Tonya R. Wiley and Colin A. Simpfendorfer
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1 BULLETIN OF MARINE SCIENCE, 80(1): , 2007 The ecology of elasmobranchs occurring in the Everglades National Park, Florida: implications for conservation and management Tonya R. Wiley and Colin A. Simpfendorfer Abstract The elasmobranch fauna of Everglades National Park was studied using longline, gillnet, and rod and reel surveys. Thirteen species of elasmobranchs were identified including three species not previously reported in the park. Species richness was highest in the areas with the greatest influence of marine waters from the Gulf of Mexico and lower in estuarine areas and those subject to periods of hypersalinity. Most elasmobranch species were recorded as juveniles, with at least three species occurring as neonates, and there were few adults of any species. Electivity indices for salinity, temperature, and depth were calculated for Carcharhinus leucas (Valenciennes, 1841), Carcharhinus limbatus (Valenciennes, 1841), Ginglymostoma cirratum (Bonnaterre, 1788), and Negaprion brevirostris (Poey, 1868), and indicated possible habitat partitioning based on these environmental characteristics. Tag-recapture data suggested that N. brevirostris may have a high level of residency and probably remains inside the park for long periods, while all other species showed movements into and out of the park on a regular basis. Results demonstrate the utility of the park for the conservation and management of elasmobranch species and the need to consider how future changes to the environment will affect this important group of predators. The Everglades National Park (ENP) was established in 1947 to protect the unique habitats of south Florida. The adjacent marine environment of Florida Bay was added to the park in 1950, and commercial fishing banned in 1985 (Tilmant, 1989). The park covers a significant proportion of the area and habitats in south Florida, and as such represents a significant conservation area for many species, including at least 15 federally endangered species that occur within its boundaries ( gov/ever/eco/danger.htm, accessed February 2006). Although much of the conservation focus of the park is on the freshwater and terrestrial habitats, the extensive marine and estuarine areas also provide benefits to species that inhabit these areas. For example, Pristis pectinata (Table 1), a once common inhabitant of coastal and estuarine waters throughout Florida and the southeastern United States (Bigelow and Schroeder, 1953), is currently only found in significant numbers in the ENP and adjacent waters (Seitz and Poulakis, 2002; Poulakis and Seitz, 2004; Simpfendorfer and Wiley, 2005). Despite the potential benefits to many marine and estuarine species, some groups of organisms have been poorly studied in the park. One group that has been poorly documented is the elasmobranchs, for which there have been few directed studies. In one of the few, Schmidt (1986) reported the diet of juvenile Negaprion brevirostris in Florida Bay. Seitz and Poulakis (2002) and Poulakis and Seitz (2004) have reported on the occurrence of P. pectinata based on reports from anglers and boaters. In a checklist of organisms in the park that summarized both published and gray literature, Loftus (2000) reported 13 species of sharks and 10 species of batoids (Table 1). Three species of sharks (Carcharodon carcharias, Isurus oxyrinchus, and Rhincodon Bulletin of Marine Science 2007 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 171
2 172 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 Table 1. Comprehensive list of elasmobranch species reported in Everglades National Park from Loftus (2000) (L) and current study (C). Scientific name Common name Study Aetobatis narinari (Euphrasen, 1790) Spotted eagle ray L Carcharhinus acronotus (Poey, 1860) Blacknose shark C Carcharhinus brevipinna (Müller and Henle, 1841) Spinner shark C Carcharhinus isodon (Valenciennes, 1839) Finetooth shark C Carcharhinus leucas (Valenciennes, 1841) Bull shark C, L Carcharhinus limbatus (Valenciennes, 1841) Blacktip shark C, L Carcharhinus plumbeus (Nardo, 1827) Sandbar shark L Carcharodon carcharias (Linnaeus, 1758) White shark L Dasyatis americana Hildebrand and Schroeder, 1928 Southern stingray C, L Dasyatis sabina (Lesueur, 1824) Atlantic stingray L Dasyatis say (Lesueur, 1822) Bluntnose stingray C Galeocerdo cuvier (Peron and Lesueur, 1822) Tiger shark C, L Ginglymostoma cirratum (Bonnaterre, 1788) Nurse shark C, L Gymnura micrura (Schneider, 1801) Smooth butterfly ray L Isurus oxyrinchus Rafinesque, 1810 Shortfin mako L Manta birostris (Walbaum, 1792) Manta L Narcine brasiliensis (Olfers, 1831) Lesser electric ray L Negaprion brevirostris (Poey, 1868) Lemon shark C, L Pristis pectinata Latham, 1794 Smalltooth sawfish C, L Raja laevis Mitchill, 1817 Barndoor skate L Rhincodon typus Smith, 1828 Whale shark L Rhinobatos lentiginosus (Garman, 1880) Atlantic guitarfish L Rhinoptera bonasus (Mitchill, 1815) Cownose ray L Rhizoprionodon terraenovae (Richardson, 1836) Atlantic sharpnose shark C, L Sphyrna lewini (Griffith and Smith, 1834) Scalloped hammerhead L Sphyrna mokarran (Rüppell, 1837) Great hammerhead C, L Sphyrna tiburo (Linnaeus, 1758) Bonnethead C, L typus) and one species of ray (Manta birostris) are probably rare visitors to the waters of the park because of their more offshore or temperate distributions. Loftus (2000) only recorded one species as common (Rhizoprionodon terraenovae, in marine areas) and five as locally common in both marine and estuarine areas (Carcharhinus limbatus, N. brevirostris, Sphyrna tiburo, P. pectinata, and Dasyatis americana). The remaining species were listed as uncommon or rare. Most published research that has recorded elasmobranchs based on sample collection (as opposed to reports) has occurred in Florida Bay. Roessler (1970) recorded C. limbatus and D. americana in the Buttonwood canal that artificially joined Florida Bay with backcountry waterways. Sogard et al. (1989) reported catching C. limbatus, N. brevirostris, P. pectinata, and S. tiburo in gillnets set in Florida Bay. The limited capture of elasmobranchs during studies within the ENP to date has likely occurred because most studies have used gear designed to capture smaller fish. This study had three aims: (1) to document the species of elasmobranchs that occur in the ENP and determine their spatial and temporal distribution, (2) to examine environmental and habitat factors that may influence the occurrence and distribution of sharks within the park, and (3) to examine the movements of sharks using tag-recapture data to determine the level of residency for species that occurred in
