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Movement Patterns of Sphyrna tiburo (Bonnethead Shark) in a Shallow Tidal Creek System
Dontrece T. Smith and Mary Carla Curran

Southeastern Naturalist, Volume 16, Issue 2 (2017): 297–316

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Southeastern Naturalist 297 D.T. Smith and M.C. Curran 22001177 SOUTHEASTERN NATURALIST 1V6o(2l.) :1269,7 N–3o1. 62 Movement Patterns of Sphyrna tiburo (Bonnethead Shark) in a Shallow Tidal Creek System Dontrece T. Smith1,* and Mary Carla Curran1 Abstract - The purpose of this study was to use acoustic telemetry to elucidate the small-scale habitat-utilization patterns of Sphyrna tiburo (Bonnethead Shark, hereafter, Bonnethead) in relation to diel and tidal cycles in a shallow tidal creek system along the coast of Georgia. We found that Bonnetheads utilized the main channel of a tidal creek at night, dawn, and during ebb and low tides. In addition, we found the first evidence of Bonnetheads utilizing smaller 3rd-order creeks. Bonnetheads used these tributaries at night and dawn, during flood and high tides when the water level facilitated access. The movement patterns of these Bonnetheads could be representative of those in other areas with semidiurnal tides. Introduction Estuaries and nearshore habitats are dynamic environments with variable conditions (Morin et al. 1992). These areas are highly productive and support the development of many low trophic-level marine organisms (e.g., Callinectes sapidus Rathbun [Blue Crab], penaeid shrimp, and teleost fishes) (Blaber and Blaber 1980, Blaber et al. 1989, Zimmerman et al. 2000). These organisms serve as prey resources for many upper trophic level organisms (e.g., sharks) (Cortés et al. 1996, Ellis and Musick 2007). Sharks play an important role in the estuarine and nearshore foodwebs causing a top-down effect in ecosystems (Cortés 1999). Many coastal shark species utilize these ecosystems at all life stages, such as Rhizprionodon terranovae (Richardson) (Atlantic Sharpnose Shark), Carcharhinus leucas (Müller and Henle) (Bull Shark), and Sphyrna tiburo (L.) (Bonnethead Shark, hereafter, Bonnethead) (Froeschke et al. 2010, McCandless et al. 2007, White and Potter 2004). Bonnetheads are small sharks in the order Carcharhiniformes (Compagno 1984). They are found in coastal and estuarine waters along the Atlantic and Pacific coasts of both North and South America (Compagno 1984). Bonnetheads are migratory and tend to travel in aggregations of 3–15 individuals (Compagno et al. 2005). Some aspects of their life history have been well studied, including age and growth (Carlson and Parsons 1997, Frazier et al. 2014, Lombardi–Carlson et al. 2003, Parsons 1993a), feeding ecology (Bethea et al. 2007, Cortés et al. 1996, Lessa and Almeida 1998), nursery areas (Gurshin 2007), and reproductive biology (Cortés and Parsons 1996, Gelsleichter et al. 2002, Gonzalez De Acevedo 2014, Lessa and Silva 1992, Manire 2001, Manire et al. 1995, Parsons 1993b). The overall geographic distribution of Bonnetheads has been well documented, but the pattern across regions is not consistent (Driggers et al. 2014, Heupel et 1Marine Sciences Program, Box 20467, Savannah State University, Savannah, GA 31404. *Corresponding author - dtsmith@uga.edu. Manuscript Editor: Lance Williams Southeastern Naturalist D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 298 al. 2006, Ubeda et al. 2009). In South Carolina, Driggers et al. (2014) found that Bonnetheads exhibited high degrees of intra- and inter-annual site fidelity. Those authors marked a total of 2300 Bonnetheads with traditional external tags; 177 sharks were recaptured after 3 d to 8.9 y at liberty (noncontinuously), and 171 of those individuals were recaptured in the same estuary in which they were tagged. Furthermore, groups of 2–5 individuals that were tagged together were subsequently recaptured together. Driggers et al. (2014) speculated that the site fidelity of Bonnetheads in South Carolina waters may be attributed to the seasonal occurrence of energetically valuable prey (e.g., ovigerous Blue Crabs), and the social transmission of productive feeding area locations among individuals. Heupel et al. (2006) studied Bonnetheads residing in a coastal Florida estuary in the Gulf of Mexico and found that their movement was not related to time of day or tidal cycle. Bonnetheads utilized small areas of the study site on a daily basis, but did not exhibit site fidelity to any particular areas. Like Driggers et al. (2014), Heupel et al. (2006) believed these highly variable movement patterns were associated with the abundance of Blue Crabs, which are distributed throughout the area. The widespread utilization of the area by Bonnetheads could be an example of “patrolling” behavior in search of prey, which was observed by Myrberg and Gruber (1974). In another study conducted in the Gulf of Mexico, the movement patterns of Bonnetheads were affected by changes in salinity (Ubeda et al. 2009). Bonnetheads were located in northern, central, and southern zones of Pine Island