Anthropogenic modifications to a barrier island influence Bonnethead (Sphyrna tiburo) movements in the northern Gulf of Mexico
© Kroetz et al. 2015
Received: 4 May 2015
Accepted: 3 September 2015
Published: 30 September 2015
Barrier islands are dynamic features of the northern Gulf of Mexico that are affected by natural processes and more frequently, anthropogenic disturbances. In addition to providing a barrier from storms, these islands offer habitat for many marine species. In an effort to prevent oiling of the Alabama coastline following the Deepwater Horizon oil spill, an artificial rock-rubble berm was constructed in 2010 to reconnect two portions of Dauphin Island, a northern Gulf of Mexico barrier island that was separated during Hurricane Katrina. An acoustic array established prior to the closure of “Katrina Cut” was used to investigate the potential effect of this anthropogenic alteration on the movement patterns of acoustically tagged Bonnetheads (Sphyrna tiburo).
Across the entire acoustic array, the largest proportion of detections occurred on receivers before construction at Katrina Cut (0.55), followed by the period after the construction (0.25), and the period during the construction (0.20). Focusing on the area near Katrina Cut, the two hydrophones in this area had the highest proportion of detections before construction (0.10), followed by the period during construction (0.02), and then the period after construction and closure of Katrina Cut (<0.01). The post-closure location of highest activity for Bonnetheads shifted westward following the closure of Katrina Cut. Salinity values from a hydrographic model were higher at the Katrina Cut location in 2010 when the cut was open compared to 2011 and 2012 when the cut was closed, a potential explanation for the observed changes in Bonnethead distribution.
Fluctuations in salinity post-closure of Katrina Cut may effect Bonnethead movements, although other factors, including seasonal migrations and/or the redistribution of their preferred prey, may also be important. Regardless of the mechanism, this rapid shift in distribution of Bonnetheads highlights the potential effect of anthropogenic activities on sharks using coastal environments.
KeywordsAcoustic telemetry Movement patterns Shark Salinity Katrina Cut
Numerous species of elasmobranch fishes use the dynamic habitat provided by coastal ecosystems. Nearshore habitats can be highly productive, supporting a high biodiversity of fishes and invertebrates , common prey resources for coastal elasmobranchs. Understanding the degree to which small coastal elasmobranchs use these nearshore habitats can lead to better management and conservation, and strengthen our ability to predict how changes in environmental factors will affect these populations [2–4]. Shifts in habitat with ontogeny and/or as a response to environmental stressors can make evaluating habitat use, as measured by time spent in an area by a species, difficult. However, advances with in situ biotelemetry allow for movements of fishes to be monitored over extended time periods and across numerous habitats .
Numerous factors can influence nearshore habitat use by coastal elasmobranchs . Abiotic factors like temperature and salinity can affect distribution and habitat use of many coastal elasmobranch species including Bonnetheads (Sphyrna tiburo, ), juvenile bull sharks (Carcharhinus leucas, [7, 8]), and juvenile sandbar sharks (Carcharhinus plumbeus, ). For example, controlled releases of freshwater from the Caloosahatchee River greatly affected salinity levels within Pine Island Sound, FL. Movements and distributions of acoustically tagged Bonnetheads were monitored during these freshwater releases, and Bonnetheads shifted to areas of the estuary that were higher in salinity . In addition to abiotic factors, anthropogenic alterations can change nearshore environments and negatively affect coastal species. For example, populations of the endangered smalltooth sawfish (Pristis pectinata) have declined dramatically, largely the result of bycatch and habitat loss . On the other hand, anthropogenic alterations may be beneficial to other coastal species. In Texas, a dredged channel created a tidal connection between the Gulf of Mexico (GOM) and the Upper Laguna Madre. This allowed for significant ingress of the nekton of commercially important species to habitats that were previously inaccessible, potentially increasing production . Anthropogenic alterations to natural coastlines may be beneficial or detrimental to a suite of coastal species; however, the impact of such modifications remains unknown without dedicated, species-specific monitoring.