3 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 173 Figure 1. Location of (A) longline ( ), and (B) gillnet ( ) and rod and reel (Δ), sampling events in the Everglades National Park (solid line denotes park boundary). the park. This study represents the first large-scale investigation of elasmobranchs in the ENP and should provide data useful in refining management measures for the marine and estuarine sections of the park. In addition, with large-scale restoration projects planned for the Everglades, these data represent a baseline from which changes that result from restoration can be determined.
4 174 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 Methods Study Site. This study was conducted within the boundaries of the Everglades National Park (ENP) in south Florida (Fig. 1). The park spans the southern tip of the Florida peninsula and most of Florida Bay. The park is the only subtropical preserve in North America and contains over 6102 km 2 of both temperate and tropical plant communities, as well as marine, estuarine, and freshwater environments. Florida Bay, the largest body of water within the park, is a shallow basin that contains over 2072 km 2 of marine bottom, much of which is covered in seagrass, corals, and sponges and contains many mangrove islands. Deep tidally cut channels run through the grass and mud flats of Florida Bay. Forests of red mangroves (Rhizophora mangle Linnaeus, 1753), black mangroves [Avicennia germinans (L.) Stearn, 1958] and white mangroves [Laguncularia racemosa (L.) Gaertn.f., 1805] are found in the coastal channels and winding rivers around the tip of the Florida peninsula and in tidal waters where freshwater from the Everglades mixes with saltwater from the Gulf of Mexico ( eco/habitats.htm, accessed February 2005). Field Sampling. Sampling was conducted utilizing longlines, gill nets, and rod and reel in a variety of habitats throughout the park (Fig. 1). Forty-two 10-day field surveys were conducted from July 2000 to February 2005, which allowed for each month to be sampled across the different years of the study period. February, July, October, and November were sampled over 5 yrs; March and June in four; April and August in three; and January, May, September, and December during two. Longlines consisted of a m bottom set mainline of 8 mm braided nylon rope anchored at both ends. Gangions were constructed of 1 m of 5 mm braided nylon cord and 1 m of stainless steel wire leader. Mustad tuna circle hooks ranging in size from 10/0 to 16/0 were used with 62% of individual sets containing a single size hook. The majority of sets (47%) were made with 12/0 or 14/0 hooks. Hooks were baited with frozen mullet (Mugil cepahlus Linnaeus, 1758 or Mugil curema Valenciennes, 1836) and fresh hardhead catfish [Arius felis (Linnaeus, 1766)], pinfish [Lagodon rhomboids (Linnaeus, 1766)], crevalle jack [Caranx hippos (Linnaeus, 1766)], or ladyfish (Elops saurus Linnaeus, 1766). Fresh bait was only used when available, and at least half of all hooks on the lines were baited with frozen mullet. Size 10/0 hooks were also baited with frozen shrimp (Penaeus spp.) when available. Gangions were spaced approximately 10 m apart along the mainline. Gill nets were 75 m of 7.62 cm (3 inch) stretch mesh 0.52 mm (26 lbs) monofilament anchored at both ends. The float line contained a foam core and the lead line contained a lead core. Surface buoys were used to mark the location of the net every 10 m. Gill nets were monitored continuously to allow removal of animals as they were captured. Rod and reel fishing utilized Penn 7500SS reels and Star ST 15/30 rods with 40 lb monofilament line and a 10/0 Mustad tuna circle hook with approximately 0.5 m of plastic coated wire leader. Hooks were baited with the same baits used on the longlines. Rod and reel sets were conducted in areas that were too confined for use of other gear, or at times when the tide or weather precluded extended sampling periods in an area. The date, time, depth, and location of all sets were recorded. Physical parameters (water temperature, dissolved oxygen, and salinity) were recorded at each sampling location midway between the surface and bottom utilizing a YSI 85 water quality meter. Elasmobranchs captured were identified and sexed. Four measurements of straight-line length (to the nearest 0.5 cm) were taken when possible: precaudal length (PCL), fork length (FL), total length (TL), and stretched total length (STL). All length measures of sharks are given in STL, the distance from the tip of the snout to the tip of the tail, with the tail at maximum extension. Disc width (DW) was measured for stingrays. Individuals with an open or partially closed umbilical scar, indicating that they had been recently born, were classified as neonates. Individuals with a completely healed umbilical scar, and that had been born < 12 mo previously (based on size at age data), were classified as young of the year (YOY). Individuals older than 12 mo, but not mature, were classified as immature. Males were examined for the state of calcification of the claspers and determined to be immature if not completely calcified or ma-
