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Consequences of Abiotic and Biotic Factors on Limbless Locomotion

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Consequences of Abiotic and Biotic Factors on Limbless Locomotion MIAMI UNIVERSITY The Graduate School Certificate for Approving the Dissertation We hereby approve the Dissertation of Gary W. Gerald, II Candidate for the Degree: Doctor of Philosophy ___________________________________________ Director (Dennis L. Claussen) ___________________________________________ Reader (Alan B. Cady) ___________________________________________ Reader (Phyllis Callahan) ___________________________________________ (Nancy G. Solomon) ___________________________________________ Graduate School Representative (Robert L. Schaefer) ABSTRACT CONSEQUENCES OF ABIOTIC AND BIOTIC FACTORS ON LIMBLESS LOCOMOTION Gary W. Gerald II Snakes have the ability to move in a variety of ways depending on the habitat in which they are moving. All of these modes require some sort of lateral bending of the elongate body to generate the required force necessary for propulsion. However, the biomechanical mechanisms of each mode of limbless movement differ substantially among each other. Despite the potential importance of using multiple modes of movement in different ecological situations, we know very little about the influence of abiotic and biotic factors on multiple locomotor modes in these animals. The goal of this dissertation was to examine how temperature, habitat usage, and morphology affect four of the most common modes of limbless locomotion (lateral undulation, concertina, swimming, and arboreal) and shed light on the question of what ecological conditions most likely contributed to limb reduction in the early snake ancestor. The first chapter assessed the influence of temperature on different modes of locomotion. Decreasing temperature limits performance of each mode differently because of differences in the underlying physiological mechanisms governing each mode. The second chapter closely examined the combined effects of temperature and perch diameter on the speed and balance of limbless arboreal locomotion. Movement on perches was greatly limited by temperature, but not by decreasing perch diameter suggesting that snakes have a size-relative advantage compared to lizards when moving on narrow perches. The final chapter deals with assessing the relationships among microhabitat use, morphology, and locomotor performance of various modes. I found that species tend to perform better during modes they use most often in nature and perform more poorly during rarely-used modes suggesting that snakes do possess adaptations to enhance movement in preferred habitats. Moreover, morphological variables (mass, length, shape) significantly influenced each locomotor mode in somewhat similar ways. As a result, performance across various modes was either positively or not related to each other in most instances. My results suggest that morphological and physiological adaptations that promote movement via different modes do not conflict suggesting that a limbless body is beneficial in a number of different ecological situations. CONSEQUENCES OF ABIOTIC AND BIOTIC FACTORS ON LIMBLESS LOCOMOTION A DISSERTATION Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Zoology by Gary W. Gerald, II Miami University Oxford, Ohio 2008 Dissertation Director: Dennis L. Claussen TABLE OF CONTENTS General Introduction ……………………………………………………………. 1 Temperature effects on locomotion ……………………………………...…… 2 Limbless locomotion ……………………………………………………….. 3 Arboreal locomotion ………………………….....………………………….. 4 Specializations and trade-offs ….………………………………………...….. 5 Direction of dissertation ……………………………………………………. 6 Literature Cited ……….…………………….…….……….………....……. 7 Chapter 1: Thermal dependencies of different modes of locomotion in neonate Brown snakes, Storeria dekayi …………………………………………….………. 12 Introduction ………………………...…………………………………….. 13 Materials and Methods …………………………………………….………. 14 Results …................................................................................................... 16 Discussion ……………………………………………………………….. 17 Literature Cited …………………………….…………………………….. 21 Chapter 2: Effects of temperature and perch diameter on arboreal locomotion in the snake Elaphe guttata ……………………………………………………….…… 33 Introduction ………………………………………………………………. 34 Materials and Methods …………………………………………………….. 36 Results …………………………………………………………………... 39 Discussion ……………………………………………………………….. 40 Literature Cited …………………………………………………………... 46 Chapter 3: Relationships between morphology, microhabitat use, and limbless locomotion ……………………………………………………………… 55 Introduction ……………………………………………………………… 56 Materials and Methods ……………………………………………………. 58 ii Results …………………………………………………………………... 65 Discussion ……………………………………………………………….. 