Bonnetheads are small coastal sharks found in estuarine and coastal waters of the Atlantic Ocean and GOM . Bonnetheads are long-term residents of coastal estuarine systems  and exhibit site fidelity to certain estuaries, often returning to these areas after extended periods of time [14, 15]. Species that exhibit such site fidelity provide an opportunity to examine how environmental changes affect movement patterns . While factors that influence Bonnethead movements have been well studied in the eastern GOM [6, 16], comparatively less is known about the movements of this species in the northern GOM [but see 17]. Identifying the region-specific factors influencing the distribution of this species is essential for understanding potential impacts induced from anthropogenic alterations to coastal ecosystems.
Both anthropogenic (e.g., coastal development) and natural (e.g., hurricanes) disturbances can change the geomorphology of coastal habitats [18, 19]. These shifts can affect environmental conditions, thus affecting species using nearshore habitats . As these disturbances to coastlines become increasingly common, it is imperative to investigate the potential impact these alterations have on species that reside in these habitats. Herein, we provide data on Bonnethead movements in response to the artificial closure of a natural passageway in a barrier island. Our objectives were twofold. The first objective was to assess residency and moment patterns of Bonnetheads across coastal Alabama. Our second objective was to investigate if an anthropogenic alteration to natural coastline affected the movement patterns of Bonnetheads in that same region. Using acoustic telemetry we were able to show a relatively rapid shift in Bonnethead movement in response to an anthropogenic alteration.
All research was conducted in accordance with the University of South Alabama (USA) animal ethics protocol 437256 for fish telemetry. This research was approved by the Institutional Animal Care and Use Committee (IACUC) and the state of Alabama authorities. All sharks were supplied with flowing seawater during tagging procedures and were handled quickly and carefully. No additional samples were taken from sharks during tagging procedures.
Specimen collection and tagging
Field sampling occurred in the coastal and estuarine waters around Dauphin Island, AL, USA. Targeted gillnet sampling was used to collect Bonnetheads for acoustic tagging. Once captured, sharks were carefully removed from gillnets and were measured (precaudal, fork, and total length in mm), weighed (to the nearest kg), sexed, and tagged. Maturity in females was estimated from data on fork length (FL, mm) at 50 % maturity  and maturity in males was determined by external characteristics of claspers following the methodology of Clark and von Schmidt . Sharks were tagged with two tag types; an external, plastic swivel tag (Dalton ID, Henley-on-Thames, UK) and an internal ID only acoustic tag (Lotek model MM-MR-16-50, 16 × 80 mm, 35 g in air, tag life estimated 389 days). The acoustic tags were multi-mode transmitters that emitted two ID codes: every 60 s on an Rcode frequency (69 kHz) and every 5 s on a MAP code frequency (76 kHz). A small 13-mm incision was made above the abdominal midline for insertion of the acoustic tag into the peritoneal cavity of the sharks. Once the tags were implanted, the incision was closed with surgical sutures (3.0 Ethicon Prolene monofilament) and an antiseptic wipe was applied. The same tagging locations were used before and after the closure of Katrina Cut; near the west end of Dauphin Island and near Katrina Cut (Fig. 2). Eleven Bonnetheads were tagged in 2010 and nine were tagged in 2011.
Data from the acoustic array were analyzed to determine residency and movement patterns of Bonnetheads before, during, and after the construction of the rock-rubble berm that closed Katrina Cut. “Before” Katrina Cut refers to the period of time when Katrina Cut was open prior to construction of the berm (May 2010–early July 2010) while “after” Katrina Cut refers to the period of time when the cut was completely closed and construction of the berm was completed (May 2011–June 2012). “During” Katrina Cut refers to the period of time when construction of the berm was underway and includes a period when the cut was open (mid July 2010–December 2010) as well as when the cut was functionally closed off (December 2010–April 2011). Detections logged on the hydrophones were analyzed as proportions of each tagged individual, i.e., the proportion of detections was calculated for individual sharks and then averaged for each receiver. The occurrence of tagged Bonnetheads was plotted to provide a visual timeline of presence throughout the study. To determine residency, Bonnetheads were considered present in the study area if more than one detection occurred on any given receiver within a single day. Days at liberty were calculated as the difference between the time when a Bonnethead was first detected in the array and the time of the last detection within the array. Detection data were plotted in ArcMap GIS (ESRI ArcView 10.1) to visualize overall detections and relative receiver use within the array.
