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1 DISTRIBUTION, MOVEMENTS, AND HABITAT USE OF BULL SHARKS ( Carcharhinus leucas, Mller and Henle 1839) IN THE INDIAN RIVER LAGOON SYSTEM, FLORIDA By TOBEY HAYWARD CURTIS A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORI DA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2008
2 2008 Tobey Hayward Curtis
3 To my grandparents, Stanley and Marjorie Faulkner, and Roland and Beth Curtis Let your light from the lighthouse shine on me
4 ACKNOWLEDGMENTS There are a great many people th at contributed to the succes s of this project, and I am forever grateful for their generous efforts. My degree committee, Franklin Buck Snelson, Michelle Heupel, George Burgess, Daryl Parkyn, and Edward Phlips have been instrumental in guiding me through my program of study, and supporting me throughout the progress of my research. For various forms of logistical support during field work I wish to thank Marc Epstein, Nancy Corona, and the staff of Merritt Island Nati onal Wildlife Refuge, John Stiner, the staff and park rangers of Canaveral National Seashore, Doug Adams, Derek Tr emain, Richard Paperno, and Robert McMichael of the Fl orida Fish and Wildlife Research Institute, and Jane Provancha, Doug Scheidt, Russell Lowers, and Eric Reyier of the Dynamac Corporation at Kennedy Space Center. For assistance during field work, often endur ing hot, sharkless days and without whom this project would have never b een completed, I gratefully acknow ledge Tabitha Vigliotti, Laura Macesic, Taylor Sullivan, Eric Reyier, Travis Ford, Steve Larsen, Buck Snelson, Bryan Delius, Vanessa Jordan, Peter Cooper, Corey Accardo, S ean Morey, Rachel Schwab, Erika Wasner, Christine Wasner, Travis Minter, Jennifer Zimme rman, Christy MacDonald, Aletris Neils, Alex The Brit, Ben Loughran, Kelly Hennessy, Mari a Herrick, Sara Bauder, Taylor Chapple, Laughlin Siceloff, Rebecca Scarbrough, Amanda Harford, Meghan Hibbert, Patrick Rellihan, Alana Schoenberg, Eric Rodrigu ez, Nick Trippel, Dieldric h Bermudez, Shannon Tough, David McGowan, Andrew Piercy, Charlene Mauro of the National Science Foundations ARMADA Program, Kate Brattan, Kate Ba rzan, Nadine Niederauer, Rach ael Hallman, Leslie Babonis, Cheryl Nicholson, Simon Gulak, and Rena Bryan. For sharing bull shark capture r ecords, I am grateful to Buck Snelson, the Florida Fish and Wildlife Conservation Commissions Fishery-In dependent Monitoring Program, Stacy Kubis,
5 Dean Bagley, and Llewellyn Ehrhart at the Univ ersity of Central Florida, Megan Stolen and Frank Murru of the Hubbs-Sea World Research Institute, and Sharon Tyson of the Florida Department of Environmental Protection. For assi stance with data analysis I would additionally like to thank John Kelly, Jason Blackburn, Chri stina Conrath, and Bob Hamilton. For prior training in the methods applied during this study I am grateful for the mentorship of Peter Klimley, Wes Pratt, and Cami McCandless. This research was funded by a grant from th e National Marine Fisheries Service (NMFS) Highly Migratory Species Divisi on to the National Shark Rese arch Consortium (Award No. NA17FL2813), and by a grant from the Disney Wildlife Conservation Fund (Award No. UF-0313) awarded to G. Burgess, F. Snelson, and D. Parkyn. Shark tagging supplies and sampling guidelines were provided by the Apex Predators Program Cooperative Atlantic States Shark Pupping and Nursery (COASTSPAN) survey at the NMFS Northeast Fisheries Science Center, Narragansett, RI. This project was carried out under permits from the Florida Fish and Wildlife Conservation Commission (Permit No. 02R-718), Merritt Island National Wildlife Refuge (Permit No. SUP 35 Burgess), and Canaveral National Seashore (Permit No. CANA-2002-SCI0007). Finally, I wish to acknowledge my family, par ticularly my parents and my wife, for their constant motivation and support. I can not than k them enough for their patience, guidance, and love.
6 TABLE OF CONTENTS page ACKNOWLEDGMENTS...............................................................................................................4 LIST OF TABLES................................................................................................................. ..........8 LIST OF FIGURES.........................................................................................................................9 ABSTRACT...................................................................................................................................13 CHAP TER 1 BACKGROUND AND OBJECTIVES.................................................................................. 15 Introduction................................................................................................................... ..........15 Shark Fisheries................................................................................................................15 Shark Nursery Areas........................................................................................................16 Study Species The Bull Shark......................................................................................17 Purpose and Need for Research..............................................................................................20 Objectives...............................................................................................................................21 2 REVIEW OF THE DISTRIBUTION AND HABITAT OF BULL SHARKS IN THE INDIAN RI VER LAGOON SYSTEM.................................................................................. 24 Introduction................................................................................................................... ..........24 Methods..................................................................................................................................26 Study Site..................................................................................................................... ....26 Data Sources....................................................................................................................27 Capture Methods.............................................................................................................27 Data Analysis...................................................................................................................30 Results.....................................................................................................................................31 Population Structure........................................................................................................ 31 Spatio-Temporal Patterns of Distribution....................................................................... 32 Tag-Recapture Data......................................................................................................... 34 Habitat Utilization........................................................................................................... 35 Discussion...............................................................................................................................36 3 SHORT-TERM MOVEMENTS AND HABI TAT USE OF YOUNG-OF-THE-YE AR AND JUVENILE BU LL SHARKS........................................................................................ 60 Introduction................................................................................................................... ..........60 Methods..................................................................................................................................62 Tagging and Tracking......................................................................................................62 Data Analysis...................................................................................................................64 Results.....................................................................................................................................66 Bull Shark Tracks............................................................................................................ 67
7 Shark B1...................................................................................................................67 Shark B2...................................................................................................................67 Shark B3...................................................................................................................68 Shark B4...................................................................................................................68 Shark B5...................................................................................................................68 Shark B6...................................................................................................................69 Shark B7...................................................................................................................69 Shark B8...................................................................................................................69 Shark B9...................................................................................................................70 Shark B10.................................................................................................................70 Shark B11.................................................................................................................70 Activity Space.................................................................................................................71 Horizontal Swimming Behavior...................................................................................... 72 Habitat Use.................................................................................................................... ..73 Discussion...............................................................................................................................76 4 CONCLUSIONS AND APPLICATIONS ........................................................................... 112 Bull Shark Ecology in the Indian River Lagoon.................................................................. 112 Applications to Shark Management and Conservation........................................................ 114 Recommendations for Future Research................................................................................115 LIST OF REFERENCES.............................................................................................................118 BIOGRAPHICAL SKETCH.......................................................................................................130
8 LIST OF TABLES Table page 2-1. Summary of IRL bull shark data sources used for analysis, 1975 to 2005. .......................... 47 2-2. Range of environmental parameters sa m pled in the IRL by sub-region, during the current study, 2003 to 2005...............................................................................................47 2-3. Catch of bull sharks and gillnet effort (NetDay24) in the IRL by sub-region and season from Snelson et al. (1984), 1976 to 1979...........................................................................48 2-4. Catch of bull sharks and hook gear effo rt (hh = hook hours) in the IRL by sub-region and season during the current study, 2003 to 2005. ...........................................................48 2-5. CPUE of bull sharks in the IRL by sub -region and season from Snelson et al. 1984 (NetDay24), and the current study (hh)............................................................................. 48 2-6. Summary of habitat use by bull shar ks in the IRL by life stage, 1975 to 2005..................... 49 3-1. Details of ten bull sharks tracked in the IRL between 2003 and 2005.................................. 89 3-2. Summary of movement and activity space parameters estimated for ten bull sharks tracked in the IRL. .............................................................................................................90 3-3. Environmental parameters observed during the tracks of ten bull sharks in the IRL. .......... 91
9 LIST OF FIGURES Figure page 1-1. Annual U.S. Atlantic landings of la rge coastal sharks, 1975 to 2001. The arrow indicates the year that shark m anage ment was implemented in the U.S........................... 23 2-1. Chart of the Indian River Lagoon, FL study site. The boxes delineate the three lagoonal sub-regions described in the Me thods: ML = Mosquito Lagoon; NIR = northern Indian River/Bana na River; MS = Melbour ne Sebastian area. ........................50 2-2. Mean monthly water temperatures (C) from the three s ub-regions of the IRL study site and two power plant outfalls near P ort St. John, 2004-2005. Sources: ML, Haulover Canal (USGS 2007); NIR and N. Plant, Mr. W. Baker (Reliant Energy, unpubl. data); MS, Sebastian Inlet (Florida Ins titute of Technology); and S. Plant, Mr. R. Hix (Florida Power and Light, unpubl. data)..................................................................... 51 2-3. Distribution of gillnet sampling locations (N = 1,133) in the IRL carried out by FW C, 1990 to 1997. The dashed line delineates the boundary of the NASA Security Zone. Circles represent IRL gillnet sets. Triangle s represent nearshore gillnet sets. Stars represent locations of fixed-station gillnet sets. Large open triangles represent capture locations of Sphyrna lewini Taken from Adams and Paperno (2007), with permission..................................................................................................................... .....52 2-4. Distribution of hook and line sampling lo cations (N = 155) in the IR L during the current study, 2003 to 2005...............................................................................................53 2-5. Locations of bull shark captures and obs ervations in ML and the NIR, 1975 to 2005. Pentagons = Dodrill (1977); hexagons = Snelson et al. (1984); squares = FWC; circles = KSC; and triangles = present st udy. Note: many of the points represent multiple shark captures. *Indicates the locations of power plants.................................... 54 2-6. Locations of bull shark captures and obs ervations in the MS sub-region, 1975 to 2005. Pentagons = Dodrill (1977); squares = FWC; circles = UCF; and triangles = present study. Note: many of the points re present multiple shark captures................................. 55 2-7. Length frequency of bull sharks captu red in the IRL, 1975 to 2005 (N = 256). ................... 56 2-8. Lengths of captured bull sharks from the IRL by m onth, 1975 to 2005. The dotted line indicates the approximate length dividing neonate from YOY sharks, the dashed line indicates the approximate length dividing YOY and juvenile sharks, and the solid line indicates the approximate length at maturity for female bull sharks.......................... 57 2-9. Frequency of bull shark captures (N = 319) in the IRL by sub-region and season, 1975 to 2005. ..............................................................................................................................58 2-10. CPUE of bull sharks versus habitat para meter gradients in the IRL from the current study, 2003 to 2005............................................................................................................ 59
10 3-1. Manual acoustic track of bull shark B1, a 71 cm FL female, in Mosquito Lagoon between 22 August and 2 September, 2003. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histog ram, the outer edge of the circle represents 15 observations....................................................................................... 92 3-2. Manual acoustic track of bull shark B2, a 94 cm FL male, in the IRL between 11 March and 3 April, 2004. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD................93 3-3. Manual acoustic track of bull shark B3, a 82 cm FL female, in the IRL on 7 May, 2004. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly sti ppled area represents seag rass beds. The gray line surrounding the track positions represents the 95% KUD................................................. 94 3-4. Manual acoustic track of bull shark B4, a 79 cm FL female, in the IRL between 10 and 12 June, 2004. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 15 observations............. 95 3-5. Manual acoustic track of bull shark B5, a 82 cm FL female, in the IRL between 17 and 25 May, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 15 observations............. 96 3-6. Manual acoustic track of bull shark B6, a 83 cm FL female, in the IRL between 18 and 19 May, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 15 observations............. 97 3-7. Manual acoustic track of bull shark B7, a 60 cm FL female, in the IRL between 7 and 8 June, 2005. Points represent 15-min tracking positions. A couple positions appear to overlap land because of the coarse reso lution of the GIS coastline data at this scale. The dashed lines represent 1 m dept h contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD.....................................................................................................................98 3-8. Manual acoustic track of bull shark B8, a 66 cm FL male in the IRL between 20 July and 4 August, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 15 observations............. 99
11 3-9. Manual acoustic track of bull shark B9, a 65 cm FL male in the IRL between 23 and 24 July, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 10 observations........... 100 3-10. Manual acoustic track of bull shark B10, a 61 cm FL female, in the IRL between 2 and 3 August, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD........................ 101 3-11. Site fidelity (days detected) of an acoustically tagged YOY bull shark (B11) at two power plants in the northern IRL during the summ er and fall of 2004. Power plant 1 is the Florida Power and Light plant in Frontenac, FL, and power plant 2 is the Reliant Energy plant in Delespine, FL. The distance between the power plant outfalls is 3.4 km............................................................................................................. .102 3-12. Scatter plot of ROM calculations versus the tim e of day for nine tracked bull sharks (B2 excluded due to positional error) in the IR L. The vertical dashed lines indicate the median times of sunrise and sunset across all tracks................................................. 103 3-13. Box plots of ROM calculations compar ing day and night observations to exam ine potential diel activity patterns. The box a nd whiskers represent (from bottom to top) the 10th, 25th, 50th, 75th, and 90th percentiles of observati ons. The square symbol represents the mean.......................................................................................................... 104 3-14. Comparison of rates-of-movement (mean 1 SE) obtained from ultrasonic tracking of four juvenile bull sharks captured in Indian River Lagoon, FL in the first 2 hours following release and after tw elve hours post-release.....................................................105 3-15. Environmental parameters observed durin g tracks of ten bull sharks in the IRL, including (a) depth, (b) tem p erature, (c) salinity, (d) di ssolved oxygen concentration, and (e) secchi depth......................................................................................................... 106 3-16. Tracking positions for seven bull sharks tracked near Crane Creek in the IRL during dry (brown position s, N=3) and wet (blue positions, N=4) periods, as defined by the surface salinity at the mouth of Crane Creek................................................................... 108 3-17. Cumulative 95% UDs for seven bull shar ks tracked near Crane Creek in the IRL during dry (brown lines, N=3) and wet (blu e lines, N=4) periods, as defined by the surface salin ity at the mouth of Crane Creek (><10 ppt). Note the sharks high site fidelity to the creek during dry periods............................................................................ 109 3-18. Box plots comparing the salinity utilizat ion of seven bull sharks tracked near Crane Creek in th e IRL during dry (N=3) and wet (N=4) periods, as defined by the surface salinity at the mouth of Cran e Creek. Note that the 25th percentiles of observations are nearly equivalent at approximately 11 ppt................................................................. 110
12 3-19. Linear correlation between bull shark acti vity space and salinity at the m outh of Crane Creek (N=6). Indicates an outlier (B7) which was not included in the regression...... 111
13 Abstract of Thesis Presen ted to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science DISTRIBUTION, MOVEMENTS, AND HABITAT USE OF BULL SHARKS ( Carcharhinus leucas, Mller and Henle 1839) IN THE INDIAN RIVER LAGOON SYSTEM, FLORIDA By Tobey Hayward Curtis May 2008 Chair: Daryl C. Parkyn Major: Fisheries a nd Aquatic Sciences Distribution and habitat use of the bull shark ( Carcharhinus leucas ) were examined using fishery-independent sampling data tagging, and ultrasonic telemetr y to assess the potential role of the Indian River Lagoon (IRL) as a nursery area for this species. Fishery-independent sampling data were compiled and synthesized to examine patterns of seasonal occurrence, spatial distribution, and habitat associa tions. These data provided a comprehensive overview of bull shark ecology in the study site over a span of 30 years, based on data collected from 390 individual sharks. Tagging and acoustic telemetry methods were also employed to acquire more fine-scale information on shark movements, daily ac tivities, and habitat util ization. A total of 50 sharks were marked with conventional tags, with four fish recaptured over the course of the study. Eleven of these sharks were tagged addi tionally with ultrasonic pingers, ten of which were tracked manually and one of which was m onitored by moored liste ning stations (Vemco VR2). The manual tracking data provided fine-s cale information on the patterns of movements of a small number of individuals. Integra tion of multiple methodologies provided a more complete picture of habitat use by this important apex predator in the IRL. Bull sharks occurred over a broad range of habitats, including de pths of 0.2 4.0 m, temperatures of 18 37 C,
14 salinities of 1 42 ppt, dissolved oxygen concentrat ions of 3 8 mg/L, and water clarity levels of 70 170 cm. In addition, they were located ov er seagrass, sand, and mud substrates. Overall catch-per-unit-effort was low, relative to other systems. However, higher than average catch rates were observed at power plant outfalls and near freshwater creeks. These results may prove useful to the continued management and conser vation of bull shark stocks in the northwest Atlantic.
