Journal of Experimental Marine Biology and Ecology 459 (2014) 61–69

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Journal of Experimental Marine Biology and Ecology

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Site fidelity of migratory bonnethead sharks Sphyrna tiburo (L. 1758) tospecific estuaries in South Carolina, USA

William B. Driggers III a,⁎, Bryan S. Frazier b, Douglas H. Adams c, Glenn F. Ulrich b, Christian M. Jones a,Eric R. Hoffmayer a, Matthew D. Campbell a

a National Marine Fisheries Service, Southeast Fisheries Science Center, Mississippi Laboratories, P.O. Drawer 1207, Pascagoula, MS 39567, United Statesb South Carolina Department of Natural Resources, 217 Ft. Johnson Rd., Charleston, SC 29412, United Statesc Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, 1220 Prospect Ave., #285, Melbourne, FL 32901, United States

⁎ Corresponding author. Tel.: +1 228 762 4591.E-mail address: william.driggers@noaa.gov (W.B. Drig

http://dx.doi.org/10.1016/j.jembe.2014.05.0060022-0981/Published by Elsevier B.V.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 21 February 2014Received in revised form 8 May 2014Accepted 9 May 2014Available online xxxx

Keywords:BonnetheadHabitat utilizationMovement patternsResidencySite fidelity

To examine the migratory patterns, habitat utilization and residency of bonnethead sharks (Sphyrna tiburo(L. 1758)) in estuarine systems within coastal South Carolina, a tag-recapture experiment was conducted from1998 to 2012 during which 2300 individuals were tagged. To assess the intra and inter-annual movements oftagged sharks, six estuaries within state waters were monitored using multiple gear types in addition to thecooperative efforts of recreational anglers throughout the southeastern United States. Over the course of theexperiment 177 bonnetheads were recaptured after 3 days to 8.9 years at liberty, representing a recapture rateof approximately 8%. All bonnetheads were recaptured within the same estuary where they were originallytagged on intra and/or inter-annual scales, with the exception of six individuals, which were recaptured duringmigratory periods (i.e. late fall, winter and spring) in coastalwaters off Florida, Georgia, North Carolina, and SouthCarolina. On 23 occasions cohesionwas demonstrated by groups ranging in size from 2 to 5 individuals that weretagged together and recaptured together,with times at liberty ranging from 12 days to 3.6 years. Additionally, 13individualswere recapturedmultiple timeswith times at liberty ranging from12days to 8.9 years; all individualswere recaptured in the same estuary where they were initially tagged. We hypothesize that bonnetheads areusing South Carolina's estuaries as summer feeding grounds due to the relatively high abundance of blue crabs(Callinectes sapidus), including ovigerous females during spring and summer months, and the location of theseephemeral yet predictable feeding areas is socially transmitted to relatively young, naïve sharks by experienced,older individuals. The high degree of intra and inter-annual site fidelity demonstrated by bonnetheads in thisregion offers unique opportunities for in situ study of various aspects of the biology of this species, includingidentification of essential habitats, growth, homing mechanisms, mortality rates, movement patterns and socialbehavior.

Published by Elsevier B.V.

1. Introduction

Among aquatic organisms, information pertaining to the move-ments of marine fishes is perhaps the least understood, especially forthose species that are highly migratory. Recent advances in acousticand satellite tracking have allowed researchers to obtain more detailedinformation of themovement patterns of somemarine fishes; however,the applicability of these technologies can be limited by the reliabilityand expense of electronic tags, the availability and maintenance ofacoustic receivers aswell as the size of the species in question in relationto the tag. As a result, many tagging studies continue to utilize conven-tional tags, which have been shown to be effective in assessing themovements and habitat utilization of many marine fishes, includingsharks (Kohler and Turner, 2001).

gers).

Distinct feeding, mating, nursery and pupping areas are utilizedduring the lifecycle of most coastal shark species (e.g. Castro, 1993;Driggers et al., 2008), all of which could be considered habitats essentialto survival and proliferation of populations. Although studies examiningthe relationship between long-term movement patterns and the use ofdistinct habitats for explicit purposes by sharks are relatively limited, abasic understanding is beginning to emerge for certain species(Simpfendorfer and Heupel, 2004; Speed et al., 2010). For example,Pratt and Carrier (2001) demonstrated that specific nurse sharks(Ginglymostoma cirratum (Bonaterre 1788)) repeatedly utilize adiscrete area around the Dry Tortugas as a mating area on a predictablecycle. Similarly, Goldman and Anderson (1999) reported that individualwhite sharks (Carcharodon carcharias (L. 1758)) regularly returned tothe South Farallon Islands to feed on northern elephant seals (Miroungaangustirostris (Gill 1866)), and Chapman et al. (2009) documented thathalf of the immature lemon sharks (Negaprion brevirostris (Poey 1868))remained in close proximity to their natal origin around Bimini,

62 W.B. Driggers III et al. / Journal of Experimental Marine Biology and Ecology 459 (2014) 61–69

Bahamas for approximately six years. Furthermore, Feldheim et al.(2014) demonstrated that on at least six occasions, female lemon sharksreturned 14–17 years after birth to their natal area in Bahamian watersto give birth. These and other examples (see Speed et al., 2010 for arecent review) suggest that site fidelity to specific habitats duringimportant periods in the life history of sharks could be more commonthan currently recognized.

In the western North Atlantic Ocean, the nearshore waters of SouthCarolina are a well-documented seasonal habitat for several species ofsharks, including bonnetheads (Sphyrna tiburo (L. 1758)) (Castro,1993; Ulrich et al., 2007). Bonnetheads, which occur in temperate,subtropical and tropical waters throughout the western Atlantic Ocean(Castro, 2011), inhabit South Carolina coastal waters from May untilOctober and are one of the most common coastal species found in thebays and estuaries of the region during that period (Ulrich et al.,2007). This small coastal hammerhead species is common in estuarineand nearshore areas throughout its range and frequently captured inrecreational and commercial fisheries operating in United States (U.S.)coastal waters. Total U.S. recreational and commercial landings in2011 were 161,302 kg, with approximately 92% of that total from therecreational sector (National Marine Fisheries Service, 2014). Bycatchof bonnetheads is also significant in some fisheries, including the GulfofMexico shrimp trawl fishery (Zhang et al., 2013). Despite the relative-ly high abundance of the species in shallow water habitats within thewestern North Atlantic Ocean and the regularity with which they arecaught in commercial and recreational fisheries, seasonal patterns inhabitat utilization of bonnetheads off the southeastern United Statesremain enigmatic. The objectives of this studywere to examine seasonalpatterns in habitat utilization of bonnetheads in the estuarine waters ofSouth Carolina and determine if individuals make repeated use of theseinshore habitats on short and/or long temporal scales.

