • S. P. GerryEmail author
  • L. K. Brodeur
  • M. DeCaprio
  • A. J. Khursigara
  • S. Mazzeo
  • D. L. Neubauer
Article

Abstract

Fishes may increase the flexibility of their feeding apparatus with a specialized morphology or by altering their behavior during capture or processing. Alternatively, fishes can modulate the timing of jaw muscle activation between the left and right sides of the head. Batoids have a unique cranial morphology including an overall flattened body shape, euhyostylic jaw suspension and typically, a loose symphysis at the jaw midline. These features promote flexibility and mobility of the jaws during feeding. Several batoid species have shown asymmetrical movements of their jaws, enabling them to diversify their feeding habits. Using two asynchrony indices, we investigated pairwise activation of the jaw muscles in four species of batoids in order to compare synchronous versus asynchronous activation patterns during prey capture and processing. The four species we investigated all use synchronous activation when feeding on small or large pieces of squid, in contrast to previous studies. Therefore, we recommend future studies that utilize complex prey in order to attempt to elicit asynchronous behaviors.

Keywords

Stingray Feeding Asynchrony index Electromyography 

Notes

Acknowledgements

This research was funded by a Fairfield University Faculty Research Grant and NSF grant IOS-1354469 to SPG, a Hardiman Scholarship to LKB, a Hardiman Scholarship to AJK and a Lawrence Scholarship to DLN. We would like to thank Mason Dean for his advice on the experimental methods and Clinton Moran for comments that improved this manuscript. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Almeida MP, Lins PM, Charvet-Almeida P, Barthem RB (2010) Diet of the freshwater stingray Potamotrygon motoro (Chondrichthyes: Potamotrygonidae) on Marajó Island (Pará, Brazil). Braz J Biol 70:155–162CrossRefGoogle Scholar
  2. Aschliman NC, Nishida M, Miya M, Inoue JG, Rosana KM, Naylor GJP (2012) Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea). Mol Phylogenet Evol 63:28–42CrossRefGoogle Scholar
  3. Cundall D, Lorenz-Elwood J, Groves JD (1987) Asymmetric suction feeding in primitive salamanders. Experientia 43:1229–1231CrossRefGoogle Scholar
  4. Dean MN, Motta PJ (2004a) Feeding behavior and kinematics of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea). Zoology 107:171–189CrossRefGoogle Scholar
  5. Dean MN, Motta PJ (2004b) Anatomy and functional morphology of the feeding apparatus of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea). J Morphol 262:462–483CrossRefGoogle Scholar
  6. 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 1:357–361CrossRefGoogle Scholar
  7. Dean MN, Bizzaro JJ, Summers AP (2007) The evolution of cranial design, diet, and feeding mechanisms in batoid fishes. Integ Comp Biol 47:70–81CrossRefGoogle Scholar
  8. 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
  9. Fontenelle JP, Loboda TS, Kolmann M, De Carvalho MR (2017) Angular cartilage structure and variation in Neotropical freshwater stingrays (Chondrichthyes: Myliobatiformes: Potamotrygonidae), with comments on their function and evolution. Zool J Linnean SocGoogle Scholar
  10. Friel JP, Wainwright PC (1999) Evolution of complexity in motor patterns and jaw musculature of tetraodontiform fishes. J Exp Biol 202:867–880Google Scholar
  11. Gerry SP, Ramsay JB, Dean MN, Wilga CD (2008) Evolution of asynchronous motor activity in paired muscles: effects of ecology, morphology and phylogeny. Integ Comp Biol 48:272–282CrossRefGoogle Scholar
  12. Gerry SP, Summers AP, Wilga CD, Dean MN (2010) Pairwise modulation of jaw muscle activity in two species of elasmobranchs. J Zool 281:282–292Google Scholar
