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Locomotor Biomechanics and Behaviour in the Ocellate River Stingray

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Locomotor Biomechanics and Behaviour in the Ocellate River Stingray University of Calgary PRISM: University of Calgary's Digital Repository Graduate Studies The Vault: Electronic Theses and Dissertations 2020-04-22 Locomotor biomechanics and behaviour in the ocellate river stingray Seamone, Scott G. Seamone, S. G. (2020). Locomotor biomechanics and behaviour in the ocellate river stingray (Unpublished doctoral thesis). University of Calgary, Calgary, AB. http://hdl.handle.net/1880/111920 doctoral thesis University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca UNIVERSITY OF CALGARY Locomotor biomechanics and behaviour in the ocellate river stingray by Scott G. Seamone A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY GRADUATE PROGRAM IN BIOLOGICAL SCIENCES CALGARY, ALBERTA APRIL, 2020 © Scott G. Seamone 2020 Abstract Stingrays are fishes that are dorsoventrally flattened in the same plane as the substrate, similar to a hydrofoil, with long thin tails that have an absent or reduced caudal fin, and anterior to the pelvic girdle the longitudinal body axis is relatively rigid. These characteristics would appear to constrain or preclude many of the locomotor behaviours that are employed by fishes that typically swim via undulations of the longitudinal body axis and caudal fin, and which tend to dominate descriptions of fish swimming in the literature. In contrast, stingrays exhibit a variety of locomotor behaviours powered via enlarged and flexible pectoral fins that wrap around the body and head (i.e. the pectoral disc), yet an in depth understanding of the biomechanical mechanisms that permit these behaviours has not been formed. Potamotrygon motoro, the ocellate river stingray, lives along the substrate in a benthic environment, and possesses an extremely rounded pectoral disc, from the dorsal view. It is used in these studies to represent the flattened shaped, low profile, and relatively rounded disc common to benthic stingrays, to better understand how these animals achieve different locomotor behaviours. The studies described in this thesis offer insight into how the shape of P. motoro is employed to accomplish behaviours exhibited by many benthic stingrays such as fast- start maneuverability, station holding and burying. Chapter 1 reviews our current and somewhat limited understanding of how shape impacts swimming behaviour in fishes that are flattened in the same plane as the substrate, described here as foil fishes, and explores relationships of shape and ecology observed in stingrays. Chapter 2 describes studies where video analysis was used to reveal that flexibility in the movements of the pectoral fins around the flattened and nearly symmetrical disc shape permits fast-start escape in all directions across the benthic plane with similar performance, regardless of initial orientation of the fish, which appears to challenge the conventional description of maneuverability typically used to evaluate fishes. Chapter 3 describes studies where recordings of changes of pressure beneath the pectoral disc, and video observations of movements of dye, are used to argue that stingrays can exercise movements of the body and fins to flush water from beneath the ventral surface to create and maintain a seal between the pectoral disc and benthos, to achieve suction pressures via a vacuum ii and possibly Stefan adhesion, that can resist an upwards displacing force to hold station along the benthos. Chapter 4 describes studies that used video analysis and particle image velocimetry to explain how rapid and vigorous movements of the body and fins in stingrays fluidize and suspend vortices of sediment below the ventral surface of the fins, which are then directed up and over onto the dorsal surface to cover the fish with sediment and effect burying, and that the fish appear to direct and control these vortices to modulate the extent and pattern of burying. Chapter 5 describes studies that used time-lapse photography and video analysis to reveal that in the presence of sediments that differ in grain size, stingrays mostly choose to inhabit and bury in finer grained sediments when threatened, and this appears to reflect these fishes being more effective at burying in finer sediments, such that the rate of coverage of the dorsal surface is faster for a given finbeat speed. Chapter 6 provides a summary of what has been revealed by these studies, conclusions and future directions. These studies advance our understanding of how a flattened and rounded disc shape in