Volitional Swimming Kinematics of Blacktip Sharks, Carcharhinus limbatus, in the Wild
Abstract
:1. Introduction
2. Materials and Methods
2.1. Video Collection
2.2. Kinematic Analysis
2.3. Statistical Analyses
3. Results
3.1. Whole Body Kinematics
3.2. Body Curvature
3.3. Body Region
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Long, J.; John, H.; Porter, M.E.; Root, R.G.; Liew, C.W. Go Reconfigure: How Fish Change Shape as They Swim and Evolve. Integr. Comp. Biol. 2010, 50, 1120–1139. [Google Scholar] [CrossRef][Green Version]
- Long, J.H. Morphology, mechanics, and locomotion: The relation between the notochord and swimming motions in sturgeon. Environ. Biol. Fishes 1995, 44, 199–211. [Google Scholar] [CrossRef]
- Root, R.G.; Courtland, H.-W.; Pell, C.A.; Hobson, B.; Twohig, E.J.; Suter, R.B.; Iii, W.R.S.; Boetticher, N.C.; Long, J.H. Swimming fish and fish-like models: The harmonic structure of undulatory waves suggests that fish actively tune their bodies. In Proceedings of the 11th International Symposium on Unmanned Untethered Submersible Technology (UUST), Autonomous Undersea Systems Institute, Lee, NH, USA, 23–25 August 1999; Volume 11, pp. 378–388. [Google Scholar]
- Long, J.H.; Adcock, B.; Root, R.G. Force transmission via axial tendons in undulating fish: A dynamic analysis. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2002, 133, 911–929. [Google Scholar] [CrossRef]
- Porter, M.E.; Roque, C.M.; Long, J.H., Jr. Turning maneuvers in sharks: Predicting body curvature from axial morphology. J. Morphol. 2009, 270, 954–965. [Google Scholar] [CrossRef]
- Kajiura, S.M.; Holland, K.N. Electroreception in juvenile scalloped hammerhead and sandbar sharks. J. Exp. Biol. 2002, 205, 3609. [Google Scholar] [CrossRef][Green Version]
- Kajiura, S.M.; Forni, J.B.; Summers, A.P. Maneuvering in juvenile carcharhinid and sphyrnid sharks: The role of the hammerhead shark cephalofoil. Zoology 2003, 106, 19–28. [Google Scholar] [CrossRef][Green Version]
- Kajiura, S.M. Electroreception in neonatal bonnethead sharks, Sphyrna tiburo. Mar. Biol. 2003, 143, 603–611. [Google Scholar] [CrossRef]
- Hoffmann, S.L.; Warren, S.M.; Porter, M.E. Regional variation in undulatory kinematics of two hammerhead species: The bonnethead (Sphyrna tiburo) and the scalloped hammerhead (Sphyrna lewini). J. Exp. Biol. 2017, 220, 3336–3343. [Google Scholar] [CrossRef][Green Version]
- Lowe, C. Kinematics and critical swimming speed of juvenile scalloped hammerhead sharks. J. Exp. Biol. 1996, 199, 2605–2610. [Google Scholar]
- Watts, A.C.; Perry, J.H.; Smith, S.E.; Burgess, M.A.; Wilkinson, B.E.; Szantoi, Z.; Ifju, P.G.; Percival, H.F. Small unmanned aircraft systems for low-altitude aerial surveys. J. Wildl. Manag. 2010, 74, 1614–1619. [Google Scholar] [CrossRef]
- Bouché, P.; Lejeune, P.; Vermeulen, C. How to count elephants in West African savannahs? Synthesis and comparison of main gamecount methods. Biotechnol. Agron. Soc. Environ. 2012, 16, 77–91. [Google Scholar]
- Dunham, K.M. Trends in populations of elephant and other large herbivores in Gonarezhou National Park, Zimbabwe, as revealed by sample aerial surveys. Afr. J. Ecol. 2012, 50, 476–488. [Google Scholar] [CrossRef]
