Movement Patterns and Habitat Use of Smalltooth Sawfish, Pristis Pectinata, Determined Using Pop-Up Satellite Archival Tags J

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2014 Movement Patterns and Habitat Use of Smalltooth Sawfish, Pristis Pectinata, Determined Using Pop-up Satellite Archival Tags J. Carlson, S. Gulak, Colin Ashley Simpfendorfer, Dean Grubbs, J. Romine, and G. Burgess

Follow this and additional works at the FSU Digital Library. For more information, please contact [email protected] AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS Aquatic Conserv: Mar. Freshw. Ecosyst. (2013) Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/aqc.2382

Movement patterns and habitat use of smalltooth sawﬁsh, Pristis pectinata, determined using pop-up satellite archival tags

J. K. CARLSONa,*, S. J. B. GULAKa, C. A. SIMPFENDORFERb, R. D. GRUBBSc, J. G. ROMINEd,e and G.H. BURGESSd aNational Marine Fisheries Service, Southeast Fisheries Science Center, Panama City Laboratory, Panama City, FL, USA bCentre for Sustainable Tropical Fisheries & Aquaculture and School of Earth and Environmental Sciences, James Cook University, Townsville, Queensland, Australia cFlorida State University Coastal and Marine Laboratory, St. Teresa, FL, USA dFlorida Program for Shark Research, Florida Museum of Natural History, University of Florida, Gainesville, FL, USA eUnited States Geological Survey Western Fisheries Research Center, Columbia River Research Laboratory, Cook, WA, USA

ABSTRACT 1. Research on rare and threatened species is often limited by access to sufficient individuals to acquire information needed to design appropriate conservation measures. 2. Using a combination of data from pop-up archival transmitting (PAT) tags across multiple institutional programmes, movements and habitat use of endangered smalltooth sawfish, Pristis pectinata were determined for animals from southern Florida and the Bahamas. 3. All P. pectinata (n = 12) generally remained in coastal waters within the region where they were initially tagged, travelling an average of 80.2 km from deployment to pop-up location. The shortest distance moved was 4.6 km and the greatest 279.1 km, averaging 1.4 km day-1. Seasonal movement rates for females were significantly different with the greatest movements in autumn and winter. 4. Pristis pectinata spent the majority of their time at shallow depths (96% of their time at depths <10 m) and warm water temperatures (22–28°C). 5. Given sawfish show a degree of site fidelity punctuated by limited migratory movements emphasizes the need for conservation and management of existing coastal habitats throughout the species’ range. Published 2013. This article is a U.S. Government work and is in the public domain in the USA.

Received 27 November 2012; Revised 1 May 2013; Accepted 25 May 2013

KEY WORDS: elasmobranch; conservation; endangered species; recovery

INTRODUCTION conservation measures (Thompson, 2004). This is Research on rare and threatened species is often especially true of species that live in marine habitats limited by the access to sufﬁcient individuals to where they can be difﬁcult to locate and capture. acquire the information needed to design appropriate These challenges can result in delays to conservation

*Correspondence to: J. Carlson, National Marine Fisheries Service, Southeast Fisheries Science Center, Panama City Laboratory, Panama City, FL, USA. E-mail: [email protected]

