American Fisheries Society Symposium 50:237–250, 2007 © Copyright by the American Fisheries Society 2007

Notes on the Occurrence and Distribution of Elasmobranchs in the Ten Thousand Islands Estuary, Florida

PASCALE A. STEINER* Pèsch viv, Büro für Fischereifragen und Gewässerökologie Via Sogn Paul 1, 7403 Rhäzüns, Switzerland

MARCEL MICHEL Department of and Game, Grisons, Loestrasse 14, 7001 Chur, Switzerland

PATRICK M. O’DONNELL Rookery Bay National Estuarine Research Reserve 300 Tower Road, Naples, Florida 34113, USA

Abstract.—The goal of this report is to contribute to existing information on the occurrence and distribution of elasmobranch species found in the mangrove estuary of the Ten Thousand Islands located in southwest Florida. A planned hydrologic restoration shall occur in this area in the near future, and this baseline data will be beneficial in documenting how changes in freshwater flow may influence top predators in this system. Sampling was conducted from 1997 to 2002 using a combination of gill nets and longlines. A total of 1862 elasmobranchs, including 17 species representing eight families, were reported. A total of 1,377 sharks, including nine species from three families, and 485 rajiformes, including eight species from five families, were captured. Sharks and rajiformes were caught in every month of the year, though there was large variation in the occurrence of species per month. Comparing fishing gears, 94% of all sharks were caught with gill nets and 6% were caught with longlines, while 100% of rajiformes were caught in gill nets. More than 52% of all shark catches were bonnetheads Sphyrna tiburo, 24% were blacktip sharks Carcharhinus limbatus, and 15% were bull sharks C. leucas. All other shark species were far less abundant (<5% of total sharks). Cownose rays Rhinoptera bonasus comprised almost 50% of the total catches of rajiformes, followed by stingrays Dasyatis sp. at 24% and spotted eagle rays Aetobatus narinari at 18%. All other rajiformes were less abundant (≤6%). This study delivers the first comprehensive account of the Ten Thousand Islands’ elasmobranch community with indica- tions of its use as a shark nursery area.

Introduction (Branstetter 1987; Killam and Parsons 1989; Simpfendorfer and Milward 1993; Castro 1996), Fringing the southwest coast of Florida is a rela- and the young spend their first weeks or even tively undisturbed mangrove forest that supports years in the nurseries (Castro 1993). large populations of mammals, birds, fish, and An inventory of the flora and fauna of the invertebrates. Compared to nonvegetated waters, Ten Thousand Islands estuary is reported in mangrove may provide a greater degree Carter et al. (1973), Weinstein et al. (1977), and of food or refuge from predators or both (Heck Nalley et al. (1997). Since these studies prima- and Thoman 1981; Rozas and Odum 1987; rily used trawls, few elasmobranchs were re- Thayer and Chester 1989; Wilson 1989). Such ported, including Atlantic Dasyatis habitats are known to function as nurseries for sabina, southern stingray D. americana, spotted many different species (Van der Velde et al. 1992). eagle ray Aetobatus narinari, cownose ray Some shark species use mangrove areas as nurs- Rhinoptera bonasus, bonnethead Sphyrna eries (Snelson and Williams 1981; Castro 1993; tiburo, lemon shark Negaprion brevirostris, Holland et al. 1993; Carrier and Pratt 1998), blacktip shark Carcharhinus limbatus, bull shark where females enter the shallow bays to give birth C. leucas, and nurse shark Ginglymostoma cirratum. Most of the sharks were reported as a * E-mail: [email protected] single catch. The gill nets and longlines used in 237 238 STEINER, MICHEL, AND O’DONNELL this study were more efficient at catching elas- east. The estuary is a narrow belt, which extends mobranchs, and we were therefore able to ob- an average distance of 8.0 km from the gulf to tain a more complete picture of their use of this the salt marshes in the extreme upper reaches of estuary. Since a hydrologic restoration is the watershed (Carter et al. 1973). The water- planned to re-establish historical flow-ways to shed is delimited by man-made barriers in most the estuary, documentation of the top predators instances, such as roads (U.S. Highway 41) and in the system (primarily sharks) will enhance cur- stream weirs. The Ten Thousand Islands contain rent knowledge of shark nursery areas and how a variety of aquatic habitats, including fresh and they might adapt to changes in freshwater flows. saltwater marshes, mangroves, mudflats, oyster bars, and grass beds. The dominant habitats, Methods however, are the extensive tidal mangrove for- Study site ests (Nalley et al. 1997), which comprise thou- sands of small islands. The islands at the gulf Sampling was conducted in the Ten Thousand front consist of hardwood hammock, but the vast Islands National Wildlife Refuge, which is lo- majority of the islands are composed primarily cated southeast of Naples, Florida. The refuge is of three species of mangroves: red mangrove a mangrove-dominated estuary that covers 79.5 Rhizophora mangle, white mangrove Lagun- km2 along the coast of the Gulf of Mexico (Fig- cularia racemosa, and black mangrove Avi- ure 1). It is encompassed within the Rookery cennia germinans. One mangrove associate, Bay National Estuarine Research Reserve and green buttonwood Conocarpus erectus is also borders Everglades National Park to the south- occasionally abundant.

