Occurrence and habitat use of the critically endangered smalltooth sawfish Pristis pectinata in the Bahamas
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1 Journal of Fish Biology (2015) 87, doi: /jfb.12825, available online at wileyonlinelibrary.com Occurrence and habitat use of the critically endangered smalltooth sawfish Pristis pectinata in the Bahamas T. L. Guttridge*, S.J.B.Gulak, B. R. Franks, J. K. Carlson, S. H. Gruber*, K. S. Gledhill, M. E. Bond**, G. Johnson* and R. D. Grubbs *Bimini Biological Field Station Foundation, Bimini, Bahamas, National Marine Fisheries Service, Southeast Fisheries Science Center, Panama City Laboratory, Panama, FL, U.S.A., Florida Southern College, 111 Hollingsworth Drive, Lakeland, FL, 33801, U.S.A., Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, FL, 33124, U.S.A., South African Shark Conservancy, Old Harbour Museum, Hermanus, 7200, South Africa, **Institute for Ocean Conservation Science/School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, , U.S.A. and Florida State University Coastal and Marine Laboratory, St Teresa, FL, 32358, U.S.A. This study documents and discusses recent ( ) sightings and captures of smalltooth sawfish Pristis pectinata in the Bahamas. Movement patterns and habitat preferences of five P. pectinata are examined: two tracked with acoustic telemetry in Bimini and three tagged with pop-up archival transmitting tags in Andros. Historically, P. pectinata may have been distributed throughout the Bahamas; however, since 2002 only 61 encounters were recorded including: Andros (30), Bimini (19) and a handful across other Islands (12). In Bimini, all P. pectinata were >225 cm (stretched total length, L ST ) suggesting that it is not used as a nursery area. Pristis pectinata in Andros ranged from c. 80 to 450 cm (L ST ) indicating that this island might be an important nursery and breeding habitat. Pristis pectinata tracked in both islands remained at depths <3 m, often adjacent to mangrove habitats, displaying residency from 42 days (Bimini) to 180 days (Andros). These preliminary findings confirm the Bahamas as an important habitat for P. pectinata and emphasize the urgent need for national protection and management of this population The Fisheries Society of the British Isles Key words: active tracking; Caribbean; elasmobranch; endangered species; mangrove; telemetry. INTRODUCTION A thorough understanding of abundance, distribution, habitat use and movement patterns is critical to improved management and conservation of rare and endangered animals. Generating this type of information for large marine species is particularly challenging due to the vast geographic ranges they occupy and the fact that upper level predators naturally occur in low abundance (McClenachan et al., 2012). This is compounded by a concealing environment and the logistical constraints of capture. These Author to whom correspondence should be addressed. Tel.: ; tristanguttridge@gmail.com The Fisheries Society of the British Isles
2 PRISTIS PECTINATA IN THE BAHAMAS 1323 features not only slow scientific progress, but also complicate and impede the implementation of legislation and ultimately effective management and protection. Sawfish (family Pristidae) are among the world s most threatened marine fishes (Simpfendorfer, 2005; Dulvy et al., 2014a; Harrison & Dulvy, 2014). They are a small group of elasmobranchs usually occurring in shallow, coastal habitats in tropical and subtropical waters including estuarine and freshwater habitats (Waters et al., 2014; Hollensead et al., 2015). Sawfishes are among the largest of the chondrichthyans and are characterized by an elongated rostrum with lateral tooth-like denticles presumably used for feeding and defence (Bigelow & Schroeder, 1953; Wueringer et al., 2009). All five species (Faria et al., 2013) face a very high risk of global extinction based on severe declines in their numbers and geographical distribution over the past century (Dulvy et al., 2014b). This perilous status is due to commercial and recreational fishering mortality, primarily as by-catch, combined with the loss of critical near-shore habitat due to coastal development and low reproductive potential making the species vulnerable to anthropogenic effects (Thorson, 1982; Seitz & Poulakis, 2006; Carlson & Simpfendorfer, 2015). Most notably among Pristidae, smalltooth sawfish Pristis pectinata Latham 1794 is potentially at greatest risk because it has the smallest and most fragmented remaining geographic range (Harrison & Dulvy, 2014). Historically found in the waters of 47 Atlantic nations, P. pectinata is now considered extirpated from 26 countries, presence uncertain in 16 and extant in only five, with a geographic range contraction of 81% (Dulvy et al., 2014b). Importantly, the documentation of such declines on a global scale has led to P. pectinata being assessed as critically endangered on the IUCN Red List of threatened species (Carlson et al., 2013; Harrison & Dulvy, 2014). In 2007, all five sawfish species were listed in Appendix I of the Convention on International Trade in Endangered Species (CITES: June 2007, The Hague, Netherlands), which restricts commercial trade. Further, more recently all were included under Appendices I and II for protection under the Convention on Migratory Species (CMS: November 2014, Quito, Ecuador). For P. pectinata, inclusion in these treaties is a critical step for future recovery, and will enhance cooperation between countries which is necessary to restore their population to its former expansive range. In the U.S.A., P. pectinata is currently listed as endangered under the Endangered Species Act (NMFS, 2003, ESA Listing Rule for the U.S.A. DPS, Federal Register 68 FR 15674). This was due to widespread declines, estimated as great as 95% last century, as a consequence of mortality and habitat loss (Simpfendorfer, 2000; NMFS, 2009). As a result, a recovery plan was developed and implemented for this species (NMFS, 2009), which has generated research that has advanced the understanding of critical habitat use, population structure, movement patterns, life-history parameters and genetic diversity (Chapman et al., 2011; Faria et al., 2013; Carlson et al., 2014; Waters et al., 2014; Hollensead et al., 2015; Papastamatiou et al., 2015). Moreover, there are promising indications that their decline has been halted (Carlson et al., 2007), and population viability analysis suggests that the U.S. population is more productive than previously estimated and may have a higher capacity to recover (Carlson & Simpfendorfer, 2015). Whilst this is greatly encouraging for P. pectinata, ultimately the protection afforded in the U.S.A. is not sufficient for their conservation on a global scale, which requires the development and implementation of focused, regional research and recovery programmes (Dulvy et al., 2014b).