Published 2013. This article is a U.S. Government work and is in the public domain in the USA. J. K. CARLSON ET AL. action, increasing the probability of further declines in on a synthesis of tagging data across institutional abundance. One approach to overcoming these programmes. The aims of the study were: (1) to challenges is for different groups of researchers to collate pop-up archival tagging data from four aggregate results from projects that separately may different institutions, (2) to use the data to describe be of limited use. Such an approach, however, horizontal movements and habitat use of large presents challenges, including synthesizing data that P. pectinata in southern Florida and The Bahamas, may have been collected in different ways, for and (3) to report on the conservation implications of different purposes and in different places. Successful the results both in US waters, and more broadly aggregation of data in these situations may provide throughout the historic range of the species. improved conservation outcomes. The smalltooth sawfish, Pristis pectinata,isararely encountered species (Wiley and Simpfendorfer, 2010) METHODS that is currently listed as Critically Endangered by the IUCN Red List of Threatened Species (Adams et al., Depending on the institutional study, P. pectinata 2006). In addition, the United States (US) population were captured with bottom longline gear, rod and was listed as Endangered on the US Endangered reel, or by dip net and placing a tail rope around the Species Act (ESA) in 2003 (68 FR 15674) and a caudal peduncle. PAT tags were rigged with 300-lb recovery plan developed (National Marine Fisheries monofilament leaders and a Pfleger Institute of Service (NMFS), 2009). Historically, smalltooth Environmental Research (PIER) nylon “umbrella” sawfish were distributed throughout coastal and dart or a modified harness consisting of 1.8 mm estuarine areas of the tropical and subtropical stainless steel cable surrounded by chafe tubing, then western and eastern Atlantic Ocean, regularly clear surgical tubing with polyolefin heat-shrinkable making summer forays into temperate waters (Wiley tubing at each end. After capture the sawfish were and Simpfendorfer, 2010; International Sawfish restrained alongside the research vessel. Various Encounter Database (ISED)/G.H. Burgess, measurements (precaudal length (PCL), fork length unpublished data). In the US, smalltooth sawfish (FL), total length (TL) or stretch total length (STL), are now only regularly found in southern Florida in cm) were taken, depending on research institution (Simpfendorfer, 2005) where the population is either and sex was recorded. For standardization, all stable or slowly increasing (Carlson et al., 2007; lengths are reported in stretched total length Carlson and Osborne, 2012). The collection of (the length of the sawfish from the tip of the rostrum conservation-relevant data has focused mostly on to the end of the caudal fin bent down). When not smaller juveniles (Simpfendorfer et al., 2010, 2011; available, lengths were converted to stretch total Poulakis et al., 2011) because of their accessibility length using the following equations: STL = 1.1876 and higher relative abundance in estuarine areas. (PCL)–2.0984, r2 =0.99; STL=1.061(FL)–0.4926, Information on adults, however, has been limited r2 =0.99; and STL=1.018(TL)–1.1681, r2 =0.99 because of their rarity and difficulty of capture. As a (D.M. Bethea and J.K. Carlson, unpublished). result, conservation actions for adults have lagged Most sawfish were tagged by making a small behind those for juveniles (e.g. critical habitat has incision lateral to the middle of the first dorsal fin been identified and protected only for juveniles in approximately 5 cm below the fin base and the southern Florida; Norton et al., 2012). Owing to the dart was inserted into the dorsal musculature, paucity of captures, initial research on larger seating the anchor at a depth of 6–10 cm. For juvenile and adult P. pectinata has concentrated on sawfish tagged with the modified harness, a small the use of pop-off archival transmitting (PAT) tags to hole was made through the anterior portion of the investigate movements and habitat use. However, this first dorsal fin. The free end of the harness hasoccurredinafragmentedfashionwithmultiple assembly was threaded through the dorsal fin and institutions undertaking the work, each programme extracted from the opposite side of the dorsal fin. tagging limited numbers of individuals. To provide The harness was pulled through the dorsal fin, and conservation-relevant information this paper reports the free end of steel cable was inserted into the

Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Aquatic Conserv: Mar. Freshw. Ecosyst. (2013) SAWFISH MOVEMENTS open sides of two double copperlock crimps. The Raw estimates of longitude and latitude cable was pulled through the crimps to decrease geolocation were processed through the Kftrack the loop in the harness until the crimps rest just program (Sibert et al., 2003) in the ‘R’ statistical under the free rear tip of the dorsal fin. The crimps environment (http://cran.r-project.org). Points that were then closed (crimped) to secure the harness in were on land or theoretically out of the individual's place and the excess steel cable was removed with track (i.e. if the distance between the origin and the wire cutters. The PAT tag trailed just behind the next position was farther than an animal could dorsal fin when the sawfish was released. reasonably travel in a 24 h period) were eliminated. Pristis pectinata were tagged with multiple If the maximum daily depth attained by each generations of pop-up archival transmitting tags P. pectinata was greater than the known depth at the (PAT2, PAT3, PAT4 and Mk10) manufactured by estimated location shown on oceanographic charts, Wildlife Computers. Pop-up archival transmitters then the geolocation was considered anomalous and (i.e. PAT tags) archive depth, light and temperature discarded from the dataset. The data were then dataandareprogrammedtoreleaseatadate smoothed using a state-space Kalman filter and the specified by the user, at which time they float to the resulting geolocation points from the model surface and relay data to orbiting Argos satellites. represented the most probable track. The final suite Light level data can be used to estimate position by of geolocation points from the model was plotted determining day length and the timing of sunrise using Arcview version 9.3.1 for each individual. and sunset. Initially, because no previous work had After running the Kftrack algorithm, the daily been conducted on P. pectinata and multiple geographical position of the tagged fish was used to institutions were involved in tagging, PAT tags were estimate the times of sunrise, sunset, and local noon programmed in a variety of ways (Table 1). Tags using standard astronomical formulae (Duffett- were programmed to pop-up after 45–180 days and Smith, 1988). Depth and temperature data were data collection frequency was set from 10–60 s. assigned to a time-of-day period (i.e. day, night and Depending on research institution, tags were transition) according to times of local dusk and programmed to record temperature and depth dawn derived from longitude and latitude estimates binned into 4, 6 or 12 h histograms. Bins ranges from the most probable tracks (Musyl et al., 2011). varied from 0 m to >300 m and from 2° to 32°C. Although most satellite telemetry studies have used only day and night periods, the transition period was necessary to define since one histogram a day Estimates of geolocation will contain sunrise and another sunset. Depending on the PAT tag model used, a version of To examine differences in depth selection (by proprietary software from the tag manufacturer institutional programme) among occupied depths, (WC-GPE Suite, Wildlife Computers, USA) was analysis of variance (ANOVA) was performed used to correct for light attenuation and to estimate using the binned proportion of time spent at a longitudes from the transmitted light level data. depth as the dependent variable and time of day Longitude was estimated from the time of local (i.e. day, night, transition) and depth as independent noon or midnight using standard astronomical variables among tagged P. pectinata by programme. algorithms (Hill, 1994; Ekstrom, 2004). To refine The dependent data were transformed taking the the data for accuracy, only consecutive longitude arcsine of the square root (Zar, 1984) to normalize estimates <3° apart per day were used for further the data. Violations of assumptions of normality geolocation estimates (Sims et al., 2003). Latitude were tested post hoc using normal probability and was calibrated by correlating the actual light-level quantile–quantile plots of residuals. All statistical curves collected by the tag for a known day at a analysis was performed in SAS Statistical Software known location with theoretical curves generated by (SAS, version 9 · 1, SAS Inst., Inc., Cary, NC, USA). the geolocation algorithms. Latitude estimates were Seasonal movement rates were examined by evaluated using ‘root-mean-squared difference’ as calculating daily rate of movement in winter described in the WC-GPE Suite. (December, January, and February), spring (March,