Sound, FL, where salinity was ≥20.0–25.5 psu (Ubeda et al. 2009). Similarly, Belcher (2008) found that salinity and turbidity influenced the presence of Bonnetheads in coastal Georgia, where individuals were found in areas with low turbidity (mean = 16.3 NTU) and high salinity (mean = 32.0 ppt). Although several ecological studies on Bonnetheads have been conducted in the Gulf of Mexico and South Carolina, little is known about their behavior in relation to tidal and diel cycles in the coastal waters of Georgia, where there are high tidal ranges of ~2.5 m that provide access to a wide range of geographical areas and creek orders that are inaccessible during low tide. These areas consist of Crassostrea virginica Gmelin (Eastern Oyster) beds and Spartina alterniflora (Loisel) (Smooth Cordgrass) salt marshes that support many marine organisms (e.g., callinectid crabs) that serve as a prey for Bonnetheads and other elasmobranchs (Hettler 1989, Rozas and Reed 1993, Wells 1961). Heupel et al. (2006) determined that the movement patterns of Bonnetheads were not correlated to tidal height or time of day in a coastal Florida estuary that experienced a mixed semidiurnal tidal cycle with a lower tidal range of ~1.0 m. These smaller tidal ranges allow Bonnetheads and other shark species to frequent all areas throughout the entire tidal cycle. However, Bonnetheads can only access certain areas of the estuaries during flooding and high tides in coastal Georgia. Understanding the behavior of Bonnetheads across a variety of tidal regimes in the southeastern US could elucidate the importance of tidal-creek systems and estuarine waterways to the life history of elasmobranchs. Therefore, the purpose of the present study was to provide the first information on the small-scale movement patterns of Bonnetheads in relation to diel and tidal cycles within a Georgia coastal system. Southeastern Naturalist 299 D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 Field–site Description The Romerly Marsh Creek system (31°55'46.45''N, 80°59'4.66''W) is located near Savannah, GA (Fig. 1). This estuarine area has a semidiurnal tidal cycle, with a tidal range of 0.25–2.84 m. For the purposes of this study, we divided the creek system into 2 components: the main channel of Romerly Marsh Creek and its smaller tributaries. We followed the methods of Horton (1945) and classified the main channel, which was the widest waterway, as a 4th-order creek and the tributaries as 1st–3rd-order creeks. The 1st-order creeks in this area are exposed during low tide (Brinton 2015). The main channel is ~1.5 km long and varies in depth from 0.6 m to 11.9 m at mean lower low-water level. Several creek tributaries that vary in width from 5 m to 120 m and in depth from 0.5 m to 6 m flow into the main channel. Smooth Cordgrass is the dominant vegetation, and there are numerous live and dead oyster beds along the creek banks. Methods Shark sampling Shark collection and tagging protocols were approved by the Savannah State University Institutional Animal Care and Use Committee (IACUC). We collected 13 Bonnetheads using a hook and line baited with Loligo spp. (squid) during August– September 2011 and April–June 2012. We determined the sex, took measurements, and assessed maturity based on size (Compagno et al. 2005) of all Bonnetheads caught. We predetermined the minimum size for tagging as 70 cm total length (TL) and/or 0.6 kg so that the tag was no more than 2% of the body weight. We removed each captured shark from the water and placed it in tonic immobility by dorsoventrally inverting the individual, a technique described by Watsky et al. (1990). We outfitted each shark with a VEMCO coded V16–4H acoustic transmitter tag (16 mm x 67 mm, 158-dB power output, 12 g in water, 69 kHz, 60-s nominal delay; VEMCO, Bedford, NS, Canada) and Dalton rototag (Dalton, Fort Atkinson, WI). Transmitters were externally attached to the anterior margin of the first dorsal fin using cable ties and marine epoxy by drilling 2 holes through the base of the first dorsal fin (Simpfendorfer et al. 2010). We attached a rototag near the posterior margin of the first dorsal fin. We completed the attachment procedure within 5 min of removing the shark from the water. After tagging, we held the shark by the caudal peduncle and placed it back Figure 1 (following page). Map of Romerly Marsh Creek, Wassaw Sound, GA, with locations of 7–8 VEMCO VR2W acoustic receivers deployed from (a) 18 August–22 November 2011 and( b) 2 February–31 July 2012. Each black dot represents a VR2W acoustic receiver. All sharks were caught and released in the main channel or tributaries within the study area between both gates. The percentage of Bonnethead Shark detections per receiver during each deployment is shown in parentheses. The creek orders are listed as 2nd, 3rd, or 4th. Receivers 8, 9, and 11 were placed in tributaries in 2012. Maps were created in ArcGIS® 9.3 (ESRI, Inc., CA, USA), using the National Hydrography Dataset (NHD) from the United States Geological Survey (USGS; http://nhd.usgs.gov/). Maps were created using the