3 1324 T. L. GUTTRIDGE ET AL. To date, besides the U.S.A., the only other country where P. pectinata can be reliably encountered in the western Atlantic Ocean is the Bahamas (Carlson et al., 2013). Despite huge swathes of suitable habitat, such as the west side of Andros (24 61 N; W), however, recently documented encounters in the Bimini Islands (Jennings et al., 2012) and anecdotal encounters from a handful of islands identified by Harrison & Dulvy (2014), very little is known about P. pectinata in the region (Carlson et al., 2014). This is particularly concerning considering the recent mangrove removal and coastal habitat degradation (Jennings et al., 2012), the lack of fishery management enforcement in the Bahamas and its proximity and potential connectivity to U.S. populations (Faria et al., 2013). Moreover, in the IUCN Global Conservation Strategy Report (Harrison & Dulvy, 2014), the Bahamas was assessed as a priority to have a more comprehensive and species-specific national protection. With the above in mind, this study reports encounters, captures and preliminary movement tracks of P. pectinata throughout the Bahamas between 2002 and It examines the current known spatial and temporal distributions of P. pectinata in the Bahamas and identifies key areas of conservation and research focus. Further, through acoustic and satellite tracking, this study preliminarily explores habitat use and movement patterns of five large juvenile and adult P. pectinata in Bimini and Andros. ENCOUNTERS AND CAPTURES MATERIALS AND METHODS For each encounter, reporters were asked to provide details including date, exact location, GPS co-ordinates when possible, water depth and any other environmental information (i.e. habitat type). Reports documented by scientific researchers were often captures, thus exact length measurements were frequently available along with sex. On these occasions, P. pectinata were either inadvertently captured in shallow water gillnets set to catch other elasmobranchs (Gruber et al., 2001) or caught using dip-nets, snares or rod and reel (Carlson et al., 2014). Lengths of the remainder of P. pectinata were estimated during public encounters and are therefore probably susceptible to large measurement error. Where possible, photographic evidence or video footage was also requested which allowed for species confirmation and in some cases sex determination and size estimates, through presence of prominent claspers and length of rostrum, respectively. When photographic or video evidence was not available, a series of questions about the body form were asked (i.e. colour, presence of rostral teeth, gills and number or location). It was assumed that all sawfish reported from public encounters were P. pectinata. In a comprehensive study of Pristis pristis (L. 1758) in the Atlantic Ocean, none were reported from the Bahamas (Fernandez-Carvalho et al., 2013). Moreover, the species presence historically in the Caribbean Sea is uncertain and early records may have been P. pectinata (Carlson et al., 2013). TELEMETRY Acoustic manual tracking Two individuals (Table I) in Bimini, Bahamas, were acoustically tracked to investigate short-term, fine-scale movements. One animal was captured inadvertently by gillnet and the other via dip-net. On capture, P. pectinata were secured alongside the vessel and processed (measured, stretched total length, L ST, sex determined and tagged with a U.S.A. National Marine Fisheries Service M-type dart tag). A continuous acoustic transmitter (P. pectinata BI-07-02: CHP-86-L-18, battery life 18 months; P. pectinata BI-12-01: PT-4, battery life
4 PRISTIS PECTINATA IN THE BAHAMAS days, Sonotronics; was attached using 68 kg (150 lb) test monofilament to a modified M-type dart and secured with a copper crimp. The transmitter was fitted to P. pectinata externally, by making a small incision lateral to the middle of the first dorsal fin c. 5 cm below the fin base with the dart inserted into the dorsal musculature, seating the anchor at adepthof3 5cm(Carlsonet al., 2014). Once the tag was fitted, P. pectinata were released in the immediate area of capture. Both animals were tracked from a shallow-draft research vessel (5 m) using directional hydrophone (DH-4, Sonotronics) and manual tracking receiver (USR-96, Sonotronics). Pristis pectinata locations were recorded every 5 15 min with hand-held (Garmin 72H; GPS along with a compass bearing and estimated distance (nearest 5 m) to the animal (based on audible signal intensity). A distance of >20 m was maintained between the boat and animal in order to minimize disturbance of P. pectinata natural movements. When possible, water depth was measured at 15 min intervals with a PVC pole (nearest 0 5m) and the substratum type was recorded (e.g. sand bottom, seagrass and macro-algae). Acoustic monitoring Between January 2007 and November 2008, nine submersible ultrasonic receivers (Sonotronics, SUR-1) were deployed as part of an ongoing study on juvenile lemon shark Negaprion brevirostris (Poey 1868) (Fig. 1; Guttridgeet al., 2012). In 2012, 13 underwater receivers (UR) were deployed the day following individual BI capture (6 May to 22 June 2012). URs were housed in a PVC pipe with a concrete base (Guttridge et al., 2012) and recorded the time, date and identity of the acoustic transmitter fitted to an animal that swam within range. Detection ranges