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Table 1. Summary of various programmes utilized for pop-up archival transmitters

Programme Mote1 Mote2 Mote3 Mote4 Mote5 FSU UF PC

Histogram 10 10 10 10 10 1 60 1 sampling interval (s) Histogram (h) 1 12 n/a 3 6 4 6 4 Depth bin (m) 1 Surface 0.0 0.0 0.0 Surface 0.0 0.0 0.0 2 0.0-2.0 2.0-4.0 2.0-4.0 5.0-10.0 0.0-2.0 0.5-2.0 0.5-2.0 0.5-2.0 3 2.5-4.0 4.5-6.0 4.5-6.0 10.5-15 2.5-4.0 2.5-4.0 2.5-4.0 2.5-4.0 4 4.5-6.0 6.5-8.0 6.5-8.0 15.5-20.0 4.5-6.0 4.5-6.0 4.5-6.0 4.5-6.0 5 6.5-8.0 8.5-10.0 8.5-10.0 20.5-30.0 6.5-8.0 6.5-8.0 6.5-8.0 6.5-8.0

6 8.5-10.0 10.5-15.0 10.5-15.0 30.5-40.0 8.5-10.0 8.5-10.0 8.5-10.0 8.5-10.0 CARLSON K. J. 7 10.0-15.0 15.5-20.0 15.5-20.0 40.5-60.0 10.5-15.0 10.5-20.0 10.5-15.0 10.5-15.0 8 15.5-20.0 20.5-25.0 20.5-25.0 60.5-80.0 15.5-20.0 20.5-30.0 15.5-20.0 15.5-20.0 9 20.5-25.0 25.5-30.0 25.5-30.0 80.5-100.0 20.5-25.0 30.5-40.0 20.5-25.0 20.5-25.0 10 25.5-30.0 30.5-50.0 30.5-50.0 100.5-150.0 25.5-50.0 40.5-50.0 25.5-30.0 25.5-30.0 11 30.5-50.0 50.5-75.0 50.5-75.0 150.5-200.0 50.5-75.0 50.5-100.0 30.5-50.0 30.5-40.0

12 50.5-1000 75.0-1000 75.0-1000 200.5-1000 75.5-100.0 100.5-200.0 50.5-100.0 40.5-50.0 AL ET 13 >1000 >1000 >1000 >1000 100.5-150.0 200.5-300.0 100.5-150.0 50.5-100.0 14 >150.0 >300.0 >150.0 >100 . Temperature bin 1 10.0-15.0 10.0-12.0 10.0-12.0 10.0-15.0 2.0-10.0 12.1-14.0 6.0-8.0 12.1-14.0 2 15.1-17.0 12.1-14.0 12.1-14.0 15.1-17.0 10.1-12.0 14.1-16.0 8.1-10.0 14.1-16.0 3 17.1-19.0 14.1-16.0 14.1-16.0 17.1-19.0 12.1-14.0 16.1-18.0 10.1-12.0 16.1-18.0 4 19.1-21.0 16.1-18.0 16.1-18.0 19.1-21.0 14.1-16.0 18.1-20.0 12.1-14.0 18.1-20.0 5 21.1-23.0 18.1-20.0 18.1-20.0 21.1-23.0 16.1-18.0 20.1-22.0 14.1-16.0 20.1-22.0 qai osr:Mr rsw Ecosyst. Freshw. Mar. Conserv: Aquatic 6 23.1-25.0 20.1-22.0 20.1-22.0 23.1-25.0 18.1-20.0 22.1-24.0 16.1-18.0 22.1-24.0 7 25.1-27.0 22.1-24.0 22.1-24.0 25.1-27.0 20.1-22.0 24.1-26.0 18.1-20.0 24.1-26.0 8 27.1-29.0 24.1-26.0 24.1-26.0 27.1-29.0 22.1-24.0 26.1-28.0 20.1-22.0 26.1-28.0 9 29.1-31.0 26.1-28.0 26.1-28.0 29.1-31.0 24.1-26.0 28.1-30.0 22.1-24.0 28.1-30.0 10 31.0-33.0 28.1-30.0 28.1-30.0 31.1-33.0 26.1-28.0 30.1-32.0 24.1-26.0 30.1-32.0 11 33.1-60.0 30.1-60.0 30.1-60.0 33.1-60.0 28.1-30.0 32.1-34.0 26.1-28.0 32.1-34.0 12 >60 >60 >60 >60 30.1-32.0 34.1-36.0 >28.0 34.1-36.0 13 >32.0 >36.0 >36.0 (2013) SAWFISH MOVEMENTS