25°57‘

25°54‘

25°51‘

81°41‘ 81°36‘ 81°32‘

FIGURE 1. The Ten Thousand Islands estuary, Florida. THE OCCURENCE AND DISTRIBUTION OF ELASMOBRANCHS IN THE TEN THOUSAND ISLANDS ESTUARY 239

The estuary is relatively shallow, ranging shark hooks. An anchor and a buoy were attached from 3 to 10 m, averaging 2 m. During the wet on each end of the line with an additional weight season (June to November), salinity is lower attached in the middle to stabilize the longline. within the estuary than in the gulf and the accu- A small float on each gangion allowed the baited mulation of freshwater runoff can reduce salinity hook to remain up in the water column. The in the upper reaches down to nearly 0‰ for short longline was set for 4 h but checked every hour periods followed by recovery to high salinities to free caught and replace missing bait. within 2 months (Carter et al. 1973). During the A total of 1,699 gill nets and 203 longlines were dry season (December to May), evaporation can set during the study period (Table 1). Catch per exceed river flow plus precipitation, which re- unit effort (CPUE) was only calculated for the sults in seasonally hypersaline conditions net catches and was expressed as the number of (Weinstein et al. 1977). The water temperature elasmobranchs caught per gill net set time and ranges from 30°C during summer to 20°C in win- net area (CPUE = total number of specimens per ter (Nalley et al. 1997). Since tidal range within hour per 100-m2 gill net). the Ten Thousand Islands is large relative to the All sharks were identified and measured as shallow water depth, the estuary can be classified follows: precaudal length (PCL), fork length (FL), as tidal-dominated (Dyer 1997). total length (TL, dorsal caudal lobe not de- pressed), stretched total length (STL, dorsal cau- Sampling dal lobe depressed into line with body axis), clasper length (CL, outer length) and body Different habitats from the lower to the upper weight (W). The life stage of most animals was reaches of the estuary were sampled on an ir- reported as either young of the year (umbilical regular basis using the principles of simple ran- scar open or healed, but still visible), immature dom sampling. Sampling was conducted at (male: soft, not calcified claspers, rhipidion can- various times of the day and night. Since most not be opened; female: estimated according to of the estuarine bays were not navigable during TL) or mature (male: hardened, calcified clasp- low tide, sampling was undertaken 2.5 h before ers, rhipidion opens freely; female: estimated ac- high tide until 2.5 h after high tide. At each sam- cording to TL). Sharks were tagged with yellow pling location, water temperature (°C), salinity plastic dart tags (Hallprint Inc.) provided by (‰) and dissolved oxygen (mg/L) were measured Mote Marine Laboratory, Sarasota, Florida. with a combined handheld multimeter (YSI 100 Sharks were released, and their release condi- or YSI 85, Yellow Springs Corp., Yellow Springs, tion was classified as good, weak, or dead. The Ohio). These measurements were taken by plac- release conditions were judged as follows: ing the probe 15 cm above the bottom. Depth good—swam away from sight vibrantly; weak— was recorded using a graduated pole at each sam- barely swam away and sometimes drifted toward pling location. the bottom; dead—not released due to no signs Elasmobranchs were caught with gill nets of life after revival attempts were made. A small or longlines. Gill nets were 91.5 m long by 2.4 (1.5-m-diameter) ‘kiddie’ pool was used to al- m deep, made of nylon monofilament compris- low smaller sharks the opportunity to swim ing 6.5-cm stretch mesh. The net was anchored around in circles while tagging and measure- on both ends to prevent drifting and marked ments were collected. Additionally, sharks were with inflatable buoys. Gill nets were either re- held alongside the forward idling boat until they trieved after a set time of 30 min or they were soaked for 4 h but checked every 30 min. En- TABLE 1. Sampling periods with total net and longline tangled animals were removed immediately. In hours during each period. addition to gill nets, a 10-hook longline with a Time period Total net hours Total longline hours mainline of 120 m, and two 10-hook longlines with a mainline of 50 m were used. The mainline April–May 1997 57.5 – February–August 1998 145.0 276 was made of 0.8 cm hollow, braided, nylon May–October 1999 280.0 204 polypropylene rope. The gangions consisted of May–December 2000 419.5 224 2 m of multifilament stainless steel cables with January–December 2001 144.0 – standard snap-on connectors and #1 Mustad January–September 2002 108.0 108 240 STEINER, MICHEL, AND O’DONNELL

swam away on their own or appeared to have micrura, smalltooth , and lesser electric regained vitality. Rajiformes were also identi- ray Narcine brasiliensis. Environmental condi- fied, sexed, and measured (DL = disk length, DW tions inhabited by all elasmobranch species = disk width, and TL = total length for smalltooth caught are listed in Tables 3 and 4. The listed sawfish Pristis pectinata and Atlantic environmental condition ranges of shark and ray Rhinobatos lentigenosis). catches are based on data from the sampling sea- sons from 1999 through 2002. Individual spe- Results cies catch information is reported in the following species profiles, which are listed in decreasing A total of 1377 sharks were caught by gill net order of abundance with sharks (Table 2) listed (94%) and longline (6%) in the Ten Thousand before rajiformes (Table 3). Islands estuary between 1997 and 2002 (Table 2). Bonnetheads (52%) were the most abundant Bonnethead shark species caught, followed by blacktip (24%), bull (15%), and lemon (5%) sharks. Less All bonnetheads were caught with gill nets. The than 5% of the shark catch consisted of nurse size range of bonnetheads was 25–80 cm PCL shark, S. mokarran, Atlantic (Table 2; Figure 2). The size distribution for sharpnose shark Rhizoprionodon terraenovae, these sharks showed a difference between the scalloped hammerhead S. Lewini, and tiger shark sexes, with the males being significantly smaller Galeocerdo cuvier. An overview of the length- than the females (male: mean PCL = 48.9 cm; frequency distribution for these nine shark spe- female: mean PCL = 55.3 cm; t-test p < 0.01). A cies is illustrated in Figure 2. Of these sharks, total of 464 bonnetheads were tagged and re- 890 (64.6%) individuals were tagged, with 40 leased, with 18 of these being recaptured once of these being recaptured at least once (recap- (3.9%) and three individuals recaptured twice ture rate = 4.5%). An overall shark mortality rate (0.6%). The longest duration between tag and of 7.8% was reported by the time of release, while recapture was 1,231 d, and this specimen was 81.5% of the sharks caught were released in good recaptured within 0.5 km of the tagging site. The condition and 10.7% of the specimens were clas- longest distance traveled between the site of sified as weak. capture and recapture was 11.1 km (straight line) All 485 rajiformes caught in the Ten Thou- over a time span of 5 d (Table 5). sand Islands estuary between 1997 and 2002 Bonnetheads were caught in every month were caught with gill nets (Table 3). Cownose of the year except January (Figure 3). Overall rays (50%) were the most abundant rajiformes CPUE was by far the highest (0.63) reported for caught, followed by stingrays Dasyatis sp. any elasmobranch species in the Ten Thousand (24%), spotted eagle rays (18%), and Atlantic Islands vicinity. Considering the monthly gill- guitarfish (6%). Less than 5% of the rajiformes net effort, this species showed the highest abun- catch consited of smooth Gymnura dance in February, August, and November (CPUE