Universal Transverse Mercator (UTM) projection. Southeastern Naturalist D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 300 Figure 1. [Caption on previous page.] Southeastern Naturalist 301 D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 in the water. Each individual was released once it was able to swim away on its own, a period of 1–3 min. Methods are further described in Smith (2012). Receiver array and deployment We employed acoustic receivers to passively monitor the movement patterns of tagged Bonnetheads. In 2011, the receiver array consisted of 7 VEMCO VR2W single channel acoustic receivers (Fig. 1a). We deployed 7 receivers in the main channel on 17 and 18 August 2011. Four of the 7 receivers (receivers 1, 2, 6, and 7) were configured as “gates” in the study area (Fig. 1a). We defined a gate as 2 receivers with overlapping detection ranges spanning the entire creek width. In 2011, the receiver array was designed to determine the utilization of this creek system in relation to time and tidal cycle. We removed all receivers on 22 November 2011 and redeployed them on 1 and 2 February 2012, at which time we deployed an additional receiver and reconfigured the receiver array to accommodate the new receiver; receivers were still used to form gates. We redesigned the array in order to monitor Bonnethead activity in smaller tributaries as well as in the main channel in relation to time and tidal cycle. This array consisted of 5 receivers (#1, 2, 4, 5, 10) in the main channel and 3 receivers (#8, 9, 11) in 3 of 6 adjoining tributaries (Fig. 1b). We caught and released all sharks in the main channel or tributaries within the study area between both gates. Statistical analyses We included for analysis only sharks detected for ≥7 days, as recommended by Heupel et al. (2006), who also studied Bonnetheads that were using the study area on a consistent basis. Eight out of 13 sharks met this criterion. We downloaded and sorted detection data into hourly bins. We used these data to analyze the presence and movement of Bonnetheads in relation to tide and time of day. We determined presence and movement based on whether a shark was detected on a receiver in a given hour instead of on the total number of detections because several environmental factors such as seasonal temperature changes daily tides, and episodic weather events (Mathies et al. 2014), and biotic noises, such as Alpheidae (snapping shrimp) (Cotton 2010), could potentially interfere with the detection range of acoustic receivers and thereby make the absolute number of detections uninformative. We considered a Bonnethead as present during a given hour only if ≥2 detections were recorded per hour on that same day by ≥2 receivers and we classified any Bonnethead as moving during a given hour if ≥2 detections were recorded by ≥2 receivers in the same hour for that day. This approach helped eliminate any possibility of counting false detections in the statistical analyses. We analyzed the main channel for both Bonnethead presence and movement in relation to time and tide. Only one receiver was placed in each tributary; thus, only presence was analyzed in these areas. We employed a Rao’s spacing test to determine if the presence and movements of Bonnetheads were evenly distributed over an entire day. To perform the Rao’s spacing tests, we used the Naval Oceanography Portal (2011) sunrise/sunset data to define hourly bins as dawn (0500–0559), day (0600–1859), dusk (1900–1959), or night (2000–0459). Therefore, dawn and dusk were each only 1 h, while day and Southeastern Naturalist D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 302 night were each 11 h. We displayed the number of detections or movements during each hour as rose diagrams with 24 sections, each representing 1 h. We also classified hourly bins as high, low, ebb, or flood tide; a complete tidal cycle was ~12 h 25 min. We converted the classified bins converted to angles between 0° and 360° so that they could be used to create rose diagrams with 24 sections representing 1 of the 4 tidal stages. We used NOAA Ocean Service Education data (NOAA 2011) to assign each tidal classification to a portion of the rose diagram (0–360º): low (357–002º; 45 min), flood (003–176º; 327.5 min), high (177–182º; 45 min), and ebb (183–356º; 327.5 min). We employed Rayleigh’s uniformity test to determine if the presence and movements of Bonnetheads were uniformly distributed or showed some directionality/uniform direction over time and tidal cycle. We created all rose diagrams in Oriana (v.3) software (Kovach Computing Services, Pentraeth, UK). We report significance of results where P < 0.05. Results Range test We performed range tests in 2011 and 2012 to determine the reliable detection range of receivers and transmitters. The range test transmitter had a 180-s nominal delay in contrast to the 60-s delay of the transmitters that were attached to Bonnetheads. We conducted repeated range tests 10–100 m from a VR2W receiver in the main channel of Romerly Marsh Creek. We submerged the transmitter 1 m above the benthos for 