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At Bimini, Bahamas SPATIAL AND TEMPORAL VARIATION IN DIET AND PREY PREFERENCE OF NURSERY-BOUND JUVENILE LEMON SHARKS (Negapri011 brevirostris) AT BIMINI, BAHAMAS. By STEVEN PAUL NEWMAN A thesis submitted to the University of Plymouth In partial fulfilment for the degree of DOCTOR OF PIDLOSPHY Department of Biological Sciences Faculty of Science In collaboration with Bimini Biological Field Station, Bahamas October 2003 Ill ,. I l!JNIVEF.tSITY ()F ,PLVM0llJliH: UeniNo.. ~j00·58} ~84-4 I pate I 0~5; MAY 2004 I • !Class No. -T+IESIS 9\Rik-~li ,.u; . ' w. I 'coR I. No. I' I Pll'ZMOUi'H LIB!=IAAV: I I Abstract Spatial and temporal variation in the diet and prey preference of juvenile lemon sharks Prey selection has never been determined in an elasmobranch, primarily because of the large home ranges possessed by adults making accurate quantification of prey in the environment problematic. Juvenile lemon sharks spend their first few years of life within protected nursery grounds, enabling the first quantification of prey selection due to the restricted area that they inhabit. Growth and survival of juvenile lemon sharks strongly influences adult fitness and recruitment, and therefore prey selection may play an important role in the life history of lemon sharks. The selection of a preferred species or size of prey by juvenile lemon sharks was determined by comparing the proportions of prey in the diet with proportions of prey in the environment at Bimini, Bahamas, between March 2000 and March 2003. The diet of lemon sharks was quantitatively described from the analysis of 642 shark stomachs (54.7 ± 0.3 cm precaudal length PCL, mean ± S.E., range 43.5 to 90.0 cm), of which 396 (62 %) contained food items. The main prey of juvenile lemon sharks at Bimini were mojarras (69% index of relative importance, IRI), parrotfish (5.5 % IRI), swimming crabs (5.1 %) and barracuda (3.1 % IRI). The yellowfin mojarra Gen·es cinereus was the main prey of lemon sharks regardless of location, season, shark size or sex. Contingency table analysis revealed the diet of juvenile lemon sharks to be specific to location et = 65.54, p < 0.0001), but homogeneous with season eX: = 17.91, p = 0.118), shark size et = 64.36, p = 0.057) and 2 shark sex (X = 13.21, P = 0.354). Prey sizes were measured where possible, or calculated using least squares linear regression equations relating bone or carapace dimensions with original size. Original size was obtained for 350 dietary items, with 85 % calculated using bone regressions. Juvenile lemon sharks demonstrated no significant spatial or temporal variation in the size of prey consumed (Kolmogorov-Smimov and Student's /-tests, P > 0.05), but juveniles over 60.0 cm PCL conswned significantly larger prey than smaller sharks (ANOVA, P < 0.001). Bone-length regressions also enabled a more accurate estimate of meal size (2.17 ± 0.17 % BW, mean± S.E., range 0.0 I to 21.4 % BW, n = 407) and subsequently daily ration, 1.31 - 1.80% BW (depending on shark size), in comparison to traditional back­ calculation techniques. Forty-three blocknets, 540 seine nets and 498 trawls were closed to sample mangrove and seagrass communities, resulting in the capture, identification and measurement of 216,150 fish and macro invertebrates. Catches were extrapolated over the entire study area providing an estimate of population sizes. Prey preference was estimated using chi-square residuals and a traditional electivity index. Values and rankings of selection varied with technique, but both revealed similar trends in prey preference. Proportions of prey families and prey sizes in the diet of lemon sharks from Bimini were significantly different to those found in the environment Ci, P < 0.001 and Kolmogorov-Smirnov test, P < 0.001 respectively). Lemon sharks demonstrated a preference for slower moving prey that were easier to capture (e.g. mojarras, toadfish, parrotfish and filefish), while avoiding larger, faster and harder to catch prey. Yellowfin mojarra were consumed in proportion to the distribution of fish lengths in the environment, suggesting that their importance in the diet may be due to preferred sizes in the environment as well as their ease of capture. Lemon shark diet was closely correlated with mangrove communities, demonstrating the importance of mangroves and the need for their protection in the Bahamas. The degree of selection exhibited by juvenile lemon sharks was greatest when prey were more abundant (off South Bimini and in the wet season), suggesting that lemon sharks conform to the optimal foraging theory. iv CONTENTS Page number Copyright statement Dedication ii Title page iii Abstract iv Contents V List of Figures 1 List of Tables 3 Acknowledgements 6 Authors declaration 8 Work in support of this thesis 9 CHAPTER ONE GENERAL INTRODUCTION TO PREY SELECTION IN SHARKS l Introduction 11 1.1 What is prey selection and why is it important? 