TABLE 2. Number, percentage of total catch, sex, life stage and size range of all shark species caught in the Ten Thousand Islands, Florida from 1997 to 2002 during both gill-net and longline sets. (m: male, f: female, ns: not sexed; imm: immature, yoy: young of the year and neonates; PCL: precaudal length) Sex Life stage PCL (cm) Species Number % m f ns mature imm yoy min max Bonnethead 722 52.4 395 318 9 436 281 5 25 80 Blacktip shark 328 23.8 139 179 10 0 19 309 33 128 Bull shark 211 15.3 101 99 11 0 133 78 43 120 Lemon shark 65 4.7 26 35 4 0 57 8 54 163 Nurse shark 28 2.0 12 10 6 0 28 0 45 141 Great hammerhead 13 0.9 2 11 0 0 13 0 101 150 Atlantic sharpnose shark 7 0.5 4 2 1 1 5 1 24 66 Scalloped hammerhead 2 0.1 2 0 0 0 1 1 36 52 Tiger shark 1 0.1 1 0 0 0 1 0 153 153 TOTAL 1,377 100.0 682 654 41 437 538 402 THE OCCURENCE AND DISTRIBUTION OF ELASMOBRANCHS IN THE TEN THOUSAND ISLANDS ESTUARY 241 150.8 55.7 155.9 37.1 154.7 44.3 156.9 59.9 80–300 99–210 81–420 119–153 140.4 12.6 100–154 119.0 20.6 80–288 152 62.5 61–330 152 58.8 75–250 120 34.5 81–420 165 46.8 76–400 155 47.3 100–310126–149 162 138 52.9 11.5 0.9 84–400 g gill-net and longline sets. SD to 2002 during gill-net sets; (%: 3.7–5.3 4.6 0.6 4.9–6.6 5.7 0.7 2.7–7.3 5.2 0.9 3.3–8.4 5.1 0.8 4.8–6.7 6.0 0.8 3.2–10.6 5.3 33.7 2.8 32.9 2.5 36.1 4.0 30.836.1 6.8 5.0 30.6 4.9 5.0–6.6 5.8 0.8 3.6–7.1 4.6 1.0 3.1–6.6 4.9 0.9 2.5–7.3 4.6 1.1 2.2–8.6 5.0 1.3 3.4–8.6 5.0 0.7 2.7–8.7 4.8 0.9 Salinity (ppt)(mg/L) DO (cm) Depth 30.6–38.2 30.6–37.7 25.9–42.5 21.6–40.9 18.2–42.7 22.8–34.0 37.7 0.3 36.2 2.6 35.1 3.4 31.6 5.8 22.4 11.3 35.6 3.6 31.3 5.6 29.6 0.9 29.0 0.7 27.6 2.7 27.627.5 2.8 3.5 26.2 4.9 Salinity (ppt)(mg/L) DO (cm) Depth 26.3 38.3 5.3 190 range mean SD range mean SD range mean SD range mean SD 28.0–30.6 28.1–29.7 20.2–32.7 17.3–33.6 20.5–33.1 20.9–31.5 0.5–41.7 37.4–37.9 32.4–41.4 30.6–40.9 18.4–39.1 18.7–41.6 14.4–41.7 a 27.5 0.5 28.2 2.3 28.8 0.9 28.5 2.3 28.8 2.8 29.1 1.7 28.6 2.4 253.0 DL DW (°C) Temperature a was measured. 50.5 67.0 15.0 22.0 25.0 54.0 36.0 80.0