To visualize differences in Bonnethead movement patterns before, during, and after construction of the rock-rubble berm at Katrina Cut, we applied inverse distance-weighted (IDW) interpolations in ArcMap GIS. The IDW measures the complete set of values (i.e., proportion of detections) surrounding prediction locations (i.e., receivers in the array). Measured values that were closer to the prediction location were weighted higher than those farther away. Locations where activity was the highest were determined using 50 and 90 % contours of the interpolated values for periods before, during, and after the construction of the rock-rubble berm at Katrina Cut.
A three-dimensional hydrodynamic model previously developed for coastal Alabama including Mobile Bay and eastern Mississippi Sound was available for this study . The model, when forced by observed open boundary water levels, freshwater discharge, and wind gave a good representation of the observed surface elevation, current velocity, and salinity for both total and subtidal components . The model was also shown to reproduce the observed salinity in the Cedar Point Reef area at the eastern end of Mississippi Sound for 2 years in 2008–2010 . We used this model to simulate salinity variations before and after the closure of Katrina Cut. Model simulations were conducted for the years 2010–2012 to encompass the entirety of this study, with Katrina Cut open in 2010 and with it closed in 2011–2012. The forcing conditions of the model runs were prepared following the procedures described in Kim and Park  and Park et al. .
Tagging and biological data for acoustically tagged Bonnetheads detected within the acoustic array
Days at liberty
Number days detected
All five Bonnetheads displayed interesting movement patterns during this study. For example, Bonnethead 10143 remained at Katrina Cut prior to construction of the rock-rubble berm from the time that it was tagged through the end of May 2010. This individual was not detected in our array in June, but once construction began in July, this individual returned to Katrina Cut for several hours and then shifted its movement to the northeastern part of Mississippi Sound in August. It then moved eastward to Fort Morgan Beach in October before detections ceased for 2010. The same individual returned in 2011 further west to Petit Bois Island where it remained for 1 day in April before moving to Ft. Morgan, then Orange Beach where it subsequently returned to the west end of Dauphin Island. This shark returned to Katrina Cut briefly (i.e., hours) before leaving the location in favor of the west end of Dauphin Island (a supplemental video file shows this in more detail, see Additional file 1). Bonnethead 10132 displayed similar movement behaviors, but to a lesser degree, remaining at Katrina Cut for 1 day in 2010 and returning in 2011 to Petit Bois Island. Bonnetheads 10131 and 10167 remained at Katrina Cut for the entire time that we received detections, including the period before and during construction of the rock-rubble berm. Bonnethead 10274 was tagged after the construction of the berm at Katrina Cut, remained at this location for several hours before moving west to the end of Dauphin Island and then returning even further west to Petit Bois and Horn Islands the following year. Bonnetheads 10132, 10143, and 10274 typified a general westward shift in movement from the time that Katrina Cut was open to the time that it was closed with some individuals remaining at Katrina Cut until it was closed.
On average, salinity was higher in 2010 when Katrina Cut was open. In 2010, surface salinity had a mean value of 28.2 (±4.6 SD) psu and varied between 4.0 and 35.6 psu. Bottom salinities were similar with a mean value of 31.4 (±2.5 SD) psu and varied between 6.1 and 35.8 psu. After Katrina Cut was closed in 2011, mean surface salinity decreased to 23.6 (±6.5 SD) psu and the range was 1.5–33.1 psu while mean bottom salinity decreased to 25.7 (±5.3 SD) psu and the range was 1.5–34.1 psu. Over the first five months of 2012, mean surface salinity was 22.5 (±5.6 SD) psu and the range was 8.2–31.3 psu and mean bottom salinity was 24.9 (±5.0 SD) psu and the range was 8.5–32.2 psu.
Our data demonstrate the presence and shifts in movement of Bonnetheads along barrier islands in the northern GOM following an anthropogenic alteration to natural coastline. These findings indicate a relatively rapid shift in Bonnethead movement following the construction of the rock-rubble berm that closed off the passageway of Katrina Cut, suggesting that an anthropogenic modification affected Bonnethead movements.