of individual URs were dependent on substratum, water depth and wind speed (M. Van-Zinnicq Bergmann, J. S. Finger, I. Pen, R. Bullock, S. H. Gruber & T. L. Guttridge, unpubl. data) but typically ranged from a maximum of 300 m (2 3 m depth, sand substratum and low wind conditions) to minimum of 50 m (<1 m, seagrass substratum and high wind speed conditions). URs were retrieved once per month to download data and were returned to the recording location in the same 24 h period. Data were filtered to remove spurious detections, which were defined as any single transmitter detection occurring alone within a 24 h period. All other detections were treated as genuine and were assigned a tidal phase obtained from the U.S.A. National Oceanic and Atmospheric Administration (NOAA) adjusted by 1 5 h (Guttridge et al., 2012). Satellite archival telemetry Pristis pectinata (n = 3) were tagged opportunistically with pop-up archival transmitting tags (MK 10 PAT; 2010 and MK10 PAT-F; 2014, Wildlife Computers, Inc.; that archive temperature, depth and light levels (Table II). The MK10 PAT-F is also equipped with a Fastloc GPS to provide location information if the tag breaks the water surface. PATs were rigged with a modified harness. A section of 1 8 mm, stainless steel, 7X7 (49 strand) cable was attached to the satellite tag using two 1 8 mm double copperlock crimps. A section of 2 0 mm nylon chafe tubing covered the cable in areas that make contact with P. pectinata. A hollow, stainless-steel dart applicator was pushed through the thickened, anterior portion of the first dorsal fin near the dorsal-fin origin. This region primarily consists internally of connective tissue with very little vascularization; therefore, the insertion results in no bleeding. The free end of the harness assembly was threaded into the applicator through the dorsal fin and the applicator was then extracted from the opposite side of the dorsal fin. The harness was pulled through the dorsal fin, and the free end of steel cable inserted into the open sides of the two double copperlock crimps. The cable was pulled through the crimps to decrease the loop in the harness until the crimps were just under the free rear tip of the dorsal fin. The crimps were then closed (crimped) to secure the harness in place and the excess steel cable was removed with wire cutters. The satellite tag trailed just behind the dorsal fin after the P. pectinata were released. The metal crimps corrode in <1 year, whereupon the harness slips off the animal, leaving a small hole (Carlson et al., 2014). Depth and temperature data were summarized into 4 h bins to maximize
5 1326 T. L. GUTTRIDGE ET AL. Table I. Pristis pectinata encounters across the Bahamas during Record Date Island Depth (m) Captured (Y, yes; N, no) Activity Number Sex L ST estimated (cm) AB Unknown Abaco Y Fishing 1 AB February 2014 Abaco 0 6 N Guide AN April 2004 Andros 7 N Diving AN May 2005 Andros 14 N Diving AN June 2005 Andros 17 N Diving AN June 2006 Andros 24 N Diving AN June 2006 Andros 1 N 1 AN June 2006 Andros N 1 AN May 2007 Andros 17 N Diving AN June 2009 Andros 2 N Searching AN-10-01* 7 May 2010 Andros 1 Y/dip-net Searching 1 Male 224 AN-10-02* 9 May 2010 Andros 2 Y/tailer Searching 1 Female 304 AN May 2013 Andros 1 N Searching AN January 2014 Andros 1 Y/rod reel Guide AN January 2014 Andros 1 N Guide AN March 2014 Andros 1 N Searching 1 AN-14-04a 7 March 2014 Andros 1 N Searching 1 AN-14-04b* 7 March 2014 Andros 1 Y/rod reel Searching 1 Female 307 AN March 2014 Andros 1 N Target AN March 2014 Andros 1 5 N Target AN March 2014 Andros 0 5 N Guide AN March 2014 Andros 1 N Guide AN March 2014 Andros 1 N Guide AN April 2014 Andros 1 N Guide AN April 2014 Andros 1 N Guide AN May 2014 Andros 1 N Guide 1 85 AN November 2014 Andros 1 N Guide AN March 2015 Andros 0 5 N Guide 2 80 AN March 2015 Andros 0 5 Y/rod reel Searching AN-UK-01 Unknown Andros 1 N Guide >1 AN-UK-02 Unknown Andros 1 N Guide >1 BE Unknown Berry Islands N Fishing 1 BI January 2002 Bimini 2 5 N Boating BI April 2002 Bimini 1 Y/gillnet Gillnetting 1 Male 260 BI September 2002 Bimini 2 N Boating 1 Female BI April 2004 Bimini 1 5 N Fishing 1 350
6 PRISTIS PECTINATA IN THE BAHAMAS 1327 Table I. Continued Record Date Island Depth (m) Captured (Y, yes; N, no) Activity Number Sex L ST estimated (cm) BI May 2004 Bimini 1 Y/tailer Boating 1 Male 268 BI-04-03a 6 October 2004 Bimini 1 Y/gillnet Gillnetting 1 Male 253 BI-04-03b 7 October 2004 Bimini 1 N Boating 1 Male 253 BI-04-03c 13 October 2004 Bimini 1 N Boating 1 Male 253 BI-04-03d 24 October 2004 Bimini 1 Y/tailer Boating 1 Male 253 BI October 2004 Bimini 1 N Boating 1 Male BI October 2006 Bimini 7 N Diving BI May 2007 Bimini 1 Y/gillnet Gillnetting 1 Female 260 BI-07-02a 6 June 2007 Bimini 1 Y/gillnet Gillnetting 1 Female 264 BI-07-02b 22 June 2007 Bimini 1 5 N Boating 1 Female 264 BI May 2008 Bimini 1 5 N Boating BI May 2009 Bimini 1 5 N Boating BI May 2012 Bimini 1 5 Y/tailer Fishing 1 Female 410 BI May 2012 Bimini 1 5 N Boating BI May 2013 Bimini 4 N Snorkelling 1 Female 375 CC November 2004 Cat Cay 30 N Diving CC November 2014 Cat Cay 17 N Diving 1 Male 280 CC January 2015 Cat Cay 5 N Fishing EL May 2005 Eleuthera 2 N Guide 1 Female EX September 2012 Exuma 35 N Diving EX February 2014 Great Exuma N GB May 2014 Grand Bahama 1 N Guide 1 Female 375 HI September 2010 Harbour Island 5 Handline Fishing