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Amphibious Fishes: Terrestrial Locomotion, Performance, Orientation, and Behaviors from an Applied Perspective by Noah R

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Amphibious Fishes: Terrestrial Locomotion, Performance, Orientation, and Behaviors from an Applied Perspective by Noah R AMPHIBIOUS FISHES: TERRESTRIAL LOCOMOTION, PERFORMANCE, ORIENTATION, AND BEHAVIORS FROM AN APPLIED PERSPECTIVE BY NOAH R. BRESSMAN A Dissertation Submitted to the Graduate Faculty of WAKE FOREST UNIVESITY GRADUATE SCHOOL OF ARTS AND SCIENCES in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Biology May 2020 Winston-Salem, North Carolina Approved By: Miriam A. Ashley-Ross, Ph.D., Advisor Alice C. Gibb, Ph.D., Chair T. Michael Anderson, Ph.D. Bill Conner, Ph.D. Glen Mars, Ph.D. ACKNOWLEDGEMENTS I would like to thank my adviser Dr. Miriam Ashley-Ross for mentoring me and providing all of her support throughout my doctoral program. I would also like to thank the rest of my committee – Drs. T. Michael Anderson, Glen Marrs, Alice Gibb, and Bill Conner – for teaching me new skills and supporting me along the way. My dissertation research would not have been possible without the help of my collaborators, Drs. Jeff Hill, Joe Love, and Ben Perlman. Additionally, I am very appreciative of the many undergraduate and high school students who helped me collect and analyze data – Mark Simms, Tyler King, Caroline Horne, John Crumpler, John S. Gallen, Emily Lovern, Samir Lalani, Rob Sheppard, Cal Morrison, Imoh Udoh, Harrison McCamy, Laura Miron, and Amaya Pitts. I would like to thank my fellow graduate student labmates – Francesca Giammona, Dan O’Donnell, MC Regan, and Christine Vega – for their support and helping me flesh out ideas. I am appreciative of Dr. Ryan Earley, Dr. Bruce Turner, Allison Durland Donahou, Mary Groves, Tim Groves, Maryland Department of Natural Resources, UF Tropical Aquaculture Lab for providing fish, animal care, and lab space throughout my doctoral research. I would also like to thank Drs. John Caprio, C. Jake Saunders, Wayne Silver, and Sam Van Wassenbergh for providing their sensory biology insight. I appreciate everyone from the variety of Facebook groups that responded to my walking catfish surveys. I thank the National Science Foundation Graduate Research Fellowship (NSF GRFP), a crowd-sourcing campaign through the Animal Superpowers project at Experiment.com, the Wake Forest University Department of Biology, the Vecellio Fund, and Friday Harbor Laboratories 3D Morphometrics and Image Analysis Workshop for providing funding. I would also like to thank all of my friends and family for their support and encouragement throughout my doctoral program, as they were my support system keeping me going. I especially ii thank my girlfriend, Alicia Miller, who was so supportive that she even built some of my experimental set-ups while I was recovering from serious shoulder surgery. Lastly, I thank fish for being so awesome and such fascinating organisms to study! iii TABLE OF CONTENTS List of Illustrations and Tables v List of Abbreviations vii Abstract x Introduction xii Chapter 1: Where do fish go when stranded on land? Terrestrial orientation of the mangrove rivulus Kryptolebias marmoratus (Published in the Journal of Fish Biology) 1 Chapter 2: Emersion and terrestrial locomotion of the northern snakehead (Channa argus) on multiple substrates (Published in Integrative Organismal Biology) 28 Chapter 3: Why did the catfish cross the road? Chemoreceptive terrestrial orientation and amphibious natural history of the invasive walking catfish Clarias batrachus (Submitted to the Journal of Experimental Biology) 75 Chapter 4: Reffling: a novel locomotor behavior used by Neotropical armored catfishes (Loricariide) in terrestrial environments 109 Conclusions 154 Additional References 157 Appendix 165 Curriculum Vitae 173 iv LIST OF ILLUSTRATIONS AND TABLES Ch. 1, Table I. Summary of orientation data of Kryptolebias marmoratus. Ch. 1, Figure 1. Polar rose histogram of Kryptolebias marmoratus movement during control treatments. Ch. 1, Figure 2. Polar rose histogram of Kryptolebias marmoratus movement during trial treatments. Ch. 1, Figure 3. Polar rose histogram of Kryptolebias marmoratus movement during orange trial treatment. Ch. 2, Table I. Channa argus emersion treatments, results, and statistics. Ch. 2, Table II. Summary of kinematic and performance data on multiple substrates. Ch. 2, Table III. Summary of statistical tests comparing effects of substrate and size on response variables. Ch. 2, Figure 1. Muscle activity pattern during the terrestrial forward crawl of northern snakeheads. Ch. 2, Figure 2. Northern snakehead forward crawl behavior. Ch. 2, Figure 3. Effects of substrate and length on kinematics and performance. Ch. 2, Figure 4. Juvenile northern snakehead tail-flip jump. Ch. 3, Table I. Results of orientation experiment statistical