Barrier islands shift and naturally change geomorphology, often returning to their previous state before a devastating event, such as a hurricane . For example, Dauphin Island, AL was previously fragmented into two islands in the early 1900s with an 8.5-km-wide channel that eventually filled due to longshore sediment transport during several years without large storms [18, 28, 29]. Human intervention to accelerate or facilitate natural processes often comes with unanticipated consequences that may affect marine taxa. For example, closing off a corridor between the GOM and Mississippi Sound may negatively affect species using the corridor as a means to ingress into shallower and more protective waters for biological or reproductive strategies. Bonnetheads using Katrina Cut as a means of moving into and out of Mississippi Sound may have been prohibited from reaching an area of preferred habitat, and may have thus shifted movement patterns.
When Katrina Cut was open, Bonnetheads generally remained in a small area near that passageway. The highest proportion of detections occurred at Katrina Cut when it was open, both before and during construction of the rock-rubble berm, and then decreased in the proportion of detections once the cut was closed. As we observed a relatively rapid decline in the proportion of detections at Katrina Cut following the installation of the rock-rubble berm, we suggest that Bonnetheads were using this passageway as a means to enter Mississippi Sound and that the area near Katrina Cut was a preferred habitat. However, the high proportion of detections at Katrina Cut may reflect seasonal habitat use. Bonnetheads have been shown to use estuarine waters more frequently during the summer months  and thus our high proportion of detections may be a function of season. In addition, Bonnetheads have been shown to have a high degree of site fidelity to specific estuaries . Since 2010 was the first year of this study, we were unable to examine the degree of site fidelity Bonnetheads exhibit to Katrina Cut. However, we suggest that there is likely some plasticity to Bonnethead site fidelity and that Katrina Cut was a preferred location for Bonnetheads to reside in this region.
Changes in salinity offer the most intuitive explanation for the changes in habitat use shown by tagged Bonnetheads, in line with previous findings for this species [4, 6, 15]. We found that Bonnetheads generally remained at Katrina Cut while the cut was open and made a general westward shift once the cut was closed, as seen from the IDW analysis. The IDW analysis was based on our subset of tagged individuals, and thus areas with higher proportions of use could be biased by the five individuals that we focused on; however, this analysis is a good visual representation of the areas with the highest proportion of use for these individuals. Modeled salinity for 2010, when Katrina Cut was open, demonstrates high-frequency fluctuations in both surface and bottom salinities. Clearly, the presence of Katrina Cut allowed for higher salinity GOM water to be advected into Mississippi Sound by flooding tidal currents, creating high-frequency tidal fluctuations in both surface and bottom salinity. It is important to note that in 2010, salinity was the highest despite the largest freshwater discharge, likely due to the tidal connection with the GOM providing a source of higher salinity water. While we lack a complete set of data to test this relationship, relatively small fluctuations in salinity due to freshwater discharge and tidal cycles may be sufficient to alter Bonnethead movements in our study area.
Salinity may have indirectly altered the distribution of Bonnetheads, through a redistribution of their preferred prey. Previous studies have indicated the importance of prey availability in determining the distribution of coastal sharks [30, 31]. Bonnetheads have been widely documented to consume crustaceans, particularly blue crabs (Callinectes sapidus [32, 33]). It has been suggested that Bonnetheads use estuaries along the east coast as summer feeding grounds, likely due to the high availability of blue crabs . Seagrass is an important habitat for blue crabs  and changes in habitat may play a role in prey redistribution. For example, when Katrina Cut was open, shoal grass (Halodule wrightii) was present in large abundance stretching over 6 km in length for several years while the cut was open (KL Heck unpublished observations). The closure of Katrina Cut was followed by a marked decline in shoal grass (KL Heck unpublished observations), which could potentially alter habitat use by blue crabs. Diet analysis of Bonnetheads in the current study region confirms that Bonnetheads primarily consume portunid crabs, notably blue crabs [Kroetz, unpublished data]. While not directly tested in the current study, a shift in blue crab distribution due to changes in habitat, salinity, dissolved oxygen, or temperature generated by the closure of Katrina Cut may be a factor in the shift in Bonnethead habitat use observed in this study.
