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Migratory patterns and habitat use of the sand tiger shark
(Carcharias taurus) in the western North Atlantic
Shara M. Teter
A
,Bradley M. Wetherbee
A
,
B
,
E
,Dewayne A. Fox
C
,Chi H. Lam
D
,
Dale A. Kiefer
D
and Mahmood Shivji
A
A
Guy Harvey Research Institute and Save Our Seas Shark Research Center, Nova Southeastern
University, Dania Beach, FL 33004, USA.
B
Department of Biological Sciences, University of Rhode Island, 9 East Alumni Road, Kingston,
RI 02881, USA.
C
Agriculture and Natural Resources, Delaware State University, 1200 N DuPont Highway, Dover,
DE 19901, USA.
D
Department of Biological Sciences, University of Southern California, University Park Campus,
Los Angeles, CA 90089, USA.
E
Corresponding author. Email: wetherbee@uri.edu
Abstract. Globally, population declines for the sand tiger shark (Carcharias taurus) have resulted in calls for informed
management of populations, including in the western North Atlantic, where they have been listed as a Species of Concern
by NOAA Fisheries. However, information on movements and habitat use, critical for informed management of this sand
tiger population, is limited. We investigated horizontal and vertical movements of sand tigers along the US east coast using
pop-up archival satellite transmitters, supplemented by acoustic telemetry. Thirteen sand tiger sharks were tagged with
satellite and acoustic transmitters in Delaware Bay in late August and early September 2008. Ten of these provided satellite
data for horizontal tracks using a Kalman filter. Males left Delaware Bay in autumn and moved south along the continental
shelf until reaching waters off North Carolina. Females moved east to waters near the edge of the continental slope.
Average depth of males was positively correlated with shark size. All individuals spent at least 95% of their time in waters
of 17–238C. Sand tiger sharks appear most susceptible to fisheries in November and December. Slight expansion of the
boundaries and timing of an existing shark-directed bottom longline area closure would likely reduce by-catch of sand
tiger sharks and enhance recovery of the stock.
Additional keywords: acoustic telemetry, essential habitat, satellite telemetry, vertical and horizontal movements.
Received 13 May 14, accepted 27 June 2014, published online 20 October 2014
Introduction
For animals that are vulnerable to overexploitation, under-
standing movements and habitat use are fundamental for
application of effective management measures and successful
conservation of populations (Rubenstein and Hobson 2004).
A combination of slow growth,late maturation, and exceptionally
low fecundity (two young biennially) has resulted in sand tiger
sharks (Carcharias taurus) being extremely vulnerable to
overexploitation (Cliff 1989;Branstetter and Musick 1994;
Goldman et al. 2006) and has generated considerable concern
about their populations on a global scale (Pollard et al. 1996;
Carlson et al. 2009;Lucifora et al. 2009). Dramatic declines in
sand tiger shark (hereafter ‘sand tiger’) abundance, largely as a
result of commercial fishing, spearfishing, and bang stick fishing
have been documented for populations off the east coast of
Australia and in the western South Atlantic (Pollard et al. 1996;
Otway et al. 2003,2004;Chiaramonte et al. 2007). Conse-
quently, sand tigers have been listed as globally ‘Vulnerable’ on
the IUCN Red List (Pollard and Smith 2009), and as critically
endangered along the east coast of Australia (Pollard et al. 2003)
and the western South Atlantic (Chiaramonte et al. 2007). In US
waters, where this species ranges from the Gulf of Maine to
Florida and into parts of the northern Gulf of Mexico (Castro
2011), similar, dramatic population declines, estimated to be as
high as 75% (Musick et al. 1993) and 99% (Ha 2006) have been
reported. A more recent attempt to quantify the magnitude of
sand tiger declines in US waters based on different databases and
time scales estimated a much more modest decrease in abun-
dance, but also cautioned of the vulnerability of sand tigers to
overexploitation due to low reproductive output (Carlson et al.
2009). Hence, sand tigers were designated a Species of Concern,
and have been federally prohibited from fishery landings since
1997 as managed under the US National Marine Fisheries
Services Consolidated HMS Fishery Management Plan (http://
www.nmfs.noaa.gov/pr/pdfs/species/sandtigershark_detailed.pdf,
accessed 10 August 2013).
CSIRO PUBLISHING
Marine and Freshwater Research, 2015, 66, 158–169
http://dx.doi.org/10.1071/MF14129
Journal compilation ÓCSIRO 2015 www.publish.csiro.au/journals/mfr
Interest about sand tiger movements and habitat use, primarily
for conservation purposes, has prompted several studies
using acoustic and satellite telemetry and conventional tagging
methods (Dicken et al. 2007;Bansemer and Bennett 2011;
Otway and Ellis 2011;Kneebone et al. 2014). Investigations
of movements of sand tigers along the continental coasts of
Australia, South Africa and South America together have
revealed patterns of fairly large-scale, north–south seasonal
migrations. However, information on movements and migrations
of sand tigers along the US east coast is much more fragmentary
and patterns for this population are not well understood (Gilmore
et al. 1983;Kohler et al. 1998). Juvenile sand tigers have been
tracked along the US east coast, primarily with acoustic trans-
mitters, but information on movements of larger sand tigers is
sparse (Kneebone et al. 2014). Identification of nurseries and
core areas of activity for sand tigers in US waters would provide
both state and federal marine resource managers with informa-
tion on spatial and temporal habitat requirements and would
increase understanding of interactions between sand tigers and
human activities. Specifically, such information would aid
assessment of current management measures directed towards
enhanced survival of sand tigers, or protection of their essential
habitat. For example, quantifying habitat use of sand tigers in
relation to existing US longline shark fishery effort as well as
time/area closures, such as the Mid-Atlantic Shark Area (MASA)
is of interest. The MASA is closed to bottom longline fishing
from 1 January until 31 July and is designed to reduce juvenile
mortality for other species of prohibited shark, but could also
serve to reduce susceptibility of sand tigers to capture in shark
fisheries if sand tigers use this area during the closure period.