- Watts, A.; Ambrosia, V.; Hinkley, E. Unmanned aircraft systems in remote sensing and scientific research: Classification and considerations of use. Remote Sens. 2012, 4, 1671–1692. [Google Scholar] [CrossRef][Green Version]
- Erbe, C.; Parsons, M.; Duncan, A.; Osterrieder, S.K.; Allen, K. Aerial and underwater sound of unmanned aerial vehicles (UAV). J. Unmanned Veh. Syst. 2017, 5, 92–101. [Google Scholar] [CrossRef]
- Christiansen, F.; Rojano-Doñate, L.; Madsen, P.T.; Bejder, L. Noise levels of multi-rotor unmanned aerial vehicles with implications for potential underwater impacts on marine mammals. Front. Mar. Sci. 2016, 3, 277. [Google Scholar] [CrossRef][Green Version]
- Kiszka, J.J.; Heithaus, M.R. Using Aerial Surveys to Investigate the Distribution, Abundance, and Behavior of Sharks and Rays. In Shark Research: Emerging Technologies and Applications for the Field and Laboratory; Carrier, J.C., Heithaus, M.R., Simpfendorfer, C.A., Eds.; CRC Press: Boca Raton, FL, USA, 2018; pp. 71–83. [Google Scholar] [CrossRef]
- Lowe, C.G.; White, C.F.; Clark, C.M. Use of Autonomous Vehicles for Tracking and Surveying of Acoustically Tagged Elasmobranchs. In Shark Research: Emerging Technologies and Applications for the Field and Laboratory; Carrier, J.C., Heithaus, M.R., Simpfendorfer, C.A., Eds.; CRC Press: Boca Raton, FL, USA, 2018; pp. 93–111. [Google Scholar] [CrossRef]
- Koski, W.R.; Allen, T.; Ireland, D.; Buck, G.; Smith, P.R.; Macrander, A.M.; Halick, M.A.; Rushing, C.; Sliwa, D.J.; McDonald, T.L. Evaluation of an unmanned airborne system for monitoring marine mammals. Aquat. Mamm. 2009, 35, 347. [Google Scholar] [CrossRef]
- Gough, W.T.; Segre, P.S.; Bierlich, K.; Cade, D.E.; Potvin, J.; Fish, F.E.; Dale, J.; di Clemente, J.; Friedlaender, A.S.; Johnston, D.W.; et al. Scaling of swimming performance in baleen whales. J. Exp. Biol. 2019, 222. [Google Scholar] [CrossRef]
- Gray, P.C.; Fleishman, A.B.; Klein, D.J.; McKown, M.W.; Bézy, V.S.; Lohmann, K.J.; Johnston, D.W. A convolutional neural network for detecting sea turtles in drone imagery. Methods Ecol. Evol. 2019, 10, 345–355. [Google Scholar] [CrossRef]
- Arranz, P.; Benoit-Bird, K.J.; Friedlaender, A.S.; Hazen, E.L.; Goldbogen, J.A.; Stimpert, A.K.; DeRuiter, S.L.; Calambokidis, J.; Southall, B.L.; Fahlman, A.; et al. Diving Behavior and Fine-Scale Kinematics of Free-Ranging Risso’s Dolphins Foraging in Shallow and Deep-Water Habitats. Front. Ecol. Evol. 2019, 7, 53. [Google Scholar] [CrossRef][Green Version]
- Durban, J.W.; Fearnbach, H.; Barrett-Lennard, L.; Perryman, W.; Leroi, D. Photogrammetry of killer whales using a small hexacopter launched at sea. J. Unmanned Veh. Syst. 2015, 3, 131–135. [Google Scholar] [CrossRef]
- Raoult, V.; Tosetto, L.; Williamson, J.E. Drone-based high-resolution tracking of aquatic vertebrates. Drones 2018, 2, 37. [Google Scholar] [CrossRef][Green Version]
- Raoult, V.; Williamson, J.E.; Smith, T.M.; Gaston, T.F. Effects of on-deck holding conditions and air exposure on post-release behaviours of sharks revealed by a remote operated vehicle. J. Exp. Mar. Biol. Ecol. 2019, 511, 10–18. [Google Scholar] [CrossRef]
- Raoult, V.; Tosetto, L.; Harvey, C.; Nelson, T.M.; Reed, J.; Parikh, A.; Chan, A.J.; Smith, T.M.; Williamson, J.E. Remotely operated vehicles as alternatives to snorkellers for video-based marine research. J. Exp. Mar. Biol. Ecol. 2020, 522, 151253. [Google Scholar] [CrossRef]