15 CHAPTER 1 BACKGROUND AND OBJECTIVES Introduction Shark Fisheries The expansion of commercial shark fisheries o ff the Atlantic coast of the United States over the past 30 years has led to population declin es in many of the species taken (Figure 1-1) (Musick et al. 1993; NMFS 1993; 2006; Burgess et al. 2005). The rise of these fisheries has primarily been driven by the increased demand for shark fin products in Asia, as well as increased demand for shark meat in domestic and foreign markets (NMFS 1993; Brown 1999). The species captured in these fisheries, many from the family Carcharhinidae, are considered to have a K -selected life history (McArthur and W ilson 1967; Hoenig and Gruber 1990), meaning that they are long-lived, have sl ow growth rates, mature at a late age, and produce few, highly developed offspring (Pitcher and Hart 1982). Animals that are K -selected do not cope well with heightened levels of mortality, and take ma ny years to repopulate an area once depleted (Jennings et al. 1998; Gedamke et al. 2007). According to th e 1993 Fishery Management Plan for Sharks of the Atlantic Ocean (FMP), the abundance of the large coastal species management unit could have declined as much as 75% from the 1970s to the 1980s (NMFS 1993). The FMP also identified an alarming lack of information on shark fisheries, and biological data needed for adequate fisheries management. It stated that delineation of essential fish habitat (EFH), specifically mating and nursery grounds, is of key importance. Estuarine nurseries were determined to be the habitats of greatest concern for coastal sharks in that these areas continue to suffer from dramatic human-induced altera tion and destruction. Th e re-authorized MagnusonStevens Fishery Conservation a nd Management Act (Sustainable Fisheries Act of 1996) also
16 legally mandated that government fisheries agencies identify and protect EFH for commercially exploited species of fish. This continues to be an important component of the MagnusonStevens Reauthorization Act of 2007. Along with habitat degradation, impacts from water quality degradation in coastal areas were also id entified as a potential th reat, but the effects of these alterations on sharks remains mostly unkno wn (NMFS 1993). Before these impacts can be properly assessed, the spatial and temporal boundaries of shark nursery areas must first be isolated. Shark Nursery Areas In the most simplistic definition, shark nursery areas are part of a species range where gravid females give birth to their pups, and where the young spend the first weeks, months, or years of their lives (Castro 1993). There are two main types of shark nursery areas. Primary nursery habitats are zones where parturition and young-of-the-year (YOY) sharks occur. Secondary nursery habitats are zones that are used only by juveniles and sub-adults (immature sharks at least 1 year old) of a species (Ba ss 1978). Many shark species use productive shallow coastal zones and estuaries as nursery areas because they are hypothesi zed to offer two key selective benefits, 1) low levels of predation from other larger sharks, and 2) an abundance of prey like small fishes and crustaceans (Springe r 1967; Castro 1983; Branstetter 1990). In the northwest Atlantic and Gulf of Mexico, shark nurseries have been found along the U.S. coast from Massachusetts to Texas (McCandless et al. 2002; 2007). This traditional definition of estuarine nursery areas functioning as cr itical habitats has recently met with some criticism. Beck et al (2001) argued that just because the young of a species occur in a specific environment in high densities does not necessarily mean that that specific habitat is providing ref uge from predation and abundant food resources. They suggested that an area is a nursery if its contribution per unit area of r ecruits to the adult population is
17 greater than other areas where young individuals also occur. Th is contribution results from increases in numbers, rates of growth, juvenile survival, or fa cilitation of movement to adult habitats. Heithaus (2007) has fu rther argued that an essential habitat could be defined as habitat where density-dependent se lection occurs. With referenc e to shark nursery areas, he hypothesized that risk of predati on and intraspecific competition should influence the habitat use of sharks within their nurseries. Both studies highlight the fact that information on the movements of species within their nurseries ar e lacking, yet are essential to understanding the factors influencing habitat select ion. In a recent review of th e shark nursery area concept, Heupel et al. (2007) attempted to reconcile the various proposed definitions for what constitutes a shark nursery area, and provided th ree testable criteria for an area to be characterized as a shark nursery: 1) density of juvenile sharks is greater in the putativ e nursery area relative to other areas, 2) juvenile sharks exhibit hi gher than average site fidelity to these areas, and 3) the area is used repeatedly by juvenile sharks across years. According to the authors, this definition does not discount the importance of prey availability, predation risk, a nd intraspecific competition in a potential nursery area, but provides the means to collect hard data in the field (through surveys, mark-recapture experiments, acoustic tracking, stab le isotope analysis, genetic techniques, etc.) that will support or refute the ch aracterization of a part icular area as a nurse ry. If these three criteria are met, then the area is likely to support increased pr oduction in the shark population in question, as required by the Beck et al. (2001) definition of nursery habitat. Study Species: The Bull Shark The bull shark, Carcharhinus leucas Mller and Henle 1839, is a cosmopolitan species in tropical to subtropical coastal waters, typically occurring in waters less than 30 m deep (Compagno 1984). Few studies have examined the movements and patterns of habitat use of the bull shark (Thorson 1971; Steiner 2002). However, the general biology and life history of the
18 bull shark has been studied in a number of popul ations around the world including the Gulf of Mexico (Springer 1940; Clark a nd von Schmidt 1965; Caillouet et al. 1969; Branstetter 1981; Branstetter and Stiles 1987; Cruz-Martinez et al. 2002; Neer et al. 2005), the Atlantic coast of Florida (Dodrill 1977; Snelson et al. 1984), Central America (Thor son et al. 1966; Thorson 1976; Tuma 1976; Thorson and Lacy 1982; Montoya and Thorson 1982), Brazil (Sadowsky 1971; Thorson 1972), South Africa (Bass et al. 1973; Cli ff and Dudley 1991), in a ddition to studies in captivity (Weihs et al. 1981; Schmid et al. 1990; Schmid and Murru 1994). The bull shark frequents brackish estuarine wa ters and has been documented to penetrate rivers and into numerous freshwater lake s around the world (Tuma 1976; Garrick 1982; Compagno 1984; Martin 2005). Ther e are verified records of bu ll sharks captured from the Peruvian Amazon River up to 3,480 km from the Atlantic (Thorson 1972), and a record from Alton, Illinois, 2,800 km up the Mississippi Rive r (Thomerson et al. 1977). A population in Lake Nicaragua in Central America, previously believed to be a completely landlocked and separate species, C. nicaraguensis has since been shown to be comprised of C. leucas that navigate the rapids of the San Juan River from the Caribbean Sea into the lake (Thorson et al. 1966; Thorson 1971). The bull sharks unique p hysiology and osmoregu latory capabilities enable its euryhaline habits (Thorson 1962; Oguri 1964; Thorson et al. 1973; Pillans et al. 2005). The bull shark can grow to lengths of 350 cm TL and weigh over 230 kg, making it one of the largest of its genus and or der (Castro 1983). Consequently, th e size at birth is also large at 60-80 cm TL (Clark and von Schmidt 1965, Dodrill 1977). In the northern Gulf of Mexico maturity is reached at 210-220 cm TL (14-15 years) for males, and >225 cm TL (18+ years) for females, which also tend to reach greater total lengths (Branstetter and Stiles 1987, Neer et al. 2005). Bull sharks are opportunistic roving predators, their diet pr imarily consisting of teleosts
19 and smaller elasmobranchs (Compagno 1984, Snelson et al. 1984). Its large size, its tendency to inhabit shallow coastal zones, a nd its opportunistic feeding habits make the bull shark one of the most dangerous sharks, being implicated in at least 75 unprovoked attacks on humans around the world, 23 of those resulting in fatality (G. Burg ess, unpubl. data, International Shark Attack File, University of Florida). Most of the existing literature on the life history, ecology, and distributions of C. leucas in Florida waters has come fr om multi-species surveys (Clark and von Schmidt 1965; Snelson and Williams 1981; Hueter and Manire 1994; Huet er and Tyminski 2002). For example, the seasonal occurrence, size, reproductive habits, and diet of bull sharks were examined along with 16 other species of sharks that occur along Floridas central Gulf Coast by Clark and von Schmidt (1965). The bull shark was the most a bundant species in their catch (N = 135), ranging in size from 88-264 cm TL. They were cap tured year-round, though catch was highest from March to October, particularly during the summer months. Adult individuals of both sexes were equally represented in their se asonal distribution, indicating no seasonal sexual segregation. They found that parturition occurred in April, following a gestation period of 10-11 months. The mating season was determined to be in June and Ju ly. Analysis of stomach contents revealed a diet dominated by bony fishes Archosargus probatocephalus Caranx spp., Centropomus undecimalis, Euthynnus alletteratus Arius felis Acanthostracion quadricornis, Megalops atlanticus, Mugil spp., and Prionotus spp., as well as parts of sharks, crustaceans, and mollusks. Other surveys have yielded complementary info rmation on the diets of Florida bull sharks (Snelson et al. 1984; Hueter and Manire 1994; Michel 2002). Bull sharks also opportunistically scavenge on marine mammal carcasses (Compa gno 1984; M. Stolen, Hubbs-SeaWorld Research Institute, pers. comm.).
20 Purpose and Need for Research Many large coastal shark populat ions have been overfished along the Atlantic coast of the United States, in recent decades (NMFS 1993). Effective management measures to rebuild these depleted stocks have been unsuccessful, undoubtedly due in part, to a lack of data on shark life history, population dynamics, dist ribution, and habitat requirements (NMFS 2006). The impacts of ever-increasing coastal devel opment and habitat alteration of nearshore regions has made the delineation of shark estuarine nu rsery areas a priority. Altho ugh progress has been made in recent years to help identify essential habitats for sharks (e.g. Simpendorfer and Milward 1993; McCandless et al. 2002; 2007), season al distribution and habitat us e information is incomplete for most shark species. More information is needed to help characterize critical nursery areas for commercially exploited species. This is particular ly true for species that may rely on disturbed and heavily impacted inshore systems. The reco very of these species may be dependent upon the ability to protect their essential habitats be fore they are lost or permanently altered by anthropogenic activities. To maintain sustainable exploitation of shark resources, it is prudent to protect immature portions of the stocks and the habitats on whic h they rely (NMFS 1993; Cortes 2002). As a result, there has been a recent increase in the numb er of studies investigating the distribution and habitat use of sharks within their nursery ar eas (Simpfendorfer and Milward 1993; Hueter and Manire 1994; Merson and Pratt 200 1; Michel 2002; McCandless et al. 2002; 2007). Bull sharks have been commercially harvested off the south eastern U.S. for over 30 years, and as a member of the large coastal shark management complex, may currently be overfis hed (Cortes et al. 2002; NMFS 2006). More effective management require s a better understand ing of how exploited sharks, such as the bull shark, utilize their essential nursery habitats. A few recent studies have focused on the abundance, distribution, and habitat us e of juvenile bull sharks in some of their
21 Gulf of Mexico nursery areas (Michel 2002; Simpfendorfer et al. 2005 ; Blackburn et al. 2007), but potential Atlantic coast nurse ries such as the Indian Ri ver Lagoon (IRL) have not been studied since the recent rise of the U.S. shark fish ery (Snelson et al. 1984). In addition, there is very little information available on the day-to-day movements, activities, and habitat preferences of immature bull sharks in their nursery areas. The purpose of this study is to describe the historic and current distribution of bull sharks within the IRL, and provide much-needed insights into daily movements and habitat use of the young sharks that utilize this coastal lagoonal system. Objectives This study takes two primary approaches to addr ess the needs described above. The first is to use fishery-independent sampling methods to collect, tag, and release immature bull sharks in the IRL. Augmentation of this data with existing fishery-independent data sets for bull sharks in the IRL is used to provide a robust and comprehe nsive synthesis of information for this site. Catch rates are used as predicto rs of habitat use, and tag reca ptures provide insights into movements. The second approach is to actively track th e movements of individual YOY and juvenile bull sharks via acoustic telemetry. This is the most effective method to examine the short-term, high-resolution movements of fish es in their natural environment (Nelson 1990; Sundstrm et al. 2001; Sibert and Nielsen 2001). This techniqu e provides information on the daily activities, swimming behaviors, and patterns of habita t use of these young sharks relative to the environmental parameters of temperature, depth, dissolved oxygen, and salinity. With these data I addressed th e following research questions: Question 1. Do immature bull sharks show any dis tinct patterns of habitat use in the IRL with regards to depth, temperat ure, salinity, water clarity, diss olved oxygen, or substrate?
22 Question 2. Do bull sharks of different size/age classes (YOY vs. juvenile) have similar activity spaces, and habitat utilization patterns? Question 3. Do immature bull sharks exhibit any diel changes in activity levels or space use? Question 4. Does the Indian River Lagoon system meet the definition of a shark nursery area, as proposed by Heupel et al. (2007)? With a better understanding of how this commercially-im portant shark utilizes this important coastal environment, we will be better equipped to develop more effective management and conservation strategies for th e species and its EFH. By delineating and protecting this EFH, it may help increase the surv ivorship of juveniles, and therefore promote successful recruitment to the adult stocks and fisheries (Cortes 2002). Thus, a primary contribution of this study is to increase our understanding of the ecol ogy and behavior of bull sharks, and provide information needed to he lp conserve bull sharks and their EFH.
23 Figure 1-1. Annual U.S. Atlantic landings of large coastal sharks, 1975 to 2001. The arrow indicates the year that shark manage ment was implemented in the U.S..
24 CHAPTER 2 REVIEW OF THE DISTRIBUTION AND HAB ITAT OF BULL SHARKS IN THE INDIAN RIVER LAGOON SYSTEM Introduction Fishery-independent surveys are one of the primary methods for assessing the distribution and habitat use of sharks (Simpf endorfer and Heupel 2004). Gillnet and hook gear surveys have proven particularly useful for sharks in shallow coastal and estuarine areas, often used as nursery grounds for coastal species (Clarke 1971; Snelson and Williams 1981; Simpfendorfer and Milward 1993; Hueter and Ma nire 1994; Carlson and Brusher 1999; Merson and Pratt 2001; Heithaus et al. 2002; Michel 2002; McCandless et al. 2002; 2007; Simpfendorfer et al. 2005; Wiley and Simpfendorfer 2007). Studie s such as these have dramatically improved our knowledge of the distribution and habitat asso ciations of a variety of shark species in a variety of environments around the world, and have proven useful for fishery managers in the conservation of depleted shark stocks. Distribution and habita t information for many species, however, is still lacking. Furthe rmore, even where species-specific data is available, site-specific information is needed to shed light on spatio-t emporal patterns of utiliza tion, since most sharks utilize a great variety of habitats within their ranges. As a component of the NMFS multi-species large coastal shark management complex, the bull shark is a commercially exploited shar k species for which more information on life history, movements, and habitat associations are needed. The current stock status of the large coastal shark group is unknown due to data de ficiencies for robust species-level stock assessments (NMFS 2006), but has been classed as overfished and experiencing overfishing in previous stock assessments (Cortes et al. 2002 ). Additionally, other large coastal species including sandbar ( Carcharhinus plumbeus) and dusky sharks ( C. obscurus ), have been assessed and found to be overfished. The World Conser vation Union (IUCN) Red List of Threatened
25 Species classifies C. leucas as near threatened due to eviden ce of population declines in certain locations around the world (e.g. Thorson 1982; Cli ff and Dudley 1991). The bull shark may be particularly at risk because its life history trai ts make it vulnerable to overfishing (Thorson and Lacy 1982; Branstetter and Stiles 1987; Cruz-Martinez et al. 2002; Wintner et al. 2002; Neer et al. 2005) and its coastal/inshore distribution may disproportiona tely expose this species to adverse anthropogenic environmen tal impacts and habitat loss (Garrick 1982; Compagno 1984). However, the most recent stock assessment of larg e coastal sharks stated that because of their nearshore distribution off the southern United States, bull shark populations may not be as impacted by fishing mortality as other species (NMFS 2006). It states, Commercial shark fishing effort [in nearshore waters] has been lim ited or eliminated for more than a decade, which has helped to maintain a large biomass (N MFS 2006). A species-specific bull shark population stock assessment is likely warrant ed to confirm this assertion. The Indian River Lagoon (IRL) is an anth ropogenically impacted waterway (Gilmore 1995) that is utilized by immature bull sharks (S nelson et al. 1984; Castro 1993). The seasonal occurrence and diet of bull sharks in the IRL was previously de scribed by Snelson et al. (1984), but information on distribution and habitat use patte rns in the nursery area were not discussed in detail. The study also only surveyed a portion of the northern IRL, so data has not been reported for much of the remainder of the expansive lagoon system. Due to the bull sharks current conservation status and the appa rent importance of this Atlan tic coast estuary to their young (Snelson et al. 1984), more detailed information c ould prove beneficial to fisheries management and conservation efforts. This information will also help to further describe the ecology of this apex lagoon predator.
26 The objectives of this chap ter are to compile and synthe size all available bull shark records from the IRL, including records from the scientific literature, unpublished fisheryindependent data, and personal communications, to provide a comprehensive description of their seasonal distribution and habitat util ization patterns in this intra-coastal environment. These data will help to determine whether the IRL functions as a bull shark nursery area (Heupel et al. 2007). Methods Study Site The IRL is a shallow, estuarine, barrier island system that stretches over one third of Floridas central Atlantic coast, between the lati tudes of 29 04 N (Ponce de Leon Inlet) and 26 56 N (Jupiter Inlet) (Figure 2-1). This syst em is comprised of three main water bodies: Mosquito Lagoon, Indian River Lagoon proper, and Banana Rive r Lagoon, which are interconnected by canals. There are five inlets along the length of the system which connect these bodies to the ocean. The study area covere d the northern half of the lagoon between Ponce de Leon Inlet (Volusia County) and Sebastian Inle t (Brevard County) (Figure 2-1). Portions of the study area fall under the jurisd iction of Canaveral Na tional Seashore, Merr itt Island National Wildlife Refuge, and the National Aeronautic s and Space Administrations (NASA) Kennedy Space Center (KSC). The IRL spans a climatic transition zone between tropical and warmtemperate environments (Phlips et al. 2002), a nd therefore contains a diverse ichthyofauna (Gilmore 1995). In addition, IRL co ntains a variety of habitat types including seagrass beds, fringing mangroves, saltmarshes, oyster bars, open sand bottom, lagoon reefs, tidally influenced freshwater tributaries, and ocean inlets (Gilm ore 1977; Kupschus and Tremain 2001). It is home to at least 397 species of temperate to tropical fishes, many of these juvenile phases of offshore
27 species (Gilmore 1977; 1995). The mean annual sa linity for the entire IRL is 25.6 ppt, and water temperatures can annually range from 11 32.5 C (Figure 2-2) (Gilmore 1977). Data Sources To synthesize bull shark di stribution information from the IRL, verified bull shark capture and sighting records were compiled from thr ee main sources: (1) the scientific literature (Dodrill 1977; Snelson and Williams 1981; Snelson et al. 1984, Schmid and Murru 1994; Tremain et al. 2004); (2) fisher y-independent sampling data: the Florida Fish and Wildlife Conservation Commission (FWC) Fishery-Independent Monitoring Program; sea turtle netting studies at the University of Central Florida (UCF) and the KSC/Dynamac Corporation; sampling efforts conducted as part of the current tagg ing study; and (3) persona l communications from cooperating scientists an d local fishermen. Table 2-1 summar izes the data sources, the gears used, the years represented, and the number of sharks captured in each of these studies. Capture Methods Sampling effort, spatial distri bution, and techniques varied considerably be tween each of the studies from which data were compiled. The distribution of sa mpling effort spanned approximately half the length of th e IRL, from Ponce de Leon Inle t at the north end of Mosquito Lagoon, to Sebastian Inlet, 145 km to the south (F igure 2-1). The primary capture gears were gillnet and bottom longline, but also included rod and reel and haul seine (Table 2-1). Direct visual observations were also in cluded in this synthesis. Hook gear, including bottom longlines and rod and reel, was utilized by Dodrill (1977) to collect sharks in the IRL and off Melbourne Beach between 1974 and 1977. The longline was 200 m in length, and was comprised of 1590-kg test nylon mainline. Ten baited hooks were evenly spaced along the length of the mainline, on 3.7 m long steel chain gangions. The hooks alternated in size, and in cluded Mustad 51 mm and 63 mm shark hooks, and 14/0 tuna hooks.