The objectives of our study were to: (1) examine seasonal
migration of sand tigers along the US east coast and compare
findings with patterns observed for other sand tiger stocks, (2)
characterise habitat use of sand tigers in terms of water temper-
ature and depth during seasonal migrations, and (3) evaluate
potential spatial and temporal interactions with shark fisheries
along the US east coast.
Methods and Materials
Tagging
On 26 August and 8 September 2008, 13 pop-up satellite
archival transmitting (PSAT) tags were deployed on sand tigers
in Delaware Bay. Two models of PSAT tags, PTT-100 and
X-tags (Microwave Telemetry Inc., Columbia, MD), were
deployed on 10 male and three female sharks (Table 1). Sharks
were caught using longlines (366 m, 0.64 cm braided nylon)
with 25 baited circle hooks placed every 12 m (McCandless
et al. 2007), with a soak time of ,2 h. Sharks were kept in the
water alongside the boat while they were tagged, measured,
sexed and fitted with transmitters. Lengths hereafter refer to
total length (TL). PSAT tags were attached using an umbrella
dart connected to the transmitter with 20 cm of 400-kg test
monofilament encased in surgical tubing, with the dart inserted
into the dorsal musculature lateral to the first dorsal fin
(Domeier et al. 2005). PSAT tags were labelled with contact
information in the event of recovery, and programmed to detach
after periods ranging from 123 to 184 days. All sharks carrying
PSAT tags were also tagged internally with acoustic transmitters
(V16–6H, VEMCO Ltd, Halifax, Nova Scotia) for possible
detection on acoustic receivers (VR2 and VR2W, VEMCO Ltd)
within Delaware Bay, as well as on receivers at the mouth of the
bay, along the Delaware and Maryland coastline and at distant
locations on the US east coast. Acoustic transmitters, coated
with biologically inert silicone elastomer (Dow Corning Silas-
tic) to minimise rejection rate, were surgically inserted into the
shark’s body cavity through a 2.5-cm-long incision and the
wound closed with several stitches of a degradable suture
material (PDS Maxon-Polyglyconate 1).
Analyses
PSAT tags archived temperature, depth and light-based geolo-
cation data, which were downloaded from the Argos satellite
system when the tags detached from the sharks and floated to the
surface. Daily latitude and longitude positions were generated by
built-in proprietary software (Microwave Telemetry) from times
of sunrise and sunset processed onboard by each tag. To reduce
geolocation errors associated withusing only light data, a Kalman
filter state-space model (kftrack package) in the R statistical
environment (R Development Core Team; The R Project) was
used to obtain the most probable horizontal track for each shark
from the raw positions (Sibert et al. 2003). For tracks that did not
obtain proper model convergence when all parameters were set
to be optimised, the mean rate of displacement in the xand y
directions (uand vparameters) were fixed at their initial value
Table 1. Sand tiger sharks (C. taurus) that were tagged with pop-up satellite archival transmitting (PSAT) tags in Delaware Bay and that provided
data during migration
Shark
number
Sex Tag
model
Total length
(cm)
Tagging date Pop-off date Programmed
duration (days)
Actual track
duration (days)
Displacement
(km)
1 Female PTT-100 197 26-Aug-2008 23-Jan-2009 154 151 490
2 Female PTT-100 217 26-Aug-2008 9-Sep-2008 185 76 203
3 Female PTT-100 228 26-Aug-2008 28-Dec-2008 185 125 621
4 Male PTT-100 168 26-Aug-2008 26-Dec-2008 123 123 514
5 Male X-tag 186 8-Sep-2008 8-Jan-2009 123 123 490
6 Male PTT-100 202 26-Aug-2008 26-Dec-2008 123 123 688
7 Male X-tag 213 8-Sep-2008 7-Feb-2009 154 153 503
8 Male X-tag 216 8-Sep-2008 8-Feb-2009 154 154 619
9 Male PTT-100 222 26-Aug-2008 28-Oct-2008 154 64 n.a.
10 Male PTT-100 228 26-Aug-2008 26-Dec-2008 123 123 554
11 Male X-tag 232 8-Sep-2008 8-Jan-2009 123 123 412
Sand tiger shark movements Marine and Freshwater Research 159
(refer to kftrack documentation and Sibert et al. 2003). Once a
most probable track was estimated, bathymetry correction was
applied, utilising the maximum daily depth recorded (Galuardi
et al. 2010), with the exception of Shark 2, which had shallow
maximum depth, short track duration and limited displacement.
Because of the possibility that sand tigers might spend extended
periods near the bottom, the constant depth feature of the PSAT
tags was disabled to avoid premature pop-off of transmitters.
This prevented determination of exact pop-off locations for two
tags (Sharks 2 and 3) because of a lag time between tag
detachment and first transmission; however, most probable
tracks were estimated for both sharks by back-calculating to
location at pop-up date. The ‘fix.last’ option in ‘kftrack’ is set to
be false to treat the best-guessed end point as another observa-
tion along the track. This allowed the model to estimate the end
point instead of assuming it to be a known position.
Shark detections on acoustic receivers located inside and
immediately outside Delaware Bay were used to further refine
departure date of sand tigers with PSAT tags from the bay.
Because acoustic receivers have a detection range of ,800 m, as
determined by range tests (D. Fox, unpubl. data), a detection on a
receiver placed a shark within a small area at a known date and
time, and therefore the location and date of the last acoustic
detection for each shark was used as a much more accurate
starting point for constructing the most probable migratory track
from PSAT tag data.