109.0 Temperature (°C) Temperature 30.6 37.3 6.2 186 27.7 38.2 4.9 450 range mean SD range mean SD range mean SD range mean SD 2.9 20.0 35.0 20.0 40.0 27.0–28.0 23.4–30.5 25.9–30.5 21.9–32.1 19.7–33.6 23.5–33.6 20.0–33.6 4. Environmental conditions inhabited by all shark species caught in the Ten Thousand Islands, Florida from 1997 to 2002 durin Thousand Islands, Ten all shark species caught in the conditions inhabited by 4. Environmental 3. Number, size range and range of environmental conditions of all rays caught in the Ten Thousand Islands, Florida from 1997 Ten conditions of all rays caught in the size range and range of environmental Number, 3. sp. 118 24.3 ABLE ABLE T T The total length of the smalltooth sawfish Atlantic sharpnose shark Scalloped hammerhead Great hammerhead Nurse shark Lemon shark Bull shark Blacktip shark = standard deviation; DO dissolved oxygen. Species Bonnethead Tiger shark Smalltooth sawfish 6 1.2 Atlantic guitarfishSmooth butterfly ray 29 14 6.0 percentage of total catch, DL: disc length, DW: disk width, DO: dissolved oxygen, SD = standard deviation. Species Number %TOTAL mina max min max 485 100 Cownose rayDasyatis Spotted eagle ray 228 89 47.0 18.4 30.0 98.0 46.0 150.0 Lesser 1 0.2 242 STEINER, MICHEL, AND O’DONNELL

170

1 160 1 1 1 150 1 512 140 62 52 130 172 1411 120 131 453 110 444 21121 2 100 16114 16 2 2 90 13 2 1 171 80

Precaudal Length (cm) 12 22 1 2 40 4 25 3 70 50 3 16 49 8 23 5 60 115 11 38 2 1 190 44 10 1 50 79 154 1 3 1 37 83 2 1 40 87 5 1 1 50 1 30 2 1 20 bull shark tiger shark nurse shark bonnethead lemon shark blacktip shark great hammerhead scalloped hammerhead Atlantic sharpnose shark

FIGURE 2. Length-frequency distribution of the nine species of sharks examined during the longline and gill-net survey of the Ten Thousand Islands estuary, Florida between 1997 and 2002. THE OCCURENCE AND DISTRIBUTION OF ELASMOBRANCHS IN THE TEN THOUSAND ISLANDS ESTUARY 243

TABLE 5. Shark recaptures within the Ten Thousand 5.4 kg) was retrieved from the net, carrying 18 Islands, Florida, 1997–2002. The number of days expresses embryos. Both uteri contained nine embryos (left the time passed between capture and recapture; dist (km) is uterus: six males, three females; right uterus: two the straight line distance travelled between site of capture males, seven females). Size range of the embryos and recapture; 0.0 km indicates that the shark was caught within 500 m of the original capture site. was 15.8–17.0 cm PCL. On 27 May 2000, an- other dead female bonnethead was found in the Species Sex Days Dist (km) gill net, carrying nine embryos (five males and Bull shark f 0 0.0 four females). The bonnethead’s mortality rate was Bull shark m 29 0.0 Bull shark m 39 3.6 10.8% at the time of release; 75.5% of the indi- Bull shark f 59 3.6 viduals were released in good condition and Bull shark m 63 0.0 13.7% were classified as weak. Bull shark f 158 0.0 Bull shark f 165 0.0 Bull shark f 209 0.0 Blacktip shark Blacktip shark m 0 0.0 Most blacktip sharks (97%) were caught with Blacktip shark f 2 0.0 Blacktip shark m 3 0.0 gill nets, while 11 specimens were caught with Blacktip shark m 14 0.0 longlines. Size range of this species was 33–128 Blacktip shark f 17 0.0 cm PCL (Table 2; Figure 2). A total of 193 (59%) Blacktip shark f 25 1.0 Blacktip shark f 25 4.7 blacktip sharks were tagged, of which 11 were Blacktip shark m 32 1.0 recaptured (5.7%). The longest duration between Blacktip shark f 35 ? tag and recapture was 87 d, where the individual Blacktip shark f 48 0.0 was recaptured in the same bay as the original Blacktip shark f 87 0.0 Lemon shark f 1 0.0 capture site. The longest distance traveled by a Lemon shark m 3 0.0 blacktip shark was 4.7 km (straight line) over a Lemon shark m 58 0.0 time period of 25 d (Table 5). Bonnethead m 0 0.0 Bonnethead f 0 0.0 Blacktip shark captures were rare (CPUE < Bonnethead m 1 0.0 0.1) or even absent early and late in the season Bonnethead f 5 11.1 (Figure 3). Blacktip sharks were most abundant Bonnethead f 6 0.0 between May and August, with clear peaks in Bonnethead m 9 0.0 Bonnethead f 15 0.0 June (CPUE = 0.8) and July (CPUE = 0.5). Speci- Bonnethead m 30 0.0 mens still showing an umbilical scar were re- Bonnethead f 32 0.0 ported from the beginning of May through the Bonnethead f 42 0.0 beginning of August. Immature blacktip sharks Bonnethead f 60 10.5 Bonnethead f 127 0.0 were occasionally caught in the estuary, but they Bonnethead m 323 3.0 usually stayed around the Gulf front islands. Bonnethead m 338 0.0 Almost 83% of the individuals caught were re- Bonnethead m 358 0.0 Bonnethead f 392 8.2 leased in good condition. Mortality rate at the Bonnethead m 404 0.0 time of release was 5.2% and 12% of the sharks Bonnethead f 461 4.7 were released in a weak condition. Bonnethead f 1144 0.0 Bonnethead m 1176 0.0 Bonnethead m 1231 0.0 Bull shark