5 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 175 ture if the claspers were fully calcified. Female sharks were considered mature when they were larger than the size at maturity given by Castro (1983). Live sharks and sawfish were tagged with a cattle ear rototag or jumbo rototag (Dalton, England) on the first dorsal fin and a nylon or steel anchor streamer tag (Hallprint, South Australia) at the base of the first dorsal fin. Data Analysis. Locations of sampling events and elasmobranch captures were plotted using a Geographic Information System (ArcView 3.3). The release and recapture locations of tagged individuals were also plotted using the GIS and distances between the points calculated. Data layers for the GIS were obtained from the Florida Fish and Wildlife Research Institute (Florida coastline) and the National Parks Service (Everglades National Park boundary). Tagging data from several other projects at Mote Marine Laboratory was also queried to provide data on movements of elasmobranchs to or from the ENP. Chi-squared tests were used to determine if sex ratios differed significantly from equal numbers of males and females for each species. Ivlev s (1961) electivity index (E) was used to investigate the affinity for specific salinity, depth, and temperature habitats: E = ri - pi ri + pi, where r i is the proportion of samples in which the species was caught in habitat i, and p i is the proportion of habitat i in all samples. The value of E can range from 1 (indicating full avoidance) to 1 (indicating full affinity), with a value of zero indicating no electivity. Electivity analysis did not examine interaction effects between habitat variables. Only those shark species that were represented by over 100 individuals in the samples were used in this analysis, and all size classes were combined for a particular species. Catch per unit effort (CPUE) of longlines (for all years combined) was used to determine if there were seasonal changes in occurrence in the ENP. CPUE was expressed as the number of sharks caught per 100 hook hrs. The number of hook hours for each set was calculated by multiplying the number of hooks set by the soak time (time from first hook in to last hook out). Data were log-transformed [(ln (x+1)] and one-way ANOVAs used to determine if there were significant differences in CPUE between months. Post-hoc comparison of means using Tukey s HSD with α = 0.05 was used to determine which months grouped together. Results Four hundred and twenty eight longline sets were carried out for periods of min, with a median of 130 min. The targeted set time was 120 min (to reduce mortality and haul before substantial bait loss) with longer sets the result of lengthy haul periods due to high catch rates and shorter sets due to inclement weather. Fortytwo gill net sets and 55 five rod and reel sets were completed. In total, 1015 elasmobranchs of 13 species were captured (Table 2). Two species of Dasyatis were recorded (D. americana and Dasyatis say, with the former the most common), but most were only identified to genus so these were not included in data analysis. Longline sets captured the majority of elasmobranchs in terms of both numbers (940) and species (13). Rod and reel captured 51 individuals of 7 species, and gillnets 13 individuals of 4 species. The most frequently encountered species were Carcharhinus leucas, N. brevirostris, Ginglymostoma cirratum, and C. limbatus (Table 2). Greater proportions of females than males were captured of C. limbatus, Galeocerdo cuvier, N. brevirostris, Sphyrna mokarran, and S. tiburo (Table 2). Conversely, male G. cirratum and R. terraenovae were more commonly captured than females. The largest elasmobranchs captured were P. pectinata, with six individuals longer than 350 cm (Fig. 2). No other species was captured at a size > 300 cm, and most individuals were between 70 and 210 cm. Carcharhinus leucas, N. brevirostris, and P.
6 176 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 Table 2. Species composition, size range, and sex ratio of elasmobranchs captured in the Everglades National Park. * indicate sex ratios significantly different from 1:1 based on χ 2 test. Species n Size range (cm) Sex ratio (% male) P (sex ratio not 1:1) Carcharhinus acronotus Carcharhinus isodon Carcharhinus leucas Carcharhinus limbatus < * Dasyatis spp Galeocerdo cuvier * Ginglymostoma cirratum * Negaprion brevirostris < * Pristis pectinata Rhizoprionodon terraenovae * Sphyrna mokarran * Sphyrna tiburo < * pectinata were captured over the largest size ranges (Table 2). Three species C. leucas, C. limbatus, and P. pectinata were captured as neonates or at sizes corresponding to their size at birth, indicating that at least some were most likely born within the ENP. Two species Carcharhinus acronotus and S. tiburo were captured mostly as adults; two species G. cirratum and P. pectinata were captured as both adults and juveniles; the remaining species were captured mostly as juveniles. Most species were not captured at sizes close to their reported maximum sizes. Size frequencies differed substantially among species, indicating that the gear was not highly selective for a specific size of elasmobranch. Spatial and Temporal Distribution. The most commonly captured species (C. leucas, N. brevirostris, G. cirratum, and C. limbatus) occurred throughout the marine sections of the ENP (Fig. 3). Conversely, C. acronotus was only captured in the vicinity of Cape Sable. Carcharhinus leucas and P. pectinata were the only two species captured in areas separated from marine environments by relatively large distances. The former of these was especially abundant throughout the Whitewater Bay region at sizes < 150 cm. Larger size classes of C. leucas occurred in coastal marine areas (Fig. 3B). Carcharhinus limbatus, Dasyatis spp., N. brevirostris, and S. tiburo all occurred in estuarine areas, but remained in the areas influenced by significant tidal flow from marine areas (Figs. 3C, 3D, 3F, 3H). In all of these species it was the smallest size classes that penetrated into the estuaries. Catches in the northeast portion of Florida Bay were dominated by S. tiburo, and juvenile-sized N. brevirostris and Dasyatis spp. Few other species were regularly encountered in this section of the park. Ginglymostoma cirratum was only captured in marine areas of the park (Fig. 3E). The log-transformed catch rates of the four most commonly caught species all showed significant differences among months (Fig. 4; ANOVA, df = 11, C. leucas P < , C. limbatus P = 0.038, G. cirratum P = 0.014, N. brevirostris P = ). All species were captured in all months, indicating a year-round presence. Post-hoc comparison of monthly mean catch rates showed no separation of groups, despite monthly differences, suggesting no consistent or clear pattern in seasonal abundance.