28 As part of a sea turtle monitoring study, Snelson and Williams (1981) used large-mesh gillnets to capture elasmobranchs in the nor thern IRL between 1975 and 1979. Details of the bull shark catch data were described by Snelson et al. (1984). The gillnets were comprised of braided nylon twine with stretch mesh of 305 406 mm, net lengths from 90 230 m, and a net depth of 3.7 m. The nets were deployed monthly in Mosquito Lagoon and the northern IRL for periods of 24 147 h, as described by Snelson et al. (1984). Catch-per-u nit-effort (CPUE) was calculated as the number of sharks captured per 24-h net day (NetDay24 = [m net deployed/100] x [h net deployed/24]). Schmid and Murru (1994) used small botto m longlines to capture neonate bull sharks from the IRL for captive study and display at Sea World of Florida, Orlando. Collecting occurred during the summer of 1985 near the power plant outfalls at Port St. John (Mr. F. Murru, Sea World, pers. comm.). No detailed information on fishing effort or habitat associations were available. The bull shark data contributed by FWC was from gillnet captures in the IRL between 1990 and 1997 (Figure 2-3), and from haul seine captures in 2000 and 2001. The gillnets used were multi-panel monofilament gillnets, 208 m in length and 1.8 m deep, with 127-mm diameter polypropylene float line and 127-mm di ameter lead core lead-line. The net consisted of five panels; a 25-m long panel of 50-mm stretch mes h, and four 45.7-m panels, with 76-, 102-, 127-, and 152-mm stretch mesh (Adams and Paperno 2007). All sets were conducted during crepuscular or nighttime periods. Soak times ranged from 1.53 4.25 h (mean = 2.65 h). The haul seine was 183 m long and 3 m deep, with 38 -mm meshes (D. Adams, FWC, pers. comm.). Water temperature, salinity, and dissolved oxygen measurements were collected at all sampling
29 sites. All sharks were sexed and measured to the nearest mm, and then tagged below the first dorsal fin with a spaghetti-style dart tag. Sampling gear in the present study, include d a 50-hook bottom longline, comprised of 305 m of 6.4-mm braided nylon mainline. Gangions were made of braided nylon, 1.5-m in length, with 1.6-mm stainless steel cable leader attached to a ba ited 12/0 circle hook (with barbs depressed for easier release). On some occasi ons only half of the mainline was set with 25 hooks. Gangions were spaced evenly along the length of the longline. Bait included fresh or frozen fish ( Mugil spp., Alosa spp., Dorosoma petenense Elops saurus Arius felis Dasyatis spp., Caranx spp.). The line ends were anchored, and marked by visible surface floats. Soak time (defined as the time between the setting of the last hook and the retrieval of the first hook) varied depending on environmenta l conditions, and ranged from 20 65 min, but the majority of sets soaked for 45 min. Short soak times were intended to minimize incidental mortality of the captured sharks. This longline design is the same as that used by Pratt et al. (1998). Rod and reel was also used at many locations where set ting the longline was not feasible, using the same terminal tackle and bait, attached to 13.6-kg (30-lb) test monofilament fishing line. While rod and reel fishing, the boat was anchored, and lines were soaked until the bait degraded or a fish was caught. CPUE was measured as the number of sharks captured per 100 hook hours (hh) of effort (1 hh = 1 baited hook soaking for 1 h). At each sampling location (Figure 2-4) the date time of day, latitude and longitude, water depth, bottom type, wind velocity and direction, air temperature, surface water temperature, salinity, dissolved oxygen (DO) concentration, and water clarity (Secchi depth) were recorded (Table 2-2). All captured sharks immediately had the hook removed and were restrained on the deck. Straight-line fork (FL) and total length (TL) were measured with a meter stick to the
30 nearest cm. Sex of sharks was determined by external examination for the presence of claspers. A small fin clip was also removed from the sec ond dorsal fin for subsequent genetic analysis by other researchers. Each shark was ID-tagged with a numbered plastic rototag (Dalton Co., UK) punched through the first dorsal fin, which included tag-return instructio ns to the NMFS Apex Predators Program, Narragansett, RI. The sharks were then promptly released. Handling time was normally less than 3 min, to minimize the st ress experienced by the shark during capture and tagging. The condition of the shar k at release was classified as excellent, good, fair, or poor, depending on how vigorously the shark swam upon release. The direct visual observation of free-swimming bull sh arks was also recorded, and lo cation and habitat data were noted at the time of observation. Additional observations were provided by Jane Provancha (KSC), Sharon Tyson (Florida Dept. of Environmental Protecti on), Megan Stolen (Hubbs Sea Wo rld Research Institute), and several resident lagoon sport fishermen. Data Analysis For the purposes of this synthesis, the study si te was divided into th ree sub-regions: (1) Mosquito Lagoon (ML), (2) northern Indian River and Banana River (NIR), and (3) the Melbourne Sebastian (MS) ar ea (Figure 2-1). All known bull shark capture and sighting locations were plotted using Geographic Information Systems (GIS) software (ArcView 3.2, Environmental Systems Research Institute Inc., Redlands, California). Descriptive statistics were used to characterize the catch and habita t parameters observed from each of these subregions, and for the study site overall. CP UE was summarized by region and season for each study from which sampling effort information was av ailable: i.e., Snelso n et al. (1984) and the current study. The designation of seasons follows Snelson et al. (1984): Winter = December February; Spring = March May; Summer = June August; and Fall = September November.
31 Habitat data were available from Snelson et al. (1984), FWC, KSC, and this study. Linear correlation analysis was used to examine potential relationships between CPUE from the current study and habitat parameters including depth, temper ature, salinity, and DO. Results Population Structure All the data sources combined represented a total of 390 individual bull shark records from the IRL from 1975 2005 (Table 2-1). Shark capt ure locations are shown in Figures 2-5 and 26. The population of bull sharks in the IRL was dominated by immature sharks (mean 1 sd = 121 38 cm TL), including neonates (less than c 75 cm TL), YOY (less than c 90 cm TL), juveniles (less than c 190 cm TL), and maturi ng subadults (less than c 210 cm TL) (Figure 2-7). Of the sharks in which sex was noted, 86 were male and 113 were female, yielding a male to female ratio of 1:1.3. Juvenile bull sharks ( c 90 190 cm TL) were the dominant size/age class in the lagoon, and were captured ye ar round in the IRL (Figure 2-8) The few adult-sized sharks were only captured during the la te spring/early summer. Neonate-sized sharks, with fresh umbilical scars, were only captured between Ma y and August (Figure 2-8). The smallest freeswimming bull shark captured in the IRL was 61 cm TL, and was captured in August 1985 (Schmid and Murru 1994). The smallest bull shark captured during the current study was a 66 cm TL male, weighing 1.8 kg, that was captured in June near the power plant outfall at Delespine, FL (Figure 2-5). To date, the only mature bull sharks captured within the IRL (N = 6) have been gravid females approaching parturition (Dodrill 1977; Sn elson et al. 1984). Dodrill (1977) discussed a large (> 250 cm TL) female bull shark harpooned by a fisherman north of Sebastian Inlet in late
32 Spring/early Summer 1976. Sn elson et al. (1984) captured two large mature females ( c 225 249 cm TL) in ML; one in May 1975 and one in May 1979. One shark was not fully examined but appeared gravid. The other carried 12 nea r-term embryos, 60.8 70.6 cm TL. An anecdotal report from a local sport fisherman also indicated the observation of a large (> 250 cm TL) shark, presumably C. leucas, of unknown sex off the Whale Tail at the southern end of ML in May 2005. A large bull shark (sex unknown) was also re ported from the southern IRL near Ft. Pierce Inlet in August 2002 (Capt. S. Bachman, Ft. Pierce, FL, pers. comm.). Additionally, an adult female bull shark that was tagged at Walkers Cay, Bahamas with a pop-up satellite archival tag in April 2003 traveled 210 km and into the sout hern IRL through St. Lucie Inlet, where its tag popped off after 12 days at liberty (Brunnschweiler and Buskirk 2006). Mature male bull sharks have not been doc umented within the IR L. Although all size classes less than 210 cm TL are represented in th e catch, the length frequency of IRL bull sharks appears to be bimodal (Figure 2-7), with a peak at the 70 109 cm TL size classes and a peak at the 150 169 cm TL size class. Spatio-Temporal Patterns of Distribution In general, bull shark occurrence was lower in ML, the northernmos t portion of the study site, than in the NIR or MS regions, with 70 sh arks caught in ML, 127 sh arks in the NIR, and 122 sharks in the MS area (Figure 2-9). A lthough somewhat influenced by the spatial distribution of fishing effort, th e spatial distribution of catches was not homogeneous in any of the sub-regions. Catches of sharks tended to be cl ustered at specific sites within each sub-region (Figures 2-5 and 2-6). In ML most sharks were captured so uth of Haulover Canal along the western shoreline of the lagoon (Figure 2-5). In the NIR, shark catches were clustered near the power plant outfalls at Frontenac and Delespine (Figure 2-5). In the MS area, most bull shark catches occurred within or adjacent to the freshwater creeks that flow into the lagoon from its
33 western shoreline, and also at Sebastian Inlet (F igure 2-6). Few sharks were captured in deeper mid-lagoon waters, or from the intracoastal waterway which runs through the entire study site. Bull sharks were captured year round in the IRL, although based upon all available catch data, there appears to be some variation in th eir seasonal distribution and occurrence (Figure 29). In ML, sharks were only captured between March and November. During winter months, no sharks were captured in ML despite various levels of sampling effort (Tables 2-3 and 2-4). In the NIR and MS areas, sharks were document ed year round, though with less frequency during the winter. Only five bull sharks were docum ented in the NIR during winter, three of which were dead or moribund following severe hypothe rmal events in the lagoon (Dodrill 1977; Snelson and Bradley 1978; Snelson et al. 1984). The other two sharks were tagged individuals which were recaptured in the NIR (see Tag-Recapture Data). The MS ar ea, however, yielded the capture of 13 juvenile bull sharks during the winter primarily near Sebastian Inlet. This is the only area sampled where non-moribund bull sharks were regularly captured during winter. During spring months, juvenile bull sharks were present in all three la goon regions, though most common in the NIR and least common in ML (Fi gure 2-9). During the summer, with the influx of neonate sharks (Figure 2-8), numbers peaked in ML and MS areas, and dropped somewhat in the NIR. Sharks remained abundant in all region s into the fall, particularly in the NIR and MS areas, until dropping off as wint er approached (Figure 2-9). The available CPUE data reflect these patterns of occurrence in both Snelson et al. (1984) and the present study (Table 2-5). In the curren t study, CPUE was greatest in the MS region and lowest in ML (Table 2-5). Sn elson et al. (1984) also found that CPUE was notably lower in ML than in the NIR (Table 2-5). Across seasons, catch rates in ML range d from 0.0 0.18 sharks per NetDay24, and in the NIR, catch rates ranged from 0.0 0.69 sharks per NetDay24 (Table 2-
34 5). Seasonal catch rates in the current study were highest (6.52 sharks per 100 hh) during summer in the MS region. CPUE was substant ially lower (0 1.42 shar ks per 100 hh) in all other regions and seasons (Table 2-5). Snelson et al. (1984) reported th e highest seasonal CPUE of their study (1.15 sharks per NetDay24) durin g fall 1976 in ML and NIR. Other temporal trends in shark distribution may have been more a pparent had more effort data been available for analysis. Tag-Recapture Data Tagging efforts conducted by FWC (Tremain et al. 2004) and during th e current study led to the tag and release of 50 bu ll sharks in the IRL between 1991 and 2005. A total of 25 sharks were tagged by FWC between 1991 and 1997, and 25 sharks were tagged in the current study between 2003 and 2005. Two bull sharks were re captured by each program in the IRL, yielding a total of 4 recaptures (8%). Time at liberty ranged from 3 214 days, and the minimum distance traveled betw een tag and recapture locations ranged from 0.1 34.5 km. No bull sharks were recaptured outside of the IRL. One juvenile bull shark that was tagged south of the Frontenac power plant on 25 October 1995 was recaptured 33 km to the north near Haulover Canal on 14 December 1995. A YOY bull shark that was tagged on 24 June 1996 in the northern Banana River KSC no-entry zone was subsequently recaptured in the NIR near the Rt. 405 causeway in Titusville on 23 January 1997 (Tremain et al. 2004). The two bull sharks recaptured from the current study moved very little over comp aratively short times at liberty. One neonate was tagged off the Delespine power plant, and re captured by a sportfisherman three days later less than 100 m from the taggi ng location. The othe r recaptured shark, a YOY male that was tagged south of Crane Creek in Melbourne, was recap tured by the author less than 1 km from its tagging location after two weeks at liberty.
35 Habitat Utilization There are broad ranges of physical and biological habitats in the IRL system (Table 2-2; Figure 2-2; Gilmore 1995); most of which are utili zed by bull sharks at le ast occasionally. The available habitats also varied to some degree between each of the sub-regions (Table 2-2; Figure 2-2). The water temperatures encountered du ring sampling ranged from 12.1 37.0 C, with bull sharks being captured in 20.0 37.0 C waters (Table 2-6). The mean temperature of occurrence was 29.7 3.5 C. The single shark captured at 37 C, a juvenile swimming in the heated effluent of the Delespine power plant in A ugust 2004, appeared emaciated and weak. YOY bull sharks were captured in a warmer and narrower te mperature range than ju veniles (Table 2-6). The mean temperature of capture was 30.4 1.8 C for YOY and 29.7 3.3 C for juveniles. Although there was no significant correlation between CPUE and water temperature detected in the current study, CPUE was highest in 27 33 C water temperatures (Figure 2-10). The range of salinities encountered during sampling was 0.7 42.0 ppt (Table 2-2), with bull sharks captured at salinities of 1.2 42.0 ppt (23.2 10.0 ppt, mean 1SD) (Table 2-6). YOY bull sharks tended to be captu red in lower salinity waters (17.0 7.7 ppt) than juveniles (21.6 7.9 ppt) (Table 2-6). Ther e was no significant correlati on between CPUE and salinity, but CPUE was high in 9 15 ppt and 28 30 ppt salinity levels (Figure 2-10). The range of DO concentrations enco untered during sampling was 2.4 10.2 mg/L (Table 2-2), with bull sharks cap tured at concentrations of 3.2 9.2 mg/L (Table 2-6). The mean DO of occurrence was 5.5 1.5 mg/L. YOY bull sharks were cap tured in areas with a slightly lower mean DO level (4.8 1.5 mg/L) than juveniles (6.0 1.2 mg/L) (Table 2-6). There was no correlation between CPUE and DO, but CPUE was highest between 4.5 and 7.5 mg/L (Figure 2-10).