2. Materials and methods

2.1. Sampling gear and locations

To examine the spatial and temporal utilization of South Carolina'scoastal waters by bonnetheads, gillnets and longline fishing gear were

Fig. 1. Sampling locations within the nearshore waters of South Carolina. Numbers in parenthelongline and 3 = trammel net.

deployed in several estuaries within the state boundary (Fig. 1).Sampling occurred between April and October from 1998 to 2012,with the majority of effort being expended between the months ofMay and September. Gillnets were either 231 m or 40 m long, 3 mdeep, and constructed of #177 monofilament with a stretched meshof 10.3 cm. Longline gear consisted of 305 m of 0.64 cm braided nylonmainline, with 50 gangions spaced approximately 6 m apart. Eachgangion was constructed of a 0.5 m, 91 kg test monofilament leader,size 120 snap, and a 12/0 circle hook. Additionally, longline gearwith a 1829 m 272 kg test monofilament mainline was deployed innearshore coastal waters outside of the estuaries during the sametime period. Gangions were of identical construction to the longlinegear set in estuarine waters with the exception of 14/0 and/or 15/0circle hooks being utilized. To minimize mortality, soak time waslimited to 20 min for gillnets and 60 min for longlines.

Bonnetheads were captured in five South Carolina estuaries, in-cluding Bulls Bay, Charleston Harbor, Copahee Sound, North Edisto,and St. Helena Sound (Fig. 1); however, the majority of sampling effortoccurred in Bulls Bay and North Edisto. Abiotic characteristics ofCharleston Harbor, North Edisto and St. Helena Sound are principallydictated by riverine and tidal influences while abiotic characteristics ofBulls Bay and Copahee Sound are primarily dictated by tidal forces. Assuch, the salinity of Charleston Harbor, North Edisto and St. HelenaSound is more dynamic than that of Bulls Bay and Copahee Sound.Seasonally mediated water temperatures are similar in all five estuaries(Dame et al., 2000).

2.2. Data collection and tagging

Once captured, the sex of each specimen was noted and fork length(FL) was measured in a straight line from the anterior tip of thecephalofoil to the posterior notch of the caudal fin along the axis ofthe body. ADalton Rototagwas then fixed to thefirst dorsal fin of sharksdeemed in good health based on level of vigor and nictitating eyelidresponse. Tags were imprinted with unique alphanumeric identifiersto allow individual identifications and provided contact informationto facilitate reporting of recaptures. If a shark was recaptured, whenpossible, its FL was measured and the tag was cleaned of any biofouling

ses represent gears deployed during study in the corresponding estuary: 1 = gillnet, 2 =

63W.B. Driggers III et al. / Journal of Experimental Marine Biology and Ecology 459 (2014) 61–69

before re-release. If the tag was damaged to a degree that obscuredreporting information, the tag was replaced. To test for potentialdifferences between the median size and length distribution ofbonnetheads captured and those tagged, Mann–Whitney–Wilcoxonand Kolmogorov–Smirnov tests were used, respectively. For compara-tive purposes between the current study and stretch total lengthsreported in other studies, the conversion between stretch total length(STL) and FL provided by Frazier et al. (2013a) was utilized: FL = (STL− 3.91) / 1.198.

2.3. Recapture analysis

Bonnetheads are reported to be present in South Carolina estuarinewaters from April through August (Ulrich et al., 2007), therefore, tagreturn data were separated into recaptures that occurred intra-annually (within the same calendar year; e.g. tagged in 2001 andrecaptured in 2001) and inter-annually (in a subsequent calendaryear; e.g. tagged in 2001 and recaptured in 2002) to examine sitefidelity on both temporal scales. Spatial differences in the bonnetheadsex ratios (F/M) and sex-specific tag return rates were examinedusing chi square tests with Yates' correction. The formula P = (1 / n)x

was used to calculate the probability that recaptured sharks wouldreturn to the estuary where they were originally tagged based onrandom chance alone, where n equals the number of estuarine systemseach returning individual would pass in favor of a particular location(i.e. Bulls Bay or North Edisto) and x equals the number of taggedindividuals returning to their location of original tagging. Inlets andsounds deemed to be potential habitats a bonnethead would pass infavor of a particular location during its springmigration north consistedof all major estuaries between Bulls Bay, South Carolina and Cumber-land Sound, Georgia. Estuarine waters south of Cumberland Soundwere not included as we assumed bonnetheads overwinter in thatregion before commencing their northerly spring migration.

Bonnethead capture data from a trammel net survey conducted infour South Carolina estuaries, including Bulls Bay, Charleston Harbor,St. Helena Sound, Winyah Bay, were inspected to determine if taggedsharkswere encountered in areas outside of those sampledwith gillnetsand longlines. Additionally these datawere utilized to verify the season-al presence of the species in the region reported Ulrich et al. (2007).

Fig. 2. Day of the year trammel net sets were conducted in the coastal waters of SouthCarolina from 1990 to 2013 (n = 8361 sets). Each point represents three sets. Julian dayof the year is indicated.

Trammel net surveys were conducted at least monthly duringall months of the year in multiple locations (Figs. 1 and 2). Watertemperature, dissolved oxygen and salinity data were collected ateach sampling site using an environmental profiler and sets utilized inanalyses were limited to those that occurred at salinities greater than15 (lowest salinity where a bonnethead was captured) and in locationswhere at least one bonnethead had been captured. Trammel nets usedduring these surveys were 184 m long by 2.1 m deep with 177 mmoutermesh and 63mminnermesh. Additionally, tag return informationbased on the recapture of tagged sharks in commercial and recreationalfisheries was scrutinized. These data were not included in the statisticalanalyses due to the vague recapture locations provided by the partici-pants. To differentiate between the data sets, those data collectedby us are referred to as “project” data whereas commercial and rec-reational recapture information is referred to as “participant” data. Allstatistical tests were considered significant at α = 0.05.