10 min at 10 m from the receiver and repeated this step every 10 m to a maximum distance of 100 m. We employed ANOVA to analyze whether diel period or tidal stage affected the detection frequency of the transmitter as distance increased. The Pearson correlation coefficient and a Cross–Fourier analysis performed using MATLAB® (MathWorks, Inc., Natick, MA) were used to assess the relationship between current velocity (m·s–1) and the detection frequency of the transmitter. We obtained current velocity and tidal-height data from the Nobeltec Tides and Currents software (Nobeltec, Beaverton, OR). Time of day and tidal cycle did not have a statistically significant effect on the detection frequency of the control tag (Table 1). Current velocity and detection frequency were not significantly correlated in either 2011 (P > 0.05, r2 < 0.004) or 2012 (P > 0.05, r2 < 0.004) (Table 1). We defined as reliable a detection range where at least 50% of detections were recorded by a receiver (Bertelsen and Hornbeck 2009, Bessudo et al. 2011, Kessel et al. 2014, Ramsden et Table 1. Range-test results for analysis of variance (ANOVA) on the number of detections h–1 based on time of day and tidal cycle and for Pearson correlation coefficient on the number of detections h–1 based on current velocity for the control transmitter tag in 20 11 and 2012. Statistical analyses Variables P R2 ANOVA (2011) Time of day 0.701 N/A Tidal cycle 0.681 N/A ANOVA (2012) Time of day 0.433 N/A Tidal cycle 0.554 N/A Pearson Correlation Coefficient (2011) Current velocity 0.945 0.003 Pearson Correlation Coefficient (2012) Current velocity 0.119 0.002 Southeastern Naturalist 303 D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 al. 2016). Our maximum reliable detection range was determined to be 70 m because fewer than 50% of the detections were recorded at and beyond 80 m. Detections and receivers We placed acoustic tags on 13 Bonnetheads in Romerly Marsh Creek (9 in 2011 and 4 in 2012; Table 2); 10 were females and 3 were males. We collected mature, juvenile, and neonate Bonnetheads, but did not tag neonates because of the high transmitter-to-body-weight ratio. We detected all tagged sharks after the date of release except 2 individuals (Table 2). In 2011, we recorded over 29,000 detections on the receivers; detections per shark varied from 158 to 8023 (mean = 4184.9 ± 3033.9) (Table 3). We recorded individual sharks for periods of 1–29 d (mean = 15.9 d ± 10.9; Table 2) over 2–58 tidal cycles (mean = 31.7 ± 21.7; Table 3). We recorded >14,000 detections in 2012 (variation = 436–7979 detections per shark, mean = 3659.2 ± 3165.3; Table 3). We recorded individual sharks for periods of 3–49 d (mean = 19.2 d ± 20.4; Table 2) over 3–98 tidal cycles (mean = 37.7 ± 41.7; Table 3). In both years, the number of mean detections per day was greater than 200 (Table 3). We detected females for a greater number of days and for a longer period than males in 2011 and 2012 (Table 2). Receiver 4 was located in the main channel and recorded the highest percentage of detections in 2011 (31%; Fig. 1a) and 2012 (33%; Fig. 1b). Receiver 11 was located in a 3rd-order creek and recorded the highest percentage of detections in the tributaries in 2012 (9%; Fig. 1b). No Bonnetheads tagged in 2011 returned to the study area in 2012. We detected 2 Bonnetheads (a female of 105 cm TL in 2011 and a male of 86 cm TL in 2012) a few days after they left the study area in Ossabaw Sound, GA (8 km south of Romerly Marsh Creek) for periods of 3 and 13 d, respectively (C. Kalinowsky, GA Department of Natural Resources, Richmond Hill, GA, pers. comm.). The majority of Bonnetheads (8 of 13) left the range of the receiver array during the day (Table 3) and 8 of the 13 Bonnetheads left the array during ebb or low tide (Table 3). All Bonnetheads were last recorded near the gate receivers (Table 3). Of the 13 Bonnetheads, only 8 individuals were detected for > 7d in the study area, and we included those Bonnetheads in the subsequent statistical analyses (Heupel et al. 2006). Diel period We detected 8 Bonnetheads in the main channel throughout the 24-h period. Rao’s test indicated that Bonnethead presence and movement were not uniformly distributed over 24 h in the main channel (Table 4). Although Bonnetheads were present in the main channel at all times of the day, they were primarily there at night and dawn (Fig. 2a). Results of the Rayleigh’s uniformity test also indicated that time of day had a significant effect on the presence of Bonnetheads in the main channel; individuals were present in this section primarily at dawn (mean vector = 05:48; Table 4). Time of day also had a significant effect on the movements of Bonnetheads in the main channel; individuals moved within the main channel most often at night (mean vector = 03:51; Table 4, Fig. 2b). Bonnethead presence in the tributaries was not uniformly distributed over a 24-h period (Table 4). Similar to the main channel, Bonnetheads were present Southeastern Naturalist D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 304 Table 2. Bonnethead Sharks