A total of 193 bull sharks were caught with gill = 0.7) and the lowest abundance in December and nets and 18 with longlines. Size range for this January (CPUE = 0.13 and 0.00, respectively). In species was 43–120 cm PCL (Table 2; Figure 2). March 1998, a school of 51 (28 male and 23 fe- A total of 193 bull sharks were tagged (91%), of male) immature bonnetheads ranging from 34 to which 8 individuals have been recaptured 54 cm were caught in one net set. This resulted in (4.1%). The longest duration between tag and an exceptionally high CPUE for that month. In recapture was 209 d, and the recapture location all other months, CPUE was reported between 0.4 was in the same bay as the tagging site. The long- and 0.6. Two neonate specimens were caught on est distance traveled between the site of capture 29 May 1999 and 2 June 2000. In July 1998, a and recapture was 3.6 km (straight line) for two dead female bonnethead (PCL = 74 cm; weight = bull sharks. These two bull sharks had a time 244 STEINER, MICHEL, AND O’DONNELL

bonnethead blacktip shark 2.0 140 0.8 120

120 100 1.5 0.6 100 80 80 1.0 0.4 60 CPUE CPUE

60 number number

40 40 0.5 0.2

20 20

0.0 0 0.0 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

CPUE 0.00 0.68 1.86 0.41 0.49 0.49 0.59 0.71 0.54 0.59 0.71 0.13 CPUE 0.00 0.00 0.01 0.11 0.34 0.76 0.49 0.29 0.09 0.05 0.08 0.04 number 0 32 130 22 79 70 112 105 66 86 17 3 number 0 0 1 6 55 109 93 43 11 7 2 1

bull shark lemon shark

0.8 60 0.10 20

50 0.08 0.6 15 40 0.06

0.4 30 10 CPUE CPUE number number 0.04 20 0.2 5 0.02 10

0.0 0 0.00 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

CPUE 0.04 0.23 0.06 0.15 0.10 0.08 0.25 0.33 0.21 0.11 0.21 0.67 CPUE 0.00 0.00 0.09 0.10 0.05 0.08 0.06 0.07 0.04 0.04 0.00 0.00 number 1114 8171147492616516 number 006681212105600

nurse shark great hammerhead

0.10 10 0.10 10

0.08 8 0.08 8

0.06 6 0.06 6 CPUE CPUE number 0.04 4 number 0.04 4

0.02 2 0.02 2

0.00 0 0.00 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

CPUE 0.00 0.02 0.00 0.07 0.02 0.03 0.03 0.05 0.00 0.02 0.00 0.00 CPUE 0.00 0.00 0.00 0.00 0.03 0.02 0.01 0.02 0.00 0.00 0.00 0.00 number 010444570300 number 000053230000

FIGURE 3. Monthly gill-net catch per unit effort and number of sharks caught during longline and gill-net sets within the Ten Thousand Islands estuary, Florida from 1997 to 2002.

span between capture and recapture of 39 and tion. In 2.8% of the cases, the sharks were classi- 59 d (Table 5). fied as weak, and 3.8% of the specimens were Bull sharks were caught in every month of reported as dead by the time of release. the year (Figure 3). On a monthly basis, CPUE was low from January through June (≤0.15). Lemon shark Abundance of bull sharks then slightly increased from July through November (CPUE 0.21–0.33) A total of 31 lemon sharks were caught with and peaked in December (0.67). The exceptions gill nets and 34 with longlines. The size range to this pattern were found in October when CPUE of lemon sharks caught was between 54 and was low (0.11) and February when catches were 163 cm PCL (Table 2; Figure 2). A total of 16 relatively high (CPUE = 0.23). Immature bull lemon sharks were tagged, of which 3 were re- sharks were observed all year round. Most of the captured. Time between capture and recapture bull sharks (93%) were released in good condi- was 1, 3, and 58 d. All three specimens were THE OCCURENCE AND DISTRIBUTION OF ELASMOBRANCHS IN THE TEN THOUSAND ISLANDS ESTUARY 245 recaptured in the area of the initial capture site Scalloped hammerhead (Table 5). Lemon sharks were not caught in the A total of two male, scalloped hammerheads were months of November through February (Figure caught in gill nets. One specimen was immature 3). In the remaining months, catch rates were (52 cm PCL) and one was a young of the year always low (CPUE = 0.04–0.11). The one speci- (36 cm PCL) (Table 2; Figure 2). Both speci- men still showing an umbilical scar was caught mens were dead when retrieved from the gill net on 22 June 1999. Only one lemon shark died in July 1998 and July 2000. during this investigation. More than 95% of the animals were released in good condition, Tiger shark and 3% were classified as weak by the time of A single, immature, male tiger shark was caught release. with the longline on 18 May 1999 (Table 2; Fig- ure 2). The specimen could not be tagged but Nurse shark was released in good condition. A total of seven nurse sharks were caught with gill nets; the remaining 19 sharks were caught Cownose ray with longlines. The range of PCL for this spe- cies was between 45 and 141 cm (Table 2; Fig- Cownose rays were captured in every month of the ure 2). A total of seven nurse sharks were tagged year except December (Figure 4). Peak abundance with no recaptures noted to date. Nurse sharks was in September (CPUE = 0.47). Moderate catches were absent in the following months: January, were realized in March, May, August, October, and March, September, November, and December November (CPUE = 0.17–0.29) while all other (Figure 3). In all other months, CPUE was low months showed a low CPUE (<0.1). (0.02–0.07). All nurse sharks were released in good condition. Stingray Dasyatis sp. A total of 118 stingrays were caught in gill nets. Great hammerhead shark Some were not brought aboard; therefore, they A total of 12 great hammerheads were caught with were identified to the genus level only without gill nets, with one captured by longline. All 13 identifying their sex or taking any measurements. specimens were immature (100–144 cm PCL) The two most abundant stingray species known (Table 2; Figure 2). A total of 11 great hammer- in this area are the southern stingray and the heads (85%) were tagged, but none of these have Atlantic stingray. The highest catch rates for the been recaptured to date. All specimens were stingrays were recorded in February, March, May, caught between May and August (CPUE = 0.01– and June (CPUE = 0.11–0.23) (Figure 4). In all 0.03) (Figure 3). other months of the year, CPUE was low (<0.1) or even zero (January and April). Atlantic sharpnose shark All seven Atlantic sharpnose sharks were caught Spotted eagle ray with gill nets, with six being tagged and no re- The highest catch rates for spotted eagle rays were captures to date. Range of PCL for Atlantic reported in May (CPUE = 0.21); moderate catches sharpnose sharks was between 24 and 66 cm PCL were realized in February (CPUE = 0.11) and No- (Table 2; Figure 2). Catch rates for Atlantic vember (CPUE = 0.13); none were reported in De- sharpnose sharks were highest in March (CPUE cember and January (Figure 4); and in all other = 0.06). Rare catches were recorded in February, months, catches were relatively rare (CPUE <0.1). May, and June (CPUE = 0.01–0.02). No speci- mens were caught in any other month of the year. Atlantic guitarfish The one specimen showing an umbilical scar Of the 29 Atlantic guitarfish, 50% were caught in was caught on 3 June 1999. Almost 86% of the the month of April (Figure 4). Catch rates for ev- sharks were released in good condition, and 14% ery other month were very low (<0.05) or even were classified as weak. zero (November through March). 246 STEINER, MICHEL, AND O’DONNELL