3. Results

Over the course of the study, 2743 bonnetheads were capturedduring 2095 gillnet (n = 1271 deployments) and longline (n = 824deployments) sets (Table 1). The ratio of females to males in the totalcatch of both gear types was 8.7:1.0 (n= 2435, 281 and 27 for females,males and sex not recorded, respectively). Females andmales ranged insize from 319 to 1074 mm FL (X ± SD= 820.4 ± 125.5 mm) and from345 to 860mm FL (X± SD= 652.3± 113.0 mm), respectively (Fig. 3).Tags were attached to 2300 individuals (2098 females, 188 males, 14sex not recorded) in Bulls Bay (n = 763), Charleston Harbor (n =107), Copahee Sound (n = 5), North Edisto (n = 1251) and St. HelenaSound (n= 174). Body length at the time of tagging ranged from 390 to860 mm FL for males (X ± SD = 662.5 ± 103.4 mm) and from 375 to1074 mm FL for females (X ± SD = 822.7 ± 120.5 mm) (Fig. 4 andTable 2). There were no significant differences between the median FL(W = 3.05 × 106, P = 0.22) and length distributions (K–S statistic =1.00, P = 0.27) of all sharks captured and those tagged. However,there was a significant difference in the sex ratio of all bonnetheadscaptured and those tagged (χ1

2 = 10.9, P b 0.01) with 86% of femalesand 67% of males captured being tagged.

3.1. Seasonality

There were 8361 trammel net sets conducted in all months of theyear in various locations in South Carolina's coastal waters (Figs. 1and 2). Dissolved oxygen, salinity and water temperature rangedfrom 1.8 to 17.1 mg/l (X ± SD = 6.70 ± 1.70 mg/l), from 0.0 to41.0 (X ± SD = 25.20 ± 7.14) and from 4.2 to 40.0 °C (X ± SD =21.09 ± 6.96 °C) throughout the year, respectively. Bonnetheads(n = 1781) were captured between April and mid-November (e.g.11/17/2005); however, no bonnetheads were captured during the3503 sets conducted between mid-November and March (Fig. 5).When bonnetheads were captured in South Carolina waters, dissolvedoxygen, salinity and temperature ranged 1.8 to 8.5 mg/l (X ± SD =5.63 ± 0.90 mg/l), 15.0–40.0 (X ± SD = 31.74 ± 4.12) and 17.8 to34.0 °C (X ± SD = 27.71 ± 2.79 °C), respectively.

3.2. Recaptures

A total of 141 tagged bonnetheads were recaptured with 13 individ-uals being recaptured multiple times (total number of recaptures =156). Given the low recapture rate of individuals tagged in St. HelenaSound (n = 2), Charleston Harbor (n = 1) and Copahee Sound (n =0), all further results and discussion will primarily focus on thebonnetheads recaptured in Bulls Bay and North Edisto. Within BullsBay there were 29 project recaptures resulting in a recapture rate of ap-proximately 4% after 3 to 2528 days at liberty. Within the North Edisto,there were 123 project recaptures after 3 to 3263 days at liberty,

Table 1Sampling effort by year andmonth. Numbers separated by commas indicate the number of gear deployments in Bulls Bay, Charleston Harbor, Copahee Sound, North Edisto and St. HelenaSound, respectively.

April May June July August September October

1998 0,0,0,0,0 0,0,0,0,0 0,0,0,15,0 0,0,0,4,0 12,0,0,0,0 3,0,0,2,0 0,0,0,0,01999 0,0,0,0,5 0,0,0,2,5 0,0,0,0,0 0,0,0,10,9 7,0,0,0,0 0,0,0,0,0 0,0,0,0,02000 0,0,0,0,5 7,0,0,0,4 6,0,0,5,0 0,0,0,8,0 13,1,0,7,0 4,0,0,14,0 0,0,0,0,02001 0,0,0,0,0 20,0,0,1,0 22,0,0,13,4 25,0,0,16,4 28,14,0,15,0 6,3,0,0,0 0,0,0,0,02002 0,0,0,0,0 14,6,0,0,0 9,5,0,10,0 14,7,0,8,0 11,5,0,11,0 0,6,0,0,0 0,5,0,0,02003 7,0,0,0,0 16,0,0,12,0 18,11,0,12,0 21,8,4,11,0 9,0,0,7,0 4,0,0,0,0 0,0,0,0,02004 0,0,0,0,0 8,0,0,5,0 14,5,0,0,0 10,5,0,0,0 4,0,0,0,0 5,4,0,7,0 0,0,0,0,02005 4,0,0,0,0 16,7,0,4,0 32,5,0,22,0 26,0,7,7,12 13,0,0,12,12 0,0,0,0,0 0,0,0,0,02006 0,0,0,3,0 26,0,8,4,14 17,3,0,5,35 39,0,0,5,0 31,0,0,32,11 0,0,0,0,9 0,0,0,0,02007 4,0,0,0,0 35,0,0,5,8 0,8,0,13,8 5,0,0,0,0 21,11,0,12,0 12,0,0,15,8 0,0,0,0,02008 0,0,0,11,0 19,2,0,9,0 4,0,0,17,0 10,0,0,10,0 11,0,0,0,19 36,0,0,8,0 0,0,0,0,142009 0,0,0,0,0 6,0,0,3,0 6,0,0,11,0 4,12,0,0,7 10,0,0,4,0 11,7,0,5,0 0,0,0,0,02010 0,0,0,0,0 30,8,0,12,0 18,7,0,5,23 20,0,0,12,16 14,0,0,0,0 0,9,0,0,0 0,0,0,0,02011 0,0,0,0,0 31,5,0,5,16 38,10,0,8,9 11,0,0,6,9 21,0,0,6,9 0,0,0,0,0 0,0,0,0,02012 9,0,0,6,0 24,0,0,6,14 40,29,0,13,8 45,0,0,7,16 24,0,0,0,9 5,0,0,0,0 0,0,0,0,0