69 Literature Cited …………………………………………………………... 79 General Conclusions ………………………………………………………….…. 109 Conclusion ………………………………………………………………. 113 Literature Cited …………………………………………………………... 114 iii LIST OF TABLES Chapter 1 Table 1. Pearson correlation coefficients for absolute velocities of 26 neonate brown snakes (Storeria dekayi) among locomotor modes and temperature. Pairwise α = 0.05. * p < 0.05. b Table 2. Allometric relationships (y = ax ) between log transformed SVL and log transformed mean and maximum absolute (m • s-1) velocities for 26 neonate brown snakes (Storeria dekayi) during 3 modes of locomotion at 10, 20, and 30 C determined by power functions. Numbers in parenthesis represent standard errors of the parameter estimates for the intercepts (a) and slopes (b). No significant (p < 0.0167) relationships were detected for any mode at any temperature. Table 3. Q10 values for maximum absolute velocities attained by various species of snake during swimming (s) and undulatory crawling (c). 1 = Stevenson et al. (1985), 2 = Heckrotte (1967), 3 = Finkler (1995), 4 = Finkler and Claussen (1999), 5 = present study. Table 4. A summary of body length-relative velocities of concertina locomotion by limbless squamates reported from this and previous studies. TL = total length, SVL = snout-vent length, WT = wide tunnel(s). Chapter 2 Table 1. Parameters of least-squares regression models showing the relationship between number of body loops formed during movement/total body length (predictor) and mean head-tail distances/total body length (response) at three temperatures (10, 20, and 30 C) at three different perch diameters (3, 6, and 10 cm). Chapter 3 Table 1. The reported habits and morphological data for the five snake species used in this study. Numbers represent means with the standard deviation in parentheses. SVL = snout-vent length, Body condition = total length (cm)/mass (g). iv Table 2. Statistically significant differences in terrestrial, aquatic, and arboreal microhabitat use between five species of snake (n = 12/species). The order of use is listed from left to right with the species on the left using that particular microhabitat the most and the one on the right using it the least. Superscript letters denote statistical differences. Ea = Elaphe alleghaniensis, Eg = Elaphe guttata, Ns = Nerodia sipedon, Pc = Pituophis catenifer, Ts = Thamnophis sauritus. Table 3. Linear regression parameters for the relationships (y = α + βx) between uncorrected morphology and stamina of three different modes of limbless locomotion in 5 species of snake (n = 12/species). SVL = snout-vent length, Body condition = total length (cm)/mass (g). Table 4. Statistically significant differences in maximal snout-vent length (SVL)-relative speeds and stamina of multiple modes of limbless locomotion between five species of snake (n = 12/species). The order of use is listed from left to right with the species on the left displaying superior performance and the one on the right displaying poorer performance abilities. Superscript letters denote statistical differences. Ea = Elaphe alleghaniensis, Eg = Elaphe guttata, Ns = Nerodia sipedon, Pc = Pituophis catenifer, Ts = Thamnophis sauritus. Table 5. Linear regression parameters for the relationships (y = α + βx) between uncorrected data on performance during each of four locomotor modes and amount of time spent in each microhabitat type by 5 snake species (n = 12/species). Table 6. Pearson product-moment correlation coefficients between locomotor performance measures (maximal snout-vent length-relative velocity and stamina) of four modes of limbless locomotion in 5 snake species (n = 12/species). Arb = arboreal, LU = terrestrial lateral undulation, Conc = concertina, Swim = swimming. * = statistical significance at the 0.05 level. v LIST OF FIGURES Chapter 1 Figure 1. The influence of temperature on absolute mean (A) and maximum (B) velocities and snout-vent length (SVL) relative mean (C) and maximum (D) velocities attained during terrestrial lateral undulation, terrestrial concertina, and swimming by 26 neonate Brown Snakes (Storeria dekayi). Error bars represent ± SE. Figure 2. The influence of temperature on maximum snout-vent length (SVL) relative crawling speeds of 26 neonate Storeria dekayi (present study), 10 adult Nerodia sipedon (Finkler and Claussen 1999), 10 adult Regina septemvittata (Finkler and Claussen 1999), and 206 adult Natrix maura (Hailey and Davies 1986). Figure 3. The influence of temperature on maximum snout-vent length (SVL) relative swimming speeds in snakes, 26 neonate Storeria dekayi (present study), 10 adult Nerodia sipedon and 10 adult Regina septemvittata (Finkler and Claussen 1999). Figure 4. The relationship between body width relative to tunnel width and maximum snout-vent length relative speeds of concertina locomotion in
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