Daily positions from the most probable tracks of all sharks
were used to create 25, 50, 75 and 95% kernel utilisation
distributions (KUDs) in ArcGIS (ver. 9.2; Hawth’s Tools). For
analyses, we used 50% KUDs as ‘core areas’ that indicated areas
of high activity and for comparison with fishing activity. Fishing
effort data in the US pelagic longline fishery (number of hooks
set) were obtained from Guillermo Diaz (NOAA HMS, pers.
comm.). The 50% KUDs were also the basis for examination of
spatial and temporal overlap of sand tiger activity within the
boundaries of the MASA closure. Comparison of 50% KUDs of
sand tigers with fishing effort in the US bottom longline fishery
was limited because of confidentiality requirements in reporting
details of fishing effort (Hale et al. 2010); however, by-catch
data along the US east coast from the NOAA National By-catch
Report (NMFS 2011) were examined to attain preliminary
assessment of the vulnerability of sand tigers in the bottom
longline fishery.
PSAT tags archived temperature (0.16–0.238C) and pres-
sure (5.4 m) at 15-min intervals, and for deployments exceed-
ing 4 months 15-min readings were sequentially overwritten
with 30-min readings. Depth and temperature data were plotted
as temporal profiles and as frequency histograms (10 m; 18C
bins) to examine vertical habitat use of individual sand tigers.
Kolmogorov–Smirnov (K–S) tests were used to determine
whether depth and temperature use differed significantly among
individuals or on a diel basis. Relationships between size of
shark (TL, cm) and depth (m), temperature (8C), displacement
rate (km day
1
), and date of departure were examined using
linear regression.
Detections of additional sand tigers (i.e. sharks lacking PSAT
tags), tagged in Delaware Bay with acoustic transmitters
(n¼167; deployed 2008–11) on receivers located at various
locations along the US east coast were also examined for
comparison of timing of seasonal movements of acoustically
and PSAT-tagged sand tigers.
Results
Tag performance
Twelve of the thirteen PSAT tags that were deployed reported
successfully. One tag detached in Delaware Bay after only
14 days, resulting in 11 tags that provided data for sharks that
underwent seasonal migrations (Table 1), including eight
males (168–232 cm), and three females (197–228 cm). One tag
generated light data suitable for only a few daily locations,
allowing construction of tracks for 10 sharks (seven males and
three females) (see Fig. 1). Eight of the 11 transmitters (73%)
used for analyses remained attached either for the entire pro-
grammed time or, in the case of two tags, to within 3 days of the
programmed release date (Table 1). Three transmitters
released prematurely, after 64, 76 and 125 days, resulting in
overall tag deployments of 64–154 days (mean ¼121.6 days).
Transmitters generated a very large number of daily locations
as well as depth and temperature records. In total, 1338 days
tracked for all individuals combined were obtained, in addition
to a total of 83 138 temperature records and 83 178 depth
records from the 11 PSAT tags used for analyses.
Seasonal migrations
Because of error associated with geolocations based on PSAT
tag light data, dates for departure of sharks from Delaware Bay
based on PSAT tag data could only be estimated. However, all
PSAT-tagged sharks were also implanted with an acoustic
transmitter, providing estimates of departure date from Delaware
Bay for each individual based on last detections on acoustic
receivers located inside Delaware Bay and initial detections on
receivers immediately outside of the bay. Depth data archived
by PSAT tags also indicated departure date from the bay in the
form of obvious and rapid onset of depths exceeding the maxi-
mum depth of the bay. PSAT-tagged sharks were last detected
on acoustic receivers in Delaware Bay between 29 August and
19 October, which coincided well temporally with both initial
detections on acoustic receivers outside the bay, and dramatic
increases in depth archived by PSAT tags. These combined
datasets resulted in estimated times of departure for all three
females and six of eight males as occurring between 6 and 19
October. The last detection on acoustic receivers in the bay
occurred in late August–early September for the remaining two
males, with rapid increases in depth observed for one individual
in early September and for the other at the end of September.
After leaving Delaware Bay, all seven males for which
horizontal tracks were constructed moved south along the
continental shelf and all eventually reached waters off North
Carolina, most arriving in the vicinity of Cape Hatteras in
December (Fig. 1). Five of seven males slowed their directed
movement south at locations on the continental shelf, near the
continental slope, and remained within fairly small areas for
2–4 weeks at ‘rest-stops’ before continuing south. Both the
location of rest-stops and timing of use of the areas varied among
sharks, but most were located off Virginia, near the North
Carolina border. Upon reaching waters off Cape Hatteras all
males remained in neritic waters close to the edge of the
160 Marine and Freshwater Research S. M. Teter et al.
August
September
October
November
December
January
February
0 150
Kilometres
Shark 1 Shark 2 Shark 3
Shark 4 Shark 5 Shark 6
Shark 7
Shark 11
Shark 8 Shark 10
300 N0 150
Kilometres
300 N0150
Kilometres
300 N
0150
Kilometres
300 N0150
Kilometres
300 N0 150
Kilometres
300 N
0150
Kilometres
300 N
0150
Kilometres
300 N
0150
Kilometres
300 N0 150
Kilometres
300 N
Fig. 1. Horizontal tracks of female (Sharks 1–3) and male (Sharks 4–11) sand tigers (see Table 1 for details on individuals). Black circles represent
tagging location, with tracks beginning at the location of the last acoustic detection in Delaware Bay. Triangles indicate tag pop-off locations. Gray
shading indicates the 95% confidence interval around the most probable track.
Sand tiger shark movements Marine and Freshwater Research 161
continental shelf south of the cape until detachment of their
PSAT tags between December and February, with the exception
of one individual, which did not move south of the cape.