April, and May), summer (June, July and August), occupying temperature bins 28–30°C (Figure 3). and autumn (September, October, and November). Pristis pectinata tagged off Andros Island generally Mean seasonal movement rate was then estimated occupied water temperatures above 28°C (69% of and compared between seasons using ANOVA. If the time). No significant difference was found in mean seasonal movement rate was significantly the occupied temperature bins between day, night different, a Tukey honestly significant difference and the transitional time period (P > 0.05) for (HSD) test was used corrected for multiple tests P. pectinata tagged off south Florida (Table 3). (False Discovery Rate) to compare seasons However, individuals in Andros Island occupied (Benjamini and Hochberg, 1995). higher temperatures during the day than the other time periods (P = 0.03). All P. pectinata remained in coastal waters within the region where they were initially tagged. Based on RESULTS geolocation data from initial tagging location to In total, 28 P. pectinata were fitted with PAT tags pop-up location, the mean straight-line distance from 2001–2010 (Table 2). Most sawfish were (assuming the earth is a perfect sphere with a radius tagged in the south-west Florida area but two of 6378.0 km) P. pectinata moved was 80.2 km. The animals were tagged at Andros Island, Bahamas shortest distance moved was 4.6 km and the (Figure 1). For all sawfish tagged, size ranged from greatest was 279.1 km. Pristis pectinata travelled an 157 cm to 450 cm STL (average 332 cm STL) and average of 1.4 km day-1 but one individual moved the majority were female (17 females: 11 males). Of up to 9.2 km day-1 over 13 days while another the 28 tags, 12 tags on sawfish covering 1140 days moved only 0.1 km day-1 over 105 days. provided data that could be used for analysis. Seasonal movements of females were significantly Data excluded from further analysis included those different between seasons (P < 0.0001, Figure 4). tags that prematurely detached (1–2 days, n = 2), Average movement rate for females was greatest in transmitted data that could not be processed autumn (mean = 6.61, sd = 5.4 km day-1) and winter (n = 3), or tags that failed to transmit any data (mean = 5.09, sd = 5.6 km day-1). Female sawfishes (n = 11). Overall, P. pectinata retained tags for up moved at slower rates in the spring (mean = 2.35, to 180 days but the mean length of retention was sd = 3.85 km day-1) and summer (mean = 0.87, 95 days (n = 12). The average sizes of sawfish tagged sd = 0.83 km day-1). Post hoc tests showed for which data were processed was 347 cm STL significant differences between mean movement (range 227–450 cm STL) and most were female. rates in winter and summer (difference = 4.2 km Regardless of tag programme used, binned depth day-1, P = 0.0017); autumn and summer and temperature profile data indicated that (difference = 5.7 km day-1, P = 0.0003); autumn and P. pectinata spent the majority of their time at spring (difference = 4.3 km day-1, P = 0.0035) and shallow depths and warm water temperatures. winter and spring (difference = 2.7 km day-1, Mean proportions of time at depth for all P = 0.0291). Only females were analysed owing to programmes found P. pectinata spent about 96% of the lack of seasonal coverage for males and the low their time at depths <10 m (Figure 2). Sawfish number of males tagged. rarely ventured below 20 m (~2% of time) and the Most P. pectinata remained in the same general area maximum recorded depth was 88 m (average (Florida Bay or west coast of Andros Island) where maximum depth = 41.7 m) (Table 2). No significant they were tagged, but some individuals meandered difference was found in the occupied depth bins during their tracking periods (Figure 5–7). between day, night and the transitional time period Florida-tagged sawfishes moved around the Florida among any programme used (P > 0.05) (Table 3). Keys, but despite ready access to adjacent deeper Sawfishes tagged in areas off south Florida spent waters, all P. pectinata remained in depths shallower most (65.3%) of their time in waters 22–28°C. than 100 m. Two P. pectinata (Sawfish 1 and Sawfish However, individuals tagged using the University of 11) tagged in the northern part of Florida Bay near Florida (UF) programme spent the majority of time Flamingo, FL, travelled south until the tags popped