analyses. Ch. 3, Figure 1. Polar rose histograms of C. batrachus movement directionality during direct contact terrestrial orientation treatments. Ch. 3, Figure 2. Polar rose histograms of C. batrachus movement directionality during distant terrestrial orientation treatments. Ch. 3, Figure 3. Positioning of C. batrachus barbels while at rest on a terrestrial substrate. Ch. 3, Figure 4. Categorical counts of survey results and YouTube video analyses. v Ch. 4, Table I. ANCOVA results. Ch. 4, Figure 1. Representative reffling behavior of a P. multiradiatus. Ch. 4, Figure 2. Representative reffling behavior of a H. punctatus from the FTIRT experiments. Ch. 4, Figure 3. Example head trace of a Hypostomus punctatus during a single terrestrial locomotor sequence. Ch. 4, Figure 4. Body patterns of H. punctatus during two representative reffling strides as determined by the FTIRT experiments. Ch. 4, Figure 5. Boxplots of COM WA by species. Ch. 4, Figure 6. Body length has negligible effects on most kinematics and performance parameters across species. Ch. 4, Figure 7. Distributions of slopes of parameters changing over time that are significantly different between species. Ch. 4, Figure 8. Segmented µCT scans displaying unusual loricariid morphology. Ch. 4, Figure 9. µCT scans displaying loricariid neural and hemal spines. vi LIST OF ABBREVIATIONS A = Armor Ab = Abductor Add = Adductor AITC = Allyl isothiocyanate ANCOVA = Analysis of Covariance ANOVA = Analysis of Variance AP = Anterior Process of the Basipterygium BPT = Basipterygium CC = Curvature Coefficient COM = Center of Mass CT = Computed Tomography dCO2 = Dissolved Carbon Dioxide DenDF = Denominator Degrees of Freedom DI = Deionized (Water) dO2 = Dissolved Oxygen DR = Distance Ration EMG = Electromyography Epax = Epaxial Muscles ETA = Extra Test Area vii FPS = Frames per Second FTIRT = Frustrated Total Internal Reflection Table HP = Hypostomus punctatus HS = Hemal Spine HSD = Honest Signficant Difference Hyp = Hypaxial Muscles IACUC = Institutional Animal Care and Use Committee LA = Left Anterior LP = Left Posterior LPT = Lateropterygium MA = Maxillary Barbel MANCOVA = Multivariate Analysis of Variance MB = Mental Barbel MDDNR = Maryland Department of Natural Resources MS-222 = Tricaine Mesylate/Methanesulfonate N = Number NA = Nasal Barbel NS = Neural Spine NumDF = Numerator Degrees of Freedom PD = Pterygoplicthys disjunctivus viii PF = Pectoral Fin PG = Pterygoplicthys gibbiceps PM = Pterygoplicthys multiradiatus PP = Posterior Process of the Basipterygium PPB = Parts per Billion PPT = Parts per Thousand RA = Right Anterior RO = Reverse Osmosis-filtered RP = Right Posterior SE = Standard Error Seq = Sequence Number SF = Stride Frequency TA = Test Area TL = Total Length UF = University of Florida WA = Wave Amplitude WFU = Wake Forest University ix ABSTRACT A wide diversity of fishes exhibit amphibious behaviors for a variety of reasons. However, it is unknown how most amphibious fishes orient in terrestrial environments. Furthermore, while there has been some research into why fish emerge onto land, motivations for emersion can differ between species and data is deficient for many. Additionally, the terrestrial behaviors of many amphibious fishes have not yet been described. The goals of this dissertation are to determine the senses and cues mangrove rivulus (Kryptolebias marmoratus) and walking catfish (Clarias batrachus) use to orient in terrestrial environments, describe the conditions that encourage emersion in northern snakehead (Channa argus) and walking catfish, and describe the terrestrial locomotor behaviors of northern snakeheads and Neotropical suckermouth catfishes (Loricariidae). Behavioral assays with a variety of visual and chemical stimuli were used to determine the cues these fish use to orient while emerged. Experiments with a variety of environmental conditions and crowd-sourcing surveys on walking catfish observations were used to determine conditions that promote terrestrial emersion. High-speed videos were used to describe terrestrial behaviors. Vision is widely used in amphibious fishes and mangrove rivulus use reflections, colors, and contrast to orient on land, in addition to the otolith-vestibular system. Walking catfish also use chemoreception to orient with respect to chemical signals they are in direct contact with and over a distance. This is the first confirmed case of fish using chemoreception for orientation out of the water, which appears to involve aerial taste using their barbels. Snakeheads emerge under poor aquatic conditions, including low pH, high salinity, and high [dCO2]. Walking catfish emerge under a variety of conditions, but primarily emerge during the rain, particularly out of flooding storm drains. Snakeheads use a form of axial-appendage-based terrestrial locomotion, but perform better on complex substrates. Armored catfishes use an entirely new
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