  13. Gilliam DS, Sullivan KM (1993) Diet and feeding habits of the southern stingray Dasyatis americana in the Central Bahamas. Bull Mar Sci 3:1007–1013Google Scholar
  14. 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 208:3553–3571CrossRefGoogle Scholar
  15. Kolmann MA, Huber DR, Dean MN, Grubbs RD (2014) Myological variability in a decoupled skeletal system: batoid cranial anatomy. J Morph 275:862–881CrossRefGoogle Scholar
  16. Kolmann MA, Crofts SB, Dean MN, Summers AP, Lovejoy NR (2015) Morphology does not predict performance: jaw curvature and prey crushing in durophagous stingrays. J Exp Biol 218:3941–3949CrossRefGoogle Scholar
  17. Kolmann MA, Welch KC Jr, Summers AP, Lovejoy NR (2016) Always chew your food: freshwater stingrays use mastication to process tough insect prey. Proc R Soc B 283:20161392CrossRefGoogle Scholar
  18. Lauder GV, Norton SF (1980) Asymmetrical muscle activity during feeding in the gar, Lepisosteus oculatus. J Exp Biol 84:17–32Google Scholar
  19. Laurence-Chasen JD, Ramsay JB, Brainerd EL (2019) Shearing overbite and asymmetrical jaw motions facilitate food breakdown in a freshwater stingray, Potamotrygon motoro J Exp Biol 222:1–11.Google Scholar
  20. Lieberman DE, Crompton AW (2000) Why fuse the mandibular symphysis? A comparative analysis. Am J Phys Anthropol 112:517–540CrossRefGoogle Scholar
  21. Liem KF (1978) Modulatory multiplicity in the functional repertoire of the feeding mechanism in cichlid fishes. J Morphol 158:323–360CrossRefGoogle Scholar
  22. Liem KF (1979) Modulatory multiplicity in the feeding mechanism in cichlid fishes, as exemplified by the invetebrate pickers of Lake Tanganyika. J Zool (Lond) 189:93–125CrossRefGoogle Scholar
  23. Liem KF (1980) Adaptive significance of intra- and inter-specific differences in the feeding repertoires of cichlid fishes. Am Zool 20:295–314CrossRefGoogle Scholar
  24. Mara KR, Motta PJ, Huber DR (2010) Bite force and performance in the durophagous bonnethead shark, Sphyrna tiburo. J Exp Biol 313A:95–105Google Scholar
  25. Spieler RE, Fahy DP, Sherman RL, Sulikowski J, Quinn TP (2013) The yellow stingray, Urobatis jamaicensis (Chondrichthyes Urotrygonidae): a synoptic review. Caribb J Sci 1:67–97CrossRefGoogle Scholar
  26. Summers AP (2000) Stiffening of the stingray skeleton- an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). J Morph 243:113–126CrossRefGoogle Scholar
  27. Wainwright PC, Mehta RS, Higham TE (2007) Stereotypy, flexibility and coordination: key concepts in behavioral functional morphology. J Exp Biol 211:3523–3528CrossRefGoogle Scholar
  28. Wilga CW (2002) A functional analysis of jaw suspension in elasmobranchs. Biol J Linn Soc 75:483–502CrossRefGoogle Scholar
  29. Wilga CW, Motta PJ (1998) Feeding mechanism of the Atlantic guitarfish Rhinobatos lentiginosus: modulation of kinematic and motor activity. J Exp Biol 201:3167–3184Google Scholar
  30. Wilga CW, Motta PJ (2000) Durophagy in sharks: feeding mechanics of the hammerhead Sphyrna tiburo. J Exp Biol 203:2781–2796Google Scholar
  31. Williams SH, Vinyard CJ, Wall CE, Hylander WL (2007) Masticatory motor patterns in ungulates: a quantitative assessment of jaw-muscle coordination in goats, alpacas and horses. J Exp Zool 307A 307A:226–240CrossRefGoogle Scholar
  32. Yokota L, Goitein R, Gianeti MD, Lessa RTP (2013) Diet and feeding strategy of smooth butterfly ray Gymnura micrura in northeastern Brazil. J App Ichthy 29:1325–1329CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Biology DepartmentFairfield UniversityFairfieldUSA
  2. 2.Novartis Institutes for Biomedical Research (NIBR)CambridgeUSA
  3. 3.Quinnipiac UniversityHamdenUSA
  4. 4.The University of Texas at Austin Marine Science InstitutePort AransasUSA
  5. 5.New York Institute of Technology College of Osteopathic MedicineOld WestburyUSA
  6. 6.University of Saint JosephWest HartfordUSA

Personalised recommendations