LI April 2010 Long Island 20 N Diving 1 Female 300 L ST, stretched total length. *Fish was tagged with a satellite tracking device. Fish was tagged with acoustic tracking device. the amount of successful data packet transmissions, and also allow direct comparison with a previous study (Carlson et al., 2014). The MK10 PATs were programmed to release after 180 days, float to the surface and transmit data to passing Argos satellites. The MK10 PAT-F is equipped with the same onboard battery pack as the MK10 PATs, but has greater energy requirements due to the Fastloc GPS. This tag was programmed to release after 60 days to ensure that there was sufficient battery power remaining to transmit the summarized archive data. DATA ANALYSIS Acoustic tracking and encounter data To obtain more accurate positional estimates for the tracked P. pectinata, an Excel geometry function add-in (Spherical Earth Geometry: National Marine Mammal Laboratory, 2000) that incorporated the signal bearing and distance from the research vessel to the animal was used. All tracking positions and encounter locations were visualized using GIS (ESRI ArcMap 10.2; ESRI, 2011). Further, when a reporter supplied a length estimate for the encountered P. pectinata, the median value was entered (e.g. if the range cm L ST was given, the median 325 cm was recorded). Rate of movement (ROM) was calculated by dividing the distance moved by the time between two positions (Sundstrom et al., 2001). Pristis pectinata swimming was
7 1328 T. L. GUTTRIDGE ET AL km Fig. 1. Ultrasonic acoustic receiver locations with number of diurnal and night-time detections for Pristis pectinata in Bimini Islands, Bahamas. Node size is proportional to the number of periods individual P. pectinata were detected, i.e. six night-time v. three daytime periods (, 2007 receivers;, 2012 receivers;,day;, night;, one;, 10). calculated with two estimates of linearity: (1) short term, each hour of the track (i.e. distance between the first and last point of the hour divided by the distance covered within the hour) and (2) overall, distance between the first and last point divided by the total distance covered. Linearity scores vary between 0 (start and end points are the same) and 1 (perfect straight line between points). The closest straight-line distance in m was calculated from each tracking location to the shoreline using the Near Table function from the Spatial Analyst extension for ESRI ArcMap (ESRI, 2011). Archival satellite telemetry Swimming speed and distance travelled were estimated for P. pectinata with the MK10 PAT-F. Satellite locations were first limited to those with error estimates of <1 5 km, allowing the time and distance between concurrent locations to be calculated. Light location data for the MK10 PATs previously processed (Carlson et al., 2014) were combined with Argos positions and Fastloc GPS co-ordinates from the MK10 PAT-F and analysed using kernel density estimation (KDE) with the spatial analyst extension for ESRI ArcMap. The cell size was set to 50 m and the search radius to 2000 m. Isopleths were produced using Geospatial Modelling Environment software (Beyer, 2012) which creates contour lines based on a raster data set representing a probability surface. Isopleths represent the boundary lines that contain a specified volume of a surface. Lines were drawn to represent 5, 25, 50, 75 and 95% intervals.
8 PRISTIS PECTINATA IN THE BAHAMAS 1329 Table II. Sex, stretched total length (L ST ), tagging and pop-off localities, days at liberty and maximum depth attained for Pristis pectinata Record Days Sex L ST (cm) Tagging location Pop-off location Tagging Pop-off Days at date N W date N W liberty Maximum depth (m) AN Male May July AN Female May November AN-14-04b 60 Female March May Days, the number of days the pop-up archival transmitting tag (PAT) was programmed to release from deployment.
9 1330 T. L. GUTTRIDGE ET AL. RESULTS ENCOUNTERS OF P. PECTINATA IN THE BAHAMAS Between 2002 and 2015, a total of 61 sightings were recorded throughout the Bahamas (Fig. 2). Majority of these sightings were opportunistic observations obtained either from fisher guides (25%, n = 16), boaters (22%, n = 14), divers (16%, n = 11) or researchers targeting other elasmobranchs (20%, n = 13). Photographic evidence or video footage was provided for 41 (66%) of the 61 sightings. The number of reports remained relatively stable between 2002 and 2013, with a large peak in sightings in 2014 (c. 30% of all encounters, n = 19). This increase in sightings was due to targeted research trips to Andros and active interviews with and enlisting of local fisher guides, as well as use of social media platforms to promote reporting sightings (Fig. 3). Encounters did not appear to occur equally throughout the year with 70% (n = 35) of sightings from March to June and 11% (n = 6) from July through to October (Fig. 3). The encounter map highlighted Bimini (25 44 N; W) and Andros (24 61 N; W) as the islands with the highest probability of P. pectinata occurrence (Fig. 2). Interestingly, encounters in both of these areas were frequently in very shallow water <2 m, in close proximity to mangroves either at the entrance or inside a creek system. Throughout the Bahamas, P. pectinata encounters (n = 57) were reported in waters from 0 8 to 35 m deep with the majority occurring in depths 2 m (77%, n = 47) and