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resulting in a recapture rate of approximately 10%. Additionally, therewere a total of 36 participant recaptures, after 9 to 1220 days at liberty,resulting in an overall tag return rate of 9% for bonnetheads tagged inBulls Bay and North Edisto. Bonnetheads were recaptured by partici-pants using hook and line (87%), trammel nets (7%), gillnets (4%) andshrimp trawls (2%). Recapture data indicated that bonnetheads migrat-ed south of South Carolina waters in the fall into waters off the Atlanticcoast of Florida before returning the following spring. For example,Shark B8192 was tagged in Bulls Bay on 7/20/2001, recaptured offMelbourne Beach, FL on 3/17/2002 and recaptured again in Bulls Bayon 5/14/2002. Similarly, Shark B11753 was tagged in Copahee Soundon 7/20/2005 and recaptured in Nassau Sound, FL on 9/23/2009, andShark B15855 was tagged in North Edisto on 6/9/2008 and recapturedoff northern Florida on 4/23/2010 (Fig. 6).

3.2.1. Intra-annual program recapturesTherewere a total of 77 intra-annual program recaptures with times

at liberty ranging from 3 to 104 days (mean = 41.9 days, SD = 24.6)(Table 2). In all cases, individuals were recaptured in the same systemwhere they were initially tagged and there were no examples ofmovements into other areas. On 17 occasions, groups ranging in sizefrom 2 to 5 individuals were tagged and recaptured on the same dayand in the same location with times at liberty ranging from 12 to 76days (X ± SD = 41.1 ± 22.8 days) (Table 3). For example, SharksB2586, B2588, B2614, B2621 and B2600were tagged in theNorth Edistoon 6/12/2001 and recaptured in the North Edisto on 8/27/2001. Therewas no obvious sexual or size segregation as both sexes were presentin five of the cohesive groups and sizes of sharks within groups wereusually not similar (Table 3). In three cases, individualswere recapturedtwice in the same location within the same year. For example, Shark

Fig. 3. Length frequency distribution of bonnetheads (Sphyrna tiburo) captured during thestudy from 1998 to 2012. Gray and white bars represent females and males, respectively.

531829 was initially tagged in the North Edisto on 5/28/2008 andrecaptured in the North Edisto on 6/09/2008 and 09/09/2008.

3.2.2. Intra-annual participant recapturesDays at liberty for the 12 intra-annual participant recaptures ranged

from 9 to 82 days (X ± SD = 51.0 ± 21.4 days). All individuals wererecaptured within the estuary in which they were tagged with theexception of two sharks. Shark B2134 was tagged in the North Edistoon 7/8/1999 and was recaptured on 9/28/1999 in the coastal waters ofsouthern Georgia. Shark B8245 was originally tagged in Bulls Bayon 8/6/2001 and recaptured off Johns Island, SC on 10/3/2001. Bothindividuals were recaptured south of their original tagging locations atthe time that coincides with the movement of bonnetheads out ofSouth Carolina's estuarine waters (Fig. 5).

3.2.3. Inter-annual project recapturesA total of 83 bonnetheads (81 females, 2 males) were project

recaptures at least one calendar year after tagging, with times at libertyranging from 278 to 3263 days (X±SD= 695.3± 548.9 days). Each ofthe recaptures occurred in the same estuary where the individualwas initially tagged. Nine individuals were recaptured in multipleyears (Table 4). For example, Shark B2077 was tagged in Bulls Bay on8/19/1998 and recaptured in Bulls Bay on 8/6/2001 and 7/21/2005.Sharks with multiple inter-annual program recaptures were at libertyfor 283 to 3263 days (X ± SD = 1053.7 ± 802.7 days). In sevencases, female bonnetheads in groups of two to four were tagged andrecaptured on the same days and in the same exact locations aftermore than one calendar year at liberty with times at liberty rangingfrom 283 to 1329 days (X±SD= 629.7± 427.0 days) (Table 3). Addi-tionally, two females, tagged two days apart in Bulls Bay (8/27 and 8/29

Fig. 4. Length frequency distribution of bonnetheads (Sphyrna tiburo) tagged during thestudy from 1998 to 2012. Gray and white bars represent females and males, respectively.

Table 2Summary of capture, tagging and recapture information for bonnetheads (Sphyrna tiburo) collected in Bulls Bay and North Edisto in the coastal waters of South Carolina.

Bulls Bay North Edisto

Female Male Female Male

Total caught 872 33 1241 190Size range (mm FL) 319–1074 392–815 371–1065 345–860Mean size ± SD (mm FL) 844.1 ± 126.6 560.3 ± 128.9 800.9 ± 123.1 682.7 ± 92.1

Number tagged 743 16 1106 137Size range (mm FL) 375–1074 412–741 429–1065 440–860Mean size ± SD (mm FL) 846.3 ± 118.9 598.2 ± 122.8 803.9 ± 210.2 687.6 ± 83.0

Total intra-annual recaptures 11 0 55 11Range of days at liberty 14–70 – 3–100 13–76Mean days at liberty ± SD 39.9 ± 15.2 – 41.7 ± 25.3 44.77 ± 30.1

Total inter-annual recaptures 18 0 62 3Range of days at liberty 282–2528 – 278–3263 230–367Mean days at liberty ± SD 870.8 ± 632.8 – 662.9 ± 525.2 313.0 ± 73.0

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2003),were recaptured in the same gillnet set in Bulls Bay on 7/10/2006after 1046 and 1048 days at liberty.

3.2.4. Inter-annual participant recapturesThere were 29 inter-annual participant recaptures with time

at liberty ranging from 159 to 1526 days ( X ± SD = 600.6 ±364.1 days). All participant recaptured sharks captured after onecalendar year at liberty were females and 20 were recaptured in thesame estuary where they were originally tagged. Of the nine that wererecaptured outside of their original tagging location, three were caughtoff the coast of Florida during winter months and five were caught inSouth Carolina coastal waters during times that coincided withmigrations into or out of estuaries. One of these individuals, SharkB8192, subsequently returned to their original estuarine tagginglocation. Two individuals, Shark B1909 and Shark B13150, wererecaptured in estuaries approximately 46 km and 300 km south andnorth, respectively, of their original tagging locations; however, bothsharks were tagged during the early spring at the time that coincidedwith migrations.