36 Most depths available in the IRL (0.2 6.0 m) were sampled for bull sharks. Despite this, sharks were captured in de pths of 0.2 3.4 m (Table 2-6). The mean depth of occurrence was 1.0 0.6 m, which was equivalent for both YOY and juvenile sharks (Table 2-6). However, there was no significant correlation between CPUE and depth, but CPUE wa s highest in depths less than 2 m (Figure 2-10). The water clarity levels encountered dur ing sampling, as measured by Secchi depth, ranged from 0.2 3.0 m (Table 2-2). Bull sharks were captured in Secchi depths of 0.3 1.5 m (Table 2-6). The mean Secchi depth where sharks occurred was 0.9 0.3 m, and was similar for both YOY and juveniles (Table 2-6). Discussion Based on thirty years of bull shark captur e data, it appears that the northern IRL is commonly utilized by immature C. leucas, and appears to function as a nursery area. In addition, bull sharks of several size/age classes are seas onally distributed thr oughout the lagoon system and occupy a broad range of habitats. These findi ngs are mostly consistent with the findings of previous studies on bull sharks in the IRL (Dodril l 1977; Snelson et al. 1984), as well as for bull sharks in some other documented nursery areas (Simpfendorfer et al. 2005; Blackburn et al. 2007). This chapter is intended to provide a comprehensive review of bull shark captures in the IRL and provides a reference source for management and conservation efforts for bull sharks and their habitats in the IRL. The reduced frequency of bull sharks in the 110 129 cm TL size class may be an artifact of gear bias, and varia tion in the sampling techniques and effort of the different studies included in this synthesis. There did appear to be some differen ces in gear selectivity, with the
37 mean TL of sharks captured by hook gear (98 31 cm, N = 97) being notably less than the length of sharks captured by gillnet (135 34 cm, N = 160). The reduced frequency of bull sharks in that size classes coul d indicate that the gears utilized were inefficient at capturing sharks of that size, rather than their reduced occurrence in the st udy site. Snelson et al. (1984), a study that utilized large-mesh nets, failed to capture any sharks in the 86 116 cm TL length range, and postulated that this was also a result of gear bias, rather than absence from the lagoon. Bull shark data from the other sources compiled he rein corroborate that conjecture. In fact, sharks 90 109 cm TL appear to be the dominant size class in the lagoo n (Figure 2-7). These findings underscore the importance of using gears of various size selectivities for characterizing shark populations in nursery areas. The low catches of sharks gr eater than 190 cm TL, however, was not considered to be influenced by gear bias, as large bull sharks were readily taken by cer tain gears (Dodrill 1977; Snelson et al. 1984), and would likel y have been visually observed if they were more abundant. Sharks greater than c 190 cm TL appear to be at the si ze which they may leave the nursery and fully transition to offshore adult habitats (Figure 2-7). According to age at length estimates for bull sharks (Neer et al. 2005), individuals of that size are approximately 9 years of age. In the Caloosahatchee River estuary on Floridas Gulf of Mexico coast, Simpfe ndorfer et al. (2005) captured bull sharks 68 189 cm stretched TL, an d estimated their ages at 0 10 years. Blackburn et al. (2007) also report ed that bull sharks in coastal Louisiana waters ranged from 44 136 cm FL ( c 55 166 cm TL), and Steiner et al. (2007) reported that bull sharks in Floridas Ten Thousand Islands estuary we re 43 120 cm precaudal length ( c 60 162 cm TL). Based on these length ranges (see Neer et al. 2005 for le ngth conversions), bull sharks from both of Floridas coasts and the Gulf of Mexico appear to transition from nursery to adult habitats at
38 lengths of c 160 180 cm TL. Bull shark length frequenc y data from U.S. Atlantic large coastal shark fisheries may help confirm this by examini ng the length at recruitment to the fishery. Bull sharks primarily utilize the northern half of the IRL (Sebastian Inlet to Ponce de Leon Inlet) during spring, summer, and autumn (F igure 2-9). In the late spring, gravid adult female bull sharks enter the lagoon via one of the inlets, and parturition occurs between May and August, after which time the adult sharks exit the lagoon (Figure 2-8; Dodrill 1977; Snelson et al. 1984; Brunnschweiler and Buskirk 2006). The occu rrence of gravid female bull sharks in nursery areas prior to parturition was also observed by Bass (1978) in So uth Africa. Beginning in October or November, YOY and juvenile sharks appear to migrate out of the northern portions of ML and the NIR. It is not currently known if the bull sharks exit ML via Ponce de Leon Inlet to the north, or through Haulover Ca nal and into the NIR. While a few sharks remain in the NIR during winter, particularly near th e heated power plant outfalls (F igure 2-5), it is speculated that most sharks leave the area either presumably mo ving either offshore or south in the IRL. The higher catches of bull sharks near Sebastian Inlet, at the southern extent of the study site, in December seem to support this hypothesis. Additionally, Dodrill (1977) captured YOY bull sharks off the ocean beaches outside of the IRL in November and January. Based on the available data, it is not known if bull sharks also occur during winter in the IRL south of Sebastian Inlet, but based on the increases in winter catches with decreasing latitude (Figure 29), it is likely that they utilize or transit the s outhern portions of the lagoo n during this time. Bull sharks begin to migrate back into th e northern IRL around March of each year. Snelson et al. (1984) noted that emigration from the lagoon duri ng winter could be difficult to differentiate from reduced activity of sharks th at could actually remain within the IRL. Since bull sharks are ectothermic, dropping water temperatures during winter could depress
39 metabolism and activity to a degree that could allo w the sharks to avoid capture in passive gears like gillnets and longlines. Though further resear ch will be necessary to investigate this possibility, it may be unlikely for a few reasons. First, a significant amount of fishing effort was expended in the ML and NIR sub -regions during winter (Tables 2-3 and 2-4) and few sharks were captured or visually observed. Of those that were observed in the NIR, they were primarily located in warm power plant effluents (Figure 2-2), or were moribund from hypothermal (4 C) conditions (Dodrill 1977; Snelson and Bradley 1978; Snelson et al. 1984). Second, based on data from other nursery areas, young bull sharks tend to avoid water temperatures below 18 21 C (Hueter and Tyminski 2002; Wiley and Si mpfendorfer 2007). Lower temperatures are commonly experienced in the shallow water of ML and the NIR during winter periods (Gilmore 1977; Gilmore et al. 1978; Snelson and Bradley 1978; Figure 2-2). Third, bull sharks in south Florida nursery areas, such as the Everglades National Park re gion, show no clear trends in seasonal abundance and are pr esent year round (Wiley and Simpfendorfer 2007). This is consistent with the latitudinal gradient of wi nter bull shark occurrence discussed above. Many other carcharhinid shark species migrate south alo ng the Atlantic coast of the U.S. during winter (Kohler et al. 1998), and immature bull sharks do not appear to be an exception (Hueter and Manire 1994). This suggests that migration, rather than inactivit y, is a more plausible explanation for the lack of bull shark catches in the northern IRL in winter months. Given the low catch rates of bull sharks in ML, even dur ing warmer summer and fall months, and the low reported catches of immature bull sharks in estuaries north of ML (McCandless et al. 2002), ML may represent the northern extent of bull shar k nursery habitat along the Atlantic coast. A primary determinant in the occurrence of bull sharks in the study site, as well as in their geographic range, is water temperature, as dictat ed by the sharks physiologi cal tolerance of this
40 environmental parameter. In broad terms, the ra nge of the bull shark is limited to tropical and subtropical climes (Garrick 1982; Compagno 1984) Since the northern IRL is located in a climatic transition zone (Gilmore 1995), and temp eratures seasonally fl uctuate (Gilmore 1977; Figure 2-2), sometimes dramatically (e.g., Snel son and Bradley 1978), bull shark occurrence in the system should fluctuate in response. The avoi dance of low water temperatures by bull sharks has been documented in a few studies (Huete r and Tyminski 2002; Si mpfendorfer et al. 2005; Wiley and Simpfendorfer 2007), and unusually low wa ter temperatures (< 10 C) can clearly be lethal to small sharks (Dodrill 1977; Snelson and Bradley 1978). Healthy (non-moribund) immature bull sharks have been recorded from water temperatures as low as 15 C (Blackburn et al. 2007). Bull sharks in putative nursery areas app ear to be limited to temperatures greater than 20 C (McCandless et al. 2007). This temperature range may be a migratory cue for immature bull sharks at higher latitudes, inducing them to seek warmer waters. This is supported by the seasonal distribution of bull sharks in the IRL (Fi gure 2-9). The locations of bull shark captures during winter months were almost exclusively limited to areas with mean water temperatures greater than 20 C during those months. Thes e include Sebastian Inlet and the power plant outfall areas (Figure 2-2), the latter of which is thought to function as a thermal refuge (Snelson et al. 1984). Other lagoon species, including manatees ( Trichechus manatus latirostris ) utilize these same heated power plant outfalls as ther mal refugia during winter (Deutsch et al. 2003; Laist and Reynolds 2005). This hypothesis is further supported by the year round presence of immature bull sharks in nursery areas with warm er mean temperatures than the IRL (Wiley and Simpfendorfer 2007). The distribution of bull sharks in the IRL also appeared to be influenced by salinity to some extent. Even though the sharks occurr ed in freshwater, brackish water, and even
41 hypersaline conditions (Table 2-6) a finding consistent with nu merous bull shark studies (e.g., Snelson et al. 1984; McCandle ss et al. 2002; 2007; Simpfendorfer et al. 2005), there was evidence of preferences for sa linities ranging from 10 29 ppt (Figure 2-10). YOY bull sharks tended to occur in lower salinity conditions than juveniles (Table 2-6). This pattern of size segregation was also observed by Simpfendorfer et al. (2005), and was thought to be associated with either the need for YOY sharks to avoid larger predators, or a physiologically driven preference to reduce the metabolic costs of osmoregulation. The bull sharks ability to osmoregulate in low salinity environments (e.g., Thorson et al. 1973; Pillans et al. 2005), and the use of such areas by immature sh arks as nurseries, may give this species a distinct survival advantage as compared to other coastal species that are less euryhaline. The risk of predation by larger sharks is certainly re duced in such shallow, low sa linity regions (B ranstetter 1990; Simpfendorfer et al. 2005), the only natural predators being larger bull sharks (Snelson et al. 1984). More research is needed to address th e salinity preferences of YOY and juvenile bull sharks in the IRL, and to understand the factors that influence salinity selection. The influence of DO on elasmobranch distributio n has been examined in a few studies, but has not been found to be a significant predic tor of habitat use (Grubbs and Musick 2002; McCandless et al. 2002; 2007). Since DO is often not limited in shallow, well-mixed estuarine areas like the IRL, temperature and salinity tend to be more important factors for elasmobranchs in coastal environments (Matern et al. 2000; Grubbs and Musick 2002; Hopkins and Cech 2003; Simpfendorfer et al. 2005). It is therefore not surprising that there was no discernible pattern or correlation between bull shark distribution and DO in this study (Table 2-6; Figure 2-10). Certainly the DO levels commonly occurring in the IRL (Table 2-2) meet the minimum oxygen
42 demands for bull shark respiration, although oxy gen consumption experiments would more completely define these demands (e.g., Miklos et al. 2003). While temperature, salinity, and DO are habitat conditions that are select ed at least in part based on physiological requirement s, other environmental factors including water clarity, bottom substrate, depth, and habitat complexity are le ss influenced by physiological tolerance than by biological factors such as predat or avoidance or the distribution of prey. The prevalence of YOY and juvenile bull sharks in waters less than 2 m deep may be linked to the distribution of prey species that utilize productive seagrass beds, th e dominant substrate at those depths (Gilmore 1995). Primary prey species such as stingrays, catfishes, a nd mullet are abundant in these shallow areas of the IRL (Snelson and Williams 1981; Snelson et al. 1989; Curtis unpubl. data). Prey density may also influence the bull sharks frequent utilizat ion of power plant effluents and the freshwater creeks near Melbou rne in the IRL. The plumes of warm water flowing from the power plant outfalls may attract forage species particularly during colder periods. The availability of structure such as piers, used as a shelter for a variety of lagoon species, may also draw bull sharks into low salin ity areas like Crane Creek (Fi gure 2-6). Few studies have investigated the relationships between shark distribution and pr ey distribution, and those that have found mixed results (Heupel and Hueter 2002; Torres et al. 2006; Heupel et al. 2007; Heithaus 2004; 2007). Similar investigations in the IRL, a nursery area with few shark predators, may provide greater in sights into the habitat selection patterns of bull sharks. Recent fishery management needs in the U. S., including the need to define EFH for federally managed species (NMFS 1999), have driven renewed interest in the habitat associations and critical nursery habitats in all fishes, including sharks. Bull shark habitat utilization patterns in nursery areas have been de scribed in several studies (Bass 1978; Snelson et
43 al. 1984; Hueter and Manire 1994 ; Michel 2002; McCandless et al. 2002; 2007; Simpfendorfer et al. 2005; Wiley and Simpfendorfer 2007), and the findings of this study are la rgely consistent the results of these other studies. The bull sharks captured in the IRL were found in a variety of habitat types including ocean inlets, brackish and freshwater creeks, around piers, over seagrass flats, open sand and muddy bottoms, and in dredged channels. The physical characteristics of these habitats were also broad (Table 2-6), and represent a large portion of habitats available in the IRL (Table 2-2). The increased frequency of bull sharks in specific habitats, however, is suggestive of selection for such ar eas (Table 2-6; Figure 2-10). Tag-recapture data provided limited insights into the movements of bull sharks in the IRL. Unfortunately, only four tagged sharks were recaptured over the sp an these studies ; two of which were recaptured less than two weeks from their initial release. No sharks were recaptured outside of the study site to pr ovide insights into large scale movements, and no sharks were recaptured in years subsequent to their release that might support evidence of philopatry (Hueter et al. 2005) or other information such as morta lity rates. Other bull shark tagging studies have shown that large scale movements tend to be comparatively limited (Thorson 1971; Bass 1978; Hueter and Manire 1994; Kohl er et al. 1998; Bullen and Mann 2000; Kohler and Turner 2001; Tremain et al. 2004; Brunnschweiler and Busk irk 2006). The maximum known tag-recapture distance for bull sharks is 643 km (Kohler and Turner 2001), and movement s are largely limited to coastal and contin ental shelf waters (Kohler et al. 1998). One of the earliest bull shark tagging e fforts was conducted by Thorson (1971), who tagged 2,200 bull sharks in the Lake Nicaragua/San Juan River system in Central America. The 220 recaptured sharks offered definitive proof th at the sharks in Lake Nicaragua were not landlocked as previously believed, but readily traversed the 175 km of the San Juan River to the
44 Caribbean Sea in as little as one day. Of 60 YO Y and juvenile bull sharks tagged in Tampa Bay by Hueter and Manire (1994), seve n were recaptured, including one YOY female that was tagged in July 1993 and recaptured in December 1993, 194 km south in San Carlos Bay. The other six sharks were recaptured no more than 5 km from their tagging locations afte r times at liberty of up to 113 days (Hueter and Manire 1994). Bullen and Mann (2000) reported similar findings for immature C. leucas tagged in South Africa between 1984 and 1999 (N = 254). Of 16 bull (= Zambezi) sharks recaptured, five were recaptured at the site of their initial release after times at liberty of 10 573 days. The maximum distance traveled was 539 km over 572 days (0.94 km/day). For comparison, the maximum di stances traveled by the closely-related C. limbatus and C. obscurus are 2,146 km and 3,800 km, respectively (K ohler and Turner 2001). It appears that, in general, bull sharks s how relatively high levels of si te fidelity, punctuated by limited migratory movements up and down coastlines. IRL bull sharks may exhibit similar patterns, but acoustic, satellite, and archival tagging studies w ill help to better describe these seasonal, large scale movement patterns. The consistent presen ce of immature bull sharks in the IRL, clearly demonstrates this estuarys importance to the northwestern Atlantic population of this species. However, how does the IRL compare with other known bull shark nurse ry areas in the region ? Along the Atlantic and Gulf of Mexico coas ts of the U.S., potential bull shark nursery areas appear to extend from North Carolina to Texas (McCandless et al. 2002; 2007), although the fr equency of immature bull shark captures appears to taper off north of ML on the Atlantic coast (McCandless et al. 2002; 2007). Even though habitat use patterns are quite similar across th ese nursery areas, bull shark occurrence appears to be greater in the Gulf of Mexico than in Atla ntic coast nurseries. Specifically, immature bull shark catches appear higher than the IRLs in the following nursery
45 areas: the Florida Keys (Huete r and Tyminski 2007), Everglades National Park and Florida Bay (Wiley and Simpfendorfer 2007), the Ten Thousand Islands estuary (Michel 2002; Steiner et al. 2007); the Caloosahatchee River estuary (Simpf endorfer et al. 2005), Ch arlotte Harbor and Tampa Bay (Hueter and Tyminski 2007), the Mississippi River es tuary and coas tal Louisiana (Blackburn et al. 2007), and seve ral bay systems in Texas (Jon es and Grace 2002; Hueter and Tyminski 2007). Texas, in par ticular, appears to contain so me very productive bull shark nursery areas, with over 3,500 bull sharks captured between 1975 and 1995, including 2,118 YOY individuals (Jones and Grace 2002). In this region, YOY and juvenile bull sharks were present between March and December in temperatur es of 18.6 33.5 C, and in salinities of 0 51 ppt. Consistent with evidence of overfishing, CPUE of bull shar ks declined significantly over the course of this study (Jones and Grace 2002). Bull shark nursery areas may also extend along the coast of Mexico, but no data is currently available from this region. If absolute numbers of bull sharks from these areas can be used as an index of nursery area pr oductivity, then Gulf of Mexico nursery areas likely contribute more recr uits than the IRL to bull shark stocks in the northwest Atlantic. In fact, gi ven the results of these other studies, the IRL may represent the northern/eastern extent of bull shar k nursery areas for the region. Although bull sharks may not be as abundant in the IRL as other nursery areas (McCandless et al. 2007), the la goon may still serve as an important contributor to adult bull shark populations. The relative absence of large sharks (i.e., predat ion pressures) in the IRL in conjunction with its abundant pr ey resources may supply the ideal circumstances for a nursery area, in terms of maximizing su rvival. Although empirical mortality estimates are lacking for juvenile bull sharks, the mortality of juvenile sharks of other speci es that must remain in more saline waters appears to be relatively high (Heupel and Simpfendorfer 2002; Bush and Holland
46 2003). Bull sharks in the IRL and other enclosed, low salinity areas may be relatively free from predation, and have more freedom to forage, ther eby increasing energy intake to maximize their growth rates and overall fitness (Heithaus 2007). Conversely, the bull sharks proximity to coastal development, habitat al teration and degradation in ins hore regions like the IRL, may expose young sharks to adverse water quality conditi ons, or reduced suitable habitat for foraging. The impacts of habitat loss and water pollution on shark nursery areas have received very little attention, even though such anthropogenic impacts could negate the beneficial functions of nearshore nursery areas. Bull sharks in intraco astal regions are documented to bio-accumulate high levels of contaminants (Adams and McMi chael 1999; Johnson-Restrepo et al. 2005), but the possible effects of such contam ination remains unknown. Further re search is needed to address the relative productivity of diffe rent shark nurseries, and to determine if certain nursery areas have become compromised by detrimental habitat impacts. Given the cu rrent status of large coastal shark stocks, protection of vulnerabl e nursery areas should be a high priority.
47 Table 2-1. Summary of IRL bu ll shark data sources used for analysis, 1975 to 2005. Source Sharks LocationsTL Range (cm)Years Gear Dodrill (1977) 19 19 70-250 1975-1977 Hook Snelson et al. (1984) 150 31 73-249 1975-1979 Gillnet Schmid and Murru (1994) 5 1 61-68 1985 Hook FWC FIM 40 27 72-144 1991-2001 Gillnet UCF/KSC Turtle Bycatch 52 4 130-200 1996-2005 Gillnet Personal Communications 34 8 70-250 2003-2005 Hook, Observation Current Study 90 90 66-130 2003-2005 Hook, Observation Total 390 180 61-250 1975-2005 Table 2-2. Range of environmental parameters sampled in the IRL by sub-region, during the current study, 2003 to 2005. Parameter ML NIR MS Depth (m) 0.4 6.0 0.4 4.0 0.4 3.4 Temperature (C) 20.3 31.9 12.1 37.0 17.4 33.4 Salinity (ppt) 20.6 36.6 16.4 29.4 0.7 31.1 Dissolved Oxygen (mg/L) 2.4 9.9 3.7 10.2 3.2 8.3 Secchi Depth (m) 0.8 1.5 0.2 3.0 0.2 1.5
48 Table 2-3. Catch of bull sharks and gillnet e ffort (NetDay24) in the IRL by sub-region and season from Snelson et al. (1984), 1976 to 1979. Region ML NIR NetDay24 Sharks NetDay24Sharks Winter 25.5 0 34.5 0 Spring 102.4 7 39.8 23 Summer 160.4 21 61.3 16 Fall 131.0 24 46.2 32 Total 419.3 52 181.8 71 Table 2-4. Catch of bull sharks and hook gear effort (hh = hook hours) in the IRL by sub-region and season during the current study, 2003 to 2005. Region ML NIR MS hh Sharks hh Sharks hh Sharks Winter 7.0 0 565.3 0 0.0 0 Spring 2.0 0 572.7 7 210.7 3 Summer 383.8 4 685.5 3 184.0 12 Fall 472.2 0 116.3 0 0.0 0 Total 865.0 4 1939.7 10 394.7 15 Table 2-5. CPUE of bull sharks in the IRL by sub-region and season from Snelson et al. 1984 (NetDay24), and the cu rrent study (hh). Snelson et al. (1984) Present Study ML NIR ML NIR MS Winter 0.00 0.00 0.00 0.00 0.00 Spring 0.07 0.58 0.00 1.22 1.42 Summer 0.13 0.26 1.04 0.44 6.52 Fall 0.18 0.69 0.00 0.00 0.00 Total 0.12 0.39 0.46 0.52 3.80
49Table 2-6. Summary of habitat use by bull sharks in the IRL by life stage, 1975 to 2005. Life Stage N Temperature (C)Salinity (ppt) Oxygen (mg/L) Depth (m) Secchi Depth (m) YOY 41 Mean 30.4 17.0 4.8 1.0 0.9 Range 27.9 33.5 1.6 34.2 3.2 9.0 0.2 3.4 0.3 1.1 Juvenile 71 Mean 29.7 21.6 6.0 1.0 1.0 Range 20.0 37.0 1.2 31.1 3.8 7.9 0.3 3.0 0.3 1.5 Total 136 Mean 29.7 23.2 5.5 1.0 0.9 Range 20.0 37.0 1.2 42.0 3.2 9.2 0.2 3.4 0.3 1.5
50 Figure 2-1. Chart of the Indi an River Lagoon, FL study site. The boxes delineate the three lagoonal sub-regions described in the Me thods: ML = Mosquito Lagoon; NIR = northern Indian River/Bana na River; MS = Melbourne Sebastian area. FloridaPonce de Leon Inlet Mosquito Lagoon Indian River Cape Canaveral Banana River Port St. John Melbourne Sebastian Inlet Atlantic Ocean New Smyrna Beach Titusville ML NIR MS
51 10 15 20 25 30 35 40 JanFebMarAprMayJunJulAugSepOctNovDec MonthWater Temperature (C) N. Plant S. Plant ML NIR MS Figure 2-2. Mean monthly water temperatures (C) from the th ree sub-regions of the IRL study site and two power plant outfalls near Port St. John, 2004-2005. Sources: ML, Haulover Canal (USGS 2007); NIR and N. Pl ant, Mr. W. Baker (Reliant Energy, unpubl. data); MS, Sebastian Inlet (Florida Institute of Technology); and S. Plant, Mr. R. Hix (Florida Power and Light, unpubl. data).