few >5 m (16%, n = 10; Fig. 4). There was a significant relationship between P. pectinata reported L ST and depth, with larger animals tending to be found in deeper waters (r 2 = 0 25, P < 0 001; Fig. 5). Pristis pectinata were mainly found close to shore (55%, n = 34, <100 m from shore) and (22 5%, n = 13, >1 km from shore) [Fig. 6(a)]. There was one sighting c. 14km offshore of a 300 cm L ST this was observed resting in 5 7 m water next to a boat wreck. Combined, P. pectinata of all life stages were encountered in the Bahamas ( cm L ST ; Table I). The most commonly reported P. pectinata were juveniles (50%, n = 24; cm L ST ), with few adults (12%, n = 6; >400 cm L ST ) and YOY (c. 5%,n = 2; <100 cm L ST ) [Fig. 6(b)]. All P. pectinata encountered in Bimini were large juveniles to adults (>250 cm L ST ). The only confirmed occurrence of a YOY P. pectinata (80 cm L ST ) across the Bahamas was documented in Andros Island, although a single record of a very small juvenile P. pectinata that was probably YOY from Abaco was reported. Sex was infrequently documented during reports (n = 16, female 16% n = 10; male 10% n = 6). BIMINI Movement patterns and habitat preferences Two P. pectinata were actively tracked in Bimini (Table I and Fig. 7). The first P. pectinata captured in 2007 (BI-07-02) was re-sighted 16 days post-tagging by a local tour operator. The animal was observed resting in shallow water (<2m) at a plane wreck located c. 1 km off South Bimini Island (Fig. 7). This individual was tracked from 1800 to 0400 hours on 22 to 23 June 2007 (Fig. 7). It travelled a total distance of km, with median ROM (46 2mmin 1 ) and range ( m min 1 ). ROM was correlated to distance from shore (r 2 = 0 32,
10 PRISTIS PECTINATA IN THE BAHAMAS 1331 U S A N Andros Bimini Esri, DeLorme, GEBCO, NOAA NGDC, and other contributors Legend number Esri, DeLorme, GEBCO, NOAA NGDC, and other contributors km Fig. 2. Spatial distribution of Pristis pectinata encounters across the Bahamas from 2002 to 2015 (n = 61). The size of the yellow circles is proportional to the number of sightings at that location. Andros and Bimini have been enlarged. P < 0 001) and with hourly linearity (r 2 = 0 51, P < 0 05), with the highest ROM and straightest tracks recorded at greater distances from Bimini. Interestingly, this animal spent c. 70% of its track >1 km from shore, with its final location 11 8 km east of Bimini. Further, this individual spent the first 6 5 h (60%) of its track in shallow water (0 5 2 m) and as it started to move off-shore its depth preference shifted to 4 8m. The second P. pectinata in 2012 was tracked post-capture in the main lagoon between North and South Bimini Islands (Fig. 7). Pristis pectinata BI was tracked from 1510 to 2325 hours on 5 May It travelled a total distance of 14 2 km, with median ROM (23 45 m min 1 ) and range (0 119 m min 1 ). For this individual, ROM was not correlated with distance from shore (r 2 = 0 01, P > 0 05) or linearity (r 2 = 0 18, P > 0 05). Unlike P. pectinata BI-07-02, however, it was observed to rest for 20 min on two occasions and spent >95% of its track 500 m from the mangrove shoreline of South Bimini (Fig. 7). Overall, linearity for this individual was 0 30; however, short-term scores also revealed periods of directed swimming (range: ). Throughout the track, this P. pectinata showed a strong preference for shallow water, with all locations recorded in <2 25 m (median: 1 4 m; range: m), over a mixed bottom type of seagrass, macroalgae and sand.
11 1332 T. L. GUTTRIDGE ET AL. Month December November October September August July June May April March February January Year Fig. 3. Temporal distribution of Pristis pectinata encounters across the Bahamas from 2002 to Size of circle is proportional to the number of sightings (n = 54). Residency Three P. pectinata captured in Bimini were encountered on multiple occasions and detected on ultrasonic receivers up to 6 weeks post-tagging, suggesting some degree of residency and return use of the Bimini Islands. BI was first sighted, captured and tagged on 6 October 2004 in the North Sound lagoon, North Bimini (Fig. 2). This individual was then subsequently observed to use the area on multiple days, over an 30 Frequency Reported depth (m) 30 Fig. 4. Reported depth frequency distribution of Pristis pectinata encounters across the Bahamas from 2002 to 2015 (n = 57).
12 PRISTIS PECTINATA IN THE BAHAMAS Depth (m) Reported L ST (cm) 400 Fig. 5. Relationship between depth and reported stretched total length, L ST,ofPristis pectinata from 2002 to 2015 across the Bahamas (y = 0 38x ; n = 47). 18 day period (Table I). On 24 October 2004, it was recaptured 1 2 km from its first capture site to confirm its identification. BI was detected on a UR positioned in the centre of the North Sound lagoon (Fig. 1) on three consecutive days, for up to 6 h (6 to 8 June 2007; Table I). It was opportunistically encountered in South Bimini on 22 June 2007 and followed overnight until the track was aborted on the Bahamas Bank (Fig. 7). On 1 July 2007 (0053 to 0647 hours), this individual was again detected (a) 50 (b) Frequency Distance from shore (m) Reported L ST (cm) Fig. 6. (a) Distance from shore frequency distribution (n = 60) and reported stretched total length, L ST, frequency distribution (n = 51) of Pristis pectinata encounters across the Bahamas from 2002 to 2015.