Table 2. Stretch total length, sex, tagging and pop-up localities, and days at liberty for Pristis pectinata. Tags that did not provide any useable data, popped off after short duration or did not transmit data are indicated with asterisks. Days = the number of days the PAT was programmed to release at from deployment. All sawfish except number 27 and 28 were tagged using the PIER nylon ‘umbrella’ dart. Sawfish 27 and 28 were tagged using the modified harness (see text for details)

Sawﬁsh number Programme Days Sex STL Tagging date Tagging location Pop-up date Pop-up location Days at liberty Max. depth (m)

1 Mote1 120 F 450 11/17/01 25.124 À81.067 1/10/02 24.450 À82.230 54 68 2* Mote2 120 F 214 2/17/02 24.554 À82.109 6/15/02 n/a 118 16 3* Mote2 120 M 408 3/28/02 24.965 À80.888 9/12/02 n/a 168 4* Mote2 120 F 355 11/11/02 25.376 À81.123 n/a 5* Mote3 45 M 387 3/15/03 24.964 À80.888 5/1/03 47 4 6* Mote4 120 F 157 7/18/03 25.523 À81.208 8/22/03 26.060 À82.050 35 0 À

7* Mote4 120 M 200 9/3/03 25.872 81.581 n/a CARLSON K. J. 8* Mote4 120 F 202 10/13/04 25.873 À81.581 n/a 9* Mote4 120 F 496 3/23/05 25.118 À81.022 n/a 10 Mote5 90 F 419 11/14/06 25.114 À81.033 2/20/07 24.788 À80.586 98 40 11 Mote5 90 F 407 11/15/06 25.110 À81.030 2/13/07 24.768 À81.365 90 72 12* Mote5 90 F 424 2/9/06 24.750 À80.833 n/a À À

13 Mote5 90 F 387 4/28/07 24.738 80.692 8/4/07 25.047 80.458 98 64 AL ET 14* Mote5 90 F 214 5/8/07 25.127 À81.067 n/a 15* Mote5 90 M 341 5/10/07 25.121 À81.064 n/a 16 Mote5 90 M 365 7/23/07 24.500 À82.050 8/5/07 25.038 À81.028 13 56 . 17* Mote5 90 M 213 10/10/07 25.919 À81.606 12/07/07 n/a 58 18 PC 150 F 345 11/5/07 25.114 À81.047 3/18/08 n/a 134 48 19 PC 150 F 355 11/17/07 24.775 À80.683 3/19/08 24.56 À81.697 123 88 20 PC 150 F 229 2/5/08 24.560 À82.114 7/4/08 24.437 À81.704 150 16 21* PC 150 M 304 2/25/09 24.517 À81.470 8/18/09 n/a 174 qai osr:Mr rsw Ecosyst. Freshw. Mar. Conserv: Aquatic 22 UF 140 M 391 5/4/09 25.125 À81.066 5/15/09 n/a 11 8 23 UF 140 F 286 5/5/09 25.125 À81.066 8/18/09 25.142 À81.108 105 8 24* UF 140 M 442 5/5/09 25.125 À81.066 n/a 25* PC 150 F 381 1/28/10 24.722 À80.754 n/a 26* PC 150 M 381 3/12/10 24.469 À82.012 n/a 27 FSU 180 M 227 5/7/10 24.775 À78.307 7/30/10 24.629 À78.254 84 16 28 FSU 180 F 308 5/9/10 24.630 À78.425 11/5/10 24.762 À78.243 180 16 (2013) SAWFISH MOVEMENTS

Figure 1. The locations of PAT tag attachments off southwest Florida and Andros Island, Bahamas. Symbols are as follows: spring deployments = (*), summer deployments = (●), autumn deployments = (★), winter deployments = (♦). offinthelowerpartoftheFloridaKeys(Figure5). separate datasets, has allowed for the statistical Sawfish 13 and Sawfish 16, by contrast, were tagged testing of the data, which provides for improved in the lower Keys and travelled north to the upper confidence in the conclusions (Papastamatiou and portion of the Florida Keys (Figure 5 and Figure 6). Lowe, 2012). The results of the study demonstrate Only one Florida-tagged P. pectinata (Sawfish 18) that larger juvenile and adult P. pectinata tend to emigrated out of the immediate Florida Bay area. remain in the same general location over prolonged Tagged off Flamingo, FL, on 5 November, it moved periods, primarily occupying shallow waters (<20 m) northward into the Gulf of Mexico off the southern near coastal mangroves. Large juvenile and adult part of the Ten Thousand Islands, FL. After that, no sawfishes travelled greater distances than those reliable fixes could be attained until February with exhibited by small juveniles tracked over a smaller geolocation data indicating the animal had moved to area in the Florida Everglades (Simpfendorfer et al., the east coast of Florida near Ft. Lauderdale. The 2010), suggesting an ontogenetic shift in movement tag popped off on 19 March farther to the north patterns. Given that many tracks occurred in wholly near Ft. Pierce, FL. Because the tag failed to acquire marine environments, it is also likely that larger an Argos fix, the final geolocation was determined individuals more commonly occupy higher salinity based on the drift of the tag on the surface. waters than do smaller individuals. Thus while larger juvenile and adult P. pectinata live close to areas where the juveniles occur, their movement patterns DISCUSSION and habitat use are different. To enhance population This study represents the first to document recovery, development of size-specific conservation movements and habitat use of larger juvenile and measures addressing these age classes may be needed. adult P. pectinata. Combining the data collected by Smalltooth sawfish displayed limited overall four institutions, necessarily limited if analysed as movements, with the maximum straight-line

Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Aquatic Conserv: Mar. Freshw. Ecosyst. (2013) J. K. CARLSON ET AL.

Figure 2. Histogram of the mean cumulative proportion of time spent at depth for Pristis pectinata of the by programme. A = Mote5 (n = 4), B = PC (n = 3), C = UF (n = 2) and D = FSU (n = 2) (see Table 1 for details). White bars are time spent at daytime and solid bars are time spent at darkness and grey bars represent the transitional time period. Vertical bars represent the standard error. distance being only 279 km. Historically, summer Data collected in this study demonstrated no records of P. pectinata inareasasfarnorthasNew preference for depth by diurnal period. This differs York (Schopf, 1788) indicate that sawfish made from results of an acoustic tracking study of the seasonal migrations from core areas in the south related Pristis microdon in Australia that found (Bigelow and Schroeder, 1953). Increased sample significant differences in depth use between hours size over a greater temporal scale may confirm these of the day, with age-0 sawfish occupying shallower longer migration patterns. The lack of any depths in the afternoon and larger individuals conventional tag recapture information also occupying deeper depths in the morning (Whitty precludes determining the maximum distance et al., 2009). These authors hypothesized that P. pectinata are capable of moving. However, temporal partitioning was probably related to records of P. pectinata encounters are still largely predator avoidance, feeding behaviour or confined to southern Florida (Wiley and thermoregulation. As P. pectinata tagged in this Simpfendorfer, 2010) with the most northerly study were larger individuals, it is unlikely that confirmed recent encounter (2001) recorded from predator avoidance would play a significant role in the area seaward of the South Carolina–Georgia diurnal movement patterns. Preliminary tracking border (ISED/G.H. Burgess, unpublished data). of one larger P. pectinata in Florida Bay using Given that one of the requirements for the acoustic tags has shown some differences in downlisting of P. pectinata from Endangered to diurnal movements. Over a 3-day period, the Threatened requires verified records of adult animal moved into shallower waters at night on a smalltooth sawfish in areas north of Florida, high tide and deeper into a channel during the continued tagging of animals is crucial for day on a lower tide, hypothesized to be related monitoring recovery. to thermoregulation (Y. Papastamatiou, pers.

Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Aquatic Conserv: Mar. Freshw. Ecosyst. (2013) SAWFISH MOVEMENTS

Table 3. Results of two-way ANOVA comparisons of occupied time spent at depth and temperature by time-of-day (time = day, night, transition) among all tagged sawﬁsh by programme

Programme Factors DF Type III SS F-value P-value

Mote5 Time 2 0.018 0.12 0.888 Depth 10 207.22 280.93 <0.0001 Time*Depth 20 9.28 6.30 <0.0001 Time 2 0.000018 0.000055 0.999 Temperature 6 136.69 134.71 <0.0001 Time*Temperature 12 47.66 23.49 <0.0001 PC Time 2 0.06 0.89 0.409 Depth 12 328.41 432.02 <0.0001 Time*Depth 24 15.93 10.48 <0.0001 Time 2 0.0005 0.0014 0.9985 Temperature 7 221.62 31.66 <0.0001 Time*Temperature 14 7.52 2.88 0.0002 UF Time 2 0.004 0.03 0.971 Depth 7 53.62 98.28 <0.0001 Time*Depth 14 4.49 4.12 <0.0001 Time 2 0.003 0.0053 0.994 Temperature 3 15.12 17.26 <0.0001 Time*Temperature 6 3.73 2.13 0.049 FSU Time 2 0.0004 0.0024 0.997 Depth 4 590.38 1605.78 <0.0001 Time*Depth 8 57.43 78.11 <0.0001 Time 2 0.49 3.48 0.031 Temperature 13 283.28 309.15 <0.0001 Time*Temperature 26 54.72 29.86 <0.0001

Figure 3. Histogram of the mean cumulative proportion of time spent at temperature for Pristis pectinata by programme. A = Mote5 (n = 4), B = PC (n = 3), C = UF (n = 2) and D = FSU (n = 2) (see Table 1 for details). White bars are time spent at daytime and solid bars are time spent at darkness and grey bars represent the transitional time period. Vertical bars represent the standard error.