7 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 177 Figure 2. Size frequency distribution of elasmobranchs captured in the Everglades National Park. All size classes are in stretched total length. Sizes at birth (B), male maturity (M), female maturity (F), and maximum size (X) are indicated for each species if they fall within the range shown. Sizes indicated are based on: Carcharhinus isodon, Castro (1993); Carcharhinus limbatus, Castro (1996); Ginglymostoma cirratum, Castro (2000); Galeocerdo cuvier, Randall (1992); Pristis pectinata, Simpfendorfer (2000); Sphyrna tiburo, Parsons (1993); all other species, Castro (1983). Note y-axes have different scales.
8 178 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 Figure 3. Locations of capture of the eight most commonly caught elasmobranch species in the Everglades National Park (solid line denotes park boundary) by size class.
9 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 179 Figure 4. Monthly mean (point) catch rates (log-transformed) and standard errors (error bars) of (A) Carcharhinus leucas, (B) Carcharhinus limbatus, (C) Ginglymostoma cirratum, and (D) Negaprion brevirostris in the Everglades National Park. Data are all years of study combined. Environmental Factors. Environmental preferences were analyzed for the four most frequently encountered species. The salinity range encountered during sampling was , with elasmobranchs captured in salinities of (Fig. 5A). Salinity electivity patterns varied between the four species (Fig. 6A). Carcharhinus leucas exhibited an affinity for salinities < 25 and avoidance at salinities > 30, with 50% of the catches occurring in the range of (Fig. 5A). Carcharhinus limbatus and G. cirratum had similar salinity electivity patterns, with avoidance < 30 and affinity > 30. The 50% salinity range for catches was also similar for both species (31 35). Negaprion brevirostris exhibited a salinity electivity pattern between that of C. leucas and C. limbatus. They showed affinity for salinities of and avoidance of salinities < 22, with 50% of the catches occurring from 27 to 34. The temperature range encountered during sampling was C, with elasmobranchs captured from 16.6 to 35.2 C. Temperature electivity patterns (Fig. 6B) were similar for C. limbatus, G. cirratum, and N. brevirostris with avoidance < 25 C, low affinities from 25 to 31 C and avoidance of > 31 C. The 50% ranges of catches for these three species were all approximately 4 C (Fig. 5B), with the G. cirratum range (25 29 C) slightly lower than those of C. limbatus and N. brevirostris (26 30 C). Carcharhinus leucas showed mostly low avoidance for temperatures < 30 C and increasing affinity from 30 C and higher. Fifty percent of C. leucas catches occurred in the range of C. The depth range encountered during sampling was m, with elasmobranchs captured throughout the full range. Two different patterns of depth electivity were observed (Fig. 6C). Carcharhinus leucas and N. brevirostris exhibited affinity for depths of and > 4 m, and avoided depths < 1.0 m and from 2.2 to 3.2 m. Fifty percent ranges of catches for these two species were similar: m for C. leucas and m for N. brevirostris (Fig. 5C). Carcharhinus limbatus and G. cirratum showed increasing electivity with increasing depth. Carcharhinus limbatus avoided depths < 1.5 m, while G. cirratum avoided depths < 2.25 m. The depth range in which
10 180 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 Figure 5. Environmental parameters: (A) salinity, (B) water temperature, and (C) depth at capture locations for the four most commonly captured elasmobranch species in the Everglades National Park and for all gear sets. Horizontal lines indicate median values, boxes represent 50% ranges, and whiskers are 95 th percentiles. 50% of captures were made for these two species differed, with C. limbatus from 1.8 to 3.0 m and G. cirratum from 2.5 to 3.2 m. Tag-Recapture Data. Twenty C. leucas, three C. limbatus, two S. tiburo, 16 N. brevirostris, and eight G. cirratum were recaptured during the study period. Recaptures were reported by charter fishing guides, recreational fishermen, and during our sampling. The recaptured C. leucas were at liberty d and moved km.