- Bevan, E.; Whiting, S.; Tucker, T.; Guinea, M.; Raith, A.; Douglas, R. Measuring behavioral responses of sea turtles, saltwater crocodiles, and crested terns to drone disturbance to define ethical operating thresholds. PLoS ONE 2018, 13, e0194460. [Google Scholar] [CrossRef] [PubMed]
- Raoult, V.; Colefax, A.P.; Allan, B.M.; Cagnazzi, D.; Castelblanco-Martínez, N.; Ierodiaconou, D.; Johnston, D.W.; Landeo-Yauri, S.; Lyons, M.; Pirotta, V.; et al. Operational Protocols for the Use of Drones in Marine Animal Research. Drones 2020, 4, 64. [Google Scholar] [CrossRef]
- Skomal, G.B.; Hoyos-Padilla, E.M.; Kukulya, A.; Stokey, R. Subsurface observations of white shark Carcharodon carcharias predatory behaviour using an autonomous underwater vehicle. J. Fish Biol. 2015, 87, 1293–1312. [Google Scholar] [CrossRef] [PubMed]
- Clark, C.M.; Forney, C.; Manii, E.; Shinzaki, D.; Gage, C.; Farris, M.; Lowe, C.G.; Moline, M. Tracking and Following a Tagged Leopard Shark with an Autonomous Underwater Vehicle. J. Field Robot. 2013, 30, 309–322. [Google Scholar] [CrossRef]
- Forney, C.; Manii, E.; Farris, M.; Moline, M.A.; Lowe, C.G.; Clark, C.M. Tracking of a tagged leopard shark with an AUV: Sensor calibration and state estimation. In Proceedings of the 2012 IEEE International Conference on Robotics and Automation, Saint Paul, MN, USA, 14–18 May 2012; pp. 5315–5321. [Google Scholar] [CrossRef]
- Nathan, R.; Getz, W.M.; Revilla, E.; Holyoak, M.; Kadmon, R.; Saltz, D.; Smouse, P.E. A movement ecology paradigm for unifying organismal movement research. Proc. Natl. Acad. Sci. USA 2008, 105, 19052–19059. [Google Scholar] [CrossRef][Green Version]
- Doan, M.D.; Kajiura, S.M. Adult blacktip sharks (Carcharhinus limbatus) use shallow water as a refuge from great hammerheads (Sphyrna mokarran). J. Fish Biol. 2020, 96, 1530–1533. [Google Scholar] [CrossRef]
- Colefax, A.P.; Kelaher, B.P.; Pagendam, D.E.; Butcher, P.A. Assessing White Shark (Carcharodon carcharias) Behavior Along Coastal Beaches for Conservation-Focused Shark Mitigation. Front. Mar. Sci. 2020, 7, 268. [Google Scholar] [CrossRef]
- Kiszka, J.J.; Mourier, J.; Gastrich, K.; Heithaus, M.R. Using unmanned aerial vehicles (UAVs) to investigate shark and ray densities in a shallow coral lagoon. Mar. Ecol. Prog. Ser. 2016, 560, 237–242. [Google Scholar] [CrossRef]
- Gore, M.; Abels, L.; Wasik, S.; Saddler, L.; Ormond, R. Are close-following and breaching behaviours by basking sharks at aggregation sites related to courtship? J. Mar. Biol. Assoc. UK 2019, 99, 681–693. [Google Scholar] [CrossRef][Green Version]
- Rieucau, G.; Kiszka, J.J.; Castillo, J.C.; Mourier, J.; Boswell, K.M.; Heithaus, M.R. Using unmanned aerial vehicle (UAV) surveys and image analysis in the study of large surface-associated marine species: A case study on reef sharks Carcharhinus melanopterus shoaling behaviour. J. Fish Biol. 2018, 93, 119–127. [Google Scholar] [CrossRef]
- Whitney, N.M.; Lear, O.; Gleiss, A.C.; Payne, N.; White, C.F. Advances in the Application of High-Resolution Biologgers to Elasmo-Branch Fishes. In Shark Research: Emerging Technologies and Applications for the Field and Laboratory; Carrier, J.C., Heithaus, M.R., Simpfendorfer, C.A., Eds.; CRC Press: Boca Raton, FL, USA, 2018; pp. 45–70. [Google Scholar] [CrossRef]