tagged within the Romerly Marsh Creek system near Savannah, GA. The mean number of days detected and mean period of detection ± 1 SD are presented for the 13 individuals collected. Number of days detected = the total number of days a shark was recorded during the period of detection. Period of detection = the range of days a shark was recorded in the receiver array. TL = total length. FL = fork length. N/A means information was not recorded. Bonnethead numbers marked with an asterisk (*) represent individuals that were included in the statistical ana lysis. Bonnethead Transmitter TL FL Weight Date of # of days Period of number ID Sex (cm) (cm) (kg) Date tagged last detection detected detection 2011 1 32233 F 96.0 81.0 3.8 19 August 2011 19 Aug 2011 1 1 2 32234 F 122.0 103.0 N/A 19 August 2011 N/A 0 0 3 32236 M 76.0 58.5 1.8 01 September 2011 N/A 0 0 4* 31925 F 87.0 68.0 3.5 09 September 2011 18 October 2011 29 40 5* 31927 F 105.0 85.6 5.7 09 September 2011 08 October 2011 28 30 6* 31928 F 72.0 56.0 2.1 09 September 2011 29 September 2011 17 21 7* 32235 M 80.0 61.6 2.3 13 September 2011 29 September 2011 16 17 8* 32237 F 103.0 89.0 6.3 15 September 2011 06 October 2011 17 25 9 32238 F 73.0 58.0 1.9 15 September 2011 17 September 2011 3 3 Mean ±SD 15.9 ± 10.9 19.6 ± 14.0 2012 10 31926 M 86.0 69.0 2.5 10 May 2012 12 May 2012 3 3 11* 30467 F 90.0 70.0 3.0 29 June 2012 28 Aug 2012 49 61 12* 30468 F 106.6 94.8 5.5 29 June 2012 17 July 2012 15 19 13* 30470 F 106.6 96.0 5.5 29 June 2012 19 July 2012 10 21 Mean ±SD 19.2 ± 20.4 26.0 ± 24.7 Southeastern Naturalist 305 D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 most often during night and dawn (Fig. 2c). Bonnetheads were generally less present during the day. The Rayleigh’s uniformity test indicated that time of day had a significant effect on the presence of Bonnetheads in the tributaries, with individuals present most often at night (mean vector = 00:30; Table 4, Fig. 2c). Overall, Bonnetheads were nocturnal and crepuscular in the main channel and tributaries. We did not assess movement in the tributaries because we placed only 1 receiver in each tributary. Tidal stage Neither the presence nor movement of Bonnetheads was uniformly distributed over the tidal cycle in the main channel (Table 4). Bonnetheads were present in the main channel primarily during ebb and low tide. Results from the Rayleigh’s uniformity test also indicated that tidal cycle had a significant effect on the presence of Bonnetheads; individuals were present within the main channel during ebb tide (mean vector = 348.41º) (Table 4, Fig. 3a). Tidal cycle had a significant effect on the movements of Bonnetheads—individuals moved within the main channel most often during ebb and low tide (mean vector = 347.39º) (Table 4, Fig. 3b). Table 3. Bonnethead Sharks monitored within the Romerly Marsh Creek system near Savannah, GA. The mean number of detections, detections per day, and mean number of tidal cycles over which individuals were detected ± 1 SD are presented for the 13 individuals. Number of detections = the total number of detections for each shark on all receivers regardless of presence or movement for the entire study period. N/A means information was not recorded. Rows marked with an asterisk (*) represent individuals that were included in the statistical analysis. # of Last Last Last Bonnethead TL # of Detections tidal cycles time of day tidal cycle receiver number (cm) detections per day detected detected detected detected 2011 1 96.0 183 183 2 Night Low Gate 2 122.0 N/A N/A N/A N/A N/A N/A 3 76.0 N/A N/A N/A N/A N/A N/A 4* 87.0 5080 175 58 Day Ebb Gate 5* 105.0 5297 189 56 Day Ebb Gate 6* 72.0 3890 229 34 Day Low Gate 7* 80.0 6663 392 32 Day Ebb Gate 8* 103.0 8023 472 34 Night High Gate 9 73.0 158 52 6 Day Flood Gate Mean 4184.9 241.7 31.7 ± SD ± 3033.9 ± 142.8 ± 21.7 2012 10 86.0 436 145 3 Day Ebb Gate 11* 90.0 7979 162 98 Day Low Gate 12* 106.6 3562 237 30 Day Low Gate 13* 106.0 2660 266 20 Day Ebb Gate Mean 3659.2 202.5 37.7 ± SD ± 3165.3 ± 58.2 ± 41.7 Southeastern Naturalist D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 306 Table 4. Rao’s spacing test and Rayleigh’s uniformity test for the presence and movement of Bonnethead Sharks in relation to time of day and tidal cycle in the main channel and tributaries of the Romerly Marsh Creek system near Savannah, GA. U = the test statistic; μ = the mean vector for time (time of day) and angle (tidal cycle); and r = the length of mean vector, which can range from 0–1; this value indicates whether the data were dispersed (close to 0) or clumped (close to 1). * indicates that detections were not uniformly distributed. Time of day Tidal cycle Rao’s Spacing Test Rayleigh’s Uniformity Test Rao’s Spacing Test Rayleigh’s Uniformity Test Location Variable U P μ r P U P μ r P Main channel Presence 352.96 less than 0.05* 05:48 (dawn) 0.100 less than 0.05* 354.28 less than 0.05* 348.41º (ebb) 0.304 less than 0.05* Main channel Movement 348.98 less than 0.05* 03:51 (night) 0.179 less than 0.05* 343.59 less than 0.05* 347.39º (ebb) 0.341 less than 