Water depth has been identified as an important driver of coastal shark distribution, and is likely species specific . Long-term fisheries independent gillnet surveys conducted in Texas estuaries have shown that the probability of capturing Bonnetheads was highest near tidal inlets with access to deepest waters (>1 m deep, ). Katrina Cut was a tidal inlet that was approximately 3 m deep in the middle of Dauphin Island allowing for swift currents to flow between the two land pieces . Closing off Katrina Cut effectively terminated the tidal inlet and thus reduced the swift currents as well as the higher salinity tidal connection to the GOM. The closure of the tidal inlet may be another driver for the shift in movement that we observed with acoustically tagged Bonnetheads.
During the construction of the rock-rubble berm, cranes, boats, and trucks were continuously present for several months, and these disturbances may have impacted Bonnethead habitat use. In addition to the physical water column disturbance caused by these machines, there was potential for pollution and habitat degradation during the berm construction, and these factors have been shown to affect shark resilience and abundances [5, 35]. While anthropogenic impacts were not found to influence Bonnethead occurrence in FL estuaries , Bonnetheads in our study area may have been affected by the continuous, unnatural disturbance.
Knowledge of acoustic detection range when using passive telemetry is critical for the interpretation of animal movements within an array . Many variables can affect detection range (see  for a comprehensive review), including properties of the water body such as salinity, temperature, and suspended particles and substrate . A portion of this study included monitoring movements of Bonnetheads during construction of the rock-rubble berm. During construction, sediment, mud, and silt were likely suspended in the water column, which can affect detection range of receivers . For the duration of the construction period, four Bonnetheads were detected at Katrina Cut. The proportion of detections that we received during the construction period decreased by half from the proportion we detected before construction at the same receivers. It is possible that Bonnetheads may have been present in the area for longer periods, but decreased acoustic detection range may have precluded their identification. We suggest that future work examining the movements of this species include models that incorporate other potential predictors of movement, such as detection range, temperature, and dissolved oxygen.
Our data demonstrate a relatively rapid change in habitat use for Bonnetheads, a change that could be due to altered abiotic conditions, changes in water quality, re-distribution of preferred prey, or even a decrease in the detection range of our hydrophone array resulting from prolonged construction in the area. Barrier islands are highly dynamic and subject to change either naturally or through anthropogenic modifications. Marine fishes using coastal environments must adapt to changes in their environment or leave the area to find more suitable habitat . Construction of the rock-rubble berm restored habitat at Katrina Cut to a previous state. Historically, it is likely that Bonnetheads have been adapting their movements in accordance with natural shifts in barrier island morphology, albeit on an environmental rather than an anthropogenic time frame. Given the snapshot of data before Katrina Cut was closed off, it is difficult to conclusively identify a single factor that leads to the observed shift in Bonnethead movement. Regardless, we demonstrate that Bonnetheads are capable of rapidly responding to a changing environment, a response that may prove critical in the face of future changes to coastal ecosystems.
Gulf of Mexico
Coastal Alabama Acoustic Monitoring Program
Science Applications International Corporation
Wireless Hydrophone System
Inverse Distance-Weighted interpolations
AMK conceived the study, conducted fieldwork, analyzed and interpreted data, and wrote the manuscript. SPP participated in the conception and design of the study and aided in manuscript preparation. JMD participated in design of the study, data interpretation, and aided in manuscript preparation. KP carried out hydrodynamic model simulations, interpreted the model results, and aided in manuscript preparation. All authors read and approved the final manuscript.
The authors thank the University of South Alabama and the Dauphin Island Sea Lab for funding this project. The CAAMP array was funded through a grant from the Shelby Center for Ecosystem Based Fishery Management awarded to M Ajemian and JM Drymon. Special thanks are given to A Robydek at SAIC for cooperative sharing of acoustic telemetry data. Thanks are owed to M Ajemian for assistance with this study, A Aven and S Bosarge for assistance with ArcMap, and all of the interns, technicians, and graduate students in the Fisheries Ecology Laboratory at the Dauphin Island Sea Lab for field support. We wish to thank J Carlson and three anonymous reviewers for insightful comments and suggestions that improved this manuscript.
Compliance with ethical guidelines
Competing interests The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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