Fig. 5. Day of the year bonnetheads (Sphyrna tiburo) were collected during trammel netsurveys conducted in the coastal waters of South Carolina from 1990 to 2013 (n = 1781bonnetheads). Each point represents positive catch and can represent more than oneshark captured. Julian day of the year is indicated.

3.2.5. Probability of return to tagging locationAmong project recaptured sharks, the probability that all 83 would

return to the same location where they were initially tagged after onecalendar year at liberty was 1.03 × 10−25, assuming the only twosuitable habitats for these sharks were Bulls Bay or North Edisto. Inlets

Fig. 6. Locations of recaptures of bonnethead sharks off the east coast of Florida duringwintermonths (*) and estuarine systems along the southeastern coast of theUnited statesconsidered suitable habitat for the species: 1 = Cumberland Sound, 2 = St. AndrewSound, 3 = St. Simon Sound, 4 = Altamaha Sound, 5 = Doboy Sound, 6 = SapeloSound, 7 = St. Catherines Sound, 8 = Ossabaw Sound, 9 = Wassaw Sound, 10 =Calibogue Sound, 11 = Port Royal Sound, 12 = St. Helena Sound, 13 = North Edisto,14 = Stono Inlet, 15 = Charleston Harbor, 16 = Copahee Sound and 17 = Bulls Bay.Note resolution of map does not indicate waters associated with Copahee Sound.

Table 3Bonnetheads (Sphyrna tiburo) tagged and recaptured in groups of two or more individuals on the same dates and locations in the coastal waters of South Carolina. Asterisks indicate tworecaptures of the same individuals, Sharks B8882 and B8893. Size range refers to fork lengths (FLs) of individuals in group at the time of tagging.

Group size Female: male ratio Size range (mm FL) Tagging/recapture location Tagging/recapture date Days at liberty

2 2:0 915–1013 Bulls Bay 06-21-2001/08-06-2001 462 2:0 613–742 Bulls Bay 07-10-2006/08-08-2006 293 2:1 647–974 North Edisto 06-12-2001/08-14-2001 635 1:4 643–767 North Edisto 06-12-2001/08-27-2001 762 2:0 626–872 North Edisto 07-12-2001/08-14-2001 332 2:0 634–740 North Edisto 07-12-2001/08-27-2001 463 2:1 685–996 North Edisto 08-14-2001/08-27-2001 132 1:1 735–927 North Edisto 06-03-2002/08-16-2002 742 2:0 670–955 North Edisto 07-18-2002/08-16-2002 292 2:0 772–784 North Edisto 08-16-2002/06-06-2003 2942 2:0 798–817 North Edisto 06-06-2003/08-19-2003 74*2 2:0 798–817 North Edisto 06-06-2003/05-22-2006 1081*2 2:0 854–906 North Edisto 08-19-2003/08-12-2005 7244 3:1 622–776 North Edisto 06-14-2005/06-30-2005 162 2:0 642–747 North Edisto 07-13-2005/08-12-2005 302 2:0 667–914 North Edisto 08-12-2005/05-22-2006 2834 3:1 532–832 North Edisto 08-12-2005/08-25-2005 132 2:0 720–964 North Edisto 06-06-2007/08/03-2007 582 2:0 700–952 North Edisto 06-20-2006/05-11-2007 3252 2:0 705–955 North Edisto 05-11-2007/06-06-2007 262 2:0 710–910 North Edisto 06-22-2007/08-21-2007 604 4:0 715–834 North Edisto 05-28-2008/06-04-2009 3723 3:0 720–814 North Edisto 05-28-2008/06-09-2008 122 2:0 670–779 North Edisto 09-09-2008/04-30-2012 1329

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and sounds deemed other potential bonnethead habitats during spring,summer and fall months were considered and limited to those north ofFlorida. Estuarine waters associated with Florida were not includedas recapture data indicated that the coastal waters of Florida areoverwintering grounds (see above). Seventeen systems were con-sidered potential spring and summer habitats for bonnetheads andincluded Cumberland Sound, St. Andrew Sound, St. Simon Sound,Altamaha Sound, Doboy Sound, Sapelo Sound, St. Catherines Sound,Ossabaw Sound and Wassaw Sound in Georgia waters, and CalibogueSound, Port Royal Sound, St. Helena Sound, North Edisto, Stono Inlet,Charleston Harbor, Copahee Sound and Bulls Bay in South Carolinawaters (Fig. 6). Under the assumption that all systems were equallyviable spring, summer, and fall bonnethead habitat and that all sharkshad migrated into Florida waters during the winter, the probabilitythat all project recaptured individuals would return to the sameestuary where they were initially tagged on random chance alonewas 7.46 × 10−103.

4. Discussion

The results of this study provide another example to the growingbody of literature demonstrating intra- and/or inter-annual site fidelityof chondrichthyan fishes. However, the site fidelity of bonnetheads tospecific estuaries in South Carolina waters demonstrated herein exem-plifies, to our knowledge, the highest degree of inter-annual site fidelityknown among migratory sharks. Additionally, while much importancehas been placed, and rightfully so, on natal philopatry and the repeated

Table 4Bonnetheads (Sphyrna tiburo) recaptured multiple times after at least one calendar year at libe

Shark ID number Tagging/recapture location Tagging/r

B2077 Bulls Bay 08-19-19B8434 Bulls Bay 07-25-20B2916 North Edisto 06-03-20B8882 North Edisto 06-06-20B8893 North Edisto 06-06-20B11236 North Edisto 09-09-20B11584 North Edisto 06-30-20B11933 North Edisto 08-12-20B18091 North Edisto 06-06-20

use of specific nursery areas among certain shark species, our datademonstrate that other locations occupied during the life cycle couldbe of equal importance to the health of a population. Furthermore, ourresults underline the necessity to understand habitat utilization duringall phases of the life cycle of coastal sharks and other highly migratoryfishes.