In contrast to southern movements observed for males, all
three females moved eastward and offshore to the edge of the
continental shelf rather than south after leaving Delaware Bay
(Fig. 1). Track duration for females ranged from 76 to 151 days,
with the two sharks tracked the longest continuing eastward,
with locations close to the edge of the continental slope. Tracks
of all three females were generally similar both temporally and
spatially.
KUD analysis illustrated departure from Delaware Bay and
progressive movements to the east (for females) and to the south
(for males) between late summer and winter (Fig. 2). In late
August–September sand tigers were located inside Delaware
Bay and continental shelf waters south of the bay. During
October most of the sharks left the bay and began moving south
or east, although two males (Sharks 4 and 6 in Table 1) had
already reached waters off Cape Hatteras by the end of October.
In November locations of females were concentrated several
hundred kilometres east of the bay, and those of males were
primarily off the southern border of Virginia and south of Cape
Hatteras. In December males and females continued to move in
different directions, with males in waters off North Carolina
(,358N) and the two remaining females several hundred kilo-
metres east of New Jersey, near the edge of continental shelf
(,398N). In January, the four remaining males concentrated
their movements near Cape Hatteras, and the single female still
carrying a PSAT tag remained at the edge of the continental
shelf east of New Jersey. By February PSAT tags had detached
from all but two sharks, both males and both of which remained
in waters south of Cape Hatteras.
Displacement (straight-line distance from tagging location to
pop-off location) ranged from 203 to 688 km, with an average of
509.4 (134.4) km, yielding an average displacement rate of
3.98 (0.87) km day
1
for all sharks combined (all values are
standard deviations). Displacement rate during migration only
(between location of last Delaware Bay acoustic detection to
location of PSAT pop-off) ranged from 4.9 to 7.8 km day
1
(mean ¼6.2 km day
1
) for females and 4.2–5.8 km day
1
(mean
¼5.1 km day
1
) for males, with an overall average of 5.4
(1.05) km day
1
for the sexes combined. We found no
evidence to suggest a significant relationship between size and
migratory displacement rate (P.0.05), or between size and
date of departure (P.0.1) for either sex.
Vertical habitat use
Although the focus of this study was not habitat use of sand
tigers in Delaware Bay, satellite transmitters archived a sub-
stantial amount of depth and temperature records for sharks
while in the bay. Depths occupied by PSAT-tagged sharks in
Delaware Bay were similar among individuals, but with slight
differences between sexes. All depths recorded were less than
33 m for females and less than 38 m for males within Delaware
Bay. Differences in depth utilisation between day and night were
not significant for all sharks in the bay or during their southerly
migration (P.0.1), indicating a lack of diel shifts in depth.
Rapid increases in depth were observed at times corre-
sponding to the departure of sharks from Delaware Bay,
particularly for male sand tigers, marked by an onset of depth
records more than the maximum depth of the bay, which is
,45 m (Zheng et al. 1993). Average depths recorded for males
during their southern migration were 18–73 m, with a signifi-
cant positive relationship between average depth and total
length of shark (R
2
¼0.82, P,0.01) (Fig. 3). Although sample
sizes are small, depth use for males during their southern
migrations followed three general patterns corresponding to
size of shark (Fig. 4). For the three smallest males (168–202 cm),
over 90% of depths occupied were ,40 m and with the
exception of one individual on 1 day, no depths greater than
60 m were recorded. The average maximum depth recorded for
the three smallest males was 77.0 25.4 m. Three males in the
middle size class (213–222 cm) occupied deeper water, with
slightly over 50% of records ,40 m and over 95% of depth
records ,60 m. Average maximum depth recorded for these
three males was 95.0 15.6 m. For the two largest males
(228 and 232 cm) only 38% of depths were recorded at
,40 m and ,45% of depths recorded were .80 m. Average
maximum depth for the two largest males was 180.0 8.0 m,
including a maximum depth of 188 m observed for the largest
shark tracked (232 cm). For sharks tracked for at least 120 days,
the two largest males had significantly different depth distribu-
tions than all other individuals, including females (K–S test,
P#0.05).
Average depth of females during migration ranged from 11.1
to 47.1 m, with an average maximum depth of 77.0 16.4 m.
Females occupied deeper waters as they moved east, increas-
ingfromanaverageof12.4mduringthefirst30daysof
migration (n¼3) to just over 50 m for the last 30 days of tracks
(n¼2).
Although depth varied among individuals on the basis of
season, size and sex, water temperature use, as archived by
PSAT tags, was fairly consistent among sharks. Temperatures
occupied by all sharks ranged from 13 to 268C, with more than
95% of temperature records falling between 17 and 238C,
and over 85% of temperatures recorded within the 48range of
18–228C(Fig. 5). Average temperature recorded in Delaware
Bay was 22.28C(1.6) for females, and 19.38C(1.3) for
males, with ,90% of values for both sexes falling between
19 and 238C(Fig. 5). However, differences in temperature
records between sexes, among size classes and between night
and day were not significant (K–S test, P.0.1). Temperature
recorded by PSAT tags at the estimated time of departure of
sharks from Delaware Bay ranged from 18.9 to 20.18C for
females, and 18.3 to 23.68C for males. During migration, the
average temperature recorded for females (20.18C1.7) and
males (20.98C1.6) was similar.
Protection of sand tigers
To examine potential interaction between sand tigers and the
US pelagic longline fishery, we quantified the number of hooks
set by the US pelagic fishery fleet within the geographic con-
fines of the core area of activity of PSAT-tagged sand tigers,
delineated by 50% KUDs for all sharks combined during each
month. We compared the number of hooks set within core areas
and the number of hooks set outside core areas for each month.