11 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 181 Figure 6. Electivity indices for (A) salinity, (B) water temperature, and (C) depth for the four most commonly captured elasmobranch species in the Everglades National Park. Values of electivity below zero indicate avoidance, values above zero indicate affinity. Only 3 of the 20 C. leucas showed significant spatial movement (Fig. 7A), with the longest movements exhibited by two small animals that moved into the ENP from the lower Charlotte Harbor area. In total, five C. leucas moved into the ENP from the north and one moved out of the park to the north. Carcharhinus limbatus were at liberty d and moved km (Fig. 7B). Three YOY C. limbatus were tagged north of the park along the Gulf of Mexico coast of Florida and recaptured along the mid to upper gulf coast of the park. Two C. limbatus tagged near Tampa Bay in summer (July 1996 and August 1999) were recaptured the following spring (March 1997 and April 2000, respectively) along the mid and upper gulf coast of the park. Another C. limbatus was tagged just north of the
12 182 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 Figure 7. Location of release ( ) and shortest route to recapture point (line) for five species of elasmobranch captured, or recaptured, in the Everglades National Park (solid line denotes park boundary). Solid bar indicates a distance of 40 km in each panel. park in the Ten Thousand Islands in June and recaptured the following June 23 nm to the southeast within the park. Ginglymostoma cirratum were at liberty d and moved km. Two of the eight G. cirratum moved northwards out of the park along the Gulf of Mexico coast of Florida. One juvenile male G. cirratum tagged in Florida Bay in March moved quickly north out of the park along the Gulf coast and was recaptured in Charlotte Harbor in June of the same year (Fig. 7C). Similarly, a mature male G. cirratum tagged in Florida Bay in February was recaptured off Charlotte Harbor in April of the following year. All other G. cirratum were recaptured near the original
13 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 183 tagging location and many captured months later at the same location as they were tagged. Negaprion brevirostris were at liberty d and moved km. All 16 N. brevirostris that were recaptured within the ENP were tagged in the park (Fig. 7D). Most N. brevirostris were recaptured after at least several months in the same location as originally tagged. No N. brevirostris tagged within the park were recaptured outside the park and none tagged outside the park were recaptured within the park. The two S. tiburo recaptured were at liberty 326 and 495 d, and moved 7 and 38 km (Fig. 7E). One S. tiburo was tagged just north of the park in the Ten Thousand Islands in August and recaptured the following year in December near the northern gulf boundary of the park. The other S. tiburo was tagged in northeast Florida Bay in May and recaptured nearby the following April. Discussion This study identified 13 species of elasmobranch that occurred within the waters of the Everglades National Park. Three of these species C. acronotus, C. isodon, and D. say have not previously been reported within the park. In addition to these three species, a fourth-carcharhinus brevipinna-was captured in Florida Bay during March 2005, after the study reporting period (T. Wiley, Mote Marine Laboratory, unpubl. data). Based on Loftus (2000) inventory this brings the total number of elasmobranch species recorded in the ENP to 16 sharks and 11 batoids (Table 1). The ENP thus has a relatively rich elasmobranch fauna that occurs in both the marine and estuarine sections of the park. The species composition and most abundant species (C. leucas, C. limbatus, G. cirratum, and N. brevirostris) in the current study were very similar to those reported by Michel (2002) in the Ten Thousand Islands, an area just north of the park boundary along the gulf coast with many comparable habitats. The results of the current study were not entirely consistent with previously reported findings for some species within the park. The capture of four Carcharhinus isodon in Florida Bay represents the most southerly records of this species in US waters (Castro, 1983; J. Castro, National Marine Fisheries Service, pers. comm.). None of the other species the current study recorded for the first time in the park were surprising as they are common inhabitants of the waters off southern Florida (Castro, 1983). Based on the results of the current study, Loftus s (2000) designation of R. terraenovae as common in the park seems erroneous, with extensive sampling catching only a few individuals. It is unlikely this was the result of declining abundance since the original survey (Henshall, 1891), as this species is still considered to be common throughout its range (Cortes, 2002; Simpfendorfer and Burgess, 2002). These differences could be the result of misidentification, gear differences, or lower sampling effort in prior studies. The current study also suggests that C. leucas is a relatively common and ubiquitous species in the marine and estuarine habitats of the park, a contrast to previous studies and reports that have rarely encountered this species. Tabb and Manning (1961) reported P. pectinata to be common in Florida Bay and the brackish waters of the Florida mainland. Sogard et al. (1989) also reported catching seven P. pectinata in northeast Florida Bay. The abundance of P. pectinata has declined over the last few decades (Simpfendorfer, 2002), accounting for the low number of individuals encountered in the current study. This reduced abundance of
14 184 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 P. pectinata has resulted in it being listed as endangered under the US Endangered Species Act. Historic reports of other species were mostly consistent with the results of the current study. Tabb and Manning (1961) reported that C. limbatus was the most abundant shark of the shallow waters of Florida Bay and that they invade areas of low salinity on flood tides and exit on ebb tides. Schmidt (1979) reported N. brevirostris to be among the most abundant species, by biomass, taken in western Florida Bay. Schmidt (1986) reported catching juvenile N. brevirostris in the shallow grass flats of western Florida Bay during routine seine collections, and Sogard et al. (1989) captured them throughout most of Florida Bay. In contrast to the current study which regularly caught N. brevirostris in gulf edge habitats within the ENP, Michel (2002) reported that N. brevirostris avoided the gulf edge habitats and exhibited no electivity for backwaters or transition zones in the Ten