The complete site fidelity of bonnetheads to Bulls Bay and NorthEdisto strongly suggests that these habitats are essential to the individ-uals that return to these estuaries. The question then becomes, what isthe importance of these estuaries to the bonnetheads that occupythem? As most bonnetheads that were recaptured on an inter-annualscale were females (96% of inter-annual recaptures), it is logical toassume that their fidelity to the area could be related to reproduction.Based on gross examinations of the reproductive systems of femalebonnetheads in South Carolina waters, Ulrich et al. (2007) reportedthat all mature females examined in late April and early May werecarrying embryos in the early stages of development. This timeframecoincides with the initial arrival of bonnetheads into South Carolina'sestuarine systems based on the trammel net survey data reportedherein and the findings of Ulrich et al. (2007), Castro (2011) andFrazier et al. (2013b). Although rarely observed, a limited number ofpostpartum females with mating scars have been observed in SouthCarolina waters (5% of mature females) in late September (B. Frazier,unpublished data); however, all bonnetheads captured during thisstudywere larger in size than the size at birth of 260–275mmFL report-ed by Parsons (1993) and Frazier et al. (2013a). Taken altogether, thesedata indicate that mating and parturition areas for bonnetheads are

rty in the coastal waters of South Carolina. All individuals were female.

ecapture dates Days at liberty after tagging

98/08-06-2001/07-21-2005 1083/252802/07-11-2003/08-08-2006 351/147502/05-22-2006/05-12-2011 1449/326303/08-19-2003/05-22-2006/05-11-2007 74/1081/143503/08-19-2003/05-22-2006/08-09-2006 74/1081/116004/06-30-2005/08-12-2005 294/33705/05-11-2007/05-28-2008 680/106305/05-22-2006/06-06-2007 283/66307/05-25-2008/06-23-2008 357/383

Table 5Number of trammel net sets conducted in South Carolina estuarine waters by year andlocation. Numbers in parentheses represent the number of bonnetheads caught in thecorresponding location and year.

Year Winyah Bay Bulls Bay Charleston Harbor St. Helena Sound

1998 – 138 (16) 40 (0) 74 (10)1999 – 152 (67) 46 (0) 78 (13)2000 – 159 (48) 45 (0) 76 (15)2001 – 157 (67) 43 (0) 78 (28)2002 5 (2) 149 (100) 42 (6) 77 (33)2003 17 (7) 141 (75) 41 (3) 67 (44)2004 23 (0) 142 (58) 35 (0) 69 (12)2005 24 (1) 140 (60) 41 (0) 73 (39)2006 22 (0) 134 (83) 44 (1) 71 (24)2007 43 (6) 133 (79) 40 (6) 72 (45)2008 27 (10) 138 (116) 38 (4) 75 (56)2009 28 (7) 124 (112) 38 (5) 65 (58)2010 26 (0) 136 (84) 41 (2) 76 (21)2011 36 (21) 148 (58) 44 (1) 82 (19)2012 29 (0) 158 (123) 48 (1) 74 (51)Total 280 (54) 2149 (1153) 626 (29) 1107 (468)

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likely outside of the estuarine waters of South Carolina. It couldbe suggested that parturition does occur in South Carolina's estuarinewaters and that neonates were not susceptible to the gearsemployed in this study; however, neonate Atlantic sharpnose sharks(Rhizoprionodon terraenovae (Richardson 1836)), which are approxi-mately the same size as neonate bonnetheads, were frequentlycaptured in the gillnets. Furthermore, neonate bonnetheads have beencollected during early fall in estuarine waters off the coast of Georgiausing the same gear (Ulrich et al., 2007; B. Frazier, unpublished data).Additionally, targeted sampling was conducted by SCDNR personnelin an attempt to catch neonate bonnetheads using multi-panel gillnetswith smaller mesh sizes than gillnet gear utilized in the current studyand no neonate bonnetheads were captured (B. Frazier, unpublisheddata). Limited data exist regarding parturition in bonnetheads, butneonate bonnetheads with partially and mostly-healed umbilicalscars are captured in fall trawl surveys in coastal waters off Georgia(C. Belcher, Georgia Department of Natural Resources, personal com-munication) and Florida (P. Webster, South Carolina Department ofNatural Resources, personal communication) and gravid females withnear termpups have been collected off the east coast of northern Floridaduring early fall (D. Adams, unpublished data). This informationindicates that females primarily give birth in coastal waters during fallassociated with the timing of their migration to more southern waters.Therefore, a more parsimonious scenario is that South Carolina's estua-rine waters represent an important feeding ground for bonnetheads.

We hypothesize that the site fidelity of bonnetheads to specificestuaries in South Carolina is related to the presence of a seasonallypredictable and energetically valuable prey resource. Fidelity to specificfeeding areas has been documented for several species of sharks onvarious spatial scales (e.g. Barnett et al., 2010; Domeier andNasby-Lucas, 2008; Kneebone et al., 2012). For example, Lowe et al.(2006) tracked tiger sharks (Galeocerdo cuvier (Peron and Lesueur1822)) around French Frigate Shoals using acoustic telemetry anddetermined that while some sharks were resident, the high number ofdetections of tagged individuals in a small area despite a massiveamount of adjacent habitat indicated that the sharks were visiting theislands in response to seasonally abundant food sources, includinggreen sea turtles (Chelonia mydas (L. 1758)), Hawaiian monk seals(Monanchus schauinslandi Matschie 1905) and seabirds. Similarly,Goldman and Anderson (1999) hypothesized that some large whitesharks that previously experienced feeding success in a specific areaoff the South Farallon Islands were sighted repeatedly in those sameareas within and among seasons suggesting that they had learnedwhere predictable prey sources could be located.