cow nose ray Dasyatis sp.

0.5 60 0.3 40

50 0.4 30 40 0.2 0.3

30 20 CPUE CPUE 0.2 number number 20 0.1 10 0.1 10

0.0 0 0.0 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

CPUE 0.04 0.09 0.21 0.07 0.26 0.09 0.14 0.22 0.47 0.17 0.29 0.00 CPUE 0.00 0.13 0.21 0.00 0.23 0.11 0.09 0.07 0.06 0.05 0.04 0.04 number 1 4 154 4313263258257 0 number 0 6 15 0 37 15 17 11 7 8 1 1

spotted eagle ray Atlantic guitarfish

0.3 40 0.3 20

30 15 0.2 0.2

20 10 CPUE CPUE number number

0.1 0.1 10 5

0.0 0 0.0 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec CPUE 0.00 0.11 0.07 0.02 0.21 0.11 0.06 0.04 0.02 0.04 0.13 0.00 CPUE 0.00 0.00 0.00 0.28 0.04 0.01 0.01 0.01 0.01 0.01 0.00 0.00 number 0 5 5 1 34 15 12 6 2 6 3 0 number 0001561221200

smooth butterfly ray smalltooth sawfish

0.10 5 0.10 5

0.08 4 0.08 4

0.06 3 0.06 3 CPUE CPUE number 0.04 2 number 0.04 2

0.02 1 0.02 1

0.00 0 0.00 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec CPUE 0.00 0.02 0.07 0.00 0.01 0.01 0.01 0.03 0.00 0.01 0.00 0.00 CPUE 0.00 0.06 0.00 0.00 0.00 0.01 0.01 0.00 0.01 0.00 0.00 0.00 number 015011140100 number 030001101000

FIGURE 4. Monthly gill-net catch per unit effort and number of rajiformes caught during gill-net sets within the Ten Thousand Islands estuary, Florida from 1997 to 2002.

Smooth butterfly ray Lesser electric ray

Monthly catches of this species were rare (CPUE A single specimen of the lesser electric ray was 0.01–0.03) or absent (January, April, September, caught on 22 May 2000 without being sexed nor November, December), except in March, when a measured. clear peak of catch rate was recorded (CPUE = 0.07) (Figure 4). Discussion