52 Figure 2-3. Distribution of gilln et sampling locations (N = 1,133) in the IRL carried out by FWC, 1990 to 1997. The dashed line delineates the boundary of the NASA Security Zone. Circles represent IRL gillnet sets. Triangles represent nearshore gillnet sets. Stars represent locations of fixed-station gi llnet sets. Large open triangles represent capture locations of Sphyrna lewini Taken from Adams and Paperno (2007), with permission.
53 Figure 2-4. Distribution of hook and line sampling locations (N = 155) in the IRL during the current study, 2003 to 2005. Ponce de Leon Inlet Cape Canaveral Titusville Port St. John Melbourne Atlantic Ocean
54 Figure 2-5. Locations of bull sh ark captures and observations in ML and the NIR, 1975 to 2005. Pentagons = Dodrill (1977); hexagons = Snelson et al. (1984); squares = FWC; circles = KSC; and triangles = present st udy. Note: many of the points represent multiple shark captures. *Indicates the locations of power plants. Titusville Atlantic Ocean Mosquito Lagoon Indian River Banana River KSC MINWR Port Canaveral Delespine* Frontenac* Cocoa Banana Creek Haulover Cana l
55 Figure 2-6. Locations of bull shark captures and observations in the MS sub-region, 1975 to 2005. Pentagons = Dodrill (1977); squares = FWC; circles = UCF; and triangles = present study. Note: many of the points represent multiple shark captures. Atlantic Ocean Sebastian Inlet Melbourne Sebastian River Eau Gallie River Crane Creek Turkey Creek Indian River Melbourne Beach
56 Figure 2-7. Length frequency of bull sharks captured in the IRL, 1975 to 2005 (N = 256). 0 10 20 30 40 50 60 70506 9 70-89 90-109 110-129 130-149 150-169 170-189 190-209 210+Total Length (cm)Number of Sharks
57 50 70 90 110 130 150 170 190 210 230 250 0123456789101112 MonthTotal Length (cm) Figure 2-8. Lengths of captured bull sharks from the IRL by month, 1975 to 2005. The dotted line indicates the approximate length divi ding neonate from YOY sharks, the dashed line indicates the approximate length dividi ng YOY and juvenile sharks, and the solid line indicates the approximate length at maturity for female bull sharks.
58 Figure 2-9. Frequency of bull shark captures (N = 319) in the IRL by sub-region and season, 1975 to 2005.
59 Figure 2-10. CPUE of bull sharks versus habitat parameter gradie nts in the IRL from the current study, 2003 to 2005. 0 200 400 600 800 1000 1200 1400 0.02.04.06.08.0 Depth (m)CPU E 0 200 400 600 800 1000 1200 1400 2.004.006.008.0010.0012.00 Dissolved Oxygen (mg/L)CPU E 0 200 400 600 800 1000 1200 1400 0.010.020.030.040.0 Salinity (ppt)CPU E 0 200 400 600 800 1000 1200 1400 10.0 20.0 30.0 40.0 Temperature (C)CPU E
60 CHAPTER 3 SHORT-TERM MOVEMENTS AND HABITA T USE OF YOUNG-OF-THE-YEAR AND JUVENILE BULL SHARKS Introduction Ultrasonic telemetry and active tracking of sharks have been useful tools for determining short-term movements (Nelson 1978; Nelson 1990), diel cycles of migration (e.g., Sciarotta and Nelson 1977; Tricas et al. 1981), home range (e .g., Holland and Wetherbee 1999; Morrissey and Gruber 1993a), habitat use and preference (e.g., Morrissey and Gruber 1993b; Heithaus et al. 2002), horizontal and vertical swimming behavior (e.g., Carey and Scharold 1990; Klimley et al. 2002), physiology (e.g., Carey et al. 1982; Lowe and Goldman 2001), and social interactions (Klimley and Nelson 1984). Traditionally, shark nursery areas and habitat use have been delineated through the use of catch rates from fishery-independent sampling (e.g. Snelson and Williams 1981; Castro 1993; Simpfendorfer and Milward 1993; Merson and Pratt 2001; McCandless et al. 2002, Simpfendorfe r and Heupel 2004; Chapter 2) Acoustic telemetry has also been used to help identify and delineate shark nursery areas, and sh ark habitat use within these regions (Holland et al. 1993; Wether bee et al. 2001; Heupel and Hueter 2001; Simpfendorfer et al. 2002; St einer 2002; Rechisky and Wetherbee 2003, Simpfendorfer and Heupel 2004). This method has been used on a variety of shark species in widespread geographic locations, environments, and circumst ances (for reviews see Nelson 1990; Sundstrm et al. 2001). The results garner ed from these studies are not only proving to be useful for fisheries management, but are also providing novel behavioral insight s that are difficult to obtain with other methods. Most of the information known about the movements of juvenile and adult bull sharks has been derived from studies using externally atta ched conventional tags (Thorson 1971; Hueter and Manire 1994; Kohler et al. 1998; Kohler and Turner 2001; Trem ain et al. 2004; Chapter 2).
61 These studies were important in providing some initial insights into movements and migrations, but are generally coarse in scale. These studie s demonstrate that, in general, bull sharks do not migrate as widely as many other carcharhinid sharks, with the maximum reported tag-recapture distance being 643 km (Kohler a nd Turner 2001). In addition, while their distribution and migrations appear primarily limited to neritic wate rs (Kohler et al. 1998), lengthy excursions into riverine systems have been observed (e.g., Thom erson et al. 1977). A tag-recapture study by Thorson (1971) definitively described how bull sharks reached Lake Nicaragua from the Caribbean Sea via the San Juan River, previously considered a physical ba rrier to the sharks. Because of the limited data on individual movements, such methods of tagging are unable to provide insights into fine-scale movements on a shor t-term temporal scale. Telemetry is one of the only methods to effectively acquire such information. Despite their relative abundance in a vari ety of coastal locations worldwide, their importance in many fisheries, and their notori ety for attacks on humans, movements of bull sharks have only been examined along coastal area s in southwest Florida (Steiner 2002). With their inshore distribution, the bull shark popula tion present in the IRL is a particularly good candidate for an acoustic tracki ng study. Their seasonal occurren ce and dietary habits in this region were described by Snelson et al. (1984) (also see Chapter 2). However, little is known about their daily movements and activities, home ranges, or patterns of habitat use in the IRL region. The goal of this chapte r is to investigate such activities and add to the growing knowledge of the behavior of bull sharks in their young life stages. Spec ifically, this study set out to estimate the size of bull sh arks daily activity space, their rates of movement, describe fine scale habitat use, and investigate any potential rhythmic diel patterns of movement.
62 Methods Tagging and Tracking Immature bull sharks were captured either with rod and reel or on a 50-hook bottom longline set for periods of 65 min or less, with a 12/0 Mustad circle hook baited with cut pieces of baitfish ( Mugil spp., Alosa spp., Dorosoma petenense Elops saurus Arius felis Dasyatis spp., Caranx spp.) (see Chapter 2, Methods). Once captur ed, sharks were brought aboard the boat, measured to the nearest centimeter (FL and TL), and then tagged through the ceratotrichia of the first dorsal fin with a NMFS Cooperative Shark Tagging Program blue or yellow rototag (Dalton Co., UK) (Kohler et al. 1998). Ultrasonic tr ansmitters (Vemco V16-4H and V16-6H, 51-81 kHz) with pulse periods of 1.5 seconds and a minimum battery life of over 150 days were externally attached to sharks by a tether of monel wire which was wrapped to the stem of the rototag. The transmitter trailed between the first and second dorsal fins of the shark as it swam. The wire would eventually unwrap or corrode and drop from the shark. Transmitters weighed less than 1% of the sharks body weight in air, and based on visual observations, did not appear to hinder the sharks normal swimming behavior. Only sharks in good condition at the time of release were tracked. The captu re, tagging, and release process normally took less than 5 min. Once released, the transmitter signal was tracked using an acoustic receiver (Vemco VR60) and directional hydrophone (Vemco VH10). Range tests revealed a maximum detection range of approximately 500 m, but this varied depending on transmitter frequency, ambient noise, depth, temperature, water clarity and salinity profile. During each track, geographic positions were manually recorded at 15-minute intervals using a hand-held GPS (Garmin eTrex Legend, Olath, KS, accurate to 3 m). Water te mperature, salinity, and dissolved oxygen concentration (DO) were recorded every 1-2 hour s during each track using a water quality meter (YSI 85, Yellow Springs, Ohio, USA), and water clarity was measured using a secchi disk
63 (during daylight only). The pr esence of known bull shark prey species (Snelson et al. 1984) was also noted when visually observed. The tracking vessel was preferably kept at a distance of 50 100 m from the shark, but at times when a shark en tered very shallow water (< 0.5 m), it had to be followed much more closely because of transmitter signal attenuation. Efforts were taken to minimize interference with the sharks movements, and the boats engine was turned off whenever feasible in shallow water. The boat followed the course of the sharks movements during tracking, with the assumption that the boat location, as determined by the handheld GPS, represented the location of the sh ark. Those GPS coordinates we re then used in subsequent spatial analyses. An additional bull shark ha d a long-life (641-day) co ded transmitter (Vemco V16-4H, 69 kHz, pulse period 30 79 seconds) su rgically implanted into its body cavity. The presence/absence of this individual was monitore d by moored acoustic listening stations (Vemco VR2, detection range approximately 800 m) placed near the outfalls of th e two power plants in the northern IRL. Juvenile and YOY bull sharks were actively tracked in the IRL between August 2003 and August 2005 primarily during the summer months wh en the sharks were more abundant (Snelson et al. 1984; see Chapter 2). Tracking was conducted in th ree distinct regions of the lagoon: in the southern portion of Mosquito Lagoon (N=1), in the Indian River near Port St. John (N=2), and in the Indian Rive r near Melbourne (N=7) (Figure 2-1). All of these areas had similar depth and substrate characteristics, with shallow areas (<1 m) of seagrass ( Thalassia testudinum and Syringodium filiforme ) and sand close to shore. Deeper channels (3 4 m in depth) and segments of the intracoastal waterw ay (ICW) were present in the mid-lagoon, further away from shore. The tracks that occurred in the Port St. John area were in the vicinity of two large power-generating plants that discharge warm water as effluent into the lagoon year-round
64 (Figure 2-5). The temperature regimes found at these locations were therefore not homogeneous with the rest of the lagoon system. The Melbourne area is also different from the other regions in that a series of small freshwater creeks em pty into the lagoon from its western shoreline (Figure 2-6), often reducing the salinity of the lagoon during rainfall events, and providing uncommon freshwater (<10 ppt) habitats for the sharks. Data Analysis The manually recorded 15-min GPS position fixes were plotted using ArcView 3.2 GIS software. The total distance traveled by each shark was calculated as the sum of the distances between each 15-min track segment. The rate of movement (ROM) over ground, defined as the distance between two successive positions divided by the time taken to travel that distance, was calculated to provide an indicat ion of swimming speed (e.g. Klim ley et al. 2002; Kelly et al. 2006). In active-tracking studies on fishes, RO M is used as a measure of swimming speed, though is considered an underestimate of true sw imming speed (Sundstrm et al. 2001). It can also be used as an indicato r of activity level, with hei ghtened ROM being suggestive of migrating or foraging behavior (Klimley et al 2002; 2005), and is useful for detecting diel patterns of activity (Nelson 1990). The mean ROM of YOY and juvenile sh arks were compared, as were the mean ROM between day and night by using descriptive statistics. The activity space, or size and shape of the area used by telemetered sharks, was analyzed using two methods: the minimum convex polygo n (MCP) method (Odum and Kuenzler 1955), and a fixed-kernel utilization distribution (UD) method (Worton 1989) using the Animal Movement Analysis extension for ArcView 3.2 (Hooge et al. 1999). Core area was defined as the area of the 50% UD, and total activity spac e was defined as the area of the 95% UD (e.g. Cartamil et al. 2003, Heupel et al. 2006). The term activity space rather than home range is most often used to define the area utilized by shar ks during manual tracking, because the duration of
65 tracking is rarely long enough to encompass the entire home range of the individuals tracked (Sundstrm et al. 2001). To describe the shape of the activity space of each shark, an index of eccentricity (ECC), was calculated using th e formula (3-1): ECC = L/W (3-1) where L is the maximum length of MCP, and W is the maximum width of the MCP area. When ECC = 1, the activity space would be considered symmetrical. When ECC > 1, the activity space would be considered more elongate and asy mmetrical (Rechisky and Wetherbee 2003). A measure of site attachment, the linearity index (LI), was also calculated for each shark track (Bell and Kramer 1979; Rech isky and Wetherbee 2003) (3-2): LI = (Fn F1 )/D (3-2) where Fn is the final position of the shark, F1 is the first position of the shark, and D is the total distance traveled by the shark. If LI = 1, the movements of the shark would be considered linear, with little reuse of area within the activity space. A LI near zero suggests site fidelity. To summarize the directionality of obser ved movements, circular histograms were plotted using circular statis tics software (Oriana 2.00, Kov ach Computing Services). Additionally, the vector of angular concentration ( r ) and the circular st andard deviation ( csd ) were calculated for each track (Zar 1984). Values of r range from 0 to 1, where 0 indicates that
66 bearings are uniformly distributed, and 1 indicates that all headi ng are concentrated in the same direction. A doubling of angles procedure was used for diametrically bimodal data to facilitate the calculation of r and csd which could otherwise not be ca lculated (Zar 1984). Rayleighs z test was used to test if r was statistically differe nt from a uniform distribution, therefore implying directional movement (e.g., Klimley et al. 2005). Due to low sample size in some tracks, circular statistics were only estimated for tracks longer th an 10 h. Due to the largely restricted water flow within the IRL, tidal flow was not considered to be a factor in th is study, and therefore was not assumed to influence directionality. Descriptive statistics were used to exam ine patterns of habitat use for the following parameters: depth, water temperature, salinity, DO, and secchi depth. Simple linear correlation analysis was also used to descri be the relationship between bull sh ark activity space and salinity. Bottom substrate type was described qua litatively by visual observations. Results Ten immature bull sharks were manually tracked in the IRL between August 2003 and August 2005 (Table 3-1). All of the sharks we re tracked between the months of March and September. Five of the sharks were YOY (6071 cm FL), and five were juveniles (79-94 cm FL). The duration of tracking ranged from 1.5 to 23 h total for each shark (mean 1 sd = 13.4 8.7 h, N=10), yielding a total of 134 tracking hours for all sharks combined. A total of 242 positions were recorded for YOY sharks, and 243 pos itions were recorded for juvenile sharks. Many of the tracks, however, were performed intermittently in separate tracking periods spanning days to weeks. Characteristics of the patterns of movement of the sharks are summarized in Table 3-2. Due to the low samp le size, and the lack of independence in
67 observations from each individual shark, tests of statistical significance could not be performed to compare data from sets of tracks. Bull Shark Tracks Shark B1 The first bull shark tracked (B1), a YOY fema le (71 cm FL), was captured and tagged on 22 August 2003 at 15:15 hrs in Mosquito Lagoon (F igure 3-1). She was continuously tracked until 02:30 hrs, 23 August, when lightning storms forced us to abandon the track. The shark was relocated at 08:15 hrs, 23 August, and tracked fo r another 5.5 h until 13:45 hrs. Ten days later, on 2 September, the shark was once again relocated at 10:30 hrs in the vici nity of the previous track, and tracked for an additional 5 hours, yiel ding a total of 22.5 h of total tracking time over an 11-day period. Shark B2 Bull shark B2 was captured and tagged on 11 March 2004, in the Indian River just south of the Florida Power and Light (south) power plan t in Frontenac (Figure 3-2). This shark was a juvenile male, measuring 94 cm FL. The sharks tag signal was lost upon release at 15:15 hrs, but relocated at 10:30 hrs, 12 Marc h, directly in front of the po wer plant outfall. A seasonal manatee closure zone surrounding the outfall area prevented us from follo wing the shark in the normal tracking method, but the sharks positions were calculated by r ecording the compass bearing from the boat to the shark, and the sign al strength identified by the acoustic receiver which could be used as a proxy of distance (bas ed on transmitter range tests). The shark was continuously tracked in this manner for 15.5 h, until 02:00 hrs, 13 March. The shark was again relocated at 05:45 hrs, 13 March, and tracked until 13:00 hrs when the signal was lost. Six days later on 19 March, B2 was once ag ain relocated in the same location, and tracked for an additional 2 h from 10:00-12:00 hr s. Subsequently, on 3 April, the transmitter signal was
68 detected back near the tagging location, but wa s immobile, and presumably detached from the shark. This shark was tracked for a total of 23 h over an 8-day period. Shark B3 This juvenile female bull shark, 82 cm FL was captured and ta gged at 16:00 hrs on 7 May 2004 near the outfall of the Reliant (north) powe r plant, in the Indian River near Port St. John. She was tracked continuously for 2 h, until 18:00 hrs when the signal was lost due to deteriorating sea surface conditions (Figure 3-3). The shark was never relocated. Shark B4 Bull shark B4, a 79 cm FL juvenile female was captured and tagged at 14:19 hrs on 10 June 2004, off the mouth of Crane Creek in Melb ourne (Figure 3-4). The transmitter signal was lost almost immediately, but the shark was relo cated at 07:45 hrs the following morning inside Crane Creek (Figure 3-4). The shark was then tracked continuously until midnight, and then again relocated at 08:45 hrs, 12 June. Tracking en ded at 14:00 hrs, 12 June, yielding a total of 18.75 h of tracking over a 48-h period. Shark B5 Bull shark B5 was an 82 cm FL juvenile fe male that was captured at 11:45 hrs, 17 May 2005, inside Crane Creek (Figure 3-5). Upon release, the shark swam out of the creek and into the lagoon where the transmitter signal was lost, a nd could not be immediately relocated. The shark was relocated near its tagging location in th e creek one week later on 24 May, at 09:30 hrs, and tracked continuously for 12.5 h. By 17:45 hrs the shark had moved over 1 km south of the creek, but at approximately 18:00 hrs the shark be gan to make a directed movement northward back toward Crane Creek, which it re-entered at 19:06 hrs. By 19:15 hr s, less than an hour before sunset, the shark was back at its taggi ng location within the creek boat basin, where it remained until the track was broken off at 22:00 hrs. Shark B5 was relocated again the following
69 day at 12:30 hrs, but the track wa s ended at 13:30 hrs. This shar k was tracked for a total of 15 h over an 8-day period. Shark B6 Bull shark B6, an 83 cm FL juvenile female was captured and tagged at 10:45 hrs, 18 May 2005, in Crane Creek (Figure 3-6). She was tracked continuously until 18:00 hrs, when it became too windy to track. The shark was then re located the following day at 08:00 hrs, back near its tagging location in Crane Creek. It wa s tracked for an additional 8 h, and it remained within the creek boat basin until the track ended at 16:00 hrs, 19 May. The shark was therefore tracked for 15.25 h over a 29-h period. Duri ng the 8-h tracking pe riod on 19 May, however, there was very little movement detected, and it is possible that the transmitter had detached from the shark, and was ly ing on the bottom. Shark B7 Bull shark B7 was a 60 cm FL YOY female, tagged on 7 June 2005 at 19:05 hrs in Crane Creek (Figure 3-7). The shark was tracked c ontinuously for 12.25 h, until 07:00 hrs, 8 June, but it is suspected that the shark ei ther shed the tag or died at approximately 22:00 hrs because movement of the shark ceased at this time. Du e to the exceptionally small core areas utilized by these sharks, tracking was continued throughout the night to discern whether or not small movements were occurring. Only the first 3 h of this track are considered to be valid for the purposes of these analyses. Shark B8 Bull shark B8 was a 66 cm FL YOY male, initially captured and tagged at 14:15 hrs, 20 July 2005, south of Crane Creek along the edge of the seagrass bed that runs along the western shore (Figure 3-8). The sharks signal was soon lost due to deteriora ting sea surface conditions at 16:00 hrs. He was relocated the following day, however, at 07:30 hrs, less than 1 km from his