Hooks set outside core areas included those within the US EEZ
and the latitudinal boundaries from the northernmost and
162 Marine and Freshwater Research S. M. Teter et al.
southernmost PSAT tag positions (Guillermo Diaz, NOAA
HMS, pers. comm.). This provided an indication of the scale of
fishing within core areas in relation to overall effort of the
pelagic longline fishery within the range of sand tigers tracked
in our study. There were no hooks set within core areas in
September, and only ,12 000 hooks set in core areas in October,
compared to over 340 000 set outside core areas. Nearly
120 000 hooks were set in core areas in November–December,
65W70W75W 65W70W75W
40N
35N
40N
35N
40N
35N
Fig. 2. Monthly Kernel Utilisation Distribution (KUD) for sand tigers tracked with pop-up satellite archival transmitting
(PSAT) tags. Coloured areas represent 25% (brown), 50% (red), 75% (orange) and 95% (yellow) of total distribution. The
Mid-Atlantic Shark Area (MASA, closed status begins 1 January) is shaded green and outlined in white.
Sand tiger shark movements Marine and Freshwater Research 163
compared to ,90 000 hooks set outside core areas during those
months. There were no hooks set within core areas in January
or February.
Though confidentiality requirements did not allow assess-
ment of fishing effort (number of hooks set) in core areas by the
US shark bottom longline fishery, summary data available
from the US National By-catch Report (NMFS 2011)andthe
shark bottom longline observer program (Hale et al. 2010)
documented the occurrence of sand tigers as by-catch in South-
east US shark fisheries. Additionally, the occurrence of 309
sand tigers and 14 924kg estimated as by-catch in 2005 in the
south-east region (which includes core areas of sand tigers
tracked with PSAT tags in this study) off North Carolina
demonstrate the susceptibility of sand tigers to capture in
US fisheries.
Of 477 total geolocations from the 10 horizontal tracks that
were created, only 51 (10.7%) fell within the boundaries of
the MASA; most geolocations occurred outside the MASA to
the north and east of the area boundary (Fig. 6). Though most
core areas for sand tigers fell outside the MASA, its boundaries
encompassed more core area during November and December,
when the MASA is open to fishing, than during closure months
of January and February. Additionally, although PSAT tags had
detached by February, tags on four male sharks provided
49 positions during the period that the MASA is closed to
bottom longlining (1 January to 31 July each year); only six of
these locations fell within the MASA boundary during the time
it is closed (Fig. 6).
Migration patterns inferred from acoustic detections
Although acoustic telemetry provided only fragmentary infor-
mation on movements of sand tigers, it did augment satellite
telemetry in several ways. Acoustic data from receivers inside
Delaware Bay revealed that most PSAT tagged sand tigers
returned to Delaware Bay in subsequent years. Nine of the
eleven sharks (82%) tagged with satellite transmitters in 2008
were detected in Delaware Bay in the summer of 2009 (during
June and July), including all three females and six males.
Eight of these individuals were again detected on receivers in
Delaware Bay in June and July of 2010 (two of the females and
the same six males). Data obtained from researchers with
acoustic receiver arrays at other locations along the US east
coast also provided some insight into seasonal movements of
sand tigers. Several sand tigers that had been tagged in Delaware
Bay with only acoustic tags (n¼167 deployed during 2008–11)
were detected on acoustic receiver arrays located off Cape
Hatteras, NC, as well as near Myrtle Beach and Charleston,
SC (D. Fox, unpubl. data). Immature males (n¼4) were
detected in these distant arrays in late December and mid-Jan-
uary, as well as in mid-May. Mature males (n¼8) were detected
in mid to late December, late March, and early to mid-May.
Immature females (n¼3) were detected in late December, early
April, and early May, and mature females (n¼2) were detected
in mid to late December and in mid-April. Additionally, three
individuals were detected near Cape Canaveral, FL: an imma-
ture female in July, a mature male in January, and an immature
male that was detected in two consecutive winters near Cape
Canaveral, with corresponding summer detections in Delaware
Bay (D. Fox, unpubl. data).
23
Temperature C
17
35 3525 2515 155
Percenta
g
e time
Migration Delaware Bay
5
23
22
21
20
19
18
17
Fig. 5. Temperature use for sand tigers while in Delaware Bay (grey bars)
and during migration (white bars). Migration temperatures include all sharks
(n¼11), and Delaware Bay temperatures include only sharks confirmed by
acoustic telemetry to have remained in the bay .7 days after tagging (n¼8).
R2 0.8186
80
70
60
50
40
30
20
10
0
150 170 190 210 230 250
Depth (m)
Total length (cm)
Fig. 3. Linear regression of average depth during migration versus total
length for male sand tigers with tracks .120 days (R
2
¼0.8186, P,0.01).
Blocks represent individual sharks.
200
150
100
0
8-Sep-2008 8-Oct-2008 7-Nov-2008 7-Dec-2008 6-Jan-2009 5-Feb-2009
Depth (m)
Date
50
Fig. 4. Depth profiles for three male sand tigers: Shark 5 (186 cm) in green,
Shark 7 (213 cm) in brown and Shark 11 (232 cm) in blue. Circles represent
date of last acoustic detection in Delaware Bay.
164 Marine and Freshwater Research S. M. Teter et al.
Discussion
Satellite transmitters used in this study performed well, with
nearly 75% of tags remaining on sharks the entire programmed
duration (Table 1), generating over 1300 daily locations and
over 83 000 temperature and depth records for sand tigers along
the US east coast. Tag performance in our study surpassed that
of several other satellite tagging studies on this species, partic-
ularly for sharks tagged off the US east coast (see Otway and
Ellis 2011,Smale et al. 2012,Kneebone et al. 2014). PSAT tags
detached before the programmed date from all three females
(although for one female the transmitter released only 3 days
short of programmed track duration) compared with only one of
the eight males reported. These are low sample sizes for drawing
robust inferences about sex-specific tag retention; however,
Otway and Ellis (2011) also reported lower PSAT tag retention
for females. It is possible that females engage in behaviours that
result in a higher frequency of premature PSAT tag detachment
in comparison to males.