13 1334 T. L. GUTTRIDGE ET AL km Fig. 7. Movements of two manually tracked Pristis pectinata from 2007 and 2012 in Bimini, Bahamas (, track end;, track start;, 2007;, 2012). (n = 23) in the shallow (<2 m) lagoon waters of North Bimini on a UR positioned 400 m from the mangrove-fringed shoreline (Fig. 1). Pristis pectinata BI-12-1 was captured on 5 May 2012 and was subsequently tracked for 8 h until it was lost off South Bimini. This individual was detected on 17 days between 5 May and 22 June 2012, predominantly on URs located in the east of the lagoon (Fig. 1). Typically on each day, detections occurred across short time periods (5 10 min) during various tidal stages, with an emerging pattern that the P. pectinata was detected on 16 night-time v. four daytime periods. ANDROS All three satellite tags successfully reported data from 84, 180 and 59 day deployments (Table II). The first satellite tag deployed in 2010 (AN-10-01) P. pectinata, tagged near Deep Creek, moved inland before the tag pulled out. The second animal (AN-10-02) was tagged near Williams Island and the satellite tag popped off further upstream in Deep Creek. The light levels from this animal were too low to provide position estimates, suggesting that it may have remained in muddy and silty water. The individual tagged in 2014 (AN-14-04b) moved 40 3 km to the edge of the West Side National Park. Although the mean distance from tagging to pop-off location was relatively short (mean ± s.d. = 27 0 ± 12 0 km), this individual travelled a total of 285 km
14 PRISTIS PECTINATA IN THE BAHAMAS º 78 6º 78 4º 78 2º 78º 77 8º 77 6º 25º 25º 24 8º 24 8º 24 6º 24 6º 24 6º 24 6º 24 2º 24 2º 78 8º 78 6º 78 4º 78 2º km 77 6º Fig. 8. Kernel density estimation from three satellite tagged Pristis pectinata in Andros, Bahamas. Density increases from yellow to red and the isopleth contours represent 5, 25, 50, 75 and 95% of the surface area. over 59 days with a maximum speed of 6 6kmh 1 (mean speed = 0 8kmh 1 ). This P. pectinata spent the majority of the time in water <4 m deep (99 9%) and preferred temperatures between 26 and 32 C(78 5%). The KDE identified three areas that were highly utilized by P. pectinata (Fig. 8). DISCUSSION By combining encounter reports over a 14 year period between 2002 and 2015, this study was able to gain insight into the current distribution of P. pectinata across the Bahamas. Although sightings were generally rare (n = 61), Andros was identified as a potential area for mating and pupping for P. pectinata, with evidence of mature adults observed on deep reef sites and YOY on mangrove-fringed back-country flats. Further, regular annual short-term (<2 months) use of the Bimini Island environs by large juvenile to adult P. pectinata is reported, indicating that this could be an important migratory stop-off on route to U.S.A. or Bahamas. Harrison & Dulvy (2014) highlighted the lack of comprehensive species-specific protection in the Bahamas and identified the country as a priority for improved conservation of P. pectinata. These findings contribute an important baseline and identify key areas within the Bahamas for focused conservation and research efforts.
15 1336 T. L. GUTTRIDGE ET AL. Typically with encounter data, it is difficult to avoid biases that influence the resulting distribution maps, i.e. distribution of the observational effort could influence the numbers of animals observed (Wiley & Simpfendorfer, 2010; Waters et al., 2014). With this in mind, it is possible that year-round marine research since 1990, in the Bimini Islands conducted by the Bimini Biological Field Station Foundation (BBFSF: a facility located on South Bimini Island, Bahamas, that conducts scientific research on elasmobranchs; Feldheim et al., 2014), resulted in the high proportion of Bimini encounters (20%). Similarly, targeted searches for P. pectinata in Andros by researchers in recent years have most likely lead to increased encounters since Despite these influences, it is also important to note that the Cape Eleuthera Institute (CEI; a facility located on Eleuthera that conducts scientific research on marine fauna and flora; has been operational for the past 9 years and have only encountered one P. pectinata, despite many of their research studies being conducted in suitable habitat (Danylchuk et al., 2007). Further, since 1993, Reef Environmental Education Foundation (REEF; have conducted scuba surveys to date across the Bahamas with only one confirmed P. pectinata sighting. Thus, the findings presented here are a reasonable representation of the current distribution of P. pectinata across the Bahamas. The rarity of encounters east and north of Andros is concerning, particularly considering the availability of suitable habitat in the islands such as Abaco, Eleuthera and Long Island. Preliminary interviews with artisanal fishers and bonefish Albula vulpes (L. 1758) guides in Bimini (T. L. Guttridge, pers. comm.) have revealed that P. pectinata were previously targeted for their meat, the curio trade and for aquarium exhibits as recently as Considering that P. pectinata have an affinity for shallow water coastal environments (Wiley & Simpfendorfer, 2010; Waters et al., 2014; Hollensead et al., 2015; this study), it is extremely likely that there will be continued overlap with other resource users. BIMINI ISLANDS Despite being substantially smaller and having far less suitable habitat for P. pectinata than many of the Bahamian Islands, the Bimini Islands were visited annually (some up to 6 weeks) by at least two to three juvenile to adult P. pectinata. During the 14 year period, no P. pectinata <225 cm L ST were observed, suggesting that Bimini and its surrounding habitats probably do not serve as a nursery to this species. This was further supported by an absence of P. pectinata (<225 cm L ST ) captured in standardized shallow water gillnets, set annually (May to June) since 1995 in North Bimini, targeting juvenile N. brevirostris (Feldheim et al., 2014). Through opportunistic acoustic tracking and repeated sightings, evidence of short-term residency was found, with three P. pectinata spending at least 6 weeks around Bimini. One female (410 cm L ST ) was detected on 17 days during a 40 day period, using the shallow (<2 m) waters east of the main lagoon between the north and south islands. Similarly, through acoustic and satellite telemetry, Papastamatiou et al. (2015) found that P. pectinata showed periods of residency over 1 3 months at East Cape canal, Florida Bay. Furthermore, two individuals in Bimini were observed to use the North Sound (a semi-enclosed lagoon in North Bimini); one detected over a 4 day period (2007) and the other observed to re-use the area over 3 weeks (2004).