Thousand Islands area just north of the ENP. Tabb and Manning (1961) reported catching G. cirratum in all sampling locations within Florida Bay, but none in Coot or Whitewater Bays, consistent with the results of the current study. The results of this study indicate that the Everglades National Park is important for several elasmobranch species. The occurrence of newborn C. leucas and P. pectinata in estuarine habitats, and C. limbatus in marine and estuarine habitats, suggests that these species utilize sections of the park as primary nurseries (those areas where the young are born and live for the early part of their life). The regularity with which small juvenile C. leucas were captured in estuarine sampling, and the large amount of this type of habitat within the park, suggests that the numbers born each year are considerable. Although few young P. pectinata were captured, acoustic telemetry data indicated that they remain in these areas for substantial periods (C. Simpfendorfer, unpubl. data) and juveniles are regularly observed by recreational fishers (Simpfendorfer and Wiley, 2005). The utilization of estuarine nursery areas by C. leucas and P. pectinata, including those with salinities much lower than those used by other shark species, may reduce the risk of predation and competition for food, hence increasing survival. Given the endangered status of the P. pectinata population, the protection afforded by the park, both in terms of the lack of commercial fishing and protection of nursery habitats (shallow mud banks and mangrove shorelines, Simpfendorfer and Wiley, 2005), has probably been an important factor in ensuring the population was not extirpated from US waters before other protections were implemented. In addition to containing important primary nursery habitats, the ENP is also commonly used by juveniles of most of the shark species recorded. For many species of sharks the ability of their populations to sustain fishing pressure is most sensitive to the survival rates of later juvenile phases (Cortes, 1999). As such, the occurrence of these stages in the ENP should be beneficial to their populations by providing a refuge from commercial fishing. The mangrove coasts and river mouths along the mainland sections of the park in particular were commonly used by juvenile C. leucas, C. limbatus, and N. brevirostris. All three of these species are taken in the commercial shark bottom longline fishery, with C. limbatus one of the main target species (Castro, 1996). The management practices of the ENP therefore may provide a level of protection to these species that is important in sustaining catches in commercial shark fisheries and in the recovery of overfished species. The potential level of protection afforded by the ENP to individual species was variable. The species that occur infrequently in the park probably derive little or
15 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 185 no benefit from it. The tag-recapture data, however, also showed that those species frequently found in the park may derive different benefits. Most notably, N. brevirostris were found to have very short distances between the release and recapture locations, suggesting long term residence within the park. Gruber (1982) found similar tag-recapture results in Florida Bay with 12 of 40 tagged N. brevirostris moving an average of 8.89 km and 15 recaptured < 2 km from their original release site. For this species the park probably provides a high level of protection. Although newborn N. brevirostris were not captured in the current study, they were observed during sampling and Springer (1950) reported them from the shallow banks, lagoons, and flats around mangrove islands in Florida Bay. Thus the entire juvenile phase of this species could be completed within the ENP. In contrast, other shark species moved across park boundaries relatively frequently. Thus for species such as C. leucas, C. limbatus, and G. cirratum the park probably offers a lower level of protection than for N. brevirostris. Some of the movement into and out of the park was probably the result of seasonal migrations. In particular, juvenile C. limbatus are known to undertake migrations from primary nursery areas on the west coast of Florida southwards as far as the Florida Keys in fall when water temperatures fall to around 20 C (Hueter and Tyminski, 2002). The ENP is thus likely to represent an important winter nursery area for this species, and potentially others. Thus, during cooler months the ENP may provide a higher level of refuge from commercial fishing than during warmer months for this species. Although these migrations may be important for some species, there was no strong seasonal pattern in the abundance of any of the commonly captured species. This probably reflects the fact that all of these species occur year round, possibly masking the seasonal influx from other areas. Adults of most species were either not recorded, or rarely recorded. Whether this was a function of their lack of occurrence within the park, or the selectivity of the gear for smaller individuals, is currently unknown. If the limited number of adults was due to their lack of occurrence, this may represent an evolutionary strategy where adults of many species avoid a common nursery region to reduce predation risk of the vulnerable juvenile phases (Simpfendorfer and Milward, 1993). The lack of deeper habitats within the park boundaries may also have been a factor in the lack of adults in the samples. Adults of many species prefer deeper water and so occur farther offshore (Springer, 1967). Further sampling using heavier gear will need to be undertaken to fully understand the occurrence and distribution of larger adult sharks within the ENP. The greatest number of species and individuals was found in the region of northwestern Florida Bay, in the vicinity of East Cape Sable. This observation is consistent with that of Tabb et al. (1962) who observed that the greatest number of fish species and individuals was found in the stable marine salinity region of western Florida Bay. This stable salinity regime is more favorable to the occurrence of many stenohaline elasmobranchs. The salinity electivity indices for the commonly encountered species, with the exception of C. leucas, which is known to be euryhaline (Thorson et al., 1973, Simpfendorfer et al., 2005), showed avoidance of salinities < Other areas of the park that are strongly influenced by the marine waters of the Gulf of Mexico, but that were poorly sampled in the current study, may also have higher elasmobranch species richness. In particular, this may include the western boundary of the park in Florida Bay.