Seasonal horizontal migration patterns
The results of our study support the general patterns of seasonal
movements proposed for sand tigers along the US east coast by
previous research, although with several modifications. All
males tracked with PSAT tags in our study moved south along
the US east coast, eventually arriving in waters off North
Carolina. Movements of these males are in agreement with
previously postulated north–south seasonal movements of sand
tigers along the US east coast (Bigelow and Schroeder 1948,
Gilmore 1993). PSAT tag tracks suggest that males move south
along paths close to the continental shelf edge, mostly outside
state waters. On the basis of data from additional individuals
tagged with acoustic transmitters, movement south along the US
east coast at the end of summer–early autumn is common among
sand tigers, although acoustic data are patchy and consist of
detections on acoustic receivers at several locations, rather than
a series of continuous positions as were obtained with PSAT tags
(also see Kneebone et al. 2014). Mature and immature sand
tigers of both sexes tagged with acoustic transmitters in Delaware
Bay were detected off North Carolina and Florida in winter
months, suggesting that most demographic segments of the
population take part in north–south seasonal migration along
the US east coast (also see Kneebone et al. 2014). One exception
appears to be pregnant females, which may not move north in the
summer (Gilmore 1993). There have been no observations of
obviously pregnant females in Delaware Bay in summer months
(D. Fox, unpubl. data), in agreement with Gilmore (1993), who
described the summer northward movement of non-gravid
females, mature males and juveniles, whereas pregnant females
presumably remain in waters off North Carolina and Florida
during summer.
Because most demographic segments of the sand tiger
population off the US east coast move south in colder months
(Gilmore 1993;Kneebone et al. 2014; our study), our finding of
eastward, offshore movements by females tagged with PSAT
tags was surprising. Bigelow and Schroeder (1948) suggested
long ago that some sand tigers may migrate offshore instead of
immediately migrating north or south, and Gilmore (1993)
inferred that males might move offshore in summer, but neither
reference was specific to females. Eastward movement of
PSAT-tagged females from Delaware Bay was observed for
only a small number of females within a fairly narrow size range,
VIRGINIA
NORTH
CAROLINA
Fig. 6. Daily positions estimated for sand tigers that occurred within the boundaries of the Mid-Atlantic Shark
Area (MASA) during the closure period (black circles) and daily positions outside the MASA, or inside the
boundaries but not during the closed period (white circles). The boundary of Mid-Atlantic Shark Area (MASA) is
designated by white line.
Sand tiger shark movements Marine and Freshwater Research 165
whereas acoustic telemetry has documented north–south sea-
sonal migration of females of a variety of sizes. Therefore,
eastward movement of females to an overwintering area at the
edge of the continental slope off New Jersey may be limited to
females of a particular demographic. The females tracked in
our study were 197, 217 and 228 cm long, and, based on size at
maturity being 220–230 cm for females (Gilmore et al. 1983),
were most likely nearly mature, or recently mature, but may
have not yet mated or become pregnant during their lifetime.
Females within this category may move to northern and offshore
areas during winter months to avoid mature males and remain
segregated during the mating season as a mechanism to delay
mating and pregnancy until they reach a larger size. Spatial and
temporal segregation of male and female sharks is well docu-
mented (Klimley 1987;Mucientes et al. 2009), but such behav-
iour for sand tigers remains unclear. Another possibility is that
these females move towards warmer waters and eddies of the
Gulf Stream to take advantage of elevated productivity
(Bowman and Iverson 1978;Owen 1981;Le Fe`vre 1987),
although it is unclear why this behaviour would be limited to
maturing females. Additional tracking of females would provide
more information for investigation of such possibilities.
Migratory patterns of sand tigers are complex and differ
among geographic locations around the world, which makes
species-wide generalisations challenging to characterise. The
pattern of migration for sand tigers along the US east coast is
most similar to patterns described for sand tigers along the east
coast of South America. Lucifora et al. (2002) described the
presence of juvenile and mature sharks of both sexes, as well as
an absence of pregnant females in a high-latitude summer
habitat of Anegada Bay, Argentina (408S) in late spring through
autumn, a similar situation to that observed in Delaware Bay
(398N). However, mating off South America is thought to also
occur at cooler, higher-latitude locations, in contrast to mating at
warmer, lower latitudes along the US east coast (Gilmore 1993;
Lucifora et al. 2002). Off South America sand tigers of all
demographics are thought to migrate to warmer, lower latitudes
off Brazil in autumn–winter (Lucifora et al. 2002). The follow-
ing spring–summer sand tigers migrate along the east coast of
South America to cooler, higher latitudes such as Anegada Bay,
with the exception of pregnant females, which remain in low-
latitude, warmer waters off Brazil during spring–autumn, where
they give birth (Lucifora et al. 2002). Differential movement of
pregnant and non-gravid females results in fewer mature
females occupying Anegada Bay in summer. The observed
sex ratio of 2 :1 males to females for mature sharks in Anegada
Bay is consistent with a 2-year reproductive cycle, where ,50%
of the mature females are pregnant and remain at low latitudes in
waters off Brazil during gestation (Lucifora et al. 2002). Move-
ments of mature males in colder months is uncertain because
low numbers have been captured in both Argentinian waters or
off Brazil, possibly indicating movement of mature males
offshore to continental shelf waters during winter.