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on the surface of the water, increasing its exposure to direct sunlight and elevated air temperatures. There were significant differences between seasonal movement patterns of female sawfishes. The cause is as yet unknown, but is probably a function of water temperature, food availability, or reproductive cycle. Sawfish showed much greater daily movements during winter and autumn, which may represent migration periods between summer and winter female activity spaces. A substantial number of PAT tags (50%) failed to transmit data or if data were transmitted, the downloaded portions had gaps and were deemed unusable. PAT tags failing to transmit data have been a common problem with high non-reporting Figure 4. Seasonal movement rates of tagged female sawfish. Whiskers represent the 10th and 90th percentiles, the box encompasses the 25th and failure rates for sharks ranging from, for and 75th percentiles, and the solid line is the median movement rate example, 62% for bigeye thresher sharks (Alopias -1 in km day . superciliousis) (Musyl et al., 2011), 67% for Pacific sleeper sharks (Somniosus pacificus) (Hulbert et al., comm.) or possibly feeding. As data collected by 2006) and 65% for basking shark (Cetorhinus PAT tags in this study were summarized in 4 or maximus) (Sims et al., 2006). There have been 6 h bins of 2–4 m depths, microscale movements various reasons postulated as to why satellite tags may not be detectable. Further research using may stop transmitting. Hays et al. (2007) smaller bins over shorter time periods or with suggested that tag failure might be caused by the acoustic tags may reveal more complex movement saltwater switch failure, antenna breakage or patterns. bio-fouling organisms that accumulate over time. Pristis pectinata generally occupied warm water While all these factors may have contributed to temperatures, rarely entering temperatures below the failure of tags deployed on sawfish, one 20°C. Even sawfishes that were tagged in February potential factor may be the PAT tags inability to when water temperatures were below 20°C tended connect with the satellite. Unlike many of the to avoid cooler waters. This suggests that the pelagic species whose PAT tags are released in lower thermal tolerance for P. pectinata may be unobstructed open ocean environments, sawfish around 20°C. Data from a fishery independent typically prefer near-coastal habitat in close survey for P. pectinata in the Florida Everglades proximity to mangrove stands and as such may indicate juvenile sawfish are not captured below increase the likelihood of PAT tags drifting to an 22°C (Dana Bethea, unpublished) and during an area where the view to the sky was obstructed. extreme cold snap in 2010 when water Some evidence for this comes from one tag being temperatures reached 15°C, several sawfish were recovered underneath the prop roots of red found dead probably due to cold shock (Rehage mangroves in Florida Bay. In addition tags may et al., 2010). Tagged P. pectinata were found in have been entangled in mangrove roots protruding water temperatures above 36°C and ISED down into undercut banks which may have documented observations and captures of adults in stripped the tag from the animal before very shallow waters of the Florida Keys where programmed release. such elevated temperatures are routinely There was considerable variability in the encountered. Alternatively, it is possible that the geolocation data for P. pectinata basedonlight-level higher recorded temperatures may have been the data resulting in large 95% confidence intervals result of the sawfish resting on the bottom in around the most probable tracks. Archival tags use shallow water during the day with the tag floating light-level data to estimate latitude (from day length)

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Figure 5. Most probable horizontal movements derived from light-level geolocation data for sawfish 1, 10, 11, and 13. Symbols are as follows: spring movements = (*), summer movements = (●), autumn movements = (★), winter movements = (♦), deployment locations = (■), and pop-off locations = (▲). Shaded area around each track represent the 95% confidence limits. and longitude (from time of local noon) and many movements. However, SPOTs generally are attached factors such as light attenuation, water turbidity, and to the dorsal fin of sharks (Heithaus et al., 2007) and vertical migration behaviour of the animal have been the morphology of sawfish fins, being very pliable reportedtoinfluence the geolocation estimates and laterally mobile under muscular control, (Arnold and Dewar, 2001; Musyl et al., 2001). For limits the utility of SPOTs on these animals P. pectinata, the most likely cause of the variable (Simpfendorfer, unpublished). An increase in geolocation estimates was the limited movement of developmentofnewtypesof satellite tags that can animals in relatively shallow water. Similarly, incorporate smart positioning as well as archive Carlson et al. (2010) reported poor geolocation depth and temperature will be helpful for further estimates for bull sharks tagged in shallow, turbid data collections on species that inhabit coastal waters in the Gulf of Mexico. As considerable time estuarine areas. was spent at or near the surface by P. pectinata in Under the current smalltooth sawfish recovery this study, the application of smart position and plan, the distinct population segment listed under temperature tags (SPOT) used in combination with the ESA for P. pectinata is assumed to occupy PAT tags could potentially help with refining sawfish only US waters (National Marine Fisheries Service

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Figure 6. Most probable horizontal movements derived from light-level geolocation data for sawﬁsh 16, 18, 19, and 20. Symbols are as follows: spring movements = (*), summer movements = (●), autumn movements = (★), winter movements = (♦), deployment locations = (■), and pop-off locations = (▲). Shaded area around each track represent the 95% conﬁdence limits.