16 186 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 Two habitats within the park yielded fewer species than those heavily influenced by the marine waters of the Gulf of Mexico. The first of these were the estuarine areas that were relatively far removed from the tidal influence of marine areas (e.g., Whitewater and Coot Bays). Only smaller juvenile C. leucas and P. pectinata were captured in these areas. The reason that C. leucas is found in these areas was shown by its affinity to areas with salinities < 25. The ability of C. leucas to osmoregulate in low salinity and freshwater, and hence occur in estuaries and rivers, is well known (Thorson et al., 1973). In a study of newborn C. leucas in the Caloosahatchee River on the west coast of Florida, Simpfendorfer et al. (2005) observed that the catch rates of newborn C. leucas were highest in salinities from 5 to 15. Although insufficient numbers of P. pectinata were captured to enable the same type of electivity analysis, this species is well known to be able to osmoregulate in low salinity environments (Thorson, 1976; Compagno and Cook, 1995) and occurs in the same range of salinities as C. leucas. The ability of these two species to occupy lower salinity areas of the ENP may enable them to spend the first part of their life in areas where predation risk is lower than in higher salinity areas where larger sharks more commonly occur. The second habitat in which the number of species was lower than in the marine areas was the northeast section of Florida Bay. This area is one of extreme fluctuations in salinity, from almost fresh during the wet period of summer and fall to hypersaline during the dry period of winter and spring (Tabb et al., 1962; Montague and Ley, 1993; Ley et al., 1994). These extremes occur because of the limited tidal flushing, high evaporation, and substantial periodic freshwater inflows (Tabb et al., 1962). With such extreme changes in salinity, sometimes over short periods of time, it is not surprising that richness was lower than areas with more stable salinity regimes. All of the species recorded in this area have limited tolerances for lower salinities. Ginglymostoma cirratum showed affinity for mostly marine salinities and N. brevirostris for those between 25 and 30. Sphyrna tiburo has also been shown to have limited tolerance for salinities < 16.5 (Hueter and Tyminski, 2002; Michel, 2002). Thus it is likely that these species move out of this area during periods of extreme hyposalinity or hypersalinity. The extreme salinity conditions in this section of Florida Bay may also result in a reduction of prey species, limiting the areas capacity to support larger predatory species such as sharks. Further investigation into how the species of elasmobranchs that occur in this area respond to the changing environmental conditions would help us understand how future changes to the freshwater flow into this area may affect these populations. Results of this study have shown that the Everglades National Park has a diverse elasmobranch fauna, and that the park is important for several of these species. Given the current conservation status of many elasmobranch species, the protection afforded by the park likely plays a role in sustaining commercial harvest of species, such as C. limbatus, and in protecting endangered species, such as P. pectinata. The importance of salinity to the occurrence and distribution of elasmobranchs within the park means that future changes to freshwater flows through restoration efforts may have effects on this important group of predators. The effects of these changes need to be assessed to ensure that the ENP continues to serve as a conservation area for this group.
17 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 187 Acknowledgments We gratefully acknowledge M. Amato, M. Heupel, J. Morris, B. Yeiser, and many college interns and volunteers for assisting with fieldwork and J. Tyminski for tag recapture data and assistance with field work. Special thanks to T. Schmidt, NPS/SFNRC Everglades National Park, for his support of this research and encouraging us to publish these data. Funding from NOAA Fisheries Office of Protected Resources, National Fish and Wildlife Foundation, National Geographic Committee for Research and Exploration, The Disney Wildlife Conservation Fund, and Florida Fish and Wildlife Conservation Commission supported this research. Literature Cited Bigelow, H. B. and W. C. Schroeder Sawfishes, guitarfishes, skates and rays. Fishes of the western north Atlantic. Mem. Sears Found. Mar. Res. 1: Castro, J. I The sharks of North American waters. Texas A&M University Press, College Station. 