0.05* Tributaries Presence 276.92 less than 0.05* 00:30 (night) 0.185 less than 0.05* 220.97 less than 0.05* 133.36º (flood) 0.118 less than 0.05* Southeastern Naturalist 307 D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 Figure 2. Rose diagrams representing the (a) presence and (b) movement of Bonnethead Sharks in relation to time of day in the main channel in 2011 (7 receivers, 5 individuals) and 2012 (5 receivers, 3 individuals) combined, and (c) presence in relation to time of day in the tributaries in 2012 (3 receivers; 3 individuals). Movement in the tributaries was not assessed because only 1 receiver was placed in each. The concentric circles on the diagrams represent the number of observations per hour. The black line with the arc represents the mean vector. Southeastern Naturalist D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 308 Figure 3. Rose diagrams representing the (a) presence and (b) movement of Bonnethead Sharks in relation to tidal cycle in the main channel in 2011 (7 receivers; 5 individuals) and 2012 (5 receivers; 3 individuals) combined, and (c) presence in relation to tidal cycle in the tributaries in 2012 (3 receivers; 3 individuals). Movement in the tributaries was not assessed because only 1 receiver was placed in each. Each tidal classification was represented by a portion of the 360º rose diagram: high (177– 182º), ebb (183–356º), low (357–2º), and flood (3–176º). The concentric circles on the diagrams represent the number of observations per tidal stage. The black line with the arc represents the mean vector. Southeastern Naturalist 309 D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 The presence of Bonnetheads in relation to tide within the tributaries was not uniform (Table 4). Bonnetheads were present most often during flood and high tide, but were rarely observed during ebb and low tide within the tributaries (Fig 3c). Tidal cycle had a significant effect on the presence of Bonnetheads; individuals were present most often during flood tides (mean vector = 133.36º) once water levels in the tributaries began to rise (Table 4, Fig. 3c). We recorded these differences in presence between the main channel and tributaries on multiple occasions. For example, 2 female Bonnetheads (11 and 12) were present in a small tributary (Receiver 11) during flood and high tide, and in the main channel (Receivers 1, 2, 4, 5, and 10) during ebb and low tide. Movement in the tributaries was not assessed because we placed only one receiver in each tributary . Discussion This study provides the first documentation of the habitat-utilization patterns of Bonnetheads in relation to tidal and diel cycles within a shallow tidal-creek system on the southeast US Atlantic coast. Bonnetheads utilized the main channel primarily during ebb and low tide, and the tributaries most often during flood and high tide in Romerly Marsh Creek. These results indicate that tidal stage influences the habitat utilization of this species; Bonnetheads move to shallower areas with the rising tide. Other species of elasmobranchs have exhibited similar tidally oriented movements. Triakis semifasciata (Girard) (Leopard Shark) and Carcharhinus plumbeus (Nardo) (Sandbar Shark) showed pronounced movement-patterns with the incoming and outgoing tidal currents (Ackerman et al. 2000, Medved and Marshall 1983). Wetherbee and Rechisky (2000) found that juvenile Sandbar Sharks traveled with the incoming tide into Delaware Bay, individuals were located farthest inshore at high tide and close to the mouth of the bay at low tide. Brinton and Curran (2017) reported that Dasyatis sabina (Lesueur) (Atlantic Stingray) utilized shallow creeks significantly more often during the flood tide. In Brazil, Wetherbee et al. (2007) observed neonate Negaprion brevirostris (Poey) (Lemon Shark) moving from shallow tidal creeks at high tide to small tide pools on reef flats at low tide. In the present study, Bonnetheads moved into the tributaries (e.g., 3rd-order creeks) during flood and high tides on multiple occasions. Bonnetheads may have moved into these tributaries with the incoming tides to forage or follow prey moving with the tidal currents. Blue Crabs are a primary prey species of Bonnetheads (Cortés et al. 1996), and are commonly associated with Eastern Oyster beds and Smooth Cordgrass (Rozas and Reed 1993, Wells 1961) that are often only submerged at flood or high tide. In addition, Hettler (1989) determined that callinectid crabs (e.g., Blue Crabs) were more abundant in subtidal 3rd-order creeks than 1st-order creeks. In the present study, it is possible that Bonnetheads were following mature Blue Crabs and other prey species into these 3rd-order creeks with the incoming tidal currents. The movement of other elasmobranchs in relation to tidal cycles and prey availability has been addressed in several studies. Campos et al. (2009) found that Mustelus henlei (Gill) (Brown Smoothhound) moved into mudflats in Tomales Bay, CA, during high and incoming tides, which was consistent with when prey were Southeastern Naturalist D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 