- Papastamatiou, Y.P.; Meyer, C.G.; Watanabe, Y.Y.; Heithaus, M.R. Animal-Borne Video Cameras and Their Use to Study Shark Ecology and Conservation. In Shark Research: Emerging Technologies and Applications for the Field and Laboratory; Carrier, J.C., Heithaus, M.R., Simpfendorfer, C.A., Eds.; CRC Press: Boca Raton, FL, USA, 2018; pp. 83–92. [Google Scholar] [CrossRef]
- Kajiura, S.M.; Tellman, S.L. Quantification of Massive Seasonal Aggregations of Blacktip Sharks (Carcharhinus limbatus) in Southeast Florida. PLoS ONE 2016, 11, 911. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Joyce, K.; Duce, S.; Leahy, S.; Leon, J.; Maier, S. Principles and practice of acquiring drone-based image data in marine environments. Mar. Freshw. Res. 2018, 70. [Google Scholar] [CrossRef]
- Rohr, J.J.; Fish, F.E. Strouhal numbers and optimization of swimming by odontocete cetaceans. J. Exp. Biol. 2004, 207, 1633–1642. [Google Scholar] [CrossRef] [PubMed][Green Version]
- McComb, D.M.; Tricas, T.C.; Kajiura, S.M. Enhanced visual fields in hammerhead sharks. J. Exp. Biol. 2009, 212, 4010–4018. [Google Scholar] [CrossRef][Green Version]
- Lowe, C.G.; Holland, K.N.; Wolcott, T.G. A new acoustic tailbeat transmitter for fishes. Fish. Res. 1998, 36, 275–283. [Google Scholar] [CrossRef]
- Brown, D.D.; Kays, R.; Wikelski, M.; Wilson, R.; Klimley, A.P. Observing the unwatchable through acceleration logging of animal behavior. Anim. Biotelemetry 2013, 1, 1–16. [Google Scholar] [CrossRef][Green Version]
- Saadat, M.; Fish, F.E.; Domel, A.G.; Di Santo, V.; Lauder, G.V.; Haj-Hariri, H. On the rules for aquatic locomotion. Phys. Rev. Fluids 2017, 2, 083102. [Google Scholar] [CrossRef]
- Taylor, G.K.; Nudds, R.L.; Thomas, A.L.R. Flying and swimming animals cruise at a Strouhal number tuned for high power efficiency. Nature 2003, 425, 707–711. [Google Scholar] [CrossRef] [PubMed]
- Triantafyllou, M.S.; Triantafyllou, G.S.; Gopalkrishnan, R. Wake mechanics for thrust generation in oscillating foils. Phys. Fluids Fluid Dyn. 1991, 3, 2835–2837. [Google Scholar] [CrossRef]
- Triantafyllou, G.S.; Triantafyllou, M.S.; Grosenbaugh, M.A. Optimal Thrust Development in Oscillating Foils with Application to Fish Propulsion. J. Fluids Struct. 1993, 7, 205–224. [Google Scholar] [CrossRef]
- Triantafyllou, M.S.; Triantafyllou, G.S.; Yue, D.K.P. Hydrodynamics of Fishlike Swimming. Annu. Rev. Fluid Mech. 2000, 32, 33–53. [Google Scholar] [CrossRef]
- Eloy, C. Optimal Strouhal number for swimming animals. J. Fluids Struct. 2012, 30, 205–218. [Google Scholar] [CrossRef][Green Version]
- Floryan, D.; Van Buren, T.; Smits, A.J. Efficient cruising for swimming and flying animals is dictated by fluid drag. Proc. Natl. Acad. Sci. USA 2018, 115, 8116. [Google Scholar] [CrossRef][Green Version]
- Fish, F.; Shannahan, L. The role of the pectoral fins in body trim of sharks. J. Fish Biol. 2000, 56, 1062–1073. [Google Scholar] [CrossRef]
- Webb, P.W.; Keyes, R.S. Swimming kinematics of sharks. Fish. Bull. 1982, 80, 803–812. [Google Scholar]
- Fish, F.E.; Kolpas, A.; Crossett, A.; Dudas, M.A.; Moored, K.W.; Bart-Smith, H. Kinematics of swimming of the manta ray: Three-Dimensional analysis of open-water maneuverability. J. Exp. Biol. 2018, 221. [Google Scholar] [CrossRef][Green Version]