70 tagging location, but further from shore. Th e shark was tracked continuously for 15 h, until 22:30 hrs. Two weeks later, on 4 August 2005, this shark was recaptured on hook and line several hundred meters from its original capture location. The transmitter had been shed, but the rototag remained intact, and the shark appear ed to be in a healthy condition. A second transmitter was attached, and the shark was tracked for an additional 6 h. The shark was tracked for a total of 22.5 h over a 15-day period. Shark B9 Bull shark B9, a 65 cm FL YOY male, was tagged at 11:45 hrs, 23 July 2005, on a seagrass bed south of Crane Creek (Figure 39). The shark was tracked for 4.5 h, until the weather deteriorated and the sign al was lost. It was relocated the following day at 09:15 hrs, approximately 1.5 km southeast of its last position the previous day, and was tracked for another 6 h until 15:15 hrs, yielding a total of 10.5 h of tracking over a 27.5-h period. Shark B10 Bull shark B10 was a 61 cm FL YOY female that was tagged at 11:45 hrs, 2 August 2005, just south of the mouth of Crane Creek (Fig ure 3-10). The shark was tracked for 1 h in extremely shallow water (<0.2 m), before the signal was lost. It was relocated the next day at 10:30 hrs on the eastern side of the lagoon, about 2 km from its last detected position. Position fixes were taken over the next 1.5 h, and it wa s determined that the transmitter signal was immobile, so the shark had e ither shed the tag or died. Shark B11 This YOY male bull shark (60 cm FL) was tagged and monitored by acoustic listening stations (Vemco VR2) placed near the outfalls of each power plant in the northern IRL. The shark was tagged on 5 June 2004, off the Delespine (north) power plant, and was detected at one of the two outfalls on 123 of the subsequent 156 days leading up to 3 November 2004, after
71 which it was no longer detected (Figure 3-11). The shark spent most of its time off the north power plant, but also spent a significant amount of time off the s outh power plant. On several days, the shark was detected at both listening stations which we re approximately 3.4 km apart from each other. During this period the shark also made a single foray to a third listening station approximately 6 km north of Delespine. Activity Space The activity spaces (95% UD) of these bull shar ks during their tracks were relatively small, ranging from 0.02 3.49 km2 (mean = 1.40 1.40 km2) (Table 3-2). For se veral of these tracks, particularly when the sharks sp ent much of their time close to shore, the 95% UD (as calculated by the ArcView 3.2 Animal Movements Extension) overestimates activity space to some degree by including areas of land within the UD area (e.g. Figures 3-5, 3-9). The core area (50% UD) calculations were less affected by this bias. Core area sizes ranged from 0.0001 0.911 km2 (mean = 0.275 0.320 km2), and usually included small areas utilized by multiple bull sharks (tagged and un-tagged individuals). There were notable differences between the sizes of YOY and juvenile bull shark activity spaces. Juve nile sharks had a mean activity space of 0.29 0.41 km2, and YOY sharks had a mean activity space of 2.27 1.36 km2 (Table 3-2). There was also an order of magnitude difference in the size of the core areas between juvenile and YOY sharks. Juveniles had a mean core area size of 0.04 0.07 km2, and YOY sharks had a mean core area size of 0.46 0.35 km2, despite the low number of sharks tracked, which precluded statistical analysis (Table 3-2). The shape of the MCP activity spaces, as de fined by the index of eccentricity (ECC), were >1 for all of the tracked sharks, and ranged from 1.36 3.34 (mean = 1.99 0.69) (Table 3-2). This index shows that the bull shark activity sp aces tended to be asymmetrical, and the space
72 utilized tended to have an oblong shape that pr edominantly ran parallel to the shoreline (e.g., Figure 3-1). This pattern wa s consistent in both YOY and juvenile sharks, and though YOY sharks had higher average ECC values, there wa s no notable difference in ECC between the two age classes (Table 3-2). Horizontal Swimming Behavior Due to the difficulties in estimating the posit ions of shark B2, and the inherent error associated those positional estimates data from this track were ex cluded from this analysis. The mean ROM for each of the remaining 9 bull sh arks tracked in this study ranged from 0.033 0.387 m sec-1 (mean = 0.154 0.107 m sec-1) (Table 3-2). Although it appeared that most YOY bull sharks had a slightly highe r mean ROM than juveniles ( 0.193 0.128 m sec-1, and 0.106 0.059 m sec-1, respectively). There was al so no distinct diel change in ROM detected that would be suggestive of increased nocturnal activity (Figures 3-12 and 3-13). To investigate the possibility of a post-release stress respons e in the tagged sharks, mean ROM from early in a track (0 2 h post-release) were compared to the mean ROM from late in a track (>12 h post-release). The tr acks of four individuals (B1, B 6, B8, B9) had sufficient data to make this comparison (Figure 3-14). In three out of four sharks, the initial post-release ROMs were slower than the ROMs after 12 h of tracking. In a single individu al, the initial ROM was faster (Figure 3-14). Low sample size prohib ited the evaluation of whether or not these differences were statistically significant. The LI for each of these tracks was used as an indicator of site fidelity and home ranging behavior. Overall, the LIs for these sharks we re quite low, ranging fr om 0.01 0.65, indicating a high level of area reuse during thei r tracks. The two tracks with the highest LI values (B3 and B10) were also the two shortest tracks (Table 31), suggesting that the high LI in these tracks
73 was an artifact of low sample size. Had these sh arks been tracked for lo nger periods, it is likely that the LI would have decreased. The mean LI for all tracks was 0.18 0.21 (median = 0.09). The mean LI for YOY sharks was 0.25 0.25, and 0.11 0.15 for juvenile sharks (Table 3-2). As with the size of core areas noted above, the juvenile sharks had lower LI values than YOY sharks, demonstrating that juveniles tend to exhibit a higher leve l of site attachment than do YOY sharks. The directionality of each shar k was examined to determine if the angular orientation of their movements were uniformly distributed, or whether there were nonr andom and directional patterns of movement as they reused their act ivity space (e.g., Klimley et al. 2005). Circular histograms showed that in several cases bull shark movements did appe ar to be nonrandom, though not linear in concentration. For example, sharks B1, B5, and B8 each had equivalent proportions of track segment beari ngs that ran at both northwest a nd southeast headings (Figures 3-1, 3-5, and 3-8). Shark B4 showed a pattern of primarily east and west movements (Figure 34), and shark B9 had a pattern of more north and south movements (Figure 3-9). Values of r ranged from 0.078 (p=0.577) for shark B8, to 0.503 (p <0.0001) for shark B5 (Table 3-2). Rayleighs Test indicated that sh arks B1, B4, B5, and B9 had angular distributions significantly different from uniform (Table 32), suggesting varying degrees of directional movement in these individuals. Habitat Use The bull sharks were found in a broad range of environmental conditi ons with respect to depth, temperature, salinity, DO, secchi depth, and bottom type (Table 3-3). However, some patterns of habitat utilization we re observed that may be sugges tive of some preferences. With regards to depth, the tracked sharks swam in wa ters as shallow as 0.2 m and their dorsal fins
74 often exposed above the surface. Although we c ould not definitively determine the position of the sharks in the water column except by visual observation, they were tracked in areas with water depths of up to 3.9 m, in the deepest portio ns of the ICW channels (Table 3-3). When visual observation of free-swimming sharks was possible (occasionally at depths of up to about 1.5 m), the sharks typically swam just above the bottom. However, they were also occasionally observed to swim at or just beneath the surface when over deeper waters, particularly within Crane Creek. The majority (65%) of positions however, were recorded at depths of less than 2.0 m, with a peak of utilizat ion between 1.0-1.5 m (mean = 1.6 0.5 m) (Figure 3-15a). These depths, however, represent the majority of the la goons overall depth distribution. There did not appear to be any strong differences in the m ean depth utilized by the sharks between day and night, nor between YOY (mean = 1.8 0.5 m) and juvenile (mean = 1.3 0.4 m) sharks. The sharks were tracked in wate r temperatures ranging from 18.5 34.2 C (mean = 28.3 3.2 C) (Table 3-3). However, the sharks spent over 68% of their tracks in waters warmer than 28 C (Figure 3-15b). These temperatures coincide d with the water temperatures that occur during the season of the sharks peak abundance in the IRL du ring the summer and fall (see Chapter 2). The coldest temperatures were reco rded from shark B2, which was tracked in midMarch near a power plant outfall (F igure 3-2). Temperatures clos est to the outfall were as high as 32 C, but the shark was initially captured, and made occasional forays, over a kilometer from the outfall where water temperatures were significan tly colder. It is believed that this juvenile shark was using the power plant outfall area as a thermal refuge throughout the winter months (Snelson et al. 1984). There was no observable difference in temp eratures of habitat utilized between day and night, nor between YOY (mean = 30.9 1.9 C) and juvenile (mean = 27.8 3.6 C) sharks.
75 The immature sharks were tracked in freshwat er creek habitats with salinities as low as 1.2 ppt, and in open lagoon habitats with salinities as high as 31.9 ppt (mean = 19.0 7.7 ppt) (Table 3-3). The salinities utilized by the shar ks showed a bimodal dist ribution, with separate peaks at salinities of 10-15 ppt (32%) and 25-30 ppt (26%) (Figure 3-15c) Peaks in salinity utilization essentially correlate to the time spen t inside or outside of Crane Creek. There was some evidence of diel changes in salinity preference, with some sharks spending daylight hours in more saline lagoon waters, and their nights in the less saline creek habitats (B5, Figure 3-5). This may be a function of either salinity prefer ence, or of other aspects of the creek versus lagoon environments (e.g. depth, forage, refuge). However, this could not be determined conclusively. There was also some evidence of size/age segregation by salinity, with juvenile sharks spending more time in higher salinity waters (mean = 20.7 7.9 ppt) than YOY sharks (mean = 13.7 6.4). The space utilized by the bull sharks tracked near Crane Creek varied between dry periods and wet periods, as measured by the sali nity regimes near Crane Creek (Figures 3-16, 317, 3-18, 3-19). Utilization of th e creek habitats was higher duri ng dryer periods, when the creek salinity was greater than 10 ppt and the open lagoon salinity wa s above 30 ppt. Following rain events, which lowered creek salinities below 10 ppt, and open lagoon salinity to below 20 ppt, the sharks utilized habitats in the open lagoon ad jacent to the creek more often (Figure 3-16). There was definitely some overlap, and use of the full range of salinities by some sharks, but 75% of tracking positions during bo th wet and dry periods were in salinities greater than 11 ppt (Figure 3-18), even though the sp atial distributions were substantially differe nt (Figures 3-16 and 3-17). Although sample size was small (N=7), lin ear correlation analysis revealed an inverse
76 relationship between the size of bull shark activity spaces and the salinity measured in Crane Creek (r2 = 0.820) (Figure 3-19). The movements of the sharks did not appear to be greatly influenced by DO. Though the sharks experienced a DO range of 1.8 8.2 mg/L (mean = 5.6 1.3), 64% of positions were in the 5-8 mg/L range (Figure 3-15d). The lowest DO measurements were recorded from deep channel waters during the night. Water colu mn DO, driven by primary production, naturally oscillates between day and night (Brown et al 1999). Regardless, DO utilization was similar between YOY (mean = 5.1 1.1 mg/L) and juvenile (mean = 6.1 1.5 mg/L) sharks. Water clarity, as measured by secchi depth, does not tend to vary greatly in highlyproductive estuaries such as the IRL (Brown et al. 1999). During their tracks, these sharks experienced waters with secchi depths from 0.7 1.7 m, with a mean of 1.2 0.3 m (Table 3-3, Figure 3-15e). However, water clarity was similar for YOY (mean = 1.8 0.5 m) and juvenile (mean = 1.3 0.4 m) sharks with regards to their secch i depth. Since secchi depth can not be recorded during the night, no comparisons of diel changes relative to water clarity were made. The bull sharks swam over a variety of bottom substrate types during their tracks, including sand, seagrass, mud, and in deep channels Most individual sharks utilized more than one primary substrate type. The sharks tracked near the power plants (B 2, B3) primarily swam over sandy bottoms, which predominate near th ese particular areas. The remainder of observations were made over shallow seagrass beds or the muddy bottoms in dredged channels. Discussion Few studies have examined the movements of elasmobranchs along Floridas east coast. While the seasonal occurrence and diet of bull shar ks has been described for bull sharks in the
77 IRL region of Florida (Snelson et al. 1984) (see Chap ter 2), the present study is the first to use acoustic telemetry on elasmobranchs in the IRL. In addition, it is only th e second study to report both short-term movements and ac tivity space of this apex pred ator (Steiner 2002). The 10 bull sharks that were manually tracked in this st udy displayed variability in their individual movements and behaviors, but th ere were notable patterns among them as well. Since contact with five of the sharks was lost soon after release, and later relocated (see Bull Shark Tracks ), these sharks had presumably recovered from the stress of their capt ure and were behaving normally. In three of four sharks with sufficient comparable data, the ROM of sharks immediately post-was slightly slower than was observed after 12 h of tracking (Figure 3-14), also indicating that the tagging pr ocess did not adversely affect th e sharks in a measurable way. In general, daily activity spaces of the sharks were relatively small, with high levels of area reuse in most tracks. Both juvenile and YOY sh arks occupied a broad range of available environmental parameters in the lagoon (Table 3-3), but their increa sed frequency in some habitats (Figure 3-15) sugge sted evidence of selection for specific habitats. The estimated activity spaces, movements, and ha bitat use of bull sharks in the IRL were similar to those calculated for 11 juvenile bu ll sharks tracked by Steiner (2002) in the Ten Thousand Islands (TTI) estuary off southwest Fl orida, using the similar methods and similar durations (2.5 23.2 h). The TTI estuary is physically different from the IRL, with numerous mangrove-fringed islets divided by channels, sma ll bays, tide-influenced creeks, and rivers running through the system. However, based on observation-area curves of tracking data, Steiner (2002) found that bull shark activity sp ace size did not significantly increase after tracking durations of 9 16 h (mean = 11.6 h). This suggests that this tracking duration was adequate for quantifying juvenile bull shark ac tivity space. Activity spaces quantified using
78 MCP for TTI bull sharks ranged from 0.17 3.59 km2 (mean = 1.26 1.24 km2), compared to 0.11 3.06 km2 (mean = 1.13 1.19 km2) for IRL bull sharks in this study (if sharks tracked for less than 10 h are excluded from the analysis for the sake of comparison, Table 3-1). TTI bull sharks also predominantly showed similar movement patterns, including patrolling parallel to shore, milling about in deep channels, and reusing the same space repeatedly during tracking. In addition, some sharks were actually observed to remain stationary and rest in tidal currents for periods of up to 1.5 h. The orientation of th eir movements was not influenced by tidal flow, however, as has been observed in two othe r carcharhinid species, the blacktip ( Carcharhinus limbatus) and sandbar ( C. plumbeus) sharks (Steiner 2002; Medved and Marshall 1983; Rechisky and Wetherbee 2003). Most of the TTI bu ll sharks utilized similar ranges of depth, temperature, salinity, DO, and water clarity as IRL bull sharks. The movements and activities of the TTI bull sharks were mostly limited to b ackwater areas and river mouths, and hypothesized to be primarily influenced by the distribution of prey (Steiner 2002). Larger individuals, across ma ny animal taxa, typically have larger home ranges than smaller conspecifics (McNab 1963; Kelt and Va n Vuren 2001). Although this observation has not been expressly tested in most sharks, it appears to hold true for some species (Morrissey and Gruber 1993a; Steiner 2002; Heupel et al. 2004 ) and not in other species (Goldman and Anderson 1999; Rechisky and Weth erbee 2003). The observation in the present study that small YOY sharks seem to have higher av erage activity spaces and core ar ea sizes than larger juveniles is therefore more similar to these latter studies, although more data may be needed to fully support this pattern. Contrary to my results, juvenile and YOY bull sharks tracked in the TTI estuary, showed a pattern of MCP area increasing with shark leng th (Steiner 2002). Juvenile lemon sharks
79 ( Negaprion brevirostris ) tracked in the Bahamas also s howed a positive correlation between body size and home range size, utilizing larger portions of their lagoon nur sery as they grew (Morrissey and Gruber 1993). Heupel et al. (2004) used passiv e acoustic monitoring to show that YOY blacktip sharks expanded their home range s during their first months of life in their natal nursery areas. Following parturition in early summer, blacktip shark home ranges were restricted to a very small portion of the study site in Tampa Bay. As the summer progressed, all of the tagged sharks rapidly e xpanded their activities throughout the study site. There was no significant difference in activity space detected between neonat e and juvenile sandbar sharks tracked in their Delaware Bay summer nursery (Rechisky and Wetherbee 2003). One of the only other shark spec ies reported to show the patt ern of larger sharks having smaller activity spaces is the white shark ( Carcharodon carcharias), tracked off the Farallon Islands, California by Goldman and Anderson (1 999). Large adult and subadult white sharks seasonally aggregate at this site to hunt pinnipeds. They suggested that smaller, inexperienced white sharks had not yet learned the most successf ul feeding locations or hunting strategies, and therefore roamed over broad areas in search of prey. The larger sh arks were more familiar with the terrain, and limited their space utilization to areas where they had experienced higher predation success during previous seasons. This c ould also be the case with bull sharks in the IRL. Older, larger, juvenile bull sharks may limit their activities to discrete areas where they have learned to feed successfully, while neonate bull sharks are more nave, and have not yet learned the most suitable feeding sites or strategi es. Also, since larger juvenile bull sharks are known predators of YOY bull sharks (Snelson et al. 1984), the smaller YOY sharks may actively avoid locations with high densities of juven iles (as observed by Simpfe ndorfer et al. 2005), and be forced to conduct their activities over broade r areas. Competitive ex clusion by juvenile bull
80 sharks may occur in the IRL, however, it was not detected by the methods applied in this study. Habitat selection may also play a role in this pa ttern for bull sharks in the IRL, since salinity had an influence activity space (Figur es 3-17 and 3-19). It should be noted that these observations likely only hold true for white sharks and bull shar ks when they are seasonally found at the sites where they were tracked. Juvenile and adult white sharks are known to make long-distance, oceanic migrations during specific times of the year (Weng et al 2007). I speculate that bull sharks migrate south and out of lagoon waters du ring winter months (see Chapter 2), where their behaviors may differ appreciably. The overall activity space size range of 0.05 3.49 km2 (mean = 1.40 1.40 km2) for IRL bull sharks is comparable to that reported for daily activity spaces and home ranges of other carcharhiniform shark species tracked in nursery areas. Juvenile lemon sharks tracked in the Bahamas had home ranges of 0.23 1.26 km2 (Morrissey and Gruber 1993 a), juvenile scalloped hammerhead sharks ( Sphyrna lewini ) tracked in Hawaii had ho me ranges of 0.46 3.52 km2 (Holland et al. 1993), and juvenile blacktip sharks tracked off the we st coast of Florida had daily activity spaces of 0.28 6.61 km2 (Steiner 2002) and 0.019 13.0 km2 (Heupel et al. 2004). In contrast, YOY and juvenile sa ndbar and bonnethead sharks ( S. tiburo) tended to have larger activity spaces (Rechisky and Wetherbee 2003; Heupel et al. 2006). Immature sandbar sharks tracked in Delaware Bay were reported to have daily activity spaces as high as 315.4 km2 (mean = 62.4 km2), while bonnethead sharks tracked in Ch arlotte Harbor, Florida had daily activity spaces as high as 74.41 km2 (mean = 8.31 km2) (Rechisky and Wetherb ee 2003; Heupel et al. 2006). These interspecific variations (and similar ities) in activity space could be influenced by a number of biological and physical factors that require further i nvestigation. Such studies may help to shed further light on how sharks sele ct habitats within th eir nursery areas.