Data from the current study demonstrate that bonnetheadsare present in South Carolina estuaries from April through mid-November. However, Ulrich et al. (2007), who sampled in coastal andestuarine habitats, stated that over 99% of all bonnetheadswere collect-ed in estuaries from April and August with their diet at that timeconsisting almost exclusively of blue crabs (Callinectes sapidus Rathbun1896).Wilga andMotta (2000) stated that bonnetheads are specializedto feed on hard-shelled prey through a combination of relativelyunique “morphological, behavioral and physiological characteristics.”Furthermore, these sharks are widely documented to feed primarilyon crustaceans, particularly blue crabs (Callinectes sp.) (Bethea et al.,2007; Cortés et al., 1996; Garman, 1913; Gudger, 1907; Gurshin, 2007;Hoese and Moore, 1958; Lessa and Almeida, 1998). Interestingly,Archambault et al. (1990) reported that ovigerous blue crabs occur inSouth Carolina's estuarine waters from April through August, a timethat corresponds with the seasonal presence of bonnetheads in thesame areas.

Abiotic data collected during the trammel net survey indicated thatbonnetheads were captured in estuaries at salinities ranging from 15to 40. Archambault et al. (1990) reported that 95% of ovigerous bluecrabs in estuarine waters occurred at salinities above 15 and that,when compared to males, the distribution of large females is skewed

toward higher salinity waters. Similarly, Fischler and Walburg (1962)stated that ovigerous blue crabs occupy relatively high salinity watersfrom spring through summer in waters associated with inlets. Giventhat 1) bonnetheads are reported to feed predominately on blue crabs,2) ovigerous blue crabs represent the most energetically valuableindividuals, 3) the seasonality of both bonnetheads and ovigerous bluecrabs is essentially identical in South Carolina's estuarine waters, and4) over 95% of ovigerous blue crabs occur within the same salinityrange as bonnetheads, we hypothesize that bonnetheads are utilizingSouth Carolina's estuarine waters as a feeding area where there is aprey source of high caloric value. Additionally, as Fischler and Walburg(1962) reported that 97% of the crabs they recaptured during a taggingstudy were recaptured in the same estuary where they were originallytagged, ovigerous blue crabs within each estuary represent a spatiallypredictable, yet ephemeral, prey source. This is not to imply thatbonnetheads in South Carolina waters do not also feed on male bluecrabs as they most certainly do; however, the coinciding spatial andtemporal distributions of bonnetheads and ovigerous blue crabs in thearea indicate that these specialized predators are utilizing the samehabitat occupied by the most energetically valuable individuals oftheir primary prey.

While the value of a predictable, high-quality prey resource in ageneral area is obvious, less clear is why individual bonnetheadswould show site fidelity to a specific estuary (i.e. Bulls Bay or NorthEdisto) when the prey resource is abundant in adjacent estuarieswhere other bonnetheads occur (Fig. 1 and Table 5). Perhaps the mostwell-known example of site fidelity among fishes could be attributedto several Pacific salmon (Salmonidae) species (see Scheer, 1939 foran early review). It is now generally accepted that these fishes hometo their natal streams in response to specific chemical (e.g. Hasleret al., 1978), or, as recently suggested, geomagnetic cues (Lohmannet al., 2008) imprinted on during their early life history (Dodson,1988). While not widely studied, imprinting is thought to occur duringa sensitive period when long-termmemory of a location is formed. It isunlikely that imprinting is the mechanism behind the site fidelitydemonstrated by bonnetheads to specific South Carolina estuaries asimprinting generally occurs early in life and bonnetheads do not usethese systems as parturition areas whereby neonates could imprint onunique chemical or magnetic characteristics. Furthermore, the estuarieswhere the present study was conducted are dynamic habitats wherebiotic and abiotic characteristics can change significantly on shorttemporal scales (i.e. hours). Amore likely explanation is social transmis-sion of knowledge fromolder,more experienced individuals to younger,naïve individuals regarding the location where prey resources havebeen acquired predictably in the past. While social transmission is not

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well understood, it has been demonstrated to occur in numerous teleostfishes (Brown and Laland, 2003). To the best of our knowledge, socialtransmission as suggested herein has not been demonstrated for anychondrichthyan species; however, complex social behavior amongcaptive bonnetheads was reported in, among others, the classic workby Myrberg and Gruber (1974). Of note, Meyer et al. (2010) reportedon the repeated use of French Frigate Shoals of some, but not all, tigersharks they trackedwith acoustic and satellite tags. The authors report-ed that some sharks returned repeatedly to the area using cognitivemaps to feed on young albatross (Phoebastria spp.); however, theyconcluded that social transmission of the location of the feeding areawas not a viable hypothesis and that individual sharks must locatethis area on their own. It is possible that the bonnetheads we studiedinitially locate estuaries to which they will show fidelity to in the futureby randomchance and retain a cognitivemap of a return route for futureuse, however, the grouping behavior we observed suggests differently.

The tagging and eventual recapture of several groups of two ormorebonnetheads tagged in identical space and time demonstrate that groupcohesion occurs within the species over scales ranging from days toyears. Furthermore, evidence for shoaling in bonnetheads, defined asgroups of three or more fish moving as a group, was evident on bothintra and inter-annual scales. Most shoals were observed in intra-annual recaptures, however, one shoal of four individuals was taggedand recaptured in the North Edisto on 05/28/2008 and 06/04/2009,respectively. Shoaling behavior in fishes has been hypothesized to beadvantageous due to for a number of reasons, including increased pred-ator avoidance, increased likelihood of successful mating and foragingsuccess (Pitcher, 1986). Of these hypotheses, the latter seems to bethe most likely explanation for the group cohesion observed in ourdata. We can discount predator avoidance as large sharks that wouldbe potential predators of bonnetheads are not abundant in SouthCarolina's estuarine waters (Ulrich et al., 2007) and that the smallgroups we observed would likely negate a dilution of risk from preda-tion and potentially make the group more conspicuous. Similarly, wecan discount increased mating success as, with few exceptions,bonnetheads mate prior to their arrival in South Carolina waters. If weconsider each South Carolina estuary an individual food patch duringspring through early fall, then it is clear that, due to their high sitefidelity, bonnetheads do not investigate other potential food patchesduring this time (i.e. other estuaries). This coupled with groupsconsisting of both sexes and that sharks within groups also exhibitedbroad size ranges further strengthens our argument for social transmis-sion of knowledge pertaining to historically productive discrete feedingareas among individuals. If our hypothesis is correct then during ajuvenile bonnetheads first migration to the feeding ground it wouldfollow an older and more experienced individual or individuals therebylearning the route (e.g. cognitive mapping) that it would potentiallysocially transmit to another juvenile in subsequent years. Lengthfrequency distribution of bonnetheads captured during this study(Fig. 3) lends additional support to this hypothesis asmost bonnetheadscaptured were larger juveniles or adults indicating that youngbonnetheads do not migrate into South Carolina's estuarine waters.