16 PRISTIS PECTINATA IN THE BAHAMAS 1337 Since 2010, however, this lagoon has had c. 40% (or 69 ha) of its mangrove coverage removed due to development and construction (Jennings et al., 2012). Private homes, a large-scale hotel, casino, cruise-ship terminal and an artificial island have been constructed. The remaining mangroves surrounding the northern and eastern sides of the lagoon are threatened with removal by additional development plans. Habitat destruction is one of the key factors affecting the distribution of P. pectinata in the U.S.A. (Norton et al., 2012; Waters et al., 2014) and worryingly no P. pectinata, as far as is known, have been observed to use the North Sound lagoon since In addition, despite Bimini being identified in 2002 as a site of high priority to establish a marine protected area (MPA) (Dahlgren, 2002), this (as of September 2015) has not been officially gazetted by the Government of the Bahamas, nor have boundaries, regulation and accompanying enforcement been instated (E. Carey, pers. comm.). Further, in a statement made by the Minister of Environment and Housing, on 31 August 2015, the Bimini MPA was not included in the protected areas expansion. In Bimini, P. pectinata appeared to be more abundant seasonally, with 45% of encounters documented in May. In the U.S.A., seasonal spring and summer peaks in abundance were also reported in Florida Bay and Ten Thousands Islands (Poulakis et al., 2011; Waters et al., 2014; Papastamatiou et al., 2015). Interestingly, Waters et al. (2014) suggested that adult P. pectinata perform seasonal northward migrations in Florida waters. If a similar pattern was occurring in the Bahamas, P. pectinata encountered in Bimini might be migrating north from Andros Island or possibly from Florida. Future studies incorporating tracking (i.e. satellite and acoustic) and genetic studies are required to determine the degree and rates of interchange between Andros, Bimini and other islands within the Bahamas and U.S.A. Pristis pectinata manually tracked in Bimini moved much greater daily distances (i.e. 14 and 29 km) than those of a similar life stage (mean = 1 4, range = km day 1 ) recently documented by Carlson et al. (2014). Although this could be due to the greater spatial resolution obtained from active tracking, comparable ROM values to P. pectinata in this study (ROM: median 1 4 and 2 7, maximum 7 1kmh 1 ) were generated from a female P. pectinata (mean ± s.d. = 1 1 ± 1 2, maximum 7 5kmh 1 ) manually tracked for 40 h in Florida Bay (Papastamatiou et al., 2015). Interestingly, high linearity scores suggest long periods of directed swimming which might be a consequence of being tracked in unfamiliar or distant habitats from their typical home range. ANDROS ISLAND Andros is the largest island in the Bahamian archipelago and the fifth largest island in the greater Caribbean basin. The west side of Andros is one of the most remote and pristine tropical areas in the western central Atlantic Ocean and receives very little human effect. The overall human density on Andros is only 1 3 people km 2, <1% of the density on neighbouring New Providence Island, and nearly all Andros residents live on the east side of the island, adjacent to Tongue of the Ocean and third largest barrier reef in the world. The Bahamas recently expanded the National Parks on Andros to create the ha (1 3 million acre) West Side National Park that should protect this area from anthropogenic disturbances that affect other regions of the Bahamas. The West Side National Park is roughly the same size as Everglades National Park in Florida, which is also an area critical to P. pectinata recovery (Waters et al., 2014).
17 1338 T. L. GUTTRIDGE ET AL. Andros is more pristine and has comparable potential nursery habitat to the Everglades. The occurrence of YOY P. pectinata in Andros suggests that this may be an important primary nursery area. Further, there are anecdotal data suggesting very large adult P. pectinata aggregate in shallow back-country waters in Andros where mating may take place (Nature Conservancy Rapid Ecological Assessment, pers. comm.). In addition, clustered sightings of adults in deeper waters of the insular shelf edge on the east side suggest that P. pectinata habitat use patterns in Andros may mirror those in Florida (Waters et al., 2014). Thus, Andros may support a distinct P. pectinata population that is not habitat-limited and it may prove critical to recovery of the species globally. Critical to this recovery is a determination of the connectivity between P. pectinata populations and potential spillover of P. pectinata from the Bahamas to neighbouring regions. CONSERVATION AND MANAGEMENT IMPLICATIONS Harrison & Dulvy (2014) highlighted the importance of Florida, U.S.A., as a viable population of P. pectinata; a lifeboat owing to the strict protections provided. They emphasized the importance of identifying additional lifeboat populations to protect sub-populations, as despite encouraging progress being made in the U.S.A. for the species, this alone is not sufficient for their conservation on a global scale (Dulvy et al., 2014b). The findings presented in this study confirm and highlight the importance of the Bahamas, in particular Andros Island, as another possible lifeboat population for P. pectinata. With national parks already in place and a developing research programme with local guide collaborators, there should be confidence that Andros can be a core region for P. pectinata recovery, complementing the progress made in the U.S.A. Supplementing the protection in Andros, it will be important to initiate local and regional P. pectinata encounter, awareness and outreach programmes in the Bahamas to: (1) inform and educate artisanal fishers, guides and tourists of its endangered status, (2) provide a user-friendly platform to report encounters and (3) alert the Bahamas Government to their