310 available in these areas. Teaf (1978) speculated that Atlantic Stingrays moved into salt marsh areas at high tide due to higher food abundance/availability. Ackerman et al. (2000) reported that Leopard Sharks exhibited no consistent movement pattern on the mudflats of the muddy littoral zones at high tide, which was indicative of benthic foraging for worms and clam siphons. Medved and Marshall (1983) documented that Sandbar Sharks exhibited movement patterns opposite of tidal current direction in areas where large schools of Brevoortia spp. (Menhaden) were present. No tagged individuals were observed feeding, but those authors observed untagged sharks feeding on the schools (Medved and Marshall 1983). In 2011, the receiver array was originally designed to observe the utilization of a creek system by Bonnetheads in relation to time and tidal cycle. Most detections were recorded on Receivers 3–7. After examining our 2011 data, we rearranged the array and placed a few receivers in the adjoining tributaries to determine whether Bonnetheads were also utilizing these areas. In 2012, Bonnetheads were most active near Receivers 1, 2, 4, and 11. From the rose diagrams, we determined that Bonnetheads were using the main channel during ebb/low tide, and the tributaries at flood/high tide. Combining the detection percentage per receiver and the rose-diagram data, we could firmly conclude that Bonnetheads primarily utilized the main channel during ebb/low tides. Bonnetheads tended to enter one particular tributary (Receiver 11) during flood/high tides, and rarely frequented the other 2 tributaries. Results of the present study also indicated that Bonnetheads were nocturnal and crepuscular. It is possible that food abundance and/or availability may not only influence the tidal movement patterns of Bonnetheads, but also the diel movement patterns, as seen with other elasmobranch species. Bessudo et al. (2011) speculated that Sphyrna lewini (Griffith and Smith) (Scalloped Hammerhead Shark) congregated around Mapelo Island, Colombia, during daytime and ventured away to forage at nighttime. Myliobatis californica (Gill) (Bat Ray) were present in the warmer, shallower, inner-bay waters of Tomales Bay between 02:50–14:50 h and then traveled back to the deeper, cooler outer-bay waters. Matern et al. (2000) suggested that this movement reflected their behavioral thermoregulation as well as their foraging patterns between 12:00–20:00 h. In another study, Atlantic Stingrays were most active at dusk, potentially due to the increased crepuscular activity of prey species (Brinton and Curran 2017). Based on the behavior of other elasmobranchs, the increased activity of Bonnetheads at dawn and night in the Romerly Marsh Creek system could reflect their foraging patterns or food abundance/availability. In the current study, Bonnetheads utilized Romerly Marsh Creek from August to October 2011 and May to August 2012. In other studies, Bonnetheads used coastal systems for similar periods of time. They were present in South Carolina waters from spring to early fall; Bonnnetheads were caught from April to November (Driggers et al. 2014, Ulrich et al. 2007), and they exhibited a high degree of intra–and inter-annual site fidelity to specific estuaries (Driggers et al. 2014). In Florida waters, Bonnetheads were long-term residents (≥1 year) and some individuals overwintered and did not undergo coastal migration (Heupel et al. 2006). We believe that our findings may reflect the migration of Bonnetheads into other creek Southeastern Naturalist 311 D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 systems in coastal Georgia. In 2011, we collected Bonnetheads in August and September. They were recorded in the study area on multiple occasions until most individuals left in September and October 2011. A similar pattern was observed in 2012—Bonnetheads migrated into the study area in May/June, and left in July/ August. In each year, 1 of our tagged Bonnetheads (2011 female: 105 cm TL; 2012 male: 86 cm TL) migrated south into another system (Ossabaw Sound, GA) after leaving Romerly Marsh Creek (C. Kalinowsky, pers. comm.). Based on these studies, Bonnetheads may be seasonal/transient residents in cooler regions, such as Georgia and South Carolina, and year-round residents farther south in Florida waters. This is a pattern also seen in Atlantic Stingrays (Ramsden, 2015). The occurrence of Bonnetheads in the coastal waters of Georgia may be related to parturition/reproduction. In the present study, we captured both mature and neonate Bonnetheads, though we classified most as mature females based on documentation that individuals greater than ~84 cm TL are mature (Compagno et al. 2005). In nearby South Carolina waters, pregnant female Bonnetheads caught in April/May were carrying embryos at early developmental stages, and pregnant females were carrying pups and leaving South Carolina waters in September (Ulrich et al. 2007). In early fall, 4 neonates were collected in Georgia estuarine waters (Ulrich et al. 2007, C. Belcher, Georgia Department