(NMFS), 2009). Sawfish were tagged in both the suggest that P. pectinata moved large distances and Bahamas and lower Florida Keys, but there was no continued tagging of sawfishes may reveal some evidence of exchange of animals between the trans-Gulf Stream exchange. Bahamas and US waters, suggesting any exchange That juvenile and adult P. pectinata show a between the two regions is limited. Whereas the degree of site fidelity punctuated by limited distance between Andros Island in the Bahamas migratory movements emphasizes the need for and the Florida Keys is only about 240 km, conservation and management of existing coastal P. pectinata tended to remain inside the 150 m mangrove habitats in the Florida Bay system and bathymetric contour and did not venture to deep adjacent waters. Mangrove habitats are intervening waters of the Gulf Stream. Faria et al. ecosystems of great importance for sawfish (2013) investigated patterns of geographical (Peverell, 2005; Wiley and Simpfendorfer, 2010; structuring of the world's sawfish species using Morgan et al., 2011). These areas continue to mitochondrial DNA sequences and found only one suffer from anthropogenic destruction (Valiela haplotype common to the western Atlantic Ocean et al., 2001; Duke et al., 2007). Identifying the P. pectinata. However, historical encounter data movement corridors between or along coasts will

Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Aquatic Conserv: Mar. Freshw. Ecosyst. (2013) SAWFISH MOVEMENTS

Figure 7. Most probable horizontal movements derived from light-level geolocation data for sawfish 23, 27 and 28. Symbols are as follows: spring movements = (*), summer movements = (●), autumn movements = (★), winter movements = (♦), deployment locations = (■), and pop-off locations = (▲). Shaded area around each track represent the 95% confidence limits. be of importance when formulating conservation and Wildlife Commission. Special thanks to Shelley strategies for this species in the event of localized Norton (National Marine Fisheries Service-Southeast destruction of mangrove habitats. Given that the Regional Office) for helping to secure funds to predicted reduction of mangroves on a global scale in support US research activities and the Expeditions the event of climate change is up to 10–15% of the Council of the National Geographic Society for current forest level (Alongi, 2008), data on any funding research conducted in Andros Island. We movements and use of alternative habitats will provide thank Dana Bethea, Beau Yeiser, Tonya Wiley, information necessary for recovery of this species. Brooks Doughtie, Ben Westrope, Johanna Imhoff, This inter-institutional collaborative study used Alexia Morgan, Grant Johnson and Ian Hamilton aggregate data to provide an enhanced understanding for assistance in the field. We would also like to of the movement patterns and habitat use of large thank Captains Jim Wilcox, Scott Vaeth, Pete juvenile and adult P. pectinata in southern Florida and Boehm and Luke Hill for their expertise. the Bahamas. The results underscore the importance of shallow, mangrove-lined coastal habitats to this critically endangered species. It also provides a factual REFERENCES basis for the development and implementation of Adams WF, Fowler SL, Charvet-Almeida P, Faria V, Soto J, regional and international conservation measures Furtado M. 2006. Pristis pectinata. In: IUCN 2011. IUCN addressing these age/size classes throughout the Red List of Threatened Species. Version 2011.2. www. species’ Atlantic distributional range. iucnredlist.org. [17 June 2012]. Alongi DM. 2008. Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuarine, Coastal and Shelf Science 76:1–13. ACKNOWLEDGEMENTS Arnold G, Dewar H. 2001. Electronic tags in marine fisheries research: a 30-year perspective. In Electronic Tagging and All smalltooth sawfish were captured and tagged Tracking in Marine Fisheries Reviews: Methods and Technologies under guidelines provided under ESA permits in Fish Biology and Fisheries, Sibert JR, Nielsen JL (eds). Kluwer Academic Press: Dordrecht, Netherlands; 7–64. #1352 (Mote Marine Laboratory), and #1538 and Benjamini Y, Hochberg Y. 1995. Controlling the false #13330 (NMFS Southeast Fisheries Science discovery rate: a practical and powerful approach to Center). Funding for this project in US waters came multiple testing. Journal of the Royal Statistical Society Series B 57: 289–300. from the National Fish and Wildlife Foundation, Bigelow HB, Schroeder WC. 1953. Fishes of the Western North National Marine Fisheries Service, and Florida Fish Atlantic, Part 2. Sawfishes, Guitarfishes, Skates, Rays, and

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Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Aquatic Conserv: Mar. Freshw. Ecosyst. (2013)