11 1.2 Prey selection and the Optimal Foraging Theory 12 1.3 How is prey selection quantified? 13 1.4 Introduction to elasmobranchs 14 1.5 Introduction to the lemon shark 14 1.6 Diet of juvenile lemon sharks 15 1.7 Prey selection in sharks 16 1.8 Shark nurseries 16 1.9 Potential of prey selection in juvenile lemon sharks 18 I . I 0 General hypothesis 19 I. 11 Aims and objectives 19 V CHAPTER TWO GENERAL MATERIALS AND METHODS 2.1 Study site 21 2.1.1 Bimini 21 2.1.2 North Sound shark nursery 24 2.1.3 South Bimini shark nursery 24 2. 1.4 Nursery demarcation 25 2.2 Collection techniques 25 2.2. I Shark collection techniques 25 2.2.2 Shark stomach content collection 26 2.2.3 Prey collection techniques 26 2.2.4 Weighing, measuring and sorting of catches 28 2.3 Nursery description 29 2.3.1 Methodology 29 2.3.2 Abiotic variables 30 2.3.3 Biotic variables 30 2.3.4 Seagrass coverage and macroalgae diversity 30 2.3.5 Coverage with distance from the mangrove fringe 31 2.3.6 Seagrass densities 33 2.3.7 Seagrass standing crop 33 2.3.8 Discussion of nursery description 36 2.4 Statistics 38 2.4.1 Routine statistics 38 2.4.2 Index of relative importance (IRI) 39 2.4.3 Measures of overlap and similarity 39 CHAPTER THREE SPATIAL AND TEMPORAL VARIATION IN THE DIET OF NURSERY-BOUND JUVENILE LEMON SHARKS, Negaprio11 brevirostris, AT BIMINI, BAHAMAS. 3.1 Introduction 43 3.2 Materials and methods 44 3.2.1 Dietary analysis 44 VI 3.2.2 Statistics 44 3.2.2.1 Variation in dietary composition 44 3.2.2.2 Dietary overlap 44 3.2.2.3 Diet breadth 44 3.3 Results 46 3.3.1 Lemon shark stomach contents 46 3.3.1.1 Lemon shark diet- teleosts 46 3.3 .1.2 Lemon shark diet- crustacea, cephalopoda and annelid a 49 3.3.2 Spatial variation in lemon shark diet 49 3.3.3 Seasonal variation in lemon shark diet 52 3.3.4 Ontogenetic variation in lemon shark diet 53 3.3.5 Variation in lemon shark diet with shark sex 57 3.4 Discussion 60 3.4.1 Lemon shark diet 60 3.4.2 Spatial variation in lemon shark diet 63 3.4.3 Seasonal variation in lemon shark diet 64 3.4.4 Ontogenetic variation in lemon shark diet 65 3.4.5 Conclusion 66 CHAPTER FOUR SPATIAL AND TEMPORAL VARIATION IN FISH AND MACRO-INVERTEBRATE COMMUNITIES AT BIMJNI, BAHAMAS. 4.1 Introduction 68 4.2 Materials and methods 69 4.2.1 Study area 70 4.2.2 Collection techniques 70 4.2.3 Statistics 70 4.2.3.1 Data preparation and transformation 71 4.2.3.2 Analysis of community composition 71 4.2.3.3 Analysis of catch diversity and biomass 71 4.2.3.4 Analysis of size distributions 72 4.3 Results 72 4.3.1 Total catch summary, all sites 72 4.3.2 Mangrove communities 72 4.3.3 Seagrass communities 73 4.3.3.1 Seine and trawl catches 73 vii 4.3.3.2 Gillnet catches 80 4.3.4 Spatial and temporal variation in mangrove and seagrass communities 80 4.3.5 Spatial variation in species catch 83 4.3.6 Temporal variation in species catch 85 4.3.7 Spatial and temporal variation in catch diversity and biomass 86 4.3. 7.1 Spatial variation in species diversity 86 4.3. 7.2 Temporal variation in species diversity 86 4.3. 7.3 Spatial variation in catch biomass 89 4.3.7.4 Temporal variation in catch biomass 89 4.3.8 Community size structure 92 4.4 Discussion 95 4.4.1 Comparison of mangrove and seagrass catches at Bimini with other regions 95 4.4.2 North Sound I South Bimini comparison 96 4.4.3 Trends in community size structure 98 4.4.4 Sampling critique 98 4.4.5 Implications on prey selection by juvenile lemon sharks 99 4.4.6 Conclusion I 00 CHAPTER FIVE LENGTH-WEIGHT AND BONE-TOTAL LENGTH REGRESSION EQUATIONS FOR ESTIMATING ORIGINAL SIZE OF PARTIALLY DIGESTED PREY ITEMS 5.1 Introduction 102 5.2 Materials and methods 103 5.2.1 Specimen collection 103 5.2.2 Specimen preparation 103 5.2.3 Bone and carapace measurements 104 5.2.3.1 Fish bone measurements 104 5.2.3.2 Shrimp measurements 107 5.2.3.3 Crab carapace measurements 107 5.2.4. Statistical analysis 107 5.3 Results 110 5.3.1 Length-weight regressions 110 5.3.2 Bone-length regressions 110 5.3.3 Teleost bone-length regressions 115 5.3.3.1 Skull measurements 115 5.3.3.2 Spine and vertebrae measurements 115 VIII 5.3.3.3 Otolith measurements liS 5.3.3.4 Pharyngeal teeth measurements 123 5.3.4 Crustacean carapace-length regressions 123 5.4 Discussion 126 5.4.1 Novelty of this study 126 5.4.2 Regression choice 126 5.4.3 Teleost measurements 127 5.4.4 Crustacean measurements 128 5.4.5 Use of internal measurements 128 5.4.6 Use of total length in this study 129 5.4.7 Considerations/use of bone-length regressions 129 5.4.8 Conclusion 130 CHAPTER SIX PREY SIZE, MEAL SIZE AND DAILY RATION ESTIMATES OF JUVENILE LEMON SHARKS 6.1 Introduction 132 6.2 Materials and methods 133 6.2.1 Study site
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