- Watanabe, Y.Y.; Lydersen, C.; Fisk, A.T.; Kovacs, K.M. The slowest fish: Swim speed and tail-beat frequency of Greenland sharks. J. Exp. Mar. Biol. Ecol. 2012, 426–427, 5–11. [Google Scholar] [CrossRef][Green Version]
- Lowe, C.G. Bioenergetics of free-ranging juvenile scalloped hammerhead sharks (Sphyrna lewini) in Kāne’ohe Bay, Ō’ahu, HI. J. Exp. Mar. Biol. Ecol. 2002, 278, 141–156. [Google Scholar] [CrossRef]
- Lauder, G.V.; Di Santo, V. 6—Swimming Mechanics and Energetics of Elasmobranch Fishes. In Fish Physiology; Shadwick, R.E., Farrell, A.P., Brauner, C.J., Eds.; Academic Press: New York, NY, USA, 2015; Volume 34A, pp. 219–253. [Google Scholar]
- Hoffmann, S.L.; Buser, T.J.; Porter, M.E. Comparative morphology of shark pectoral fins. J. Morphol. 2020, 281, 1501–1516. [Google Scholar] [CrossRef] [PubMed]
- Crofts, S.B.; Shehata, R.; Flammang, B.E. Flexibility of Heterocercal Tails: What Can the Functional Morphology of Shark Tails Tell Us about Ichthyosaur Swimming? Integr. Org. Biol. 2019, 1, obz002. [Google Scholar] [CrossRef][Green Version]
- Maia, A.; Lauder, G.V.; Wilga, C.D. Hydrodynamic function of dorsal fins in spiny dogfish and bamboo sharks during steady swimming. J. Exp. Biol. 2017, 220, 3967–3975. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Hoffmann, S.L.; Porter, M.E. Body and Pectoral Fin Kinematics During Routine Yaw Turning in Bonnethead Sharks (Sphyrna tiburo). Integr. Org. Biol. 2019, 1, obz014. [Google Scholar] [CrossRef][Green Version]
- Flammang, B.E.; Lauder, G.V.; Troolin, D.R.; Strand, T.E. Volumetric imaging of fish locomotion. Biol. Lett. 2011, 7, 695–698. [Google Scholar] [CrossRef][Green Version]
- Porter, M.E.; Ewoldt, R.H.; Long, J.H. Automatic control: The vertebral column of dogfish sharks behaves as a continuously variable transmission with smoothly shifting functions. J. Exp. Biol. 2016, 219, 2908–2919. [Google Scholar] [CrossRef][Green Version]
- Porter, M.E.; Roque, C.M.; Long, J.H., Jr. Swimming fundamentals: Turning performance of leopard sharks (Triakis semifasciata) is predicted by body shape and postural reconfiguration. Zoology 2011, 114, 348–359. [Google Scholar] [CrossRef]
- Long, J.H.; Nipper, K.S. The Importance of Body Stiffness in Undulatory Propulsion. Integr. Comp. Biol. 1996, 36, 678–694. [Google Scholar] [CrossRef]
- Hays, G.C.; Ferreira, L.C.; Sequeira, A.M.M.; Meekan, M.G.; Duarte, C.M.; Bailey, H.; Bailleul, F.; Bowen, W.D.; Caley, M.J.; Costa, D.P.; et al. Key questions in marine megafauna movement ecology. Trends Ecol. Evol. 2016, 31, 463–475. [Google Scholar] [CrossRef][Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Porter, M.E.; Ruddy, B.T.; Kajiura, S.M. Volitional Swimming Kinematics of Blacktip Sharks, Carcharhinus limbatus, in the Wild. Drones 2020, 4, 78. https://doi.org/10.3390/drones4040078
Porter ME, Ruddy BT, Kajiura SM. Volitional Swimming Kinematics of Blacktip Sharks, Carcharhinus limbatus, in the Wild. Drones. 2020; 4(4):78. https://doi.org/10.3390/drones4040078
Chicago/Turabian StylePorter, Marianne E., Braden T. Ruddy, and Stephen M. Kajiura. 2020. "Volitional Swimming Kinematics of Blacktip Sharks, Carcharhinus limbatus, in the Wild" Drones 4, no. 4: 78. https://doi.org/10.3390/drones4040078