Migratory patterns of sand tigers in South Africa and eastern
Australia differ in several ways from patterns observed along the
east coasts of North and South America. Both gestation and
parturition occur in warm, low-latitude waters off North and
South America, whereas off South Africa and Australia preg-
nant females undergo predictable and consistent migrations,
which results in three distinct reproductive habitats, one each
specifically for mating, for gestation and for parturition (Bass
et al. 1975;Dicken et al. 2006b,2007;Bansemer and Bennett
2011). In both South Africa and Australia, mating occurs at
cooler, higher-latitude locations, followed by directed move-
ment of newly pregnant females to warmer, lower latitudes. In
winter, after having spent the majority of gestation in warm,
low-latitude waters, near-term pregnant females move to cooler,
higher-latitude waters where they give birth in the late winter–
spring (Smale 2002;Dicken et al. 2006b;Bansemer and Bennett
2011). Thus, poleward movement to cooler waters for parturi-
tion by pregnant females off South Africa and Australia con-
trasts with equatorial movements to warmer water for
parturition off South America or apparent lack of migration by
pregnant females off the US east coast (Gilmore 1993;Lucifora
et al. 2002). Although migration patterns differ geographically,
separate populations do share well synchronised and consistent
movements of adults in conjunction with reproductive status,
consistent with a 2-year reproductive cycle for sand tigers in
South Africa (Dicken et al. 2007), South America (Lucifora
et al. 2002) and for the US east coast (Goldman et al. 2006).
Juvenile sand tigers in South Africa and eastern Australia
exhibit limited movements and do not appear to undergo
synchronised migrations (Dicken et al. 2006b;Bansemer and
Bennett 2011), but rather are thought to remain in geographically
distinct nurseries during the first 4–5 years of life (Smale 2002;
Dicken et al. 2006b,2007). In contrast, juveniles along the US
east coast appear to undergo long-distance seasonal migrations
and may even travel greater distances than adults in the course of
their seasonal migrations (Kneebone et al. 2014). For example,
summer nursery areas used by juvenile sand tigers are located
towards the northernmost extent of their distribution off
Massachusetts (Kneebone et al. 2012), and juveniles tagged
with acoustic transmitters in Delaware Bay were detected in
winter months on receivers as far south as Cape Canaveral,
Florida.
Vertical habitat use during migrations
PSAT-tagged sand tigers demonstrated distinct seasonal shifts
in occupied habitat, moving from a shallow-water estuarine
summer habitat of Delaware Bay to deeper, offshore continental
shelf waters during migration in autumn and winter. Lucifora
et al. (2002) also described seasonal occupancy of a shallow bay
during summer months, followed by departure from the bay in
autumn and long-shore migration of sand tigers off South
America. Sharks tracked in our study occupied a range of depths
with most records at depths of ,80 m. Such depths are similar to
previous observations for sand tigers and to reports from other
studies where sand tigers were tracked with PSAT tags
(Kneebone et al. 2014). Smale et al. (2012) found that PSAT-
tagged sand tigers tracked in South Africa spent a high proportion
of their time at depths of ,60 m, with occasional movements to
deeper continental shelf waters. Otway and Ellis (2011) reported
that both male and female sand tigers tracked with PSAT tags off
eastern Australia spent over 90% of their time at depths ,80 m.
In our study nearly 100% of depth records were also ,80 m other
than for the two largest males tracked, for which ,45% of values
were at depths .80 m. There are several reports of sand tigers
observed or captured at depths of 30–60 m both in shallow,
166 Marine and Freshwater Research S. M. Teter et al.
inshore waters as well as offshore in deep water (Bigelow and
Schroeder 1948;Boschung and Couch 1962;Bass and Ballard
1972;Bass et al. 1975;Moore and Farmer 1981;Russel 1993;
Smale 2005). Otway and Ellis (2011) noted that sand tigers off the
east coast of Australia occupied shallow water while on their
summer and wintering grounds, but moved into deeper waters
while migrating. Several malesharks tracked in our study moved
into shallower water in late December–early January while in
wintering areas off North Carolina, which may reflect a shift to
inshore, shallower water at the completion of their southern
migration. Gilmore (1993) theorised that mature female sand
tigers occupied greater depths than did other demographics.
The three females tracked in our study occupied depths similar
to those observed for males of the same size; however, these
females were immature or recently mature, and depth behaviour
of larger mature females remains unclear. Differences observed
in horizontal movements and vertical habitat utilisation among
sexes and size classes of sand tigers in our study illustrate that
these demographic segments occupy different habitats and, as
such, are exposed to different levels of susceptibility to capture
and mortality in both commercial and recreational fisheries and
are also likely exposed to habitat affected by various levels of
degradation.
All three females and half the males left Delaware Bay within
a 2-week period between 6 and 19 October, consistent with time
of departure observed for a much larger number of sharks
carrying acoustic transmitters (D. Fox, unpubl. data). The
minimum temperature recorded by PSAT tags at the time each
shark was last detected on acoustic receivers within Delaware
Bay was 188C, which corresponds well with surface tempera-
tures recorded on the same dates by Delaware Bay NOAA buoys
(the temperature fell below 188C for the first time on 19 October
2008 [NOAA, NDBC – Station BRND1], see http://www.ndbc.
noaa.gov/station_page.php?station=brnd1). Temperature may
therefore be the putative cue for departure of sand tigers from
Delaware Bay and commencement of migration, with a thresh-
old close to 188C, but the sample size of PSAT-tracked sand
tigers for evaluating such relationships was small.