81 The distribution of prey species may have also influenced the movements of these sharks during their tracks. Although pr ey distribution was not quantif ied, presence of known primary prey species (mullet, catfishes, stingrays) wa s noted when observed. When directionality histograms are overlaid on each plotted shark track, it can be clearly observed that the diametrically bimodal distribution of bearings in some of the sh ark tracks can be attributed to their behavior of predominantly swimming back-andforth parallel to the ad jacent shoreline (e.g., Figures 3-1, 3-4, 3-5). This swimming pattern is indicative of a patrol ling-style hunting strategy (Morrissey and Gruber 1993a; Klimle y et al. 2001). In addition, dur ing some tracks, the sharks appeared to exhibit foraging be havior consistent with observe d foraging behaviors of untagged sharks. Both in Crane Creek and on nearby seag rass beds, young bull sharks were seen chasing schooling mullet, which were very dense in the area at times. Bull sharks were observed on a number of instances to actually breach clear of the water in pursuit. Although no sharks were visually observed feeding on catfishes or stingray s, both known prey items (Snelson et al. 1984), they were abundant in the study ar ea (based on catch data and dire ct observations), and may have influenced the use of deeper habitats freque nted by these species (Snelson et al. 1989). The tradeoff between predator avoidance and prey distribution (i.e., energy intake) is thought to be a major biotic influence on shark ha bitat selection in nurse ry areas (Branstetter 1990; Heithaus 2007), although this con cept has been difficult to test in the field (Heupel et al. 2007). The use of shallow habitats by sandbar sh arks in Delaware Bay was postulated to be correlated to predator avoidan ce, distribution of preferred pr ey, avoidance of strong tidal currents, or a combination of those factors (Rechisky and Wetherbee 2003). Holland et al. (1993) showed that juvenile scalloped hammerhead sharks had rhythmic di el patterns of activity in which they utilized small core areas during the day, and much broader areas during the night,
82 a pattern that was considered to be influenced by predator avoidance. Heupel and Hueter (2002) demonstrated that juvenile blac ktip shark habitat use was not co rrelated to prey distribution, and was therefore hypothesized to be influenced mo re by predator avoidance. In Floridas Caloosahatchee River estuary, YOY bull sharks were spatially segregated from juveniles, and were more abundant in low salin ity, riverine habitats than th eir larger conspecifics, which occupied the adjacent Pine Island Sound (Simpfendor fer et al. 2005). This size segregation was believed to be related to predator av oidance behavior of the YOY sharks. At these sites, young sharks and their potenti al predators (i.e. la rger sharks) occupy adjacent or overlapping habitats. Immature bull sh arks in the IRL, however, are effectively free from predation risk since adult bull and lemon sharks, the only documented juvenile shark predators known to occur with in the lagoon, are exceptionally ra re (Snelson and Williams 1981). Although YOY bull sharks have been cannibalized by larger juvenile bull sharks, this does not appear to be a frequent occurrence (Snelson et al. 1984). The only other potential predators of YOY and juvenile bull sharks in the IRL are American alligators ( Alligator mississippiensis ), which I observed to be abundant along certain sh orelines adjacent to low salinity creeks, and occasionally seen in the open lagoon in salinities as high as 25 ppt, particularly around Merritt Island. Alligators, however, have not been documen ted to prey on sharks in Florida intracoastal waters, and generally seem to pr efer to feed on smaller teleosts (Rice 2004; Rice et al. 2007). However, other crocodilians have been documented to prey on small sharks (Whitfield and Blaber 1979), so the possibility do es exist in the IRL. It should be noted that in this study, few sharks were captured or tracked where there were particularly high densities of alligators (e.g. Banana Creek, Gator Creek, see Fi gure 2-2), although lone alligato rs were occasionally sighted during some of the shark tracks in Crane Creek. Nevertheless, predation pressures do not appear
83 to significantly impact young bull sharks in the IRL, so their movements and habitat use are more likely related to the distribution of their pr eferred prey items. Indeed, some bull sharks had activity spaces in whic h known prey were visibly dense, a nd sharks were observed feeding within these areas. Their observed patrolling beha vior is certainly consis tent with the hunting strategies employed by other sharks, including lemon sharks (Morrisse y and Gruber 1993) and white sharks (Klimley et al. 2001). Additiona lly, bull sharks commonly utilized prey-rich seagrass habitats, which have been document ed to support 54% of the IRLs ichthyofaunal diversity (Gilmore 1995). Further research and standardized experi mentation are needed to more accurately define the importance of these factors in the habitat selection of bull sharks in the IRL, which appears to be a low predation-risk environment. This unique feature may provide benefits to the sharks through increased growth and survival, as compared to areas where predation risks would be greater. The abiotic habitat features monitored duri ng the tracking of these sharks included water temperature, salinity, DO, depth, and secchi depth (Table 3-3, Figure 3-15). The importance of temperature in the distribution and movements of elasmobranchs has been described in several studies (e.g. Matern et al. 2000; Grubbs and Musick 2002; Simpfendorfer et al. 2005), and is generally thought to influence distribution at a broad scale; i.e., w ithin the physiological tolerances of the species in question. Since water temperatures below 10 C can be lethal to small bull sharks (Dodrill 1977; Snelson and Brad ley 1978), bull sharks likely migrate out of cooler northern IRL waters to warmer offshor e and southern waters during the winter (see Chapter 2). Even though bull sharks were tracked in temperatures as low as 18.5 C in this study, most activities were observed in temperatures greater than 28 C, and as high as 34.2 C (Figure 3-15b). This is consis tent with findings from other bul l shark habitat studies (Michel
84 2002; Simpfendorfer et al. 2005; Blackburn et al. 2007), and is also reflected in the predominantly tropical distribution of th is species around the world (Compagno 1984). The euryhaline tolerance of bull sharks has b een previously documented and investigated (e.g. Thorson 1972; Thorson et al. 1973; Pillans et al. 2005), and is further supported by this study. The broad range of salinitie s utilized by the bull sharks in the IRL (1.2 31.9 ppt) is also consistent with results from other nursery area studies (e.g. Simpfendorfer et al. 2005; Blackburn et al. 2007; Chapter 2). Since bull sharks have well known euryhaline habits and broad salinity tolerances, one may not expect ther e to be distinct preferences in relation to salinity. However, the overall trend implies that the bull sharks near Crane Creek were mostly selecting habitats with salinities > 11 ppt (Figure 3-18), even when lower salinity habitats were available to them (Figure 3-16). If these young sharks can physio logically tolerate freshwat er, why do they appear to preferentially avoid it (Figure 3-19)? Simpfendorfer et al. (2005) found that YOY and juvenile bull sharks in the Caloosahatchee River estuary segregate themselves by salinity, similar to the pattern observed in this study (T able 3-3). They observed th at YOY sharks preferred more brackish habitats with salinities between 7 and 17.5 ppt. In contrast, juve nile sharks preferred higher salinities, and the habita ts of adjacent San Carlos Ba y and Pine Island Sound. This segregation was speculated to re duce intraspecific cannibalism a nd predation by larger sharks on the YOY bull sharks. As a result, lower salinity river habitats provided a refuge for the youngest sharks in the population. However, the YOY shar ks still appeared to a void salinities below 7 ppt. For the IRL, if predator avoidance can be ruled out as discussed above, then few other explanations for this pattern remain. One possibi lity is that reduced salinities only indirectly
85 affect bull shark movements, and their distribut ion shift may be mediated by the movements of their prey, which directly respond to environmental changes. There are numerous euryhaline fishes that occur in the IRL (Gilmore 1977; 1995) many of which are documented prey of bull sharks (Snelson et al. 1984). Salinity has been shown to be a signifi cant factor in the distribution and species associations of these fishes (Kups chus and Tremain 2001; Pa perno et al. 2006), and as these fish redistribute themselves following a rain event, the bull sharks may follow. Some qualitative observations support this explanati on. Multiple untagged and tagged sharks (tracks B4, B5, B6, and Figs. 3.4, 3.5, 3.6, respectively) we re observed feeding on mullet, which shoaled in large numbers in Crane Creek during periods of low precipitation. When sharks were tracked during wet periods (Figs. 3.7, 3.8, 3.9, 3.10), mullet were visibly much less dense in Crane Creek, and more abundant in the open lagoon over seagrass beds. If mullet were indeed the major dietary component of bull sharks during this time, and/or other key prey species followed the same distribution shift (e.g. catfish), then it would make sense for the bull sharks to redistribute themselves in the lagoon accordingly. More detailed diet ary analysis and prey distribution monitoring will be needed to adequately determine if these interactions truly exist. An alternative explanation is that bull sharks directly respond to sa linity changes because the sudden drop in salinity following a precip itation event disrupts homeostasis, possibly resulting in short-term, extrane ous energetic costs. These costs (or homeostatic imbalances) may prompt individual sharks to seek out the salinit y in which they were previously acclimated to, rather than linger and acclimate over time to th e new medium. This possi bility was proposed by Simpfendorfer et al. (2005) as a nother alternative to explain bull sharks avoidance of extremely low salinities (< 7 ppt) in the Ca loosahatchee River. They cited salinity selection experiments on other fish species, such as the killifish ( Fundulus heteroclitus ), that showed that even though
86 killifish can tolerate a broad range of salinity, th ey repeatedly selected waters with salinity closest to their ow n cellular osmolarity (10 ppt) (Kidder 1997; Kidder et al. 2006). Kidder et al. (2006) hypothesized that euryhaline fishes may minimize their osmotic energy demand by selecting waters that are is otonic with their own body fluids. Even though elasmobranchs osmoregulate differently than bony fishes (E vans et al. 2004; Hamm erschlag 2006), this behavioral osmoregulation could explain the pa ttern observed in IRL bull sharks. If YOY bull sharks select habitats that minimize the energetic costs for osmoregulating and maintaining homeostasis, more energy could be devoted to growth, thereby increasing their survival. Even though Crane Creek may be a preferred habitat becau se of its refuge and forage benefits, the acute salinity drops observed during this study co uld cause enough of an i onic imbalance in the sharks to influence them to move to the open lagoon. In the open lagoon, prey items would not be as spatially concentrated as they were in the creek, hence activity space (i.e., the foraging arena) is much larger. The physiological (i.e., histological, molecular) re sponses of euryhaline elasmobranchs to reduced salinity have been examined in several studies (e.g. Oguri 1964; Thorson et al. 1973; Piermarini and Evans 1998; P illans et al. 2005). As stated by Simpfendorfer et al. (2005), future research should focus on i nvestigating the potential energetic costs of osmoregulation and acclimation to varying salin ities. Acute responses as well as chronic acclimation should be addressed, even though such responses may be difficult to quantify given the complexities of elasmobranch osmoregulation (Evans et al. 2004). Power plant outfall areas in the IRL appear to be heavily utilized by young bull sharks. This is based on observations and catch rates in this, and previous studies (Snelson et al. 1984; Chapter 2), and is also supported by the movements of the bull sharks that were actively tracked in these vicinities. Bull sharks B2 and B3 both utilized core areas directly in front of outfalls for
87 periods of 2 to 23 h (Figures 3-2 and 3-3). This site attachment behavior was not only limited to short-term periods, however. Shark B11 heavily utilized these areas during summer and fall 2004 (Figure 3-11). Based on anecdotal informati on, power plant outfall areas located further south in the IRL are also regularly utilized by bull sharks. The incr eased density of bull sharks at these outfall areas makes them particularly su sceptible to capture, especially during winter months when they appear to use the outfalls as a thermal refuge. These ar eas are also utilized by a variety of other lagoon speci es during the winter, including manatees (Laist and Reynolds 2005), stingrays ( Dasyatis sabina and D. say ), spotted eagle rays (Aetobatis narinari ), catfish ( Bagre marinus and Arius felis ), tarpon ( Megalops atlanticus ), ladyfish ( Elops saurus ), and other teleosts and invertebrates (Curti s, unpubl. data). Daily activity patterns, predator-prey dynamics, and other interspecific interactio ns in these confined outfall areas may be dramatically different during cold months, and warrant further investigation. These outfall areas should be priorities for protection to aid in the conservation of the threatened and endangered species that rely on th em during winter months. Indeed, some of the power plant outfall areas in the IRL are seasonally closed to boat access and fishing to protect vulnerable manatee aggregations creating de facto marine reserves for the sharks and other species that occur within those areas. The anthropogenic impacts of such sites on the health of lagoon sharks and other species should also be assessed. Bull sharks in the IRL and elsewhere have been shown to bioaccumulate high levels of contaminants such as mercury, polybrominated diphenyl ethers (PBDEs), and polychlorinated biphenyls (PCBs) (Adams and McMichael 1999; Johnson-Restrepo et al. 2005), as well as num erous human pharmaceuticals (Gelsleichter and Szabo 2007). The effects of these compounds on the physiology of the sharks are largely unknown. Johnson-Restrepo et al. (2 005) calculated that the concen trations of PBDEs and PCBs
88 in bull shark tissues increased exponentially between 1993 and 2004, indicating an alarming rate of increase in contamination levels of the IRL fo od web. Juvenile bull sharks are particularly at risk of accumulating these toxic chemicals due to th eir intracoastal distribution and their role as apex predators in the lagoon. Subsequently, this may also put humans at risk, since humans occasionally consume IRL bull sharks (Curtis, un publ. observation). Further investigations are needed to more clearly describe the impacts of these contaminants on the IRL food web. The site fidelity of juvenile bull sharks to altered habitats such as power plant outfalls and heavilytrafficked creeks exposes them to a variety of potentially harmful wastewater pollutants, which could have far-reaching effects on their survival and population recovery.