P. motoro might find success in a benthic environment, and might inspire engineers interested in fish for the design of underwater robotics. Keywords: biomechanics, video, locomotion, behaviour, stingray, particle image velocimetry iii Acknowledgements This research was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to DAS, and an NSERC Alexander Graham Bell and University of Calgary Killam Scholarship to SGS. Thank you to the support of my supervisor DAS, my committee members JEAB and JRP, the staff at UofC, my lab mates JR, TM and NT, and my family and friends APR, BJS, CAS, CBS, CDS, CKM, CMLU(TB), JDW, JNH, MSDS, MTA, MES, MS, NPFD, RWH, SAS and WRN. iv Table of contents Title page…………………………………………………………………………………………i Abstract……….…………………………….…………………………….……………………...ii Acknowledgements…………………………….………………………….…………………...iv List of figures and tables…….....……………….…………………………………………….vii Chapter 1: Swimming behaviours in stingrays and other foil-shaped fishes……………..1 - Abstract…………………………………………………………………………..1 - Introduction………………………………………………………………………2 - Shape and swimming in fish………………..………………………………….3 - Foil-shaped fishes ..…….……………………………………..………………..6 - The pectoral disc of stingrays ………………………………..………………17 - Thesis chapters………………………………...……….……..………………22 Chapter 2: Disc starts: the pectoral disc of the ocellate river stingray (Potamotrygon motoro) promotes omnidirectional fast starts across the substrate..…..……...…………25 - Abstract…………………………………………………………………………25 - Introduction …………………………………………………………………… 26 - Materials and methods…….………………………………………………….29 - Results………………………………………………………………………….36 - Discussion……………………………………………………………………...45 Chapter 3: The ocellate river stingray (Potamotrygon motoro) can generate suction to station hold along the substrate……………………………………………………………...56 - Abstract…………………………………………………………………………56 - Introduction……………………………………………………………………..57 - Materials and methods………………………………………………………..60 - Results………………………………………………………………………….64 - Discussion……………………………………………………………………...72 Chapter 4: The ocellate river stingray (Potamotrygon motoro) exploits vortices of sediment to bury into the substrate………………………………………………………….77 - Abstract…………………………………………………………………………77 v - Introduction……………………………………………………………………..78 - Materials and methods………………………………………………………..83 - Results………………………………………………………………………….89 - Discussion…………………………………………………………………….105 Chapter 5: Sediment selection by the ocellate river stingray (Potamotrygon motoro) is associated with constraints in burying……………………………………………………..114 - Abstract………………………………………………………………………..114 - Introduction……………………………………………………………………115 - Methods……………………………………………………………………….118 - Results………………………………………………………………………...124 - Discussion…………………………………………………………………….134 Chapter 6: A rounded disc-shaped foil can be an effective shape for a benthic environment…………………………………………………………………………………..139 - Summary……………….……………...…………………………..………….139 - Conclusions and future directions……………………………………..…...146 References……………………………………………………………………………………150 vi List of figures and tables Chapter 1: Swimming behaviours in stingrays and other foil-shaped fishes - Fig. 1. The ocellate river stingray (Potamotrygon motoro)………………..24 Chapter 2: Disc starts: the pectoral disc of the ocellate river stingray (Potamotrygon motoro) promotes omnidirectional fast starts across the substrate - Fig. 1. Disc starts: forwards, sideways and backwards escape…………..37 - Fig. 2. Body is not restricted to following the orientation of the head..…..39 - Fig. 3. Impacts of prod speed on translational performance…..……..…...42 - Fig. 4. Impacts of prod speed on yaw-rotational performance…………....46 Chapter 3: The ocellate river stingray (Potamotrygon motoro) can generate suction to station hold along the substrate - Fig. 1. Impacts of lifting force and duration of suction event on suction pressure……………..……………………………………..65 - Fig. 2. Relationships of body thrust and finbeat motions……………….....66 - Fig. 3. Impacts of finbeat and body thrust number and frequency on suction pressure………………………………….…………..…... 67 - Fig. 4. Impacts of body thrust velocity and acceleration on suction pressure…………………………………………………....68 - Fig. 5. Lateral view of fins flushing dye from beneath the pectoral disc....70 - Fig. 6. Dorsal view of fins and branchial jets flushing dye from beneath the pectoral disc…………….……………..…..………71 Chapter 4: The ocellate river stingray (Potamotrygon motoro) exploits vortices of sediment to bury into the substrate - Fig. 1. Particle image velocimetry and anterior view of a burying event…90 - Fig. 2. Particle image velocimetry and dorsal view of a burying event…. 92 - Fig. 3. Sediment coverage
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