extinction risk and urgent need for more comprehensive national conservation or species-specific management. Finally, given that juvenile P. pectinata have been shown to be obligately associated with mangrove-fringed shorelines, increased development throughout the Bahamas that includes mangrove removals may threaten potential P. pectinata nursery areas that are yet to be discovered. In conclusion, through a combination of encounter data and preliminary tracks, this study was able to provide an important current snapshot of the status of P. pectinata in the Bahamas. Positive signs of a viable population in Andros were documented, suggesting that research and conservation efforts use this core location as a platform and lifeboat to launch Bahamas-wide local and regional P. pectinata conservation and protection initiatives. With the Bahamas Government committing to protecting 20% of its near-shore marine environment by 2020 at the United Nations Convention on Biodiversity (UNCBD), there is hope that this, in combination with research, outreach and educational programmes, will help to restore robust P. pectinata populations for the benefit of coastal ecosystem function and biodiversity. This work was supported in part by the Bimini Biological Field Station Foundation (BBFSF) and the Save Our Seas Foundation Keystone Grant awarded to T.L.G. and S.H.G. We wish to acknowledge the Commonwealth of the Bahamas Department of Fisheries for issuing permits that allow us to work in the islands of Bimini and Andros. A permit (no: MAF/LIA/22) to
18 PRISTIS PECTINATA IN THE BAHAMAS 1339 conduct scientific marine animal research was supplied by the Department of Marine Resources, Bahamas. Further, we acknowledge staff and volunteers at BBFSF for reporting sightings and facilitating capture and tracking of sawfish. Funding for Andros work was supported by grants from the National Geographic Expeditions Council, A. Luskey and the M.Y. Sirenuse,the Moore Charitable Foundation and the Rackley Family Foundation. We are especially indebted to C. Bethel and C. Rimstad and the guides of the Flamingo Cay Rod and Gun Club for facilitating the Andros based research. We also thank D. Chapman, I. Hamilton, D. Bethea, J. Imhoff, M. Kolmann, S. Fordham and K. Smith for research assistance in Andros. For sighting information, we thank N. Watson Jr., B. Purdy, D. Claridge, E. Brooks, S. Cove, C. Hamby, B. Stratham, B. Hardy, J. Marion, P. Meyer, G. Willis and A. Saunders. BBFSF also wishes to thank the Guy Harvey Ocean Foundation, Sundance, Mercury Engines and Davey Marine. References Bigelow, H. B. & Schroeder, W. C. (1953). Fishes of the western North Atlantic, Part 2. Sawfishes, guitarfishes, skates, rays, and chimaeroids. In Fishes of the Western North Atlantic (Tee-Van, J., Breder, C. M., Hildebrand, S. F., Parr, A. E. & Schroeder, W. C., eds), pp New Haven, CT: Sears Foundation for Marine Research, Yale University. Carlson, J. K. & Simpfendorfer, C. A. (2015). Recovery potential of smalltooth sawfish, Pristis pectinata, in the United States determined using population viability models. Aquatic Conservation: Marine and Freshwater Ecosystems 25, Carlson, J. K., Osborne, J. & Schmidt, T. W. (2007). Monitoring the recovery of smalltooth sawfish, Pristis pectinata, using standardized relative indices of abundance. Biological Conservation 136, Carlson, J. K., Gulak, S. J. B., Simpfendorfer, C. A., Grubbs, R. D., Romine, J. G. & Burgess, G. H. (2014). Movement patterns and habitat use of smalltooth sawfish, Pristis pectinata, determined using pop-up satellite archival tags. Aquatic Conservation: Marine and Freshwater Ecosystems 24, Chapman, D. D., Simpfendorfer, C. A., Wiley, T. R., Poulakis, G. R., Curtis, C., Tringali, M., Carlson, J. K. & Feldheim, K. A. (2011). Genetic diversity despite population collapse in a Critically Endangered marine fish: the smalltooth sawfish (Pristis pectinata). Journal of Heredity 102, Dahlgren, C. P. (2002). Marine reserves in the Bahamas. Bahamas Journal of Science 9, Danylchuk, S. E., Danylchuk, A. J., Cooke, S. J., Goldberg, T. L., Koppelman, J. & Philipp, D. P. (2007). Effects of recreational angling on the post-release behavior and predation of bonefish (Albula vulpes): the role of equilibrium status at the time of release. Journal of Experimental Marine Biology and Ecology 346, Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R., Carlson, J. K., Davidson, L. N. K., Fordham, S., Francis, M. P., Pollock, C. M., Simpfendorfer, C. A., Burgess, G. H., Carpenter, K. E., Compagno, L. V. J., Ebert, D. A., Gibson, C., Heupel, M. R., Livingstone, S. R., Sanciangco, J. C., Stevens, J. D., Valenti, S. & White, W. T. (2014a). Extinction risk and conservation of the world s sharks and rays. elife 3, e Dulvy, N. K., Davidson, L. K., Kyne, P. M., Simpfendorfer, C. A., Harrison, L. R., Carlson, J. K. & Fordham, S. V. (2014b). Ghosts of the coast: global extinction risk and conservation of sawfishes (online). Aquatic Conservation: Marine and Freshwater Ecosystems. doi: /aqc.2525/full Faria, V. V., McDavitt, M. T., Charvet, P., Wiley, T. R., Simpfendorfer, C. A. & Naylor, G. J. P. (2013). Species delineation and global population structure of critically endangered sawfishes (Pristidae). Zoological Journal of the Linnean Society 167, Feldheim, K. A., Gruber, S. H., DiBattista, J. D., Babcock, E. A., Kessel, S. T., Hendry, A. P., Pikitch, E. K., Ashley, M. V. & Chapman, D. D. (2014). Two decades of genetic profiling yields first evidence of natal philopatry and long-term fidelity to parturition sites in sharks. Molecular Ecology 23, Fernandez-Carvalho, J., Imhoff, J. L., Faria, V. V., Carlson, J. K. & Burgess, G. H. (2013). Status and the potential extirpation of the largetooth sawfish, Pristis pristis, in the Atlantic Ocean. Aquatic Conservation: Marine and Freshwater Ecosystems 24,
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