180 p The shark nursery areas of Bulls Bay, South Carolina, with a review of the shark nurseries of the southeastern coast of the United States. Environ. Biol. Fish. 38: Biology of the blacktip shark, Carcharhinus limbatus, off the southeastern United States. Bull. Mar. Sci. 59: The biology of the nurse shark, Ginglymostoma cirratum, off the Florida east coast and the Bahama Islands. Environ. Biol. Fish. 58: Compagno, L. J. V. and S. F. Cook The exploitation and conservation of freshwater elasmobranchs: status of taxa and prospects for the future. J. Aquat. Sci. 7: Cortes, E A stochastic stage-based population model of the sandbar shark in the western north Atlantic. Pages in J. A. Musick, ed. Life in the slow lane: ecology and conservation of long-lived marine animals. Am. Fish. Soc. Symp. 23, Bethesda Stock assessment of small coastal sharks in the U.S. Atlantic and Gulf of Mexico. Sustainable Fisheries Division Contribution No. SFD-01/ p. Endangered Species in Everglades National Park [Internet]. Homestead, FL: National Park Service; c1999. Available from: Accessed February Gruber, S. H Role of the lemon shark, Negaprion brevirostris (Poey), as predator in the tropical marine environment: a multidisciplinary study. Fla. Sci. 45: Henshall, J. A Report upon a collection of fishes made in southern Florida during Bull. U.S. Fish. Comm. 9: Hueter, R. E. and J. P. Tyminski Center for Shark Research (CSR) U.S. shark nursery research overview Pages in C. T. McCandless, H. L. Pratt, Jr., and N. E. Kohler, eds. Shark nursery grounds of the Gulf of Mexico and the east coast waters of the United States: an overview. An internal report to NOAA s Highly Migratory Species Office. NOAA Fisheries Narragansett Lab, Narragansett. Ivlev, V. S Experimental ecology of fishes. Yale University Press, New Haven. 302 p. Ley, J. A., C. L. Montague, and C. C. McIvor Food habits of mangrove fishes: a comparison along estuarine gradients in northeastern Florida Bay. Bull. Mar. Sci. 54: Loftus, W. F Inventory of fishes of Everglades National Park. Fla. Sci. 63: Michel, M Environmental factors affecting the distribution and abundance of sharks in the mangrove estuary of the Ten Thousand Islands, Florida, U.S. Ph.D. Diss. University of Basel, Basel, Switzerland. 133 p. Montague, C. L. and J. A. Ley A possible effect of salinity fluctuation on abundance of benthic vegetation and associated fauna in northeastern Florida Bay. Estuaries 16:
18 188 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 1, 2007 Parsons, G. R Geographic variation in reproduction between two populations of the bonnethead shark, Sphyrna tiburo. Environ. Biol. Fish. 38: Poulakis, G. R. and J. C. Seitz Recent occurrence of the smalltooth sawfish, Pristis pectinata (Elasmobranchiomorphi: Pristidae), in Florida Bay and the Florida Keys, with comments on sawfish ecology. Fla. Sci. 67: Randall, J. E Review of the biology of the tiger shark (Galeocerdo cuvier). Aust. J. Mar. Freshw. Res. 43: Roessler, M. A Checklist of fishes in Buttonwood Canal, Everglades National Park, Florida, and observations on the seasonal occurrence and life histories of selected species. Bull. Mar. Sci. 20: Schmidt, T. W Ecological studies of fishes and the water quality characteristics of Florida Bay, Everglades National Park, Florida. Project report RSP-EVER N-36. Everglades N. P. South Florida Research Center, Homestead. 99 p Food of young juvenile lemon sharks, Negaprion brevirostris, near Sandy Key, western Florida Bay. Fla. Sci. 49: Seitz, J. C. and G. R. Poulakis Recent occurrence of sawfishes (Elasmobranchiomorphi: Pristidae) along the southwest coast of Florida (USA). Fla. Sci. 65: Simpfendorfer, C. A Predicting recovery rates for endangered western Atlantic sawfishes using demographic analysis. Environ. Biol. Fish. 58: Smalltooth sawfish: the USA s first endangered elasmobranch? Endangered Species Update 19: and G. H. Burgess Assessment of the status of the small coastal sharks in US waters using an age-structured model. Mote Marine Lab. Tech. Rpt. 836, 58 p. and N. E. Milward Utilisation of a tropical nursery area by sharks of the families Carcharhinidae and Sphyrnidae. Environ. Biol. Fish. 37: and T. R. Wiley Determination of the distribution of Florida s remnant sawfish population and identification of areas critical to their conservation. Final Report. Florida Fish and Wildlife Conservation Commission, Tallahassee, Florida. 40 p., G. G. Freitas, T. R. Wiley, and M. R. Heupel Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a southwest Florida estuary. Estuaries 28: Sogard, S. M., G. V. N. Powell, and J. G. Holmquist Spatial distribution and trends in abundance of fishes residing in seagrass meadows on Florida Bay mudbanks. Bull. Mar. Sci. 44: Springer, S Natural history notes on the lemon shark, Negaprion brevirostris. Tex. J. Sci. 3: Social organization of shark populations. Pages in P. W. Gilbert, R. F. Mathewson, and D. P. Rall, eds. Sharks, skates and rays. John Hopkins, Baltimore. Tabb, D. C. and R. B. Manning A checklist of the flora and fauna of northern Florida Bay and adjacent brackish waters of the Florida mainland collected during the period July, 1957 through September, Bull. Mar. Sci. Gulf Caribb. 11: , D. L. Dubrow, and R. B. Manning The ecology of northern Florida Bay and adjacent estuaries. State of Florida Board of Conservation Technical Series No p. Thorson, T. B Observations on the reproduction of the sawfish, Pristis perotteti, in Lake Nicaragua, with recommendations for its conservation. Pages in T. B. Thorson, ed. Investigations of the ichthyofauna of Nicaraguan lakes. University of Nebraska, Lincoln., C. M. Cowan, and D. E. Watson Body fluid solutes of juveniles and adults of the euryhaline bull shark Carcharhinus leucas from freshwater and saline environments. Physiol. Zool. 46: Tilmant, J. T A history and an overview of recent trends in the fisheries of Florida Bay. Bull. Mar. Sci. 44: 3 33.
19 WILEY AND SIMPFENDORFER: ECOLOGY OF EVERGLADES ELASMOBRANCHS 189 Date Submitted: 6 April, Date Accepted: 21 August, Address: (T.R.W., C.A.S) Mote Marine Laboratory, Center for Shark Research, 1600 Ken Thompson Parkway, Sarasota, Florida Corresponding Author: (T.R.W.) <twiley@mote.org>.
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