Smalltooth sawfish Species composition A total of six smalltooth sawfish were caught in With a total of 17 species recorded, elasmobranchs gill nets with three captured in February. Single showed high diversity in the Ten Thousand Is- catches were also realized in June, July, and Sep- lands estuary. Snelson and Williams (1981) tember (Figure 4). caught 15 species of elasmobranchs (eight shark THE OCCURENCE AND DISTRIBUTION OF ELASMOBRANCHS IN THE TEN THOUSAND ISLANDS ESTUARY 247 and seven ray species) in the Indian River La- diate mortality of 43% for juvenile blacktip sharks goon system on the east coast of Florida. In Florida using 1-h gill nets and estimated that an addi- Bay, only 63 specimens of three species of sharks tional 14% succumbed to postrelease mortality. (bonnethead, blacktip shark, and lemon shark) In our study, a handling mortality of 7.3%, and in were recorded, even though the net time was much the study by Steiner and Michel (2007), a longer and similar sampling gear was used postrelease mortality of 25%, was observed for (Sogard et al. 1989). Further north, Castro (1993) blacktip sharks. Shorter set durations and more reported nine species of sharks within the shark frequent checks of gears might reduce mortality. nursery of Bulls Bay, South Carolina. Conversely, bull sharks showed a very low imme- A comparison was made with a similar study diate mortality of 2.4% and a low postrelease of shark nurseries along a larger stretch of Florida’s mortality as well. Only 1 of 11 individuals west coast (Hueter 1999), revealing more infor- tracked died after release (Steiner and Michel mation on the composition of the shark commu- 2007). Bull sharks seemed to recover much bet- nity of the Ten Thousand Islands. Hueter (1999) ter than other shark species, except for nurse recorded 13 species of sharks using similar sam- sharks, of which no individual showed any signs pling gear. The higher diversity in his study may of stress. The divergent mortality rate of bull have been due to the longer sampling period, sharks versus blacktip sharks could be partially larger sampling area, and higher diversity of the explained by their differing behavior during cap- habitats sampled. ture. Blacktip sharks struggled and were literally Sixty-five percent of all sharks in our study wrapped up in the net, often unable to pass water were tagged, and the overall recapture rate was over their gills. It took several minutes to free the 5%. The highest recapture rate for a single spe- shark, and if it still had strength, the shark kept cies was 5.7% for the blacktip shark. In a study, on fighting while being measured and tagged. where fishing was also conducted in a restricted Bull sharks, on the other hand, were calm or even area, with similar intensity, the resulting recap- sluggish during their capture. Bull sharks were ture rate for young sandbar sharks Carcharhinus often totally immobile as long as they were com- plumbeus was comparable at 6.4% (Merson and pletely in the water. Bonnetheads had the high- Pratt 2001). Contrary to the recapture results in est mortality rate (20.7%). Considering the Merson and Pratt (2001), the sharks in this inves- anatomy of this species, it is not surprising that tigation did not travel far between capture and this species gets easily entangled in the net. With recapture locations. Only eight specimens (19% the wide “shovel-shaped” head, even a small of all recaptures) were recaptured at sites that were bonnethead could not just slip through the mesh. more than 1 km away from the original capture Most bonnetheads were heavily entangled, result- site, indicating a relatively low rate of movement ing in a longer handling time. of the sharks within the estuary. This suggestion was supported by the tracking data of juvenile Predation blacktip and bull sharks (Steiner and Michel 2007, this volume). Steiner and Michel (2007) reported Merson and Pratt (2001) observed predation on that, on a daily basis, bull sharks rarely left the young-of-the-year sandbar sharks in Delaware area of capture and blacktip sharks normally re- Bay. Van der Elst (1979) demonstrated that other turned to the place of capture within one tidal species of sharks can cause significant degrees of cycle. Another example of site fidelity in this predation in some nursery areas. In our study, study was a bonnethead that was recaptured at neonate blacktip sharks and bonnetheads were the same spot 337 d after tagging. Most of the attacked by other sharks. Scars on the sharks in sharks, however, were recaptured within 40 d. the net indicated that the attackers were larger sharks. Steiner and Michel (2007) observed Mortality young blacktip sharks being consumed by larger sharks during tracking. The same observation was In several studies, information on catch mortal- made by Morrissey (1991), who also lost some ity can be found. Gruber et al. (2001) observed a juvenile lemon sharks to predation during a track- handling mortality of 0% to 6.6% for juvenile ing study. Springer (1967) stated that the only lemon sharks. Hueter (1999) observed an imme- important predators of sharks are other sharks and 248 STEINER, MICHEL, AND O’DONNELL nursery areas may be chosen based on the absence inshore, might suggest that adult, female bull of large sharks. With the exception of bonnetheads sharks enter the Ten Thousand Islands estuary to and one Atlantic sharpnose shark, no adult speci- give birth. Further investigations (currently un- mens were collected during this study. The sam- derway) are needed to verify if females of other pling gear might not have been strong enough to shark species enter the estuary to give birth. catch mature sharks of the larger species. There Blacktip sharks caught in the Ten Thousand were some indications that large animals were in Islands were estimated to be a couple of days old the estuary. Occasionally, gangions of the longline (umbilical scar still open) to 5+ years. Age was were ripped apart and large holes were found regu- estimated according to the von Bertalanffy growth larly in the net. It remains unknown whether adult curve calculated by Killam and Parsons (1989). or immature sharks caused these holes. Although Since no adult blacktip sharks were caught within predation occurs within the Ten Thousand Islands the estuary, it remains unknown if their parturition estuary, it is presumed to be higher in the adjacent takes place outside the estuary or if the female open waters of the gulf where larger shark species enters the estuary to give birth. It is assumed that and individuals are abundant (S. Theberge, Oregon newborn blacktip sharks stay within the estuary State University, formally of the Florida Depart- for their first season only. In preparation for winter, ment of Environmental Protection, personal com- adult blacktip sharks of Florida migrate to winter- munication). ing grounds off southern Florida and the Keys. The young might migrate in the same general di- Nursery ground aspects rection as the adults, although the timing of their migration is usually different (Castro 1993 and The family Carcharhinidae is the most abundant 1996). Hueter (1999) found that young blacktip and diverse