89 Table 3-1. Details of ten bull sharks tracked in the IRL between 2003 and 2005. Shark No. FL (cm) Sex YOY/JuvStart Date Hours TrackedPositions Intermittent? B1 71 F Y 8/22/2003 22.50 89 Y B2 94 M J 3/11/2004 23.00 102 Y B3 82 F J 5/7/2004 2.00 8 N B4 79 F J 6/10/2004 18.75 63 Y B5 82 F J 5/17/2005 15.00 45 Y B6 83 F J 5/18/2005 15.25 25 Y B7 60 F Y 6/7/2005 3.00 12 N B8 66 M Y 7/20/2005 22.50 90 Y B9 65 M Y 7/23/2005 10.50 40 N B10 61 F Y 8/2/2005 1.50 11 Y
90 Table 3-2. Summary of moveme nt and activity space parameters estimated for ten bull sharks tracked in the IRL. Shark Total Dist. ROM MCP 95% UD50% UDLI ECC r csd Rayleigh No. (km) (m/s) (sq. km)(sq. km)(sq. km) () p-value B1 30.95 0.387 3.06 3.492 0.566 0.02 1.73 0.295 89.5 0.0004 B2 11.79 n/a 0.40 0.280 0.020 0.05 1.57 n/a n/a n/a B3 1.11 0.154 0.03 0.104 0.018 0.37 1.53 n/a n/a n/a B4 6.25 0.084 0.18 0.078 0.011 0.01 1.71 0.240 96.8 0.021 B5 8.10 0.154 0.42 1.011 0.161 0.09 2.13 0.503 67.2 <0.0001 B6 2.11 0.033 0.11 0.051 0.008 0.01 1.69 0.215 100.40.25 B7 0.38 0.050 0.01 0.020 0.0001 0.18 1.36 n/a n/a n/a B8 18.58 0.229 2.44 2.341 0.254 0.08 1.72 0.078 129.40.577 B9 7.70 0.178 1.33 3.161 0.911 0.30 3.14 0.275 92.1 0.048 B10 2.79 0.119 0.39 2.360 0.550 0.65 3.34 n/a n/a n/a Mean 8.66 0.154 0.837 1.402 0.275 0.1771.992 sd 10.03 0.107 1.086 1.403 0.320 0.2080.688
91Table 3-3. Environmental paramete rs observed during the tracks of te n bull sharks in the IRL. Temperature (C) Salinity (ppt) DO (mg/L) Depth (m) Secchi Depth (m) Bottom Substrate Shark No. Mean Min Max Mean MinMaxMeanMinMaxMeanMinMax MeanMinMax B1 29.8 29.5 30.0 24.9 22.027.56.2 5.6 6.9 1.4 0.6 2.1 1.0 1.0 1.0 seagrass, mud B2 21.4 18.5 32.2 28.2 27.529.17.2 5.5 8.1 1.3 0.7 3.0 2.0 2.0 2.0 sand B3 28.3 28.1 28.5 28.3 126.96.36.199 7.8 8.2 0.9 0.6 1.2 1.0 1.0 1.0 sand B4 30.1 27.5 33.5 21.7 7.4 31.94.8 1.8 7.6 2.0 0.4 3.9 0.9 0.8 1.0 creek/seagrass B5 30.1 28.3 31.6 14.8 8.9 17.55.4 3.0 6.0 1.3 0.3 3.2 1.5 1.5 1.5 creek/seagrass B6 28.9 26.3 30.6 10.7 5.5 13.84.9 3.4 5.8 1.1 0.3 3.1 1.1 0.7 1.3 creek/seagrass B7 28.3 27.3 30.0 9.0 1.2 17.23.3 2.0 4.3 2.3 0.9 3.5 1.0 1.0 1.0 creek B8 32.7 30.4 33.6 11.3 9.4 12.45.9 5.1 7.1 2.2 0.4 3.6 1.4 1.1 1.7 seagrass/ICW B9 32.5 31.7 34.2 11.0 10.611.25.2 3.9 7.2 1.8 0.2 3.0 1.2 1.0 1.4 seagrass/ICW B10 31.2 31.0 31.3 12.1 12.012.24.8 4.6 4.9 1.3 0.2 3.0 1.0 1.0 1.0 seagrass, mud TOTAL 28.3 18.5 34.2 19.0 1.2 31.95.6 1.8 8.2 1.6 0.2 3.9 1.2 0.7 1.7
92 Figure 3-1. Manual acoustic tr ack of bull shark B1, a 71 cm FL female, in Mosquito Lagoon between 22 August and 2 September, 2003. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histog ram, the outer edge of the circle represents 15 observations. 1. Tagged 8/22/03 15:15 hrs 4. End 8/23/03 13:45 hrs 5. Relocated 9/2/03 1 0 : 35 hr s 6. End 9/2/03 15:30 hrs Mosquito Lagoon Indian River 3. 8/23/03 12:00 hrs 0 90 180 270 1 m 2 mB1 2. 8/23/03 00:30 hrs
93 Figure 3-2. Manual acoustic trac k of bull shark B2, a 94 cm FL male, in the IRL between 11 March and 3 April, 2004. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. Power Plant Indian River 1.Tagged/End 3/11/04 15:30 hrs 7. Relocated/ Tag Dropped? 4/3/04 11:30 hrs Outfall 1 m 2 mB2 2. Relocated 3/12/04 10:30 3. 3/12/04 15:45 hrs 6. End 3/19/04 14:00 4. End 3/13/04 5. Relocated 3/19/04 10:00
94 Figure 3-3. Manual acoustic trac k of bull shark B3, a 82 cm FL female, in the IRL on 7 May, 2004. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions re presents the 95% KUD. Power Plant Indian River 1. Tagged 5/7/04 16:00 hrs 2. End 5/7/04 18:00 hrs Outfall 1 m 2 mB3
95 Figure 3-4. Manual acoustic trac k of bull shark B4, a 79 cm FL female, in the IRL between 10 and 12 June, 2004. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 15 observations. Indian River 1. Tagged/End 6/10/04 14:19 hrs Crane Creek 2. Relocated 6/11/04 07:45 6. End 6/12/04 14:00 hrs 3. 6/11/04 18:15 hrs 5. 6/12/04 08:45 hrs 4. 6/12/04 00:00 hrs 0 90 180 270 1 m 2 mB4
96 Figure 3-5. Manual acoustic trac k of bull shark B5, a 82 cm FL female, in the IRL between 17 and 25 May, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 15 observations. Indian River Crane Creek 1 m 2 m 1 m 2 m 0 90 180 270 B5 3. Relocated 5/24/05 09:30 4. 5/24/05 10:30 hrs 5. 5/24/05 13:00 hrs 6. 5/24/05 17:45 hrs 7. 5/24/05 18:45 hrs 8. 5/24/05 19:15 hrs to End 22:00 hrs 10. End 5/25/05 13:30 hrs 2. End 5/17/05 12:00 hrs 1. Tagged 5/17/05 11:45 hrs 9. Relocated 5/25/05 12:30
97 Figure 3-6. Manual acoustic trac k of bull shark B6, a 83 cm FL female, in the IRL between 18 and 19 May, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 15 observations. Indian River Crane Creek 1 m 2 m 0 90 180 270 B6 1. Tagged 5/18/05 10:45 hrs 3. End 5/18/05 18:00 hrs 4. Relocated 5/19/05 08:00 5. End 5/19/05 16:00 hrs 2. 5/18/05 11:15 hrs
98 Figure 3-7. Manual acoustic trac k of bull shark B7, a 60 cm FL female, in the IRL between 7 and 8 June, 2005. Points represent 15-min tracking positions. A couple positions appear to overlap land because of the coarse resolution of the GIS coastline data at this scale. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. Indian River Crane Creek 1 m 2 mB7 1. Tagged 6/7/05 19:05 hrs 2. End/Tag Dropped? 6/8/05 01:15 07:00 hrs
99 B8 Figure 3-8. Manual acoustic trac k of bull shark B8, a 66 cm FL male, in the IRL between 20 July and 4 August, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track pos itions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle repres ents 15 observations. Indian River Crane Creek 1 m 2 m 0 90 180 270 B8 1 m 2 m 1. Tagged 7/20/05 14:15 hrs 2. End 7/20/05 15:45 hrs 5. Relocated 8/4/05 10:30 6. End 8/4/05 16:30 hrs 3. Relocated 7/21/05 07:30 4. End 7/21/05 22:30 hrs
100 Figure 3-9. Manual acoustic trac k of bull shark B9, a 65 cm FL male, in the IRL between 23 and 24 July, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. In the inset directionality histogram, the outer edge of the circle represents 10 observations. Indian River Turkey Creek 1 m 2 m B9 0 90 180 270 1 m 2 m 1. Tagged 7/23/05 11:45 hrs 3. Relocated 7/24/05 09:15 2. End 7/23/05 16:00 hrs 4. End 7/24/05 15:15 hrs
101 Figure 3-10. Manual acoustic trac k of bull shark B10, a 61 cm FL female, in the IRL between 2 and 3 August, 2005. Points represent 15-min tracking positions. The dashed lines represent 1 m depth contours, and the lightly stippled area represents seagrass beds. The gray line surrounding the track positions represents the 95% KUD. Indian River 1 m 2 m Crane Creek B10 1 m 2 m 1. Tagged 8/2/05 11:45 hrs 3. Relocated 8/3/05 10:30 2. End 8/2/05 12:45 hrs 4. End 8/3/05 12:15 hrs
102 Date 6 / 1 4/20 0 4 6 / 2 8/20 0 4 7 / 1 2/20 0 4 7 / 2 6/20 0 4 8 / 9 / 2 00 4 8 / 2 3/20 0 4 9 / 6 / 2 00 4 9 / 2 0/20 0 4 1 0/4/20 0 4 1 0/18 / 2 0 04 1 1/1/20 0 4 1 1/15 / 2 0 04 1 1/29 / 2 0 04Power Plant 1 2 Figure 3-11. Site fidelity (days detected) of an acoustically tagged YOY bull shark (B11) at two power plants in the northern IRL during the summer and fall of 2004. Power plant 1 is the Florida Power and Light plant in Frontenac, FL, and power plant 2 is the Reliant Energy plant in Delespine, FL. Th e distance between the power plant outfalls is 3.4 km.
103 Figure 3-12. Scatter plot of RO M calculations versus the time of day for nine tracked bull sharks (B2 excluded due to positional error) in the IR L. The vertical dashed lines indicate the median times of sunrise a nd sunset across all tracks.
104 Figure 3-13. Box plots of ROM calculations comp aring day and night observations to examine potential diel activity patterns. The box a nd whiskers represent (from bottom to top) the 10th, 25th, 50th, 75th, and 90th percentiles of observati ons. The square symbol represents the mean.
105 Figure 3-14. Comparison of rates-of-movement (mean 1 SE) obtained from ultrasonic tracking of four juvenile bull sharks captured in Indian River Lagoon, FL in the first 2 hours following release and after tw elve hours post-release.
106 Figure 3-15. Environmental parameters observed during tracks of ten bull sharks in the IRL, including (a) depth, (b) temp erature, (c) salinity, (d) di ssolved oxygen concentration, and (e) secchi depth.
107 Figure 3-15. Continued e
108 Figure 3-16. Tracking positions for seven bull sharks tracked near Crane Creek in the IRL during dry (brown positions, N=3) and wet (blue positions, N=4) periods, as defined by the surface salinity at the mouth of Crane Creek. Indian River Crane Creek Atlantic Ocean Turkey Creek Melbourne
109 Figure 3-17. Cumulative 95% UDs for seven bull sharks tracked near Crane Creek in the IRL during dry (brown lines, N=3) and wet (blu e lines, N=4) periods, as defined by the surface salinity at the mouth of Crane Creek (><10 ppt). Note the sharks high site fidelity to the creek during dry periods. Indian River Crane Creek Atlantic Ocean Turkey Creek Melbourne
110 Figure 3-18. Box plots comparing the salinity utilization of seven bull sharks tracked near Crane Creek in the IRL during dry (N=3) and wet (N=4) periods, as defined by the surface salinity at the mouth of Cran e Creek. Note that the 25th percentiles of observations are nearly equivalent at approximately 11 ppt.
111 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 02468101214161820Salinity (ppt)Activity Space (sq. km) Figure 3-19. Linear correlation between bull sh ark activity space and salinity at the mouth of Crane Creek (N=6). Indicates an outli er (B7) which was not included in the regression. r2 = 0.820 *
112 CHAPTER 4 CONCLUSIONS AND APPLICATIONS This study utilized two primary methods to investigate bull shark distribution and habitat use in the IRL, and provided evidence for its ro le as a nursery area for this species. Fisheryindependent sampling data were compiled and synt hesized to provide insi ghts into patterns of seasonal occurrence, spatial distribution, and ha bitat associations. Th ese data provided a comprehensive, but coarse, overview of bull shark ecology in the study site over a span of 30 years, based on data collected from 390 indi vidual sharks. Tagging and acoustic telemetry methods were also employed to acquire more fi ne scale information on shark movements, daily activities, and habitat ut ilization. A total of 50 sharks were marked with conventional tags, with four fish recaptured over the course of the study. Eleven of these sharks were additionally tagged with acoustic pingers, ten of which were manually tracked and one of which was monitored by moored listening stations (Vemco VR2). The manua l tracking data provided finescale information on the patterns of movements of a small number of individuals. Integration of multiple methodologies provided a more complete pi cture of habitat use by this important apex predator the IRL. These results may prove usef ul to the continued management and conservation of bull shark stocks in the northwest Atlantic. Bull Shark Ecology in the Indian River Lagoon The IRL, a shallow, productive estuarine syst em, serves as a nursery area for bull sharks. All size classes of immature sharks are pr esent in the system, including neonates, YOY, young and older juveniles, and maturi ng sub-adults. In addition, the only adults reported from the system have been gravid females that arrive in the lagoon in the late spring for parturition. The immature sharks appear to u tilize the lagoon until approximately 9 years of age when they
113 transition to offshore adult habita ts. Bull sharks occur year round in the southern reaches of the study site, but appear to migrat e out of the northernmost portions during winter months when temperatures drop below approximately 20 C. As noted by Snelson et al. (1984), some bull sharks remained near heated power plant outfalls during winter months and appear to use these areas as thermal refugia. The sharks were ge nerally more abundant in the system during spring, summer, and autumn. During this time they fo rage throughout the lago on in shallow seagrass and sandy habitats, as well as in low salinity cree ks, on various species of fish (Snelson et al. 1984). Given their size and broad dietary hab its, juvenile bull shar ks are among the lagoons apex predators, and likely have an important func tion in maintaining the health of the ecosystem. The short term movements and daily activities of YOY and juve nile bull sharks appear to be limited to comparatively small activity spaces. The sharks tend to show relatively high levels of area reuse and site attachment to areas such as power plant outfalls a nd freshwater creeks. These areas are presumably used either for foragi ng activities or as refugi a from predators (i.e. larger bull sharks). Overall habitat use by bull sharks was broad, but th ere was more frequent use of depths between 1 and 2 m, temperatur es of 28 34 C, salini ties of 10 25 ppt, DO concentrations of 4 7 mg/L, and water clarity le vels of 0.8 1.4 m. Salinity appears to play an important role in the distribut ion and activity spaces of YOY and juvenile bull sharks. Youngof-the-year sharks tended to uti lize lower mean salinity areas than juveniles, creating a level of size/age segregation in the populat ion. The activity spaces of shar ks were also notably larger during wet periods than dry peri ods in the vicinity of Cran e Creek, supporting evidence of selection for low salinity environm ents in the lagoon. The mechanisms that drive these selection patterns require further investigation. These findi ngs are largely c onsistent with the results of
114 other recent investigations into bull shark nurse ry areas (Simpfendorfer et al. 2005; Wiley and Simpfendorfer 2007; McCandless et al. 2007). Applications to Shark Management and Conservation The concept of essential fish habitat (EFH) has driven much of the recent research into shark nurseries in U.S. waters (McCandless et al. 2002; 2007). The delineation, description, and conservation of such areas are necessary componen ts of federal fishery management plans, and this study can be applied to th e body of EFH information for bull sharks. The findings of the present study suggests that for most of the year the IRL as a whole func tions as a nursery area for this species, in the sense of Heupel et al. (2007). However, there are specific areas within the system that are candidates to be prioritized for protection: 1) The sout hern portion of Mosquito Lagoon, 2) the outfall areas of the Delespine (Re liant Energy) and Frontenac (Florida Power and Light) power plants, 3) Eau Gallie, Crane, and Turkey Creeks, and their adjacent shorelines in Melbourne, and 4) Sebastian Inle t. These areas had the highes t catch rates of immature bull sharks and include important sites for parturiti on, foraging, refuge, and interchange with oceanic habitats for the sharks. Such locations may be critical to the continued survival of IRL bull sharks. Should the stock status of bull sharks require greater protection of EFH, these areas could be designated as Habitat Ar eas of Particular Concern. Give n the dramatic rate of human development along Floridas Atlant ic coast (e.g. Gilmore 1995), the as sociated habitat alterations may presently be impacting sharks and other lag oon species in a detrimental manner. Given the close relationship between spawning stock and recruitment in many elasmobranchs (Hoenig and Gruber 1990; Cortes 2002), protection of juven ile portions of the populat ion will tend to have direct, positive impacts on the rebuilding of depleted stocks.
115 Recommendations for Future Research This research has expanded our understanding of the behavioral ecology of bull sharks in the IRL, but many important questions remain to be answered. Continued research efforts on bull sharks in this region will further benefit the species and its habitat. Before a more complete understanding of the bull sharks ecology in the IRL, and elsewher e, can be attained, this study identified several significant research questions that must be addressed. These include further investigations into abundance, movements, diet, habitat selection, and physiology of bull sharks in the IRL. Given the relatively low CPUE of bull sharks in much of the northern IRL (see Chapter 2), future focused studies may be mo re successful if centere d in the Melbourne Sebastian region and further south. These should include sampling in the southern IRL between Sebastian and Jupiter Inlets to investigate the seasonal distributi on and habitat use of bull sharks in this region, from which little data is currently available. Further ultrasonic tagging a nd tracking efforts, using both active and passive methods, will provide a great deal of valuable inform ation on IRL bull sharks. Concurrent passive acoustic tracking studies of multiple species will also reveal new insights into predatory-prey dynamics and the complexity of how large consumer s partition their habitats and activities in the lagoon. Acoustic tracking of bull sharks will al so help answer questions on their seasonal occurrence, site fidelity, home ra nges, and habitat selection patterns. This may be a particularly useful method to further investigate the appa rent salinity preference differences between YOY and juvenile bull sharks. With the miniaturiza tion and increase in the reliability of satellite tagging technology, these sophisticated devices may be attached to small sharks and will archive information on long term, large s cale movements, as well as dept h and temperature preferences. Telemetry techniques such as thes e should applied to a larger size range of bull sharks, so that ontogenetic changes in movements and migrations might be detected.
116 Based on the results of the current study, it can be postulated that the IRL is a low predation-risk environment, gi ven the apparent relative absenc e of large predators of small sharks. A telemetry-based study of the mortality rates of juvenile sharks using survival analysis would refute or support this conjecture. In addition, the tradeoffs between foraging and predation-risk warrant further investigation. Well-designed studies on shark activity space in relation to prey density may support or refute an optimal foraging hypothesis. Updated diet studies, including stable isotope analyses, would also support such efforts. To date, similar studies have had mixed results in other shark nurs eries, and investigators should be aware of the caveats and the importance of sampling design, including aspects of community structure, indirect interactions, anti-predator behavior of prey, and competition (Heithaus 2001; 2004; 2007). The unique physiology of bull sharks, especial ly their osmoregulator y capabilities, also requires further investigation. Though severa l studies have described the physiological mechanisms of elasmobranch osmoregulation (e.g Evans et al. 2004; Pillans et al. 2005), none have made the direct connection between physio logy and ecology. What ar e the metabolic costs for immature bull sharks to acclimate to freshw ater? Is there an en ergetic benefit for YOY sharks to remain in lower salinity waters than juveniles? Laboratorybased experiments may be required to investigate these questions, possibly by measurin g oxygen consumption rates of small bull sharks acclimating to various salinit ies. Investigations into the physiological responses of bull sharks to water contaminants would also be valuable. Because of their position as apex predators and long lifespan, bull sharks bioaccumulate many harmful chemicals in their systems, including mercury, PCBs, PBDEs, and various pharmaceuticals (Adams and McMichael 1999; Johnson-Restrepo et al. 2005; Gelsleichter and Sza bo 2007). It is not currently
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130 BIOGRAPHICAL SKETCH Tobey Hayward Curtis was born in Fitchbur g, Massachusetts on February 19, 1978. He graduated from Lunenburg High School in 1996, and graduated with a Bachelor of Science in Marine Science in 2000 from Long Island Univers ity, Southampton, New Yo rk. Before starting his Master of Science in Fisheries and Aquatic Sciences at the Univer sity of Florida in 2003, Tobey worked as an intern at the Apex Pred ators Program of the NMFS Northeast Fisheries Science Center in Narragansett, Rhode Island, studying sandbar sharks and smooth dogfish in Delaware Bay. He also worked in California as a postgraduate researcher at the University of California Davis, Bodega Mari ne Laboratory conducting telemetr y studies on white sharks and bat rays, as well as laboratory studi es on larval estuarine fishes. While in California, Tobey also worked as a scientific aide for the Californi a Department of Fish and Game, and as a port sampler for the Pacific States Marine Fisheries Commission. In 2001 he moved to Florida and worked as a fishery observer and technician for the Florida Program for Shark Research at the Florida Museum of Natural History, Gainesville Tobey currently works as a fishery policy analyst for the NMFS Northeast Regional Office in Gloucester, Massachusetts.