Variation in temperatures occupied by sand tigers was more
limited than for depth, with most temperature records falling
within a narrow range while in Delaware Bay, but also during
migration, with minimal differences among size classes and
sexes. Sharks in our study spent ,88% of their time at tem-
peratures of 18–228C, similar to values reported for sand tigers
tracked with PSAT tags off eastern Australia, where 96% of
records were between 17 and 248C(Otway and Ellis 2011) and
for juveniles off the US east coast (Kneebone et al. 2014). Smale
et al. (2012), however, reported occupancy of cooler tempera-
tures (15.3–18.48C) for sand tigers tracked with PSAT tags off
South Africa.
Vulnerability to fisheries
The modest number of sharks tracked using satellite tags in our
study, combined with the limited spatial accuracy obtained with
PSAT tags (see confidence intervals around each estimated
track) limits extrapolation of our results to sand tigers on a broad
scale. However, movement of females to the east (rather than
south) of Delaware Bay and as far as 600–700 km offshore near
the continental slope, indicates that there are areas used by a
group of female sand tigers in winter at this northern location.
The extent to which this area may be used by such females
remains uncertain, but our results reveal a previously unrecog-
nised, northern overwintering area for sand tigers. The extent of
use of such areas warrants investigation, particularly if these
types of areas are heavily utilised by females. Although our
focus was on fisheries off the south-east US, sand tigers do occur
as by-catch in fisheries off the north-eastern US, and it is pos-
sible that females are regularly part of this by-catch. The
observation that sand tigers of different size classes and sexes
occupy different locations and different depths illustrates the
likelihood that different fisheries will influence the sand tiger
population in different ways (Corte´s et al. 2010).
During their southerly migrations, male sand tigers exhibited
varying periods where they occupied small areas and demon-
strated little net southward movement. This behaviour is
reflected in areas of high use along migratory pathways illus-
trated by KUD analysis (Fig. 2). These discreet rest-stop areas
used by multiple sharks during their southerly migrations
represent locations frequented by multiple sand tigers, and
may be important habitat for successful migration between
summer and winter grounds. Migration punctuated by regular
stops at ‘resting areas’ (Otway and Ellis 2011) was also observed
off the east coast of Australia, suggesting that this behaviour may
be typical of migrating sand tigers in general. Sand tigers may be
more vulnerable to capture in fisheries in such high-use areas.
More detailed studies of these locations would also enable better
understanding of essential habitat of different segments of the
sand tiger population along the US east coast, and would expand
information on the vulnerability of sand tigers to localised
fisheries and the susceptibility of such habitats to degradation.
Heavy use by sand tigers of areas within and near to the
MASA illustrates the potential of this management area to
provide additional protection for sand tigers in terms of reduced
by-catch and lower fishing mortality from modest expansion of
the MASA boundaries and slight shifts in timing of closure. The
MASA was established to reduce capture of dusky and sandbar
sharks in an effort to enhance recovery of their populations, but
with temporal and spatial modifications the MASA has potential
to enhance recovery of the sand tigers as well. On the basis of the
results of our study, sand tigers typically arrive in the MASA
area before 1 January, the date at which closure to fishing begins.
Locations for five of seven males fell within the MASA in
December (just before area closure), and there were numerous
positions just outside the eastern boundary of the MASA
(Fig. 6). These findings suggest that modifying the timing of
the existing MASA area closure to begin in December, accom-
panied by slight extension of the eastern boundary of the MASA
could provide additional protection to sand tigers. Burgess and
Morgan (2003) reported a total of 355 sand tigers (2.3% of the
shark catch) during 1994–2003 as by-catch in the bottom
longline fishery that operated within the boundaries of the area
that would later become the MASA.
Although landing of sand tigers is prohibited in US waters,
their capture ina variety of commercial and recreational fisheries
on the US east coast persists and undoubtedly results in at least
some mortality even if sharks are released alive. Given the low
reproductive output and low intrinsic rate of increase for sand
tigers, even minimal mortality can hinder recovery of stocks
Sand tiger shark movements Marine and Freshwater Research 167
(Goldman et al. 2006;Carlson et al. 2009). The feeding habits
and tendency of sand tigers to swallow hooks and become gut
hooked, resulting in damage of internal organs, further exacer-
bates the problem of post-release fishing mortality, creating a
challenge even for well intentioned fishers who release sand
tigers alive when they occur as by-catch (Dicken et al. 2006a;
Lucifora et al. 2009). Despite the high level of protection
afforded sand tigers in US waters and the infrequent occurrence
of this species in fisheries, the potential for such interactions and
associated negative effects on the sand tiger population warrants
concern. An integral component of successful management is
identification of areas heavily utilised by sand tigers, delineation
of pathways traveled between distant seasonal habitats and
understanding of the scale of interactions between sand tigers
and humans. Our study has provided information on habitat use,
timing and location of migratory routes for different demographic
segments of the sand tiger population as well as environmental
features associated with these movement patterns. This infor-
mation improves understanding of sand tiger distribution and
biology and will contribute towards their long-term manage-
ment and conservation in the western North Atlantic.
Acknowledgements
This work was supported by the NOAA-NMFS Proactive Species Conser-
vation Program (NA09NMF4720365), the Guy Harvey Ocean Foundation,
the DuPont Clear Into the Future Programs and Nova South-eastern Uni-
versity. We thank P. and L. Howey (Microwave Telemetry Inc.) and K.
Sulak (USGS) for the donation of satellite tags. We thank E. Frederick and C.
Cilfone for data analyses. N. Willett, J. Moore, M. Breece and L. Brown
assisted with deployment of tags and maintenance of acoustic data. We are
grateful to the members of the Atlantic Cooperative Telemetry Network for
providing detections outside of Delaware: special thanks to SUNY Stony
Brook, East Carolina University, South Carolina DNR, and NASA. Dela-
ware State University provided funding for vessel operations and allowed
students and staff to donate time to field collections.
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