group of sharks in tropical coastal sharks inhabit nurseries in the coastal areas of waters (Garrick 1982; Compagno 1984), and nurs- Yankeetown, lower Tampa Bay, and Pine Island ery areas have been reported for a number of spe- Sound, Florida in spring and summer, leave the cies of this family (Van der Elst 1979; Medved nurseries in the fall, and generally migrate south, and Marshall 1981; Snelson et al. 1984; Gruber with some recaptures in winter occurring as far et al. 1988). The utilization of a single area as a south as the Florida Keys. Returns of 1- and 2- nursery by a number of species may be advanta- year-old juvenile blacktip sharks back to their na- geous in reducing predation (Simpfendorfer and tal nursery in the spring/summer of subsequent Milward 1993). The Ten Thousand Islands could years were also shown by Hueter (1999). Simp- be a multispecies nursery ground with neonates fendorfer and Milward (1993) found that blacktip of three species and young-of-the-year specimens sharks use Cleveland Bay, Australia as a seasonal of four species collected in this study. primary nursery, with neonates and young of the Based on the observed temporal and spatial year occurring only for a few months each year distribution of sharks by size, sex, and migratory immediately after birth. In this study, blacktip re- patterns, three different areas of use can be iden- captures occurred within 18 months and were re- tified (Castro 1993): (1) adult feeding areas, (2) captured within a few kilometers of their original mating areas, and (3) nursery areas. The latter are capture/tag location. characterized by the presence of both gravid fe- Bull sharks primarily utilized the backwater males and free swimming neonates. For the spe- of the Ten Thousand Islands as a nursery area. If it cies-specific classification, the category “nursery can be classified as a primary nursery remains area” was further distinguished into primary and unknown. Whether older bull sharks frequently secondary nurseries according to Bass (1978). entered the estuary, or if they stayed there for the Various elasmobranch and species utilize whole season, was not determined. Although not the Ten Thousand Islands as a nursery ground. as abundant as in the summer months, bull sharks Our capture of female bonnetheads carrying full- were also present in winter months in the back- term embryos suggests that they use the Ten Thou- waters. Bull shark catches during the cold months sand Islands as a nursery. The fact that one neonate of January and February were also reported in bull shark with a small part of the umbilical cord other studies that examined some Florida coastal still attached (indicating that the shark is only a lagoons (Dodrill 1977; Gilmore et al. 1978; day or two old) was found approximately 5 km Snelson and Bradley 1978). The results of those THE OCCURENCE AND DISTRIBUTION OF ELASMOBRANCHS IN THE TEN THOUSAND ISLANDS ESTUARY 249 studies support the statement of Snelson et al. ordinating the realization of the project. Thanks (1984) who suggested that the winter season to the crew of the Center for Shark Research at might reflect depressed bull shark activity caused Mote Marine Laboratory, Sarasota, Florida for sci- by low water temperatures rather than emigra- entific advice, tags, and tag return data. Finally, tion from lagoonal waters. Bull sharks from neo- we are grateful for the help from countless volun- nate to up to about 8 years old were caught in teers who willingly assisted in field activities, this study. Age estimates are based on the von significantly contributing to the overall success Bertalanffy curve calculated by Branstetter and of this study. Stiles (1987). References Conclusions Branstetter, S. 1987. Age and growth estimates for Similar to other shark nurseries along the Florida blacktip, Carcharhinus limbatus, and spinner, C. coast, the Ten Thousand Islands combines the brevipinna, from the Northwestern Gulf of Mexico. Copeia 4:964–974. characteristics of a valuable nursery ground for Branstetter, S., and R. Stiles. 1987. Age and growth esti- sharks: shallow waters, highly productive, abun- mates of the bull shark, Carcharhinus leucas, from dant food sources, and possible reduced preda- the northern Gulf of Mexico Environmental Biol- tion risk (Springer 1967; Castro 1987). The ogy of 20(3):169–181. presence of many neonate and young-of-the-year Bass, A. J. 1978. Problems in studies of sharks in the sharks indicates a possible multispecies nursery southwest Indian Ocean. Pages 545–594 in E. S. area. Further investigations into the use of the Hodgson and R. F. Mathewson, editors. Sensory bi- ology of sharks, skates and rays. Department of the nearly pristine Ten Thousand Islands area as a Navy, Office of Naval Research, Arlington, Virginia. shark nursery are currently underway. Elasmo- Carrier, J. C., and H. L. Pratt, Jr. 1998. manage- branch monitoring will continue in this area to ment and closure of a nurse shark breeding and nurs- document possible changes in species occurrence ery ground. Fisheries Research 39:209–213. and distribution among top predators due to hy- Carter, M. R., L. A. Burns, T. R. Cavinder, K. R. Dugger, drologic restoration of freshwater flows to the Ten P. L. Fore, D. B. Hicks, H. L. Revells, and T. W. Schmidt. 1973. Ecosystem analysis of the Big Cy- Thousand Islands estuary planned in the near fu- press Swamp and estuaries. Pages V–7 in South ture. This data will be valuable to natural resource Florida Ecological Study. U.S. Environmental Pro- managers and researchers alike to guide the res- tection Agency Region IV, Surveillance and Analy- toration of estuarine systems and increase the sis Division, Athens, Georgia. knowledge base of shark nursery areas. Castro, J. I. 1987. The position of sharks in marine bio- logical communities. Pages 11–17 in S. Cook, edi- Acknowledgments tor. Sharks, an inquiry into biology, behavior, fisheries, and use, Oregon State University Exten- Thanks to the following foundations that sup- sions Service, Corvallis. Castro, J. I. 1993. The shark nursery of Bulls Bay, South ported this work: Uarda Frutiger-Fonds der Carolina, with a review of the shark nurseries of the Freiwilligen Akademischen Gesellschaft, Basel; southeastern coast of the United States. Environmen- Stiftung für experimentelle Zoologie, Basel; tal Biology of Fishes 38:37–48. Ausbildung-Stiftung für den Kanton Schwyz und Dodrill, J. W. 1977. A hook and line survey of the sharks die Bezirke See und Gaster (Kanton St. Gallen); of Melbourne Beach, Brevard County, Florida. Stiftung Joachim de Giacomi der Schweizer- Master’s thesis. Florida Institute of Technology, Melbourne. ischen Akademie der Naturwissenschaften; Dyer, K. R. 1997. Estuaries: a physical introduction. Wiley, Schweizer Tierschutz (STS); Kommission für New York. Reisestipendien der Schweizerischen Akademie Garrick, J. A. F. 1982. Sharks of the genus Carcharhinus. der Naturwissenschaften; Dissertationsfond der NOAA Technical Report NMFS Circular 455. Universität Basel; Victorinox, Ibach, Switzerland; Gilmore, R. G., L. H. Bullock, and F. H. Berry. 1978. Swisslife, Zürich, Switzerland. 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