Social behavior in sharks is poorly known, with the first mention ofsociality being attributable to Allee and Dickinson (1954), who demon-strated the existence of a social hierarchy among smoothhound sharks(Mustelus canis (Mitchell 1815)) in captivity. Since that time, severalauthors, including Myrberg and Gruber (1974), Klimley and Nelson(1981), and Mourier et al. (2012), have investigated various aspectsof social interactions among sharks of the same species. Largely,these studies have focused on factors influencing social grouping(e.g. Jacoby et al., 2012), such as refuging, reproductive status andmigrations. Recently, it has been shown that captive smallspottedcatsharks (Scyliorhinus canicula (L. 1758)) and wild blacktip reef sharks(Carcharhinusmelanopterus (Quoy and Gaimard 1824)) can show socialpreference to a specific individual or individuals (Jacoby et al., 2010).Our study supports the findings of both of these studies and, to the

best of our knowledge, is the first example of such behavior for awide-ranging species. Whether social bonds develop due to kinshipshould be genetically tested and how individuals recognize one anotherin order to remain together at scales ranging from days to years isunknown. One hypothesis is that the black dots that are distributedalong the lateral surface of the bodies of bonnetheads could makeindividual identification possible. The use of similar body markings forintraspecific communication has been discussed by Myrberg (1991)and Wilson and Martin (2003).

Throughout the study, 90% of bonnetheads captured in South Caroli-na estuarine waters were females demonstrating that males do notutilize these areas to the same extent, assuming the sex ratio of thetotal population of bonnetheads of the east coast of the United Statesis 1:1, an assumption that is realistic based on the observed ratio of1:1 for female to male embryos in gravid female bonnetheads collectedin the study area (Frazier et al., 2013b). Differences in sex-specificmortality rates could explain why the sex ratio of females to males wecollected was heavily skewed toward females, however, 6% of thefemales and 7% of the males tagged were recaptured, a similaritywhich suggests no sex-specific difference in mortality rates. Perhapsthe reason female bonnetheads utilize South Carolina estuarine watersto a greater extent than males is related to their unique reproductivebiology among coastal sharks. For sharks that occupy the coastal watersof the western North Atlantic, gestation times typically last a minimumof ten months, with the exception of one species (Castro, 2009). Inter-estingly, the gestation time of bonnetheads has been demonstrated inseveral studies to be 4–5 months (Frazier et al., 2013b; Manire et al.,1995; Parsons, 1993), at least half that of other coastal sharks in thearea. For example, the Atlantic sharpnose shark, a shark of similar sizeas bonnetheads, has a gestation time of approximately 10–11 months,a brood size of 1–9 pups and a size at birth of approximately 250 mmFL (Hoffmayer et al., 2013; Loefer and Sedberry, 2003). By contrast,the gestation time of bonnetheads is approximately half that ofAtlantic sharpnose sharks, while the sizes at birth (260–275 mm FLfor bonnetheads, Frazier et al., 2013a; Parsons, 1993) are approxi-mately the same for both species and mean brood size is higher forbonnetheads (8.8 pups vs. 3.9 pups, Frazier et al., 2013b; Loeferand Sedberry, 2003). While purely speculative, we hypothesize thatthe relatively short gestation time of bonnetheads off the east coastof the United States is made possible, in part, due to their diet ofenergetically-rich blue crabs, including ovigerous females that are sea-sonally abundant in South Carolina's estuarine waters. Since maturefemaleswould clearly have a higher energetic demand related to repro-duction than mature males, it is possible that migrating back and forthfrom overwintering areas to northern feeding grounds is not necessaryfor males to meet their energetic needs. Cortés et al. (1996) and Betheaet al. (2007) did notfind a significant difference in the diet of female andmale bonnetheads in the northern Gulf of Mexico, however, Lessa andAlmeida (1998) found that female bonnetheads had significantly great-er volume of crabs in their stomachs and a less diverse diet than malesoff northern Brazil. Future research should examine the stomachs ofbonnetheads throughout their range in the western North Atlantic todetermine if there are spatial and sex-specific differences in diet.

The results of this study emphasize the importance of identifying allcritical habitats utilized by a given species and reinforce the statementby Hueter et al. (2004) that “it would be wise from a conservation andmanagement perspective to not view this group of marine fishes[sharks] as oceanic nomads, but rather as more sophisticated, long-distance travelers with a number of discrete homes in the sea.” The fail-ure to recognize and properlymanage critical habitats could undermineconservation efforts and result in highly localized trophic cascades,stock depletions and, ultimately, the rebound potential of speciesimpacted by anthropogenic forces. Furthermore, the high degree ofintra and inter-annual site fidelity demonstrated by bonnetheads inthe estuarine waters of South Carolina provide unique opportunitiesfor in situ study of various aspects of the biology of chondrichthyan

69W.B. Driggers III et al. / Journal of Experimental Marine Biology and Ecology 459 (2014) 61–69

fishes, including growth, homing mechanisms, mortality rates, move-ment patterns, orientation and social behavior.

Acknowledgments

We thank Karl Brenkert, Henry Davega, Carrie Hendrix, DougMellichamp,DougOakley, Catherine Riley, Ashley Shawand Paul Tuckerfor their assistance during the field portion of this study and the InshoreFisheries Division of SCDNR for use of the trammel net data. We alsothank Cami McCandless, Pat Turner, Nancy Kohler and Ruth Briggswith the NMFS Apex Program for providing tags. Aspects of this workwere funded in part by the Cooperative Atlantic States Shark Puppingand Nursery Habitat Survey and the South Carolina State RecreationalFisheries Advisory Committee.

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