of Natural Resources Coastal Resources Division, Brunswick, GA, pers. comm.). In addition, Driggers et al. (2014) only recaptured female Bonnetheads in South Carolina waters. Belcher (2008) and Gurshin (2007) determined that juvenile Bonnetheads use the coastal waters of Georgia as secondary nurseries. The arrival of pregnant Bonnetheads in South Carolina waters in April/May coincides with the arrival of Bonnetheads in the coastal waters of Georgia. Given that pregnant females were found in South Carolina waters and neonates were collected in Georgia waters, pregnant females may be pupping in the estuaries of Georgia, with their neonates subsequently utilizing these areas as primary nurseries before leaving in October . Our acoustic telemetry data on the movement patterns of Bonnetheads have very important conservation management and planning implications, even though detections were highly variable and our sample size was small. In both years, we detected tagged Bonnetheads over a span of 3–6 months with certain individuals frequenting the area regularly (≥7 days), but none was observed year-round. We recorded some sharks (38%) in the area for less than 7 days with <500 total detections. Only 13 individuals were tagged and monitored between sample years with 8 recorded for ≥7 days. In 2012, we recorded only 3 sharks, but only 1 was detected for more than 2 weeks. This one shark could have represented the majority of the acoustic data for the main channel and tributaries in 2012. It is the presence/absence of Bonnetheads at certain times and tides in a given location and the proportion of the detection data across these parameters that are most informative. However, the low number of individuals tagged and the possible disproportionate influence of a single individual, which may have been detected more than the others, are limitations of our study. In the current study, we recorded 3 of 13 Bonnetheads for ≤1 day, which could have reflected fishing/tagging mortality. Hueter et al. (2006) analyzed the mortality rate Southeastern Naturalist D.T. Smith and M.C. Curran 2017 Vol. 16, No. 2 312 of Bonnetheads during a catch–tag–release event. Those authors classified the condition of each released shark from 1–5 (1 = best, 5 = dead). From their 1992–2004 gill-net data, they estimated that 40% of Bonnetheads died post–release (Hueter et al. 2006). In our study, most tagged Bonnetheads were released in condition 2 or 3, but there were some individuals in condition 4. We estimate that only 1 tagged individual died or shed its transmitter during the study . Conclusion Our results provide some of the first information on the small-scale movement patterns of Bonnetheads within and between 3rd- and 4th-order intertidal creeks in relation to diel period and tidal cycle. In both study years, we detected individuals south of the study area a few days after their last detections in our array in Ossabaw Sound, GA, indicating utilization of multiple coastal systems along the coast within a year and possible migration south towards warmer waters. Thus, the movement patterns of Bonnetheads observed in this study could be representative of other semidiurnal tidal creek and estuarine systems in temperate waters along the East Coast, which is in contrast to Bonnetheads that are year-round residents in the warmer coastal waters of Florida and experience diurnal and mixed semidiurnal tides. In addition, our small-scale acoustic telemetry data have the potential to be used for spatial analysis for management purposes. In our study, we determined that Bonnetheads utilized the main channel and tributaries of Romerly Marsh Creek during different times of day and tidal cycle, and we observed this pattern on multiple occasions from May–October. In the future, a Bonnethead acoustic telemetry project spanning multiple creek systems along the Georgia shore or elsewhere on the East Coast could be used to further understand their large-scale spatial use of coastal estuarine waters in relation to tidal cycles and other environmental variables. Acknowledgments Funding for this research was provided by NOAA Living Marine Resources Cooperative Science Center (LMRCSC) Program (Award# 06OAR4810163) and the Department of Education Title VII (Award# P382G090003). We appreciate Dr. Matthew B. Ogburn, at the Smithsonian Environmental Research Center, for assisting in the data analysis, circular statistics, and control-tag analyses. We are grateful for the additional data from Chris Kalinowsky of the Georgia Department of Natural Resources, Coastal Resources Division. We acknowledge the field support of Dr. Charles Cotton, Michael Partridge, C.J. Carroll Schlick, Adam Sapp, Kate Doyle, Jeremy Mitchler, Vinay Arora, Courtney Pegus, Christy Pavel, Michele B. Sherman, Captain Jay Rosenweig, Captain Karega Moyo, Bull River Cruises (Captain Michael Neal and Captain Buddy Lee), and Michael Richter and Captain Harry Carter, from the Skidaway Institute